ORIGINAL_ARTICLE
Marine algae as emerging therapeutic alternatives for depression: A review
Depression is a complex heterogeneous brain disorder characterized by a range of symptoms, resulting in psychomotor and cognitive disabilities and suicidal thoughts. Its prevalence has reached an alarming level affecting millions of people globally. Despite advances in current pharmacological treatments, the heterogenicity of clinical response and incidences of adverse effects have shifted research focus to identification of new natural substances with minimal or no adverse effects as therapeutic alternatives. Marine algae-derived extracts and their constituents are considered potential sources of secondary metabolites with diverse beneficial effects. Marine algae with enormous health benefits are emerging as a natural source for discovering new alternative antidepressants. Its medicinal properties exhibited shielding efficacy against neuroinflammation, oxidative stress, and mitochondrial dysfunction, which are indicated to underlie the pathogenesis of many neurological disorders. Marine algae have been found to ameliorate depressive-like symptoms and behaviors in preclinical and clinical studies by restoring monoaminergic neurotransmission, hypothalamic-pituitary-adrenal axis function, neuroplasticity, and continuous neurogenesis in the dentate gyrus of the hippocampus via modulating brain-derived neurotrophic factors and antineuroinflammatory activity. Although antidepressant effects of marine algae have not been validated in comparison with currently available synthetic antidepressants, they have been reported to have effects on the pathophysiology of depression, thus suggesting their potential as novel antidepressants. In this review, we analyzed the currently available research on the potential benefits of marine algae on depression, including their effects on the pathophysiology of depression, potential clinical relevance of their antidepressant effects in preclinical and clinical studies, and the underlying mechanisms of these effects.
https://ijbms.mums.ac.ir/article_18461_5fecb08d67d503a2f30c4a2a83dc8f88.pdf
2021-08-01
997
1013
10.22038/ijbms.2021.54800.12291
Antidepressants
Complementary Medicine
Depression
Microalgae
Neuroinflammation
Neuronal plasticity
Seaweed
Kogilavani
Subermaniam
suwanvani@yahoo.com
1
Department of Anatomy, Faculty of Medicine, Universiti Malaya, 50603 Kuala Lumpur, Malaysia
AUTHOR
Seong
Teoh
teohseonglin@ppukm.ukm.edu.my
2
Department of Anatomy, Faculty of Medicine, Universiti Kebangsaan Malaysia Medical Center, Jalan Yaacob Latif, Bandar Tun Razak, 56000 Kuala Lumpur, Malaysia
AUTHOR
Yoon
Yow
yoonyeny@sunway.edu.my
3
Department of Biological Sciences, School of Medical and Life Sciences, Sunway University, 47500 Bandar Sunway, Selangor Darul Ehsan, Malaysia
AUTHOR
Yin
Tang
tangyinquan@gmail.com
4
School of Biosciences, Faculty of Health & Medical Sciences, Taylor’s University Lakeside Campus, 47500 Subang Jaya, Selangor Darul Ehsan, Malaysia
AUTHOR
Lee
Lim
drlimleewei@gmail.com
5
Neuromodulation Laboratory, School of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, 21 Sassoon Road, Pokfulam, Hong Kong Special Administrative Region, China
AUTHOR
Kah
Wong
wkahhui@um.edu.my
6
Department of Anatomy, Faculty of Medicine, Universiti Malaya, 50603 Kuala Lumpur, Malaysia
LEAD_AUTHOR
1. World Health Organization. Depression and other common mental disorders: global health estimates. Geneva, Switzerland: World Health Organization, 2017.
1
2. Wong SK, Chin KY, Ima-Nirwana S. Vitamin D and depression: the evidence from an indirect clue to treatment strategy. Curr Drug Targets 2018; 19:888-897.
2
3. GBD 2017 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 2018; 392:1789-1858.
3
4. Institute for Public Health. National Health and Morbidity Survey (NHMS) 2019: non-communicable diseases, healthcare demand and health literacy-key findings (pp 21-22). Selangor, Malaysia: National Institutes of Health (NIH), Ministry of Health Malaysia, 2020.
4
5. Indu PS, Anilkumar TV, Pisharody R, Russell PSS, Raju D, Sarma PS, et al. Prevalence of depression and past suicide attempt in primary care. Asian J Psychiatr 2017; 27:48-52.
5
6. Lim GY, Tam WW, Lu Y, Ho CS, Zhang MW, Ho RC. Prevalence of depression in the community from 30 countries between 1994 and 2014. Sci Rep 2018; 8:2861-2870.
6
7. Kennedy SH, Lam RW, McIntyre RS, Tourjman SV, Bhat V, Blier P, et al. Canadian network for mood and anxiety treatments (CANMAT) 2016 clinical guidelines for the management of adults with major depressive disorder: Section 3. Pharmacological Treatments. Can J Psychiatry 2016; 61:540-560.
7
8. Wang SM, Han C, Bahk WM, Lee SJ, Patkar AA, Masand PS, et al. Addressing the side effects of contemporary antidepressant drugs: A comprehensive review. Chonnam Med J 2018; 54:101-112.
8
9. Chong PS, Fung ML, Wong KH, Lim LW. Therapeutic potential of Hericium erinaceus for depressive disorder. Int J Mol Sci 2020; 21:163-180.
9
10. Lew SY, Lim SH, Lim LW, Wong KH. Neuroprotective effects of Hericium erinaceus (Bull.: Fr.) Pers. against high-dose corticosterone-induced oxidative stress in PC-12 cells. BMC Complement Med Ther 2020; 20:340-355.
10
11. Lew SY, Teoh SL, Lim SH, Lim LW, Wong KH. Discovering the potentials of medicinal mushrooms in combating depression-A review. Mini Rev in Med Chem 2020; 20:1518-1531.
11
12. Subermaniam K, Yow YY, Lim SH, Koh OH, Wong KH. Malaysian macroalga Padina australis Hauck attenuates high dose corticosterone-mediated oxidative damage in PC12 cells mimicking the effects of depression. Saudi J Biol Sci 2020; 27:1435-1445.
12
13. Chong CW, Hii SL, Wong CL. Antibacterial activity of Sargassum polycystum C. Agardh and Padina australis Hauck (Phaeophyceae). Afr J Biotechnol 2011; 10:14125-14131.
13
14. Murugan AC, Vallal D, Karim MR, Govidan N, Yusoff MBM, Rahman MM. In vitro antiradical and neuroprotective activity of polyphenolic extract from marine algae Padina autralis. J Chem Pharm Res 2015; 7:355-362.
14
15. Gany SA, Tan SC, Gan SY. Antioxidative, anticholinesterase and anti-neuroinflammatory properties of Malaysian brown and green seaweeds. Int J Biol Biomol Agric Food Biotechnol Eng 2014; 8:1269-1275.
15
16. Hannan MA, Dash R, Haque MN, Mohibbullah M, Sohag AAM, Rahman MA, et al. Neuroprotective potentials of marine algae and their bioactive metabolites: pharmacological insights and therapeutic advances. Mar Drugs 2020; 18:347.
16
17. Jiang X, Chen L, Shen L, Chen Z, Xu L, Zhang J, et al. Trans-astaxanthin attenuates lipopolysaccharide-induced neuroinflammation and depressive-like behavior in mice. Brain Res 2016; 1649(Part A):30-37.
17
18. Jiang X, Zhu K, Xu Q, Wang G, Zhang J, Cao R, et al. The antidepressant-like effect of trans-astaxanthin involves the serotonergic system. Oncotarget 2017;8:25552-25563.
18
19. Sasaki K, Othman MB, Demura M, Watanabe M, Isoda H. Modulation of neurogenesis through the promotion of energy production activity is behind the antidepressant-like effect of colonial green alga, Botryococcus braunii. Front Physiol 2017; 8:900-908.
19
20. Violle N, Rozan P, Demais H, Collen PN, Bisson JF. Evaluation of the antidepressant- and anxiolytic-like effects of a hydrophilic extract from the green seaweed Ulva sp. in rats. Nutr Neurosci 2018; 21:248-256.
20
21. Moradi-Kor N, Ghanbari A, Rashidipour H, Bandegi AR, Yousefi B, Barati M., et al. Therapeutic effects of Spirulina platensis against adolescent stress-induced oxidative stress, brain-derived neurotrophic factor alterations and morphological remodeling in the amygdala of adult female rats. J Exp Pharmacol 2020; 2:75-85.
21
22. Matraszek-Gawron R, Chwil M, Terlecka P, Skoczylas MM. Recent studies on anti-depressant bioactive substances in selected species from the genera Hemerocallis and Gladiolus: a systematic review. Pharmaceuticals 2019; 12:172-203.
22
23. Perez-Caballero L, Torres-Sanchez S, Romero-López-Alberca C, González-Saiz F, Mico JA, Berrocoso E. Monoaminergic system and depression. Cell Tissue Res 2019; 377:107-113.
23
24. Lemieux G, Davignon A, Genest J. Depressive states during Rauwolfia therapy for arterial hypertension; a report of 30 cases. Can Med Assoc J 1956; 74:522-526.
24
25. Loomer HP, Saunders JC, Kline NS. A clinical and pharmacodynamic evaluation of iproniazid as a psychic energizer. Psychiatr Res Rep Am Psychiatr Assoc 1957; 8:129-141.
25
26. Stahl SM. Selecting an antidepressant by using mechanism of action to enhance efficacy and avoid side effects. J Clin Psychiatry 1998; 59(Suppl 18):23-29.
26
27. Watkins M. Antianxiety Pharmacology. Encyclopedia of the Neurological Sciences 2014; 1:204-206.
27
28. Siddiqui PJA, Khan A, Uddin N, Khaliq S, Rasheed M, Nawaz S, et al. Antidepressant-like deliverables from the sea: evidence on the efficacy of three different brown seaweeds via involvement of monoaminergic system. Biosci Biotechnol Biochem 2017; 81:1369-1378.
28
29. Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R, et al. Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol 2016; 6:603-621.
29
30. Chen J, Evans AN, Liu Y, Honda M, Saavedra JM, Aguilera G. Maternal deprivation in rats is associated with corticotrophin releasing hormone (CRH) promoter hypomethylation and enhances CRH transcriptional responses to stress in adulthood. J Neuroendocrinol 2012; 24:1055-1064.
30
31. Juruena MF, Cleare AJ, Bauer M, Pariante CM. Molecular mechanisms of glucocorticoid receptor sensitivity and relevance to affective disorders. Acta Neuropsychiatr 2003; 15: 354-367.
31
32. Wardle RA, Poo MM. Brain-derived neurotrophic factor modulation of GABAergic synapses by postsynaptic regulation of chloride transport. J Neurosci 2003; 23:8722-8732.
32
33. Sirianni RW, Olausson P, Chiu AS, Taylor JR, Saltzman WM. The behavioral and biochemical effects of BDNF containing polymers implanted in the hippocampus of rats. Brain Res 2010; 1321:40-50.
33
34. Kim NH, Jeong HJ, Lee JY, Go H, Ko SG, Hong SH, et al. The effect of hydrolyzed Spirulina by malted barley on forced swimming test in ICR mice. Int J Neurosci 2008; 118:1523-1533.
34
35. Martinowich K, Manji H, Lu B. New insights into BDNF function in depression and anxiety. Nat Neurosci 2007; 10:1089-1093.
35
36. Duman RS, Heninger GR, Nestler EJ. A molecular and cellular theory of depression. Arch Gen Psychiatry 1997; 54:597-606.
36
37. Friedman WJ. Proneurotrophins, seizures, and neuronal apoptosis. Neuroscientist 2010; 16: 244-252.
37
38. Volosin M, Song W, Almeida RD, Kaplan DR, Hempstead BL, Friedman WJ. Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. J. Neurosci 2006; 26:7756-7766.
38
39. Bakunina N, Pariante CM, Zunszain PA. Immune mechanisms linked to depression via oxidative stress and neuroprogression. Immunology 2015; 144:365-373.
39
40. Troubat R, Barone P, Leman S, Desmidt T, Cressant A, Atanasova B, et al. Neuroinflammation and depression: a review. Eur J Neurosci 2021; 53:151-171
40
41. Maes M, Bosmans E, De Jongh R, Kenis G, Vandoolaeghe E, Neels H. Increased serum IL-6 and IL-1 receptor antagonist concentrations in major depression and treatment-resistant depression. Cytokine 1997; 9(11):853-858.
41
42. Verduijn J, Milaneschi Y, Schoevers RA, van Hemert AM, Beekman ATF, Penninx BWJH. Pathophysiology of major depressive disorder: mechanisms involved in etiology are not associated with clinical progression. Transl Psychiatry 2015; 5:1-9.
42
43. Suzuki E, Yagi G, Nakaki T, Kanba S, Asai M. Elevated plasma nitrate levels in depressive states. J Affect Disord 2001; 63:221–224.
43
44. Dhir A, Kulkarni S. Involvement of nitric oxide (NO) signaling pathway in the antidepressant action of bupropion, a dopamine reuptake inhibitor. Eur J Pharmacol. 2007; 568:177-185.
44
45. Brites D, Fernandes A. Neuroinflammation and depression: microglia activation, extracellular microvesicles and microRNA dysregulation. Front Cell Neurosci 2015; 9:1-20.
45
46. Peirce J, Alviña K. The role of inflammation and the gut microbiome in depression and anxiety. J Neurosci Res 2019; 97:1223-1241.
46
47. Müller N. Immunological aspects of the treatment of depression and schizophrenia. Dialogues Clin Neurosci 2017; 19:55-63.
47
48. Yoon RSY, Ravindran N, Ravindran A. Complementary and alternative therapies for treatment-resistant depression: a clinical perspective. In: Shivakumar K, Amanullah S (eds). Complex clinical conundrums in psychiatry. Cham, Switzerland: Springer; 2018.p. 123-142.
48
49. Pereira L. Therapeutic and nutritional uses of algae. Boca Raton, Florida: CRC Press; 2018.
49
50. Pandey A. Microalgae biomass production for CO2 mitigation and biodiesel production. J Microbiol Exp 2017; 4:00117.
50
51. Pangestuti R, Kim SK. Neuroprotective effects of marine algae. Mar Drugs 2011; 9:803-818.
51
52. Suresh D, Madhu M, Saritha C, Raj Kumar V, Shankaraiah P. Antidepressant activity of Spirulina platensis in experimentally induced depressed mice. Int J Pharm Arch 2014; 3(2):317-326.
52
53. Soetantyo GI, Sarto M. The antidepressant effect of Chlorella vulgaris on female Wistar rats (Rattus norvegicus Berkenhout, 1769) with chronic unpredictable mild stress treatment. J Trop Biodivers Biotechnol 2019; 4:72-81.
53
54. Qiao J, Rong L, Wang Z, Zhang M. Involvement of Akt/GSK3b/CREB signaling pathway on chronic omethoate induced depressive-like behavior and improvement effects of combined lithium chloride and astaxanthin treatment. Neurosci Lett 2017; 649:55-61.
54
55. Abreu TM, Monteiro VS, Martins ABS, Teles FB, da Conceicao Rivanor RL, Mota EF, et al. Involvement of the dopaminergic system in the antidepressant-like effect of the lectin isolated from the red marine alga Solieria filiformis in mice. Int J Biol Macromol 2018; 111:534-541.
55
56. Panahi Y, Badeli R, Karami GR, Badeli Z, Sahebkar A. A randomized controlled trial of 6-week Chlorella vulgaris supplementation in patients with major depressive disorder. Complement Ther Med 2015; 23:598-602.
56
57. Talbott S, Hantla D, Capelli B, Ding L, Li Y, Artaria C. Astaxanthin supplementation reduces depression and fatigue in healthy subjects. EC Nutrition 2019; 14:239-246.
57
58. Miyake, Y, Tanaka K, Okubo H, Sasaki S, Arakawa M. Seaweed consumption and prevalence of depressive symptoms during pregnancy in Japan: baseline data from the Kyushu Okinawa maternal and child health study. BMC Pregnancy Childbirth 2014; 14:301-307.
58
59. Allaert FA, Demais H, Collen PN. A randomized controlled double-blind clinical trial comparing versus placebo the effect of an edible algal extract (Ulva lactuca) on the component of depression in healthy volunteers with anhedonia. BMC Psychiatry 2018; 18:215-224.
59
60. Guo F, Huang C, Cui Y, Momma H, Niu K, Nagatomi R. Dietary seaweed intake and depressive symptoms in Japanese adults: a prospective cohort study. Nutr J 2019; 18:1-8.
60
61. Xu T, Qin S, Hu Y, Song Z, Ying J, Li P, et al. Whole genomic DNA sequencing and comparative genomic analysis of Arthrospira platensis: high genome plasticity and genetic diversity. DNA Res 2016; 23:325-338.
61
62. Okechukwu PN, Ekeuku SO, Sharma M, Chong PN, Chan HK, Mohamed N, et al. In vivo and in vitro antidiabetic and anti-oxidant activity of Spirulina. Pharmacogn Mag 2019; 15:17-29.
62
63. Zajecka JM, Albano D. SNRIs in the management of acute major depressive disorder. J Clin Psychiatry 2004; 65(Suppl 17):11-18.
63
64. Brydges NM, Jin R, Seckl J, Holmes MC, Drake AJ, Hall J. Juvenile stress enhances anxiety and alters corticosteroid receptor expression in adulthood. Brain and Behav 2014; 4:4-13.
64
65. Kanwal JS, Jung Y, Zhang M. Brain plasticity during adolescence: effects of stress, sleep, sex and sounds on decision making. Anat Physiol 2016; 6:e135.
65
66. Cheng P, Okada S, Zhou C, Chen P, Huo S, Li K, et al. High-value chemicals from Botryococcus braunii and their current applications - A review. Bioresour Technol 2019; 291:121911.
66
67. Jaafar F, Durani LW, Makpol S. Chorella vulgaris modulates the expression of senescence-associated genes in replicative senescence of human diploid fibroblasts. Mol Biol Rep 2020; 47:369-379.
67
68. Safi C, Zebib B, Merah O, Pontalier P, Vaca-Garcia C. Morphology, composition, production, processing and applications of Chlorella vulgaris: a review. Renew Sust Energ Rev 2014; 35:265-278.
68
69. Lorenz RT, Cysewski GR. Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 2000; 18:160-167.
69
70. Allewaert CC, Vanormelingen P, Proschold T, Gomez PI, Gonzalez MA, Bilcke G, et al. Species diversity in European Haematococcus pluvialis (Chlorophyceae, Volvocales). Phycologia 2019; 54:583-598.
70
71. Maeng SH, Hong H. Inflammation as the potential basis in depression. Int Neurol J 2019; 23(Suppl 2):S63-71.
71
72. Wu H, Niu H, Shao A, Wu C, Dixon BJ, Zhang J, et al. Astaxanthin as a potential neuroprotective agent for neurological diseases. Mar Drugs 2015; 13:5750-5766.
72
73. Balietti M, Giannubilo SR, Giorgetti B, Solazzi M, Turi A, Casoli T, et al. The effect of astaxanthin on the aging rat brain: gender-related differences in modulating inflammation. J Sci Food Agric 2016; 96:615-618.
73
74. Shannon E, Abu-Ghannam N. Antibacterial derivatives of marine algae: an overview of pharmacological mechanisms and application. Mar Drugs 2016; 14:81.
74
75. Phang SM, Yeong HY, Ganzon-Fortes ET, Lewmanomont K, Prathep A, Hau LN, et al. Marine algae of the South China Sea bordered by the Philiphines, Indonesia, Singapore, Malaysia, Thailand and Vietnam. Raffles Bull Zool 2016; Supplement 34:13-59.
75
76. Guiry MD, Guiry GM. No Title [Internet] AlgaeBase. World-wide electronic publication, National University of Ireland, Galway (taxonomic information republished from Algae Base with permission of M.D. Guiry). Solieria filiformis (Kützing) Gabrielson 1985. 2020 [cited 2020 May 30]. Available from: http://www.algaebase.org/search/species/detail/?species_id=686.
76
77. Shimada S, Yokoyama N, Arai S, Hiraoka M. Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. J Appl Phycol 2009; 20:529-539.
77
78. Pangestuti R, Kurnianto D. Green seaweeds-derived polysaccharides ulvan: Occurrence, medicinal value and potential applications. In: Venkatesan J, Anil S, Kim S, (eds.). Seaweed polysaccharides: Isolation, biological and biomedical applications. Amsterdam, Netherlands: Elsevier; 2017.p. 205-221.
78
79. Hughey JR, Maggs CA, Mineur F, Jarvis C, Miller KA, Shabaka SH, et al. Genetic analysis of the Linnaean Ulva lactuca (Ulvales, Chlorophyta) holotype and related type specimens reveals name misapplications, unexpected origins, and new synonymies. J Phycol 2019; 55:503-508.
79
80. Zou D, Ji Z, Chen W, Li G. High temperature stress might hamper the success of sexual reproduction in Hizikia fusiformis from Shantou, China: a photosynthetic perspective. Phycologia 2018; 57:394-400.
80
81. Watanabe Y, Yamada H, Mine T, Kawamura Y, Nishihara GN, Terada R. Photosynthetic responses of Pyropia yezoensis f. narawaensis (Bangiales, Rhodophyta) to a thermal and PAR gradient vary with the life-history stage. Phycologia 2016; 55:665-672.
81
82. Pal Singh H, Sharma S, Chauhan SB, Kaur I. Clinical trials of traditional herbal medicines in India: current status and challenges. Int J Pharmacogn 2014; 1:415-421.
82
83. Rasia-Filho AA, Fabian C, Rigoti KM, Achaval M. Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience 2004; 126:839-847.
83
84. Slattery DA, Cryan JF. Using the rat forced swim test to assess antidepressant-like activity of rodents. Nat Protoc 2012; 7:1009-1014.
84
85. Mao QQ, Huang Z, Ip SP, Xian YF, Che CT. Protective effects of piperine against corticosterone-induced neurotoxicity in PC12 cells. Cell Mol Neurobiol 2012; 32:531-537.
85
86. Fillingim RB, Price DD. What is controlled for in placebo-controlled trials? Mayo Clin Proc 2005; 80:1119-1121.
86
87. Moka D, Dietlein M, Schicha H. Radioiodine therapy and thyrostatic drugs and iodine. Eur J Nucl Med Mol Imaging 2002; 29(Suppl 2):S486-491.
87
88. Fleurence J, Morançais M, Dumay J, Decottignies P, Turpin V, Munier M, et al. What are the prospects for using seaweed in human nutrition and for marine animals raised through aquaculture? Trends Food Sci Technol 2012; 27:57-61.
88
89. Nabavi SM, Daglia M, Braidy N, Nabavi SF. Natural products, micronutrients, and nutraceuticals for the treatment of depression: a short review. Nutr Neurosci 2017; 20:180-194.
89
90. Bocquier A, Cortaredona S, Verdoux H, Casanova L, Sciortino V, Nauleau S, et al. Social inequalities in early antidepressant discontinuation. Psychiatr Serv 2014; 65:618-625.
90
91. Liu L, Liu C, Wang Y, Wang P, Li Y, Li B. Herbal medicine for anxiety, depression and insomnia. Curr Neuropharmacol 2015; 13:481-493.
91
92. Miller AH, Raison CL. The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nat Rev Immun 2016; 16:22-34.
92
93. Lindqvist D, Dhabhar FS, James SJ, Hough CM, Jain FA, Bersani FS, et al. Oxidative stress, inflammation and treatment response in major depression. Psychoneuroendocrinology 2017; 76:197-205.
93
ORIGINAL_ARTICLE
Thymoquinone against infectious diseases: Perspectives in recent pandemics and future therapeutics
The recent pandemics caused by coronavirus infections have become major challenges in 21st century human health. Scientists are struggling hard to develop a complete cure for infectious diseases, for example, drugs or vaccines against these deadly infectious diseases. We have searched papers on thymoquinone (TQ) and its effects on different infectious diseases in databases like Pubmed, Web of Science, Scopus, and Google Scholar, and reviewed them in this study. To date research suggests that natural products may become a potential therapeutic option for their prodigious anti-viral or anti-microbial effects on infectious diseases. TQ, a natural phytochemical from black seeds, is known for its health-beneficial activities against several diseases, including infections. It is evident from different in vitro and in vivo studies that TQ is effective against tuberculosis, influenza, dengue, Ebola, Zika, hepatitis, malaria, HIV, and even recent pandemics caused by severe acute respiratory syndrome of coronaviruses (SARS-CoV and SARS-CoV-2). In these cases, the molecular mechanism of TQ is partly clear but mostly obscure. In this review article, we have discussed the role of TQ against different infectious diseases, including COVID-19, and also critically reviewed the future use of TQ use to fight against infectious diseases.
https://ijbms.mums.ac.ir/article_18423_aa6bf146632a8901491e462e216d09f5.pdf
2021-08-01
1014
1022
10.22038/ijbms.2021.56250.12548
Antimicrobial natural
products Future therapeutics Infectious disease SARS
CoV Thymoquinone
Mousumi
Tania
mousumitania@yahoo.com
1
Research Division of Nature Study Society of Bangladesh, Dhaka, Bangladesh
AUTHOR
Asaduzzaman
Asad
asadjubd@gmail.com
2
Department of Biochemistry and Molecular Biology, Jahangirnagar University, Savar, Dhaka, Bangladesh
AUTHOR
Tian
Li
ltanyhh@163.com
3
The Research Center for Preclinical Medicine, Southwest Medical University, Luzhou, Sichuan, China
AUTHOR
Md. Shariful
Islam
shariful.sharifbmb40@gmail.com
4
Department of Biochemistry and Molecular Biology, Tejgaon College, National University, Dhaka, Bangladesh
AUTHOR
Shad
Bin Islam
shadbinislam@yahoo.com
5
Bachelor in Medicine and Surgery Program, Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, China
AUTHOR
Md. Munnaf
Hossen
mmhossen_nfs@yahoo.com
6
Department of Immunology, Health Science Center, Shenzhen, University, Shenzhen, Guangdong, China
AUTHOR
Mizanur Rahman
Bhuiyan
mizanur.rahman.bhuiyan59@gmail.com
7
Research Division of Nature Study Society of Bangladesh, Dhaka, Bangladesh
AUTHOR
Md. Asaduzzaman
Khan
asadkhan@swmu.edu.cn
8
The Research Center for Preclinical Medicine, Southwest Medical University, Luzhou, Sichuan, China
LEAD_AUTHOR
1. Salam AM, Quave CL. Opportunities for plant natural products in infection control. Curr Opin Microbiol 2018; 45:189-194.
1
2. Kim KJ, Liu X, Komabayashi T, Jeong SI, Selli S. Natural products for infectious diseases. Evid Based Complement Alternat Med 2016; 9459047.
2
3. Wang H, Wang Z, Dong Y, Chang R, Xu C, Yu X, et al. Phase-adjusted estimation of the number of Coronavirus Disease 2019 cases in Wuhan, China. Cell Discov 2020; 6:10.
3
4. Coronaviridae Study Group of the International Committee on Taxonomy of Viruses. The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol 2020; 5:536-544.
4
5. Ganjhu RK, Mudgal PP, Maity H, Dowarha D, Devadiga S, Nag S, et al. Herbal plants and plant preparations as remedial approach for viral diseases. Virusdisease 2015; 26:225-236.
5
6. Denaro M, Smeriglio A, Barreca D, De Francesco C, Occhiuto C, Milano G, et al. Antiviral activity of plants and their isolated bioactive compounds: An update. Phytother Res 2020; 34:742-768.
6
7. Khan MA, Tania M, Fu S, Fu J. Thymoquinone, as an anticancer molecule: from basic research to clinical investigation. Oncotarget 2017; 8:51907-51919.
7
8. Khan MA, Tania M, Wei C, Mei Z, Fu S, Cheng J, et al. Thymoquinone inhibits cancer metastasis by downregulating TWIST1 expression to reduce epithelial to mesenchymal transition. Oncotarget 2015; 6:19580-19591.
8
9. Khan MA, Chen HC, Tania M, Zhang DZ. Anticancer activities of Nigella sativa (black cumin). Afr J Tradit Complement Altern Med 2011; 8:226-232.
9
10. Yimer M, Tuem KB, Karim A, Ur-Rehman N, Anwar F. Nigella sativa L. (Black Cumin): A promising natural remedy for wide range of illnesses. Evid Based Complement Alternat Med 2019; 1528635.
10
11. Tavakkoli A, Mahdian V, Razavi BM, Hosseinzadeh H. Review on clinical trials of black seed (Nigella sativa ) and its active constituent, thymoquinone. J Pharmacopuncture 2017; 20:179-193.
11
12. Khader M, Eckl PM. Thymoquinone: an emerging natural drug with a wide range of medical applications. Iran J Basic Med Sci 2014; 17:950-957.
12
13. Khan MA, Thymoquinone, a constituent of prophetic medicine-black seed, is a miracle therapeutic molecule against multiple diseases. Int J Health Sci (Qassim) 2019; 13:1-2.
13
14. Bouchentouf S, Missoum N. Identification of compounds from Nigella Sativa as new potential inhibitors of 2019 novel coronasvirus (Covid-19): Molecular docking study. ChemRxiv 2020.
14
15. Ahmad A, Rehman MU, Ahmad P, Alkharfy KM, Covid-19 and thymoquinone: Connecting the dots. Phytother Res 2020; 34:2786-2789.
15
16. Da Costa VG, Moreli ML, Saivish MV. The emergence of SARS, MERS and novel SARS-2 coronaviruses in the 21st century. Arch Virol 2020; 165:1517-1526.
16
17. Morens DM, Daszak P, Markel H, Taubenberger JK. Pandemic COVID-19 Joins History’s Pandemic Legion. mBio 2020; 11:e00812-e00820.
17
18. Çelik I, Saatçi E, Eyüboğlu AF. Emerging and reemerging respiratory viral infections up to Covid-19. Turki J Med Sci 2020; 50:557-562.
18
19. Vabret A, Dina J, Gouarin S, Petitjean J, Tripey V, Brouard J, Freymuth F. Human (non-severe acute respiratory syndrome) coronavirus infections in hospitalised children in France. J Paediatr Child Health 2008; 44:176-181.
19
20. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, et al. SARS Working Group, A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 2003; 348:1953-1966.
20
21. World Health Organization, Global alert and response (GAR), Summary table of SARS cases by country, 1 November 2002–7. 2003; http://www.who.int/csr/sars/country/2003_08_15/en/index.html. (accessed 27 December 2012).
21
22. Cheng VC, Chan JF, To KK, Yuen KY. Clinical management and infection control of SARS: lessons learned. Antiviral Res 2013; 100:407-419.
22
23. Song Z, Xu Y, Bao L, Zhang L, Yu P, Qu Y, et al. From SARS to MERS, Thrusting Coronaviruses into the Spotlight. Viruses 2019; 11:59.
23
24. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus ADME, Fouchier RAM. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 2012; 367:1814-1820.
24
25. Ithete NL, Stoffberg S, Corman VM, Cottontail VM, Richards LR, Schoeman MC, et al. Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg Infect Dis 2013; 19:1697-1699.
25
26. World Health Organization. Middle East respiratory syndrome. MERS situation update January 2020. 2020; http://www.emro.who.int/health-topics/merscov/mers-outbreaks.html. (accessed 27 December 2020).
26
27. Paraskevis D, Kostaki EG, Magiorkinis G, Panayiotakopoulos G, Sourvinos G, Tsiodras S. Full-genome evolutionary analysis of the novel coronavirus (2019-nCoV) rejects the hypothesis of emergence as a result of a recent recombination event. Infect Genet Evol 2020; 79:104212.
27
28. Siam MHB, Nishat NH, Ahmed A, Hossain MS. Stopping the COVID-19 Pandemic: A Review on the advances of diagnosis, treatment, and control measures. J Pathog 2020; 9121429
28
29. Rothe C, Schunk M, Sothmann P, Bretzel G, Froeschl G, Wallrauch C, et al. Transmission of 2019-nCoV Infection from an asymptomatic contact in Germany. N Engl J Med 2020; 382:970-971.
29
30. To KKW, Tsang OTY, Yip CCY, Chan KH, Wu TC, Chan JMC, et al. Consistent detection of 2019 novel coronavirus in saliva. Clinical Infectious Diseases 2020; 71:841-843.
30
31. Imai Y, Kuba K, Rao S, Huan Y, Guo F, Guan B, et al. Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 2005; 436:112-116.
31
32. Meyerholz DK, Lambertz AM, Jr. McCray PB. Dipeptidyl peptidase 4 distribution in the human respiratory tract: Implications for the middle east respiratory syndrome. Am J Pathol 2016; 186:78-86.
32
33. Widagdo W, Raj VS, Schipper D, Kolijn K, van Leenders GKLH, Bosch BJ, et al. Differential expression of the middle east respiratory syndrome coronavirus receptor in the upper respiratory tracts of humans and dromedary camels. J Virol 2016; 90:4838-4842.
33
34. Jaijyan DK, Liu J, Hai R, Zhu H. Emerging and reemerging human viral diseases. Ann Microbiol Res 2018; 2:31-44.
34
35. Menachery VD, Yount Jr. BL, Debbink K, Agnihothram S, Gralinski LE, Plante JA, et al. A SARS-like cluster of circulating bat coronaviruses shows potential for human emergence. Nat Med 2015; 21:1508-1513.
35
36. Li J, Khan MA, Wei C, Cheng J, Chen H, Yang L, et al. Thymoquinone inhibits the migration and invasive characteristics of cervical cancer cells siha and caski in vitro by targeting epithelial to mesenchymal transition associated transcription factors Twist1 and Zeb1. Molecules 2017; 22:2105.
36
37. Khan MA, Tania M, Fu J. Epigenetic role of thymoquinone: impact on cellular mechanism and cancer therapeutics. Drug discovery today 2019; 24:2315-2322.
37
38. Alexander HR, Syed Alwi SS, Yazan LS, Zakarial Ansar FH. Ong YS. Migration and proliferation effects of thymoquinone-loaded nanostructured lipid carrier (TQ-NLC) and thymoquinone (TQ) on in vitro wound healing models. Evid Based Complement Alternat Med 2019; 2019:9725738.
38
39. Xu J, Liu J, Yue G, Sun M, Li J, Xiu X, et al. Therapeutic effect of the natural compounds baicalein and baicalin on autoimmune diseases. Mol Med Rep 2018; 18:1149-1154.
39
40. Nagi MN, Mansour MA. Protective effect of thymoquinone against doxorubicin-induced cardiotoxicity in rats: a possible mechanism of protection. Pharmacol Res 2000; 41:283-289.
40
41. Goel S, Mishra P. Thymoquinone inhibits biofilm formation and has selective antibacterial activity due to ROS generation. Appl Microbiol Biotechnol 2018; 102:1955-1967.
41
42. Rathore C, Upadhyay N, Kaundal R, Dwivedi RP, Rahatekar S, John A, et al. Enhanced oral bioavailability and hepatoprotective activity of thymoquinone in the form of phospholipidic nano-constructs. Expert Opin Drug Deliv 2020; 17:237-253.
42
43. Oskouei Z, Akaberi M, Hosseinzadeh H. A glance at black cumin (Nigella sativa) and its active constituent, thymoquinone, in ischemia: a review. Iran J Basic Med Sci 2018; 21:1200-1209.
43
44. Forouzanfar F, Bazzaz BS, Hosseinzadeh H. Black cumin (Nigella sativa) and its constituent (thymoquinone): a review on antimicrobial effects. Iran J Basic Med Sci 2014; 17:929-938.
44
45. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395:497-506.
45
46. Chen N, Zhou M, Dong X, Qu J, Gong F, Han Y, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet 2020; 395:507-513.
46
47. Li G, He X, Zhang L, Ran Q, Wang J, Xiong A, et al. Assessing ACE2 expression patterns in lung tissues in the pathogenesis of COVID-19. J Autoimmun 2020; 112:102463.
47
48. Shawon J, Akter Z, Hossen MM, Akter Y, Sayeed A, Junaid M, et al. Current landscape of natural products against coronaviruses: Perspectives in COVID-19 treatment and anti-viral mechanism. Curr Pharm Des 2020; 26:5241-5260.
48
49. Elfiky A. Natural products may interfere with SARS-CoV-2 attachment to the host cell. J Biomol Struct Dyn 2020; 1-10.
49
50. Jakhmola Mani R, Sehgal N, Dogra N, Saxena S, Pande Katare D. Deciphering underlying mechanism of Sars-CoV-2 infection in humans and revealing the therapeutic potential of bioactive constituents from Nigella sativa to combat COVID19: in-silico study. J Biomol Struct Dyn 2020; 1-13.
50
51. Rahman MT. Potential benefits of combination of Nigella sativa and Zn supplements to treat COVID-19. J Herb Med 2020; 23:100382.
51
52. Xu H, Liu B, Xiao Z, Zhou M, Ge L, Jia F, et al. Computational and experimental studies reveal that thymoquinone blocks the entry of coronaviruses into in vitro cells. Infect Dis Ther 2021; 1–12. Advance online publication.
52
53. Khan MA, Younus H. Potential implications of black seed and its principal constituent Thymoquinone in the treatment of COVID-19 patients. Curr Pharm Biotechnol 2020; 10.2174/1389201021999201110205048. Advance online publication.
53
54. Ulasli M, Gurses SA, Bayraktar R, Yumrutas O, Oztuzcu S, Igci M, et al. The effects of Nigella sativa (Ns), Anthemis hyaline (Ah) and Citrus sinensis (Cs) extracts on the replication of coronavirus and the expression of TRP genes family. Mol Biol Rep 2014; 41:1703-1711.
54
55. Islam MN, Hossain KS, Sarker PP, Ferdous J, Hannan MA, Rahman MM, et al. Revisiting pharmacological potentials of Nigella sativa seed: a promising option for COVID-19 prevention and cure. Phytother Res 2021; 35:1329-1344.
55
56. ClinicalTrials.gov. Honey & Nigella sativa trial against COVID-19. Identifier: NCT04347382. 2020; https://clinicaltrials.gov/ct2/show/NCT04347382.
56
57. Mahmud HA, Seo H, Kim S, Islam MI, Nam KW, Cho HD, et al. Thymoquinone (TQ) inhibits the replication of intracellular Mycobacterium tuberculosis in macrophages and modulates nitric oxide production. BMC Complement Altern Med 2017; 17:279.
57
58. Dehyab AS, Bakar MFA, Al-Omar MK, Sabran SF. A review of medicinal plant of Middle East and North Africa (MENA) region as source in tuberculosis drug discovery. Saudi J Biol Sci 2020: 27:2457-2478.
58
59. Randhawa MA. In vitro antituberculous activity of thymoquinone, an active principle of Nigella sativa. J Ayub Med Coll Abbottabad 2011; 23:78-81.
59
60. Dey D, Ray R, Hazra B. Antitubercular and antibacterial activity of quinonoid natural products against multi-drug resistant clinical isolates. Phytother Res 2014; 28:1014-1021.
60
61. Jaswal A, Sinha N, Bhadauria M, Shrivastava S, Shukla S. Therapeutic potential of thymoquinone against anti-tuberculosis drugs induced liver damage. Environ Toxicol Pharmacol 2013; 36:779-786.
61
62. Umar S, Munir MT, Subhan S, Azam T, Nisa Q, Khan MI, et al. Protective and antiviral activities of Nigella sativa against avian influenza (H9N2) in turkeys. J Saudi Soci Agri Sci 2016; In press.
62
63. World Health Organization. Dengue haemorrhagic fever: diagnosis, treatment, prevention and control. Geneva 1997; 2nd edition: Available at: https://www.who.int/csr/resources/publications/dengue/Denguepublication/en/. Extracted on December 29, 2020.
63
64. Saleem HN, Batool F, Mansoor HJ, Shahzad-ul-Hussan S, Saeed M. Inhibition of dengue virus protease by eugeniin, isobiflorin, and biflorin isolated from the flower buds of syzygium aromaticum (Cloves). ACS Omega 2019; 4:1525-1533.
64
65. Ahmed AM, Al-Olayan EM, Aboul-Soud MAM, Al-Khedhairy AA. The immune enhancer, thymoquinone, and the hope of utilizing the immune system of Aedes caspius against disease agents. Afr J Biotechnol 2010; 9:3183-3195.
65
66. Sayed SME, Abdelrahman AA, Ozbak HA, Hemeg HA, Kheyami AM, Rezk N, et al. Updates in diagnosis and management of Ebola hemorrhagic fever. J Res Med Sci 2016; 21:1-27.
66
67. Uzochukwu IC, Olubiyi OO, Ezebuo FC, Obinwa IC, Ajaegbu EE, Eze PM, et al. Ending the Ebola Virus Scourge: A case for natural products. J Pharm Res 2016; 1:000105.
67
68. United Nations Development Group (UNDG) – Western and Central Africa, Socio-Economic Impact of Ebola Virus Disease in West African Countries: A call for national and regional containment, recovery and prevention, (2015) Available at: https://ideas.repec.org/p/ags/undpar/267635.html (Extracted on December 29, 2020)
68
69. Elfiky AA. Novel guanosine derivatives against Zika virus polymerase in silico. J Med Virol 2020; 92:11-16.
69
70. World Health Organization, European Region, Zika virus technical report: Interim Risk Assessment, (2016) Available at: https://reliefweb.int/report/world/zika-virus-technical-report-interim-risk-assessment-who-european-region-may-2016 (Extracted on December 29, 2020)
70
71. Cirne-Santos CC, Barros CDS, Paixão ICNP. Natural Products against the Zika Virus. Am. J Biomed Sci Res 2020; 7:001146.
71
72. Te HS, Jensen DM. Epidemiology of hepatitis B and C viruses: A global overview. Clin Liver Dis 2010; 1-21.
72
73. Jefferies M, Rauff B, Rashid H, Lam T, Rafiq S. Update on global epidemiology of viral hepatitis and preventive strategies. World J Clin Cases 2018; 6:589-599.
73
74. Barakat EMF, Wakeel LME, Hagag RS. Effects of Nigella sativa on outcome of hepatitis C in Egypt. World J Gastroenterol 2013; 19:2529-2536.
74
75. Khan MA. Antimicrobial Action of Thymoquinone, Hina Younus (Ed), Molecular and Therapeutic actions of Thymoquinone. Springer Nature Singapore Pte Ltd; 2018.p. 57-64.
75
76. Noorbakhsh MF, Hayati F, Samarghandian S, Shaterzadeh-Yazdi H, Farkhondeh T. An Overview of hepatoprotective effects of thymoquinone. Recent Pat Food Nutr Agric 2018; 9:14-22.
76
77. Abdel-Moneim A, Morsy BM, Mahmoud AM, Abo-Seif MA, Zanaty MI. Beneficial therapeutic effects of Nigella sativa and/or Zingiber officinale in HCV patients in Egypt. EXCLI J 2013; 12:943-955.
77
78. World Health Organization (WHO). World malaria report 2020: 20 years of global progress and challenges. 2020; https://www.who.int/news-room/fact-sheets/detail/malaria (Extract on January 1, 2020).
78
79. Autino B, Noris A, Russo R, Castelli F. Epidemiology of malaria in endemic areas. Mediterr J Hematol Infect Dis 2012; 4:e2012060.
79
80. Ashcroft OF, Salaudeen OF, Mohammed K, Spencer THI, Garba MK, Nataala SU, et al. Anti-malarial effect of Nigella Sativa seeds (Black seed) extract on mice infected with plasmodium bergei (NK 65). Eur J Pharm Med Res 2018; 5:131-137.
80
81. Fröhlich T, Reiter C, Saeed MEM, Hutterer C, Hahn F, Leidenberger M, et al. Synthesis of thymoquinone–artemisinin hybrids: New potent antileukemia, antiviral, and antimalarial agents. ACS Med Chem Lett 2018; 9:534-539.
81
82. Johnson-Ajinwo OR, Ullah I, Mbye H, Richardson A, Horrocks P, Li WW. The synthesis and evaluation of thymoquinone analogues as anti-ovarian cancer and antimalarial agents. Bioorg Med Chem Lett 2018; 28(7):1219-1222.
82
83. Emeka PM, Badger-Emeka LI, Eneh CM, Khan TM. Dietary supplementation of chloroquine with Nigella sativa seed and oil extracts in the treatment of malaria induced in mice with Plasmodium berghei. Pharmacogn Mag 2014; 10:S357-S362.
83
84. World Health Organization (WHO). HIV/AIDS; Key facts. 2019; https://www.who.int/news-room/fact-sheets/detail/hiv-aids. (Extract on January 1, 2020)
84
85. United Nations Programme on HIV/AIDS (UNAIDS). Global HIV & AIDS statistics-2020 fact sheet. 2020; https://www.unaids.org/en/resources/factsheet#:~:text=GLOBAL%20HIV%20STATISTICS&text=38.0%20million%20%5B31.6%20million%E2%80%9344.5,AIDS%2Drelated%20illnesses%20in%202019. (Extracted on January 1, 2021).
85
86. Chandra S, Mondal D, Agrawal KC. HIV-1 protease inhibitor induced oxidative stress suppresses glucose stimulated insulin release: protection with thymoquinone. Exp Biol Med (Maywood) 2009; 234(4):442-453.
86
87. Onifade A, Jewell A, Ajadi T, Rahamon S, Ogunrin, O. Effectiveness of a herbal remedy in six HIV patients in Nigeria. J Herb Med 2013; 3:99-103.
87
88. Onifade AA, Jewell AP, Okesina AB. Virologic and immunologic outcomes of treatment of HIV infection with herbal concoction, A-zam among clients seeking herbal remedy in Nigeria. Afr J Tradit Complement Altern Med 2011; 8:37-44.
88
89. Onifade AA, Jewell AP, Okesina AB. Seronegative conversion of an HIV positive subject treated with Nigella sativa and honey. Afr J Infect Dis 2015; 9:47-50.
89
90. Onifade AA, Jewell AP, Adedeji WA. Nigella Sativa concoction induced sustained seroreversion in HIV patient. Afr J Tradit Complement Altern Med 2013; 10:332-335.
90
91. Negi P, Rathore C, Sharma G, Singh B, Katare OP. Thymoquinone a potential therapeutic molecule from the plant Nigella sativa: Role of colloidal carriers in its effective delivery. Recent Pat Drug Deliv Formul 2018; 12:3-22.
91
92. Gupta SK, Nayak RP. Dry antibiotic pipeline: Regulatory bottlenecks and regulatory reforms. J Pharmacol Pharmacother 2014; 5:4-7.
92
93. Elmowafy M, Samy A, Raslan MA, Salama A, Said RA, Abdelaziz AE, et al. Enhancement of Bioavailability and pharmacodynamic effects of thymoquinone via nanostructured lipid carrier (NLC) formulation. AAPS PharmSciTech 2016; 17:663-672.
93
ORIGINAL_ARTICLE
Modulatory role of atorvastatin against high-fat diet and zymosan-induced activation of TLR2/NF-ƙB signaling pathway in C57BL/6 mice
Objective(s): Accumulated evidence provides a strong connection between the immune system and vascular inflammation. The innate immune system’s main sensors are toll-like receptors (TLRs). Zymosan (Zym), a fungal product, induces an inflammatory response via activating TLR2 of the immune system. Atorvastatin, a potent statin, possesses pleiotropic effects including immunomodulatory, lipid-lowering, and anti-inflammatory. Therefore, the current study aimed to evaluate the protective role of atorvastatin against a high-fat diet (HFD) and Zym-induced vascular inflammation in C57BL/6 mice via modulation of TLR2/NF-ƙB signaling pathway.Materials and Methods: In silico study was conducted to confirm the binding affinity of atorvastatin against TLR2. Under in vivo study, mice were divided into four groups: Normal control: normal standard chow-diet fed for 30 days + Zym vehicle (sterile PBS, 5 mg/ml on 8th day); HFD (30 days) + Zym (80 mg/kg, IP, on 8th day); HFD/Zym + atorvastatin vehicle (0.5% CMC, p.o., from 10th to 30th day); HFD/Zym + atorvastatin (3.6 mg/kg, p.o., from 10th to 30th day).Results: Atorvastatin treatment along with HFD and Zym inhibited vascular inflammation by suppressing the levels of aortic TLR2, cardiac NF-ƙB and decrease in serum TNF-α and IL-6. Further, there was an increase in hepatic LDLR levels, resulting in a decrease in serum LDL-C and an increase in HDL-C levels. Histopathological examination of the aorta showed a reduction in plaque accumulation with the atorvastatin-treated group as compared with HFD and Zym-treated group.Conclusion: Atorvastatin attenuates vascular inflammation mediated by HFD and Zym through suppression of TLR2, NF-ƙB, TNF-α, IL-6, and upregulation of LDLR levels.
https://ijbms.mums.ac.ir/article_18465_2410909f49933563adc83fd0731c2aed.pdf
2021-08-01
1023
1032
10.22038/ijbms.2021.55460.12409
Atorvastatin High
fat diet Inflammation Low
density lipoprotein
receptor Nuclear factor
kappa B Toll
like receptor Zymosan
Priyanka
Arya
sarojarya24@gmail.com
1
Department of Pharmacology, School of Pharmaceutical Education & Research (SPER), Jamia Hamdard (UGC approved deemed to be University, Govt. of India), New Delhi- 110062, India
AUTHOR
Sayima
Nabi
nabisaima680@gmail.com
2
Department of Pharmacology, School of Pharmaceutical Education & Research (SPER), Jamia Hamdard (UGC approved deemed to be University, Govt. of India), New Delhi- 110062, India
AUTHOR
Uma
Bhandari
uma_bora@hotmail.com
3
Department of Pharmacology, School of Pharmaceutical Education & Research (SPER), Jamia Hamdard (UGC approved deemed to be University, Govt. of India), New Delhi- 110062, India
LEAD_AUTHOR
1. Lavin Plaza B, Phinikaridou A, Andia ME, Potter M, Lorrio S, Rashid I, et al. Sustained focal vascular inflammation accelerates atherosclerosis in remote arteries. Arterioscler Thromb Vasc Biol 2020; 40: 2159-2170.
1
2. Madan M and Amar S. Toll-like receptor-2 mediates diet and/or pathogen associated atherosclerosis: Proteomic findings. PloS One 2008; 3: e3204.
2
3. Hovland A, Jonasson L, Garred P, Yndestad A, Aukrust P, Lappegård KT, et al. The complement system and toll-like receptors as integrated players in the pathophysiology of atherosclerosis. Atherosclerosis 2015; 241: 480-494.
3
4. Cole JE, Georgiou E, Monaco C. The expression and functions of toll-like receptors in atherosclerosis. Mediators Inflamm 2010; 1-18.
4
5. Gaidhu MP, Anthony NM, Patel P, Hawke TJ, Ceddia RB. Dysregulation of lipolysis and lipid metabolism in visceral and subcutaneous adipocytes by high-fat diet: Role of ATGL, HSL, and AMPK. Am J Physiol Cell Physiol 2010; 298: C961-C971.
5
6. Han Q, Yeung SC, Ip MS, Mak JC. Dysregulation of cardiac lipid parameters in high-fat high-cholesterol diet-induced rat model. Lipids Health Dis 2018; 17: 1-10.
6
7. Liu S, Zhang J, Pang Q, Song S, Miao R, Chen W, et al. The protective role of curcumin in zymosan-induced multiple organ dysfunction syndrome in mice. Shock 2016; 45: 209-219.
7
8. Malik P, Berisha SZ, Santore J, Agatisa-Boyle C, Brubaker G, Smith JD. Zymosan-mediated inflammation impairs in vivo reverse cholesterol transport. J Lipid Res 2011; 52: 951-957.
8
9. Underhill, DM, Macrophage recognition of zymosan particles. J Endotoxin Res 2003; 9: 176-180.
9
10. Sato M, Sano H, Iwaki D, Kudo K, Konishi M, Takahashi H, et al. Direct binding of Toll-like receptor 2 to zymosan, and zymosan-induced NF-κB activation and TNF-α secretion are down-regulated by lung collectin surfactant protein A. J Immunol 2003; 171: 417-425.
10
11. Monaco C, Paleolog E. Nuclear factor κB: A potential therapeutic target in atherosclerosis and thrombosis. Cardiovasc Res 2004; 61: 671-682.
11
12. Getz GS and Reardon CA. Animal models of atherosclerosis. Arterioscler Thromb Vasc Bio 2012; 32: 1104-1115.
12
13. Kumar S, Kang D-W, Rezvan A, Jo H. Accelerated atherosclerosis development in C57Bl6 mice by overexpressing AAV-mediated PCSK9 and partial carotid ligation. Lab Investig 2017; 97: 935-945.
13
14. Feingold KR, Moser AH, Shigenaga JK, Patzek SM, Grunfeld C. Inflammation stimulates the expression of PCSK9. Biochem Biophys Res Commun 2008; 374: 341-344.
14
15. Yuan Z, Liao Y, Tian G, Li H, Jia Y, Zhang H, et al. Panax notoginseng saponins inhibit Zymosan A induced atherosclerosis by suppressing integrin expression, FAK activation and NF-kappaB translocation. J Ethnopharmacol 2011; 138: 150-155.
15
16. Oesterle A, Laufs U, Liao JK. Pleiotropic effects of statins on the cardiovascular system. Circ Res 2017; 120: 229-243.
16
17. Kavalipati N, Shah J, Ramakrishan A, Vasnawala H. Pleiotropic effects of statins. Indian J Endocrinol Metab 2015; 19: 554-562.
17
18. Peng S, Xu L-W, Che X-Y, Xiao Q-Q, Pu J, Shao Q, et al. Atorvastatin inhibits inflammatory response, attenuates lipid deposition, and improves the stability of vulnerable atherosclerotic plaques by modulating autophagy. Front Pharmacol 2018; 9: 1-17.
18
19. Araújo FA, Rocha MA, Mendes JB, Andrade SP. Atorvastatin inhibits inflammatory angiogenesis in mice through down regulation of VEGF, TNF-α and TGF-β1. Biomed Pharmacother 2010; 64: 29-34.
19
20. Bruder-Nascimento T, Callera GE, Montezano AC, de Chantemele EJ, Tostes RC, Touyz RM. Atorvastatin inhibits pro-inflammatory actions of aldosterone in vascular smooth muscle cells by reducing oxidative stress. Life Sci 2019; 221: 29-34.
20
21. Koushki K, Shahbaz SK, Mashayekhi K, Sadeghi M, Zayeri ZD, Taba MY, et al. Anti-inflammatory action of statins in cardiovascular disease: The role of inflammasome and toll-like receptor pathways. Clin Rev Allergy Immunol 2021; 60: 175-199.
21
22. Satoh M, Takahashi Y, Tabuchi T, Tamada M, Takahashi K, Itoh T, et al. Circulating toll-like receptor 4-responsive microRNA panel in patients with coronary artery disease: results from prospective and randomized study of treatment with renin–angiotensin system blockade. Clin Sci 2015; 128: 483–491
22
23. Moutzouri E, Tellis CC, Rousouli K, Liberopoulos EN, Milionis HJ, Elisaf MS, et al. Effect of simvastatin or its combination with ezetimibe on Toll-like receptor expression and lipopolysaccharide–induced cytokine production in monocytes of hypercholesterolemic patients. Atherosclerosis 2012; 225: 381-387.
23
24. Földes G, von Haehling S, Okonko DO, Jankowska EA, Poole-Wilson PA, Anker SD. Fluvastatin reduces increased blood monocyte Toll-like receptor 4 expression in whole blood from patients with chronic heart failure. Inter J Cardiol 2008; 124: 80-85.
24
25. Kapelouzou A, Giaglis S, Peroulis M, Katsimpoulas M, Moustardas P, Aravanis CV, et al. Overexpression of toll-like receptors 2, 3, 4, and 8 is correlated to the vascular atherosclerotic process in the hyperlipidemic rabbit model: the effect of statin treatment. J Vasc Res 2017; 54: 156-169.
25
26. Methe H, Kim JO, Kofler S, Nabauer M, Weis M. Statins decrease Toll-like receptor 4 expression and downstream signaling in human CD14+ monocytes. Arterioscler Thromb Vasc Biol 2005; 25: 1439-1445.
26
27. Sasidharan SR, Joseph JA, Anandakumar S, Venkatesan V, Ariyattu Madhavan CN, Agarwal A. An experimental approach for selecting appropriate rodent diets for research studies on metabolic disorders. Biomed Res 2013; 2013;1-9.
27
28. Kang JY, Nan X, Jin MS, Youn SJ, Ryu YH, Mah S, et al. Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 2009; 31: 873-884.
28
29. Kühnast S, van der Hoorn JW, Pieterman EJ, van den Hoek AM, Sasiela WJ, Gusarova V, et al. Alirocumab inhibits atherosclerosis, improves the plaque morphology, and enhances the effects of a statin. J Lipid Res 2014; 55: 2103-2112.
29
30. Bhandari U, Kumar V, Khanna N, Panda BP. The effect of high-fat diet-induced obesity on cardiovascular toxicity in Wistar albino rats. Hum Exp Toxicol 2011; 30: 1313-1321.
30
31. Demacker PN, Hijmans AG, Vos-Janssen HE, Van’t Laar A, Jansen AP. A study of the use of polyethylene glycol in estimating cholesterol in high-density lipoprotein. Clin Chem 1980; 26: 1775-1779.
31
32. Foster LB and Dunn RT. Stable reagents for determination of serum triglycerides by a colorimetric Hantzsch condensation method. Clin Chem 1973; 19: 338-340.
32
33. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18: 499-502.
33
34. Kazemi T, Hajihosseini M, Moossavi M, Hemmati M, Ziaee M. Cardiovascular risk factors and Atherogenic indices in an Iranian population: Birjand east of Iran. Clin Med Insights Cardiol 2018; 12: 1-6.
34
35. Boehmer ED, Meehan MJ, Cutro BT, Kovacs EJ. Aging negatively skews macrophage TLR2-and TLR4-mediated pro-inflammatory responses without affecting the IL-2-stimulated pathway. Mech Ageing Dev 2005; 12: 1305-1313.
35
36. Pushpan CK, Shalini V, Sindhu G, Rathnam P, Jayalekshmy A, Helen A. Attenuation of atherosclerotic complications by modulating inflammatory responses in hypercholesterolemic rats with dietary Njavara rice bran oil. Biomed Pharmacother 2016; 83: 1387-1397.
36
37. May K, Kraemer F, Chen J, Cooper A. ELISA measurement of LDL receptors. J lipid Res 1990; 31: 1683-1691.
37
38. Naiki Y, Sorrentino R, Wong MH, Michelsen KS, Shimada K, Chen S, et al. TLR/MyD88 and liver X receptor α signaling pathways reciprocally control Chlamydia pneumoniae-induced acceleration of atherosclerosis. J Immunol 2008; 181: 7176-7185.
38
39. Nguyen DH, Zhou T, Shu J, Mao J. Quantifying chromogen intensity in immunohistochemistry via reciprocal intensity. Cancer InCytes 2013; 2: 1-4.
39
40. Bhat OM, Kumar PU, Giridharan NV, Kaul D, Kumar MM, Dhawan V. Interleukin-18- induced atherosclerosis involves CD36 and NF-κB crosstalk in Apo E−/− mice. J Cardiol 2015; 66: 28-35.
40
41. Kajava AV, Vasselon T. A network of hydrogen bonds on the surface of TLR2 controls ligand positioning and cell signaling. J Biol Chem 2010; 285: 6227-6234.
41
42. Balasubramanian PK, Kim J, Son K, Durai P, Kim Y. 3, 6‐Dihydroxyflavone: A Potent Inhibitor with Anti‐Inflammatory Activity Targeting Toll‐like Receptor 2. Bull Korean Chem Soc 2019; 40: 51-55.
42
43. Koymans KJ, Feitsma LJ, Bisschop A, Huizinga EG, van Strijp JA, de Haas CJ, et al. Molecular basis determining species specificity for TLR2 inhibition by staphylococcal superantigen-like protein 3 (SSL3). Vet Res 2018; 49: 1-5.
43
44. Zhang YG, Zhang HG, Zhang GY, Fan JS, Li XH, Liu YH, et al. Panax notoginseng saponins attenuate atherosclerosis in rats by regulating the blood lipid profile and an anti‐inflammatory action. Clin Exp Pharmacol Physiol 2008; 35: 1238-1244.
44
45. Shen P, Li W, Wang Y, He X, He L. Binding mode of chitin and TLR2 via molecular docking and dynamics simulation. Mol Simulat 2016; 42: 936-941.
45
46. Mullick AE, Tobias PS, Curtiss LK. Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest 2005; 115: 3149-3156.
46
47. Olejarz W, Łacheta D, Głuszko A, Migacz E, Kukwa W, Szczepański MJ, et al. RAGE and TLRs as key targets for antiatherosclerotic therapy. BioMed Res Int 2018; 2018:1-10.
47
48. Curtiss LK, Tobias PS. Emerging role of Toll-like receptors in atherosclerosis. J lipid Res 2009; 50(Supplement): S340-S345.
48
49. Schoneveld AH, Hoefer I, Sluijter JP, Laman JD, de Kleijn DP, Pasterkamp G. Atherosclerotic lesion development and Toll like receptor 2 and 4 responsiveness. Atherosclerosis 2008; 197: 95-104.
49
50. Higashimori M, Tatro JB, Moore KJ, Mendelsohn ME, Galper JB, Beasley D. Role of toll- like receptor 4 in intimal foam cell accumulation in apolipoprotein E–deficient mice. Arterioscler Thromb Vasc Biol 2011; 31: 50-57.
50
51. Liu T, Zhang L, Joo D, Sun S-C. NF-κB signaling in inflammation. Signal Transduct and Target Ther 2017; 2: 1-9.
51
52. Baker RG, Hayden MS, Ghosh S. NF-κB, inflammation, and metabolic disease. Cell Metab 2011; 13: 11-22.
52
53. Sahar S, Dwarakanath RS, Reddy MA, Lanting L, Todorov I, Natarajan R. Angiotensin II enhances interleukin-18 mediated inflammatory gene expression in vascular smooth muscle cells: a novel cross-talk in the pathogenesis of atherosclerosis. Circ Res 2005; 96: 1064-1071.
53
54. Bhaskar S, Sudhakaran PR and Helen A. Quercetin attenuates atherosclerotic inflammation and adhesion molecule expression by modulating TLR-NF-κB signaling pathway. Cell Immunol 2016; 310: 131-140.
54
55. Han F, Xiao QQ, Peng S, Che XY, Jiang LS, Shao Q, et al. Atorvastatin ameliorates LPS‐induced inflammatory response by autophagy via AKT/mTOR signaling pathway. J Cell Biochem 2018; 119: 1604-1615.
55
56. Pun NT, Subedi A, Kim MJ, Park P-H. Globular adiponectin causes tolerance to LPS-induced TNF-α expression via autophagy induction in RAW 264.7 macrophages: involvement of SIRT1/FoxO3A axis. PLoS One 2015; 10: e0124636.
56
57. Catapano AL, Pirillo A, Norata GD. Vascular inflammation and low‐density lipoproteins: Is cholesterol the link? A lesson from the clinical trials. Br J Pharmacol 2017; 174: 3973-3985.
57
58. Ruan XZ, Moorhead JF, Tao JL, Ma KL, Wheeler DC, Powis SH, et al. Mechanisms of dysregulation of low-density lipoprotein receptor expression in vascular smooth muscle cells by inflammatory cytokines. Arterioscler Thromb Vasc Biol 2006; 26: 1150-1155.
58
59. Zhang Y, Ma KL, Ruan XZ, Liu BC. Dysregulation of the low-density lipoprotein receptor pathway is involved in lipid disorder-mediated organ injury. Int J Biol Sci 2016; 12: 569-579.
59
ORIGINAL_ARTICLE
MKK4 variants rs3826392 and rs3809728 are associated with susceptibility and clinicopathological features in colorectal cancer patients
Objective(s): The mitogen-activated protein kinase kinase 4 (MKK4) plays a key role in several processes like inflammation, apoptosis, and tumorigenesis. Several authors have proposed that genetic variations in these genes may alter their expression with subsequent cancer risk. This study aimed to examine the possible association of MKK4 rs3826392 and rs3809728 variants in Mexican patients with colorectal cancer (CRC). These variants were also compared with clinical features as sex, age, TNM stage, and tumor location.Materials and Methods: The study included genomic DNA from 218 control subjects and 250 patients. Genotyping of the MKK4 variants was performed using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) procedure. Results: Individuals with A/T and T/T genotypes for the rs3809728 (-1044 A>T) variant showed a significantly increased risk for CRC (P=0.012 and 0.007, respectively); while individuals with the G/G genotype for the rs3826392 (-1304 T>G) variant showed a decreased risk for CRC (P=0.012). Genotypes of the MKK4 rs3809728 variant were also significantly related to colon localization and advanced TNM stage in CRC patients. T-T haplotype (rs3826392 and rs3809728) of the MKK4 gene was associated with risk in patients with CRC.Conclusion: The rs3826392 variant in the MKK4 gene could be a cancer protective factor, while the rs3809728 variant could be a risk factor. These variants play a significant role in CRC risk.
https://ijbms.mums.ac.ir/article_18466_c0e4a052275af6639aa289130d350391.pdf
2021-08-01
1033
1040
10.22038/ijbms.2021.56874.12690
Colorectal cancer
Haplotypes
MKK4
Susceptibility
Variants
Kimberly
Martínez-Casillas
kimberlycemartinezcasillas@gmail.com
1
División de Medicina Molecular, Centro de Investigación Biomédica de Occidente, Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, México
AUTHOR
Anilú Margarita
Saucedo-Sariñana
saucedo.anilu@gmail.com
2
División de Medicina Molecular, Centro de Investigación Biomédica de Occidente, Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, México
AUTHOR
Patricio
Barros-Núñez
pbarros_gdl@gmail.com
3
Unidad de Investigación Seguimiento Enfermedades Metabólicas, Unidad Médica de Alta Especialidad Pediatría, Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco. México
AUTHOR
Martha Patricia
Gallegos Arreola
marthapatriciagallegos08@yahoo.com.mx
4
División de Genética, Centro de Investigación Biomédica de Occidente, Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, México
AUTHOR
Tomas Daniel
Pineda Razo
tmspnd@gmail.com
5
Servicio de Oncología Médica, Hospital de Especialidades, Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, México
AUTHOR
María Eugenia
Marín-Contreras
meugeniamarinc@yahoo.com
6
Servicio de Gastroenterología, Hospital de Especialidades, Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, México
AUTHOR
Silvia Esperanza
Flores-Martínez
sefloresm@yahoo.com
7
División de Medicina Molecular, Centro de Investigación Biomédica de Occidente, Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, México
AUTHOR
Mónica Alejandra
Rosales-Reynoso
mareynoso77@yahoo.com.mx
8
División de Medicina Molecular, Centro de Investigación Biomédica de Occidente, Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, México
LEAD_AUTHOR
1. Globocan. Colorectal cancer. 2020. URL: https://gco.iarc.fr/today/data/factsheets/cancers/10_8_9-Colorectum-factsheet.pdf [Accesed: April 15, 2021].
1
2. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin 2020; 70: 7–30.
2
3. Globocan. Mexico. 2020. URL: http://gco.iarc.fr/today/data/factsheets/populations/484-mexico-fact-sheets.pdf [Accesed: April 15, 2021].
3
4. Carr PR, Weigl K, Edelmann D, Jansen L, Chang-Claude J, Brenner H, et al. Estimation of absolute risk of colorectal cancer based on healthy lifestyle, genetic risk, and colonoscopy status in a population-based study. Gastroenterology 2020; 159: 129-138.
4
5. Ocvirk S, Wilson AS, Appolonia CN, Thomas TK, O’Keefe SJD. Fiber, fat, and colorectal cancer: New insight into modifiable dietary risk factors. Curr Gastroenterol Rep 2019; 21: 62.
5
6. Cho YA, Lee J, Oh JH, Chang HJ, Sohn DK, Shin A, et al. Genetic risk score, combined lifestyle factors and risk of colorectal cancer. Cancer Res Treat 2019; 51: 1033–1040.
6
7. Moghaddam AA, Woodward M, Huxley R. Obesity and risk of colorectal cancer: a meta-analysis of 31 studies with 70,000 events. Cancer Epidemiol biomarkers Prev 2007;16:2533-2547.
7
8. Tsong WH, Koh WP, Yuan JM, Wang R, Sun CL, Yu MC. Cigarettes and alcohol in relation to colorectal cancer: the Singapore Chinese Health Study. Br J Cancer 2007; 96: 821–827.
8
9. Thanikachalam K, Khan G. Colorectal cancer and nutrition. Nutrients 2019; 11: 164.
9
10. Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol 2019; 16: 713–732.
10
11. Song M, Chan AT, Sun J. Influence of the gut microbiome, diet, and environment on risk of colorectal cancer. Gastroenterology 2020; 158: 322–340.
11
12. Shin A, Li H, Shu X-O, Yang G, Gao Y-T, Zheng W. Dietary intake of calcium, fiber and other micronutrients in relation to colorectal cancer risk: Results from the Shanghai Women’s Health Study. Int J cancer 2006; 119: 2938–2942.
12
13. Dhillon AS, Hagan S, Rath O, Kolch W. MAP kinase signalling pathways in cancer. Oncogene 2007; 26: 3279–3290.
13
14. Guo Y-J, Pan W-W, Liu S-B, Shen Z-F, Xu Y, Hu L-L. ERK/MAPK signalling pathway and tumorigenesis. Exp Ther Med 2020; 19: 1997–2007.
14
15. English J, Pearson G, Wilsbacher J, Swantek J, Karandikar M, Xu S, et al. New insights into the control of MAP kinase pathways. Exp Cell Res 1999; 253: 255–270.
15
16. Dogan M, Guresci S, Acikgoz Y, Ergun Y, Kos FT, Bozdogan O, et al. Is there any correlation among MKK4 (mitogen-activated protein kinase kinase 4) expression, clinicopathological features, and KRAS/NRAS mutation in colorectal cancer. Expert Rev Mol Diagn 2020; 20: 851–859.
16
17. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature 2001; 410: 37–40.
17
18. Cunningham SC, Gallmeier E, Hucl T, Dezentje DA, Calhoun ES, Falco G, et al. Targeted deletion of MKK4 in cancer cells: a detrimental phenotype manifests as decreased experimental metastasis and suggests a counterweight to the evolution of tumor-suppressor loss. Cancer Res 2006; 66: 5560–5564.
18
19. Diao D, Wang L, Zhang J-X, Chen D, Liu H, Wei Y, et al. Mitogen/extracellular signal-regulated kinase kinase-5 promoter region polymorphisms affect the risk of sporadic colorectal cancer in a southern Chinese population. DNA Cell Biol 2012; 31: 342–349.
19
20. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995; 270: 1326–1331.
20
21. Cuenda A. Mitogen-activated protein kinase kinase 4 (MKK4). Int J Biochem Cell Biol 2000; 32: 581–587.
21
22. Sutherland CL, Heath AW, Pelech SL, Young PR, Gold MR. Differential activation of the ERK, JNK, and p38 mitogen-activated protein kinases by CD40 and the B cell antigen receptor. J Immunol 1996; 157: 3381–3390.
22
23. Teng DH, Perry WL 3rd, Hogan JK, Baumgard M, Bell R, Berry S, et al. Human mitogen-activated protein kinase kinase 4 as a candidate tumor suppressor. Cancer Res 1997; 57: 4177–4182.
23
24. Liu B, Chen D, Yang L, Li Y, Ling X, Liu L, et al. A functional variant (-1304T>G) in the MKK4 promoter contributes to a decreased risk of lung cancer by increasing the promoter activity. Carcinogenesis 2010; 31: 1405–1411.
24
25. Yoshida BA, Dubauskas Z, Chekmareva MA, Christiano TR, Stadler WM, Rinker-Schaeffer CW. Mitogen-activated protein kinase kinase 4/stress-activated protein/Erk kinase 1 (MKK4/SEK1), a prostate cancer metastasis suppressor gene encoded by human chromosome 17. Cancer Res 1999; 59: 5483–5487.
25
26. Yamada SD, Hickson JA, Hrobowski Y, Vander Griend DJ, Benson D, Montag A, et al. Mitogen-activated protein kinase kinase 4 (MKK4) acts as a metastasis suppressor gene in human ovarian carcinoma. Cancer Res 2002; 62: 6717–6723.
26
27. Nakayama K, Nakayama N, Davidson B, Katabuchi H, Kurman RJ, Velculescu VE, et al. Homozygous deletion of MKK4 in ovarian serous carcinoma. Cancer Biol Ther 2006; 5: 630–634.
27
28. Wei Y, Wang L, Lan P, Zhao H, Pan Z, Huang J, et al. The association between -1304T>G polymorphism in the promoter of MKK4 gene and the risk of sporadic colorectal cancer in southern Chinese population. Int J cancer 2009; 125: 1876–1883.
28
29. Burotto M, Chiou VL, Lee J-M, Kohn EC. The MAPK pathway across different malignancies: a new perspective. Cancer 2014; 120: 3446–3456.
29
30. Zhang Y, Neo SY, Wang X, Han J, Lin SC. Axin forms a complex with MEKK1 and activates c-Jun NH(2)-terminal kinase/stress-activated protein kinase through domains distinct from Wnt signaling. J Biol Chem 1999; 274: 35247–35254.
30
31. Spillman MA, Lacy J, Murphy SK, Whitaker RS, Grace L, Teaberry V, et al. Regulation of the metastasis suppressor gene MKK4 in ovarian cancer. Gynecol Oncol 2007; 105: 312–320.
31
32. Robinson VL, Shalhav O, Otto K, Kawai T, Gorospe M, Rinker-Schaeffer CW. Mitogen-activated protein kinase kinase 4/c-Jun NH2-terminal kinase kinase 1 protein expression is subject to translational regulation in prostate cancer cell lines. Mol Cancer Res 2008; 6: 501–508.
32
33. Bai R, Yuan C, Zhou F, Ni L, Gong Y, Xie C. Evaluation of the association between the -1304T>G polymorphism in the promoter of the MKK4 gene and the risk of colorectal cancer: a PRISMA-compliant meta-analysis. Ann Transl Med 2019; 7: 144.
33
34. Jiang L, Zhou P, Sun A, Zheng J, Liu B, You Y, et al. Functional variant (-1304T>G) in the MKK4 promoter is associated with decreased risk of acute myeloid leukemia in a southern Chinese population. Cancer Sci 2011; 102: 1462–1468.
34
35. Hu M, Zheng J, Zhang L, Jiang L, You Y, Jiang M, et al. The association between -1304T>G polymorphism in the promoter of mitogen-activated protein kinase kinase 4 gene and the risk of cervical cancer in Chinese population. DNA Cell Biol 2012; 31: 1167–1173.
35
36. Iqbal B, Masood A, Lone MM, Lone AR, Dar NA. Polymorphism of metastasis suppressor genes MKK4 and NME1 in Kashmiri patients with breast cancer. Breast J 2016; 22: 673–677.
36
37. Zheng J, Liu B, Zhang L, Jiang L, Huang B, You Y, et al. The protective role of polymorphism MKK4-1304 T>G in nasopharyngeal carcinoma is modulated by Epstein-Barr virus’ infection status. Int J cancer 2012; 130: 1981–1990.
37
38. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988; 16: 1215.
38
39. Siegel R, Desantis C, Jemal A. Colorectal cancer statistics, 2014. CA Cancer J Clin 2014; 64: 104–117.
39
40. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J cancer 2015; 136: 359-386.
40
41. Alberts, SR Citrin, D Schwartz, D Rodriguez M. Colon, Rectal, and Anal Cancers. Cancer Management. 2016. URL:
41
https://www.cancernetwork.com/cancer-management/colon-rectal-and-anal-cancers [Accesed: April 15, 2021].
42
42. Su GH, Hilgers W, Shekher MC, Tang DJ, Yeo CJ, Hruban RH, et al. Alterations in pancreatic, biliary, and breast carcinomas support MKK4 as a genetically targeted tumor suppressor gene. Cancer Res 1998; 58: 2339–2342.
43
43. Wang L, Pan Y, Dai J Le. Evidence of MKK4 pro-oncogenic activity in breast and pancreatic tumors. Oncogene 2004; 23: 5978–5985.
44
44. Cunningham SC, Kamangar F, Kim MP, Hammoud S, Haque R, Iacobuzio-Donahue C, et al. MKK4 status predicts survival after resection of gastric adenocarcinoma. Arch Surg 2006; 141: 1095–1099.
45
45. Gupta A, Wang Y, Browne C, Kim S, Case T, Paul M, et al. Neuroendocrine differentiation in the 12T-10 transgenic prostate mouse model mimics endocrine differentiation of pancreatic beta cells. Prostate 2008; 68: 50–60.
46
46. Riemenschneider MJ, Koy TH, Reifenberger G. Expression of oligodendrocyte lineage genes in oligodendroglial and astrocytic gliomas. Acta Neuropathol 2004; 107: 277–282.
47
47. Seike M, Gemma A, Hosoya Y, Hosomi Y, Okano T, Kurimoto F, et al. The promoter region of the human BUBR1 gene and its expression analysis in lung cancer. Lung Cancer 2002; 38: 229–234.
48
48. Smith R, Owen LA, Trem DJ, Wong JS, Whangbo JS, Golub TR, et al. Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing’s sarcoma. Cancer Cell 2006; 9: 405–416.
49
49. Heald RJ, Moran BJ. Embryology and anatomy of the rectum. Semin Surg Oncol 1998; 15: 66–71.
50
50. Iacopetta B. Are there two sides to colorectal cancer? Int J cancer 2002; 101: 403–408.
51
51. Li F, Lai M. Colorectal cancer, one entity or three. J Zhejiang Univ Sci B 2009; 10: 219–229.
52
52. Sanz-Pamplona R, Cordero D, Berenguer A, Lejbkowicz F, Rennert H, Salazar R, et al. Gene expression differences between colon and rectum tumors. Clin cancer Res an Off J Am Assoc Cancer Res 2011; 17: 7303–7312.
53
53. Slattery ML, Wolff E, Hoffman MD, Pellatt DF, Milash B, Wolff RK. MicroRNAs and colon and rectal cancer: differential expression by tumor location and subtype. Genes Chromosomes Cancer 2011; 50: 196–206.
54
54. Paschke S, Jafarov S, Staib L, Kreuser ED, Maulbecker Armstrong C, Roitman M, et al. Are colon and rectal cancer two different tumor entities? A proposal to abandon the term colorectal cancer. Int J Mol Sci 2018; 19:2577.
55
55. Tamas K, Walenkamp AME, de Vries EGE, van Vugt MATM, Beets Tan RG, van Etten B, et al. Rectal and colon cancer: Not just a different anatomic site. Cancer Treat Rev 2015; 41: 671–679.
56
56. Rosales-Reynoso MA, Zepeda-López P, Saucedo-Sariñana AM, Pineda-Razo TD, Barros-Núñez P, Gallegos-Arreola MP, et al. GSK3β polymorphisms are associated with tumor site and TNM stage in colorectal cancer. Arch Iran Med 2019; 22: 453–460.
57
57. Rosales-Reynoso MA, Saucedo-Sariñana AM, Contreras-Díaz KB, Márquez-González RM, Barros-Núñez P, Pineda-Razo TD, et al. Genetic polymorphisms in APC, DVL2, and AXIN1 are associated with susceptibility, advanced TNM stage or tumor location in colorectal cancer. Tohoku J Exp Med 2019; 249: 173–183.
58
ORIGINAL_ARTICLE
Protective effects of selenium on acrylamide-induced neurotoxicity and hepatotoxicity in rats
Objective(s): Acrylamide (ACR), has wide uses in different industries. ACR induced several toxicities including neurotoxicity and hepatotoxicity. The probable protective effects of selenium on ACR-induced neurotoxicity and hepatotoxicity in rats were evaluated.Materials and Methods: Male Wistar rats were studied for 11 days in 8 groups: 1. Control, 2. ACR (50 mg/kg, IP), 3-5. ACR+ selenium (0.2, 0.4, 0.6 mg/kg, IP), 6. ACR+ the most effective dose of selenium (0.6 mg/kg, IP) three days after ACR administration, 7. ACR+ vitamin E (200 mg/kg IP, every other day) 8. Selenium (0.6 mg/kg IP). Finally, behavioral tests were done. The levels of malondialdehyde (MDA), glutathione (GSH), Bcl-2, Bax and caspase 3 proteins in liver and cerebral cortex tissues were measured. Also, the amount of albumin, total protein, alanine transaminase (ALT) and aspartate transaminase (AST) enzymes were determined in serum. Results: ACR caused the severe motor impairment, increased MDA level and decreased GSH content, enhanced Bax/Bcl-2 ratio and caspase 3 proteins in brain and liver tissues. Besides, the level of AST was elevated while the total serum protein and albumin levels were decreased. Administration of selenium (0.6 mg/kg) (from the first day of the experiment and the third day) significantly recovered locomotor disorders, increased GSH content, and reduced MDA level. Also, selenium decreased Bax/Bcl-2 ratio and caspase 3 levels in brain and liver tissues.Conclusion: The oxidative stress and apoptosis pathways have important roles in neurotoxicity and hepatotoxicity of ACR. Selenium significantly reduced ACR-induced toxicity through inhibition of oxidative stress and apoptosis.
https://ijbms.mums.ac.ir/article_18460_8e6ad296f1c4fdadb1b86d10c0bd571e.pdf
2021-08-01
1041
1049
10.22038/ijbms.2021.55009.12331
Acrylamide
Apoptosis
Hepatotoxicity
Neurotoxicity
Oxidative stress
Selenium
Mahboobeh
Ghasemzadeh Rahbardar
ghasemzadeh_mahboobeh@yahoo.com
1
Pharmaceutical Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Hadi
Cheraghi Farmed
sarveazad68@yahoo.com
2
School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Hossein
Hosseinzadeh
hosseinzadeh@mums.ac.ir
3
Pharmaceutical Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Soghra
Mehri
mehris@mums.ac.ir
4
Pharmaceutical Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran
LEAD_AUTHOR
1. Tyl RW, Friedman MA. Effects of acrylamide on rodent reproductive performance. Reprod Toxicol 2003; 17:1-13.
1
2. Tareke E, Rydberg P, Karlsson P, Eriksson S, Törnqvist M. Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J Agric Food Chem 2002; 50:4998-5006.
2
3. Kunnel SG, Subramanya S, Satapathy P, Sahoo I, Zameer F. Acrylamide induced toxicity and the propensity of phytochemicals in amelioration: a review. Cent Nerv Syst Agents Med Chem 2019; 19:100-113.
3
4. Kadawathagedara M, Botton J, de Lauzon-Guillain B, Meltzer HM, Alexander J, Brantsaeter AL, et al. Dietary acrylamide intake during pregnancy and postnatal growth and obesity: Results from the Norwegian Mother and Child Cohort Study (MoBa). Environ Int 2018; 113:325-334.
4
5. Hong Y, Nan B, Wu X, Yan H, Yuan Y. Allicin alleviates acrylamide-induced oxidative stress in BRL-3A cells. Life Sci 2019; 231:116550.
5
6. Tabeshpour J, Mehri S, Abnous K, Hosseinzadeh H. Neuroprotective effects of thymoquinone in acrylamide-induced peripheral nervous system toxicity through MAPKinase and apoptosis pathways in rat. Neurochem Res 2019; 44:1101-1112.
6
7. Tabeshpour J, Mehri S, Abnous K, Hosseinzadeh H. Role of oxidative stress, MAPKinase and apoptosis pathways in the protective effects of thymoquinone against acrylamide-induced central nervous system toxicity in rat. Neurochem Res 2020; 45:254-267.
7
8. Yousef M, El-Demerdash F. Acrylamide-induced oxidative stress and biochemical perturbations in rats. Toxicology 2006; 219:133-141.
8
9. Hogervorst JG, Baars B-J, Schouten LJ, Konings EJ, Goldbohm RA, van den Brandt PA. The carcinogenicity of dietary acrylamide intake: a comparative discussion of epidemiological and experimental animal research. Crit Rev Toxicol 2010; 40:485-512.
9
10. Erkekoglu P, Baydar T. Acrylamide neurotoxicity. Nutr Neurosci 2014; 17:49-57.
10
11. Abdel-Daim MM, Abd Eldaim MA, Hassan AG. Trigonella foenum-graecum ameliorates acrylamide-induced toxicity in rats: Roles of oxidative stress, proinflammatory cytokines, and DNA damage. Biochem Cell Biol 2015; 93:192-198.
11
12. Abdel-Daim MM, Abd Eldaim MA, Hassan AG. Trigonella foenum-graecum ameliorates acrylamide-induced toxicity in rats: Roles of oxidative stress, proinflammatory cytokines, and DNA damage. Biochem Cell Biol 2015; 93:192-198.
12
13. Bracht A, Silveira SS, Castro-Ghizoni CV, Sá-Nakanishi AB, Oliveira MRN, Bersani-Amado CA, et al. Oxidative changes in the blood and serum albumin differentiate rats with monoarthritis and polyarthritis. Springerplus 2016; 5:36-49.
13
14. Chen J-H, Yang C-H, Wang Y-S, Lee J-G, Cheng C-H, Chou C-C. Acrylamide-induced mitochondria collapse and apoptosis in human astrocytoma cells. Food Chem Toxicol 2013; 51:446-452.
14
15. Seydi E, Rajabi M, Salimi A, Pourahmad J. Involvement of mitochondrial-mediated caspase 3 activation and lysosomal labilization in acrylamide-induced liver toxicity. Toxicol Environ Chem 2015; 97:563-575.
15
16. Ghorbel I, Elwej A, Chaabene M, Boudawara O, Marrakchi R, Jamoussi K, et al. Effects of acrylamide graded doses on metallothioneins I and II induction and DNA fragmentation: Bochemical and histomorphological changes in the liver of adult rats. Toxicol Ind Health 2017; 33:611-622.
16
17. Yerlikaya FH, Yener Y. The dietary acrylamide intake adversely affects the serum trace element status. Biol Trace Elem Res 2013; 152:75-81.
17
18. Ikemoto T, Kunito T, Tanaka H, Baba N, Miyazaki N, Tanabe S. Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver. Arch Environ Contam Toxicol 2004; 47:402-413.
18
19. Rayman MP. The importance of selenium to human health. The lancet 2000; 356:233-241.
19
20. Pillai R, Uyehara‐Lock JH, Bellinger FP. Selenium and selenoprotein function in brain disorders. IUBMB life 2014; 66:229-239.
20
21. Ansari MA, Ahmad AS, Ahmad M, Salim S, Yousuf S, Ishrat T, et al. Selenium protects cerebral ischemia in rat brain mitochondria. Biol Trace Elem Res 2004; 101:73-86.
21
22. Zafar KS, Siddiqui A, Sayeed I, Ahmad M, Salim S, Islam F. Dose‐dependent protective effect of selenium in rat model of Parkinson’s disease: neurobehavioral and neurochemical evidences. J Neurochem 2003; 84:438-446.
22
23. Look M, Rockstroh J, Rao G, Kreuzer K, Barton S, Lemoch H, et al. Serum selenium, plasma glutathione (GSH) and erythrocyte glutathione peroxidase (GSH-Px)-levels in asymptomatic versus symptomatic human immunodeficiency virus-1 (HIV-1)-infection. Eur J Clin Nutr 1997; 51:266-272.
23
24. Venardos K, Harrison G, Headrick J, Perkins A. Effects of dietary selenium on glutathione peroxidase and thioredoxin reductase activity and recovery from cardiac ischemia–reperfusion. J Trace Elem Med Biol 2004; 18:81-88.
24
25. Gu X, Manautou JE. Molecular mechanisms underlying chemical liver injury. Expert Rev Mol Med 2012; 14:e4.
25
26. Ansar S, Alshehri SM, Abudawood M, Hamed SS, Ahamad T. Anti-oxidant and hepatoprotective role of selenium against silver nanoparticles. Int J Nanomedicine 2017; 12:7789-7797.
26
27. Wang N, Tan H-Y, Li S, Xu Y, Guo W, Feng Y. Supplementation of micronutrient selenium in metabolic diseases: Its role as an anti-oxidant. Oxid Med Cell Longev 2017; 2017.
27
28. Shidfar F, Faghihi A, Amiri HL, Mousavi SN. Regression of nonalcoholic fatty liver disease with zinc and selenium co-supplementation after disease progression in rats. Iran J Basic Med Sci 2018; 43:26-31.
28
29. Humayun Fard H, Hosseini SA, Azarbayjani MA, Nikbakht M. Antiapoptotic effects of continuous training and selenium consumption on the liver tissue of cadmium-exposed rats. Middle East j rehabil 2019;6; e91278.
29
30. Dominiak A, Wilkaniec A, Adamczyk A. Selenium in the therapy of neurological diseases. Where is it going? Curr Neuropharmacol 2016; 14:282-299.
30
31. Erbil G, Ozbal S, Sonmez U, Pekcetin C, Tugyan K, Bagriyanik A, et al. Neuroprotective effects of selenium and Ginkgo biloba extract (EGb761) against ischemia and reperfusion injury in rat brain. Neurosciences 2008; 13:233-238.
31
32. Cardoso BR, Roberts BR, Bush AI, Hare DJ. Selenium, selenoproteins and neurodegenerative diseases. Metallomics 2015; 7:1213-1228.
32
33. Adedara IA, Fabunmi AT, Ayenitaju FC, Atanda OE, Adebowale AA, Ajayi BO, et al. Neuroprotective mechanisms of selenium against arsenic-induced behavioral impairments in rats. NeuroToxicology 2020; 76:99-110.
33
34. LoPachin RM, Barber DS, He D, Das S. Acrylamide inhibits dopamine uptake in rat striatal synaptic vesicles. Toxicol Sci 2006; 89:224-234.
34
35. Mehri S, Abnous K, Khooei A, Mousavi SH, Shariaty VM, Hosseinzadeh H. Crocin reduced acrylamide-induced neurotoxicity in Wistar rat through inhibition of oxidative stress. Iran J Basic Med Sci 2015; 18:902-908.
35
36. Milošević MD, Paunović MG, Matić MM, Ognjanović BI, Saičić ZS. Role of selenium and vitamin C in mitigating oxidative stress induced by fenitrothion in rat liver. Biomed Pharmacother 2018; 106:232-238.
36
37. Chen K, Fang J, Peng X, Cui H, Chen J, Wang F, et al. Effect of selenium supplementation on aflatoxin B1-induced histopathological lesions and apoptosis in bursa of Fabricius in broilers. Food Chem Toxicol 2014; 74:91-97.
37
38. Zhu Y-J, Zeng T, Zhu Y-B, Yu S-F, Wang Q-S, Zhang L-P, et al. Effects of acrylamide on the nervous tissue anti-oxidant system and sciatic nerve electrophysiology in the rat. Neurochem Res 2008; 33:2310-2317.
38
39. Uchiyama M, Mihara M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978; 86:271-278.
39
40. Moron MS, Depierre JW, Mannervik B. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta Gen Subj 1979; 582:67-78.
40
41. Sirot V, Hommet F, Tard A, Leblanc J-C. Dietary acrylamide exposure of the French population: results of the second French Total Diet Study. Food Chem Toxicol 2012; 50:889-894.
41
42. Li S-x, Cui N, Zhang C-l, Zhao X-l, Yu S-f, Xie K-q. Effect of subchronic exposure to acrylamide induced on the expression of bcl-2, bax and caspase 3 in the rat nervous system. Toxicology 2006; 217:46-53.
42
43. LoPachin RM, Gavin T. Molecular mechanism of acrylamide neurotoxicity: lessons learned from organic chemistry. Environ Health Perspect 2012; 120:1650-1657.
43
44. Al-Qahtani F, Arafah M, Sharma B, Siddiqi N. Effects of alpha lipoic acid on acrylamide-induced hepatotoxicity in rats. Cell Mol Biol (Noisy-le-grand) 2017; 63:1-6.
44
45. Rizk M, Abo-El-matty D, Aly H, Abd-Alla H, Saleh S, Younis E, et al. Therapeutic activity of sour orange albedo extract and abundant flavanones loaded silica nanoparticles against acrylamide-induced hepatotoxicity. Toxicol Rep 2018; 5:929-942.
45
46. Shukla PK, Khanna VK, Ali M, Maurya R, Handa S, Srimal R. Protective effect of Acorus calamus against acrylamide induced neurotoxicity. Phytother Res 2002; 16:256-260.
46
47. Lala V, Minter D. Liver Function Tests.[Updated 2018 Jan 12]. StatPearls [Internet] Treasure Island (FL): StatPearls Publishing 2018.
47
48. Mahmood SA, Amin KA, Salih SF. Effect of acrylamide on liver and kidneys in albino wistar rats. Int J Curr Microbiol App Sci 2015; 4:434-444.
48
49. Ahn T, Bae C-S, Yun C-H. Selenium supplementation restores the decreased albumin level of peripheral blood mononuclear cells in streptozotocin-induced diabetic mice. J Vet Sci 2016:15-0611.
49
50. Hamza RZ, Al-Motaani SE, Malik N. Protective and anti-oxidant role of selenium nanoparticles and vitamin C against acrylamide induced hepatotoxicity in male mice. Int J Pharmacol 2019; 15:664-674.
50
51. Karimani A, Hosseinzadeh H, Mehri S, Jafarian AH, Kamali SA, Hooshang Mohammadpour A, et al. Histopathological and biochemical alterations in non-diabetic and diabetic rats following acrylamide treatment. Toxin Rev 2019:1-8.
51
52. Özkan-Yılmaz F, Özlüer-Hunt A, Gündüz SG, Berköz M, Yalın S. Effects of dietary selenium of organic form against lead toxicity on the anti-oxidant system in Cyprinus carpio. Fish Physiol Biochem 2014; 40:355-363.
52
53. Abdallah EA. Potential protective role of selenium on acrylamide-induced oxidative stress in rats: A biochemical, histopathological study. Egypt J Forensic Sci 2018; 18:95-113.
53
54. Mendilcioglu I, Karaveli S, Erdogan G, Simsek M, Taskin O, Ozekinci M. Apoptosis and expression of Bcl-2, Bax, p53, caspase 3, and Fas, Fas ligand in placentas complicated by preeclampsia. Clin Exp Obstet Gynecol 2011; 38:38-42.
54
55. Kekre N, Griffin C, McNulty J, Pandey S. Pancratistatin causes early activation of caspase 3 and the flipping of phosphatidyl serine followed by rapid apoptosis specifically in human lymphoma cells. Cancer Chemother Pharmacol 2005; 56:29-38.
55
56. Salvesen GS, Dixit VM. Caspase activation: the induced-proximity model. Proc Natl Acad Sci U S A 1999; 96:10964-10967.
56
57. Guo J, Cao X, Hu X, Li S, Wang J. The anti-apoptotic, anti-oxidant and anti-inflammatory effects of curcumin on acrylamide-induced neurotoxicity in rats. BMC Pharmacology and Toxicology 2020; 21:62.
57
58. Karavelioglu E, Boyaci MG, Simsek N, Sonmez MA, Koc R, Karademir M, et al. Selenium protects cerebral cells by cisplatin induced neurotoxicity. Acta Cir Bras 2015; 30:394-400.
58
59. Zhang R, Yi R, Bi Y, Xing L, Bao J, Li J. The effect of selenium on the Cd-induced apoptosis via NO-mediated mitochondrial apoptosis pathway in chicken liver. Biol Trace Elem Res 2017; 178:310-319.
59
60. Siahkoohi S, Anvari M, Akhavan Tafti M, Hosseini-sharifabad M. The effects of vitamin E on the liver integrity of mice fed with acrylamide diet. Iran J Pathol 2014; 9:89-98.
60
ORIGINAL_ARTICLE
Pretreatment with licochalcone a enhances therapeutic activity of rat bone marrow mesenchymal stem cells in animal models of colitis
Objective(s): Colitis has a high prevalence rate, limited treatment options, and needs to be solved urgently. Application of Licochacone A (LA) or rBMMSCs alone in the treatment of colitis has a certain but limited effect. This study aims to develop an LA-based strategy to improve mesenchymal stem cells’ (MSCs’) therapeutic capacity in mice DSS-induced colitis by increasing the number of MSCs migrating to the inflammation site.Materials and Methods: In vivo, we injected MSCs pretreated with LA, MSCs alone, or PBS into the tail vein of colitis mice, and assessed the colon length, disease activity index (DAI) score, body weight, HAI score, and tracked the location of MSCs at day 10. In vitro, we knocked down the CXCR4 gene by siRNA and then treated it with LA, then tested the mRNA level of CXCR4 and the migration ability of group CXCR4, CXCR4+LA, LA, and control to verify the relationship between this effect and the SDF-1-CXCR4 signaling pathway.Results: The mice that received LA- pretreated MSCs had ameliorated body weight loss, preserved colon morphology, and decreased DAI and histological activity index (HAI) compared with the MSCs group. Besides, the number of MSCs migrating to the inflammation site significantly increased in group LA+MSCs, and expression of CXCR4 significantly increased too. Furthermore, we found that LA could partly revise the decrease of the migration of MSCs and the expression of CXCR4 mRNA caused by CXCR4-siRNA.Conclusion: LA may improve the migration ability of MSCs through increasing CXCR4 expression therapy enhancing their therapeutic activity.
https://ijbms.mums.ac.ir/article_18462_1eae063340685db3b9be346da690bcc9.pdf
2021-08-01
1050
1057
10.22038/ijbms.2021.56520.12616
Colitis
CXCR4
inflamation
Licochalcone A
Mesenchymal stem cells
Meng
Chen
2018110837@stu.cqmu.edu.cn
1
Department of Endodontics, Stomatological Hospital of Chongqing Medical University, Chongqing, China
AUTHOR
Yang
Yu
yuyang@hospital.cqmu.edu.cn
2
Department of Endodontics, Stomatological Hospital of Chongqing Medical University, Chongqing, China
AUTHOR
Shiyao
Yang
2020320210@stu.cqmu.edu.cn
3
Department of Endodontics, Stomatological Hospital of Chongqing Medical University, Chongqing, China
AUTHOR
Deqin
Yang
yangdeqin@hospital.cqmu.edu.cn
4
Department of Endodontics, Stomatological Hospital of Chongqing Medical University, Chongqing, China
LEAD_AUTHOR
1. Neurath MF. Current and emerging therapeutic targets for IBD. Nat Rev Gastroenterol Hepatol 2017; 14:269-278.
1
2. Gómez-Gómez GJ, Masedo Á, Yela C, Martínez-Montiel Mdel P, Casís B. Current stage in inflammatory bowel disease: what is next? World J Gastroenterol 2015; 21:11282-11303.
2
3. Ng SC, Shi HY, Hamidi N, Underwood FE, Tang W, Benchimol EI, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 2017; 390:2769-2778.
3
4. Verstockt B, Ferrante M, Vermeire S, Van Assche G. New treatment options for inflammatory bowel diseases. J Gastroenterol 2018; 53:585-590.
4
5. He XW, He XS, Lei L, Wu XJ, Ping L. Systemic infusion of bone marrow-derived mesenchymal stem cells for treatment of experimental colitis in mice. Dig Dis Sci 2012; 57:3136-3144.
5
6. Li X, Wang Q, Ding L, Wang YX, Zhao ZD, Mao N, et al. Intercellular adhesion molecule-1 enhances the therapeutic effects of MSCs in a dextran sulfate sodium-induced colitis models by promoting MSCs homing to murine colons and spleens. Stem Cell Res Ther 2019; 10:267-278.
6
7. Zheng XB, He XW, Zhang LJ, Qin HB, Lin XT, Liu XH, et al. Bone marrow-derived CXCR4-overexpressing MSCs display increased homing to intestine and ameliorate colitis-associated tumorigenesis in mice. Gastroenterol rep 2019; 7:127-138
7
8. Ye L, Sun LX, Wu MH, Wang J, Ding X, Shi H, et al. A simple system for differentiation of functional intestinal stem cell-like cells from bone marrow mesenchymal stem cells. Mol ther Nucleic acids 2018; 13:110-120.
8
9. Yang YU, Zhao T, Yang D. Cotransfer of regulatory T cells improve the therapeutic effectiveness of mesenchymal stem cells in treating a colitis mouse model. Exp Anim 2017; 66:167-176.
9
10. Shibata S. A drug over the millennia: pharmacognosy, chemistry, and pharmacology of licorice. Yakugaku Zasshi 2000; 120:849-862.
10
11. Kang TH, Seo JH, Oh H, Yoon G, Shim JH. Licochalcone a suppresses specificity protein 1 as a novel target in human breast cancer cells. J Cell Biochem 2017; 118:4652-4663.
11
12. Mi-Ichi F, Miyadera H, Kobayashi T, Takamiya S, Waki S, Iwata S, et al. Parasite mitochondria as a target of chemotherapy: inhibitory effect of licochalcone A on the plasmodium falciparum respiratory chain. Ann N Y Acad Sci 2005; 1056:46-54.
12
13. Yue F, Hsieh TC, Guo J, Kunicki J, Lee M, Darzynkiewicz Z, et al. Licochalcone-A, a novel flavonoid isolated from licorice root causes G2 and late-G1 arrests in androgen-independent PC-3 prostate cancer cells. Biochem Biophys Res Commun 2004; 322:263-270.
13
14. Kolbe L, Immeyer J, Batzer J, Wensorra U, tom Dieck K, Mundt C, et al. Anti-inflammatory efficacy of licochalcone A: correlation of clinical potency and in vitro effects. Arch Dermatol Res 2006; 298:23-30.
14
15. Wittschier N, Faller G, Hensel A. Aqueous extracts and polysaccharides from liquorice roots inhibit adhesion of Helicobacter pylori to human gastric mucosa. J Ethnopharmacol 2009; 125:218-223.
15
16. Liu D, Huo X, Gao L, Zhang J, Ni H, Cao L. NF-κB and Nrf2 pathways contribute to the protective effect of licochalcone A on dextran sulphate sodium-induced ulcerative colitis in mice. Biomed Pharmacother 2018; 102:922-929.
16
17. Naderi-Meshkin H, Matin MM, Heirani-Tabasi A, Mirahmadi M, Irfan-Maqsood M, Edalatmanesh MA, et al. Injectable hydrogel delivery plus preconditioning of mesenchymal stem cells: exploitation of SDF-1/CXCR4 axis toward enhancing the efficacy of stem cells’ homing. Cell Biol Int 2016; 40:730-741.
17
18. Won YW, Patel AN, Bull DA. Cell surface engineering to enhance mesenchymal stem cell migration toward an SDF-1 gradient. Biomaterials 2014; 35:5627-5635.
18
19. Liu X, Duan B, Cheng Z, Jia X, Mao L, Fu H, et al. SDF-1/CXCR4 axis modulates bone marrow mesenchymal stem cell apoptosis, migration, and cytokine secretion. Protein Cell 2011; 2:845-854.
19
20. Zheng J, Li H, He L, Huang Y, Cai J, Chen L, et al. Preconditioning of umbilical cord-derived mesenchymal stem cells by rapamycin increases cell migration and ameliorates liver ischaemia/reperfusion injury in mice via the CXCR4/CXCL12 axis. Cell Prolif 2019; 52:1-14.
20
21. Fu Y, Ni J, Chen J, Ma G, Zhao M, Zhu S, et al. Dual-functionalized MSCs that express CX3CR1 and IL-25 exhibit enhanced therapeutic effects on inflammatory bowel disease. Mol Ther 2020; 28:1214-1228.
21
22. Yu S, Chen Y, Li X, Gao Z, Liu G. Chitosan nanoparticle-delivered siRNA reduces CXCR4 expression and sensitizes breast cancer cells to cisplatin. Biosci Rep 2017; 37:1-8.
22
23. Shang F, Ming L, Zhou Z, Yu Y, Sun J, Ding Y, et al. The effect of licochalcone A on cell-aggregates ECM secretion and osteogenic differentiation during bone formation in metaphyseal defects in ovariectomized rats. Biomaterials 2014; 35:2789-2797.
23
24. Zl A, Xu WA, Yu LA, Yw A, Sw A, Kx A, et al. Design, synthesis, and evaluation of pyrrolidine based CXCR4 antagonists with invivo anti-tumor metastatic activity. Eur J Med Chem 2020; 205:112537-112555.
24
25. Xiong X, Yang X, Dai H, Feng G, Zhou W. Extracellular matrix derived from human urine-derived stem cells enhances the expansion, adhesion, spreading, and differentiation of human periodontal ligament stem cells. Stem Cell Res Ther 2019; 10:396-412.
25
26. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990; 98:694-702.
26
27. Shi G, Wang G, Lu S, Li X, Zhang B, Xu X, et al. PD-L1 is required for human endometrial regenerative cells-associated attenuation of experimental colitis in mice. Am J Trans Res 2019; 11:4696-4712.
27
28. Fan H, Zhao G, Liu L, Liu F, Gong W, Liu X, et al. Pre-treatment with IL-1β enhances the efficacy of MSC transplantation in DSS-induced colitis. Cell Mol Immunol 2012; 9:473-481.
28
29. Mosna F, Sensebé L, Krampera M. Human bone marrow and adipose tissue mesenchymal stem cells: a user’s guide. Stem Cells Dev 2010; 19:1449-1470.
29
30. Kim EJ, Kim N, Cho SG. The potential use of mesenchymal stem cells in hematopoietic stem cell transplantation. Exp Mol Med 2013; 45:1-10.
30
31. Forte D, Ciciarello M, Chiara M, et al. Human cord blood-derived platelet lysate enhances the therapeutic activity of adipose-derived mesenchymal stromal cells isolated from Crohn’s disease patients in a mouse model of colitis. Stem Cell Res Ther 2015; 6:170-186.
31
32. Boyd A, Fairchild P. Approaches for immunological tolerance induction to stem cell-derived cell replacement therapies. Expert Rev Clin Immunol 2010; 6:435-448.
32
33. Kagia A, Tzetis M, Kanavakis E, Perrea D, Sfougataki I, Mertzanian A, et al. Therapeutic effects of mesenchymal stem cells derived from bone marrow, umbilical cord blood, and pluripotent stem cells in a mouse model of chemically induced inflammatory bowel disease. Inflammation 2019; 42:1730-1740.
33
34. Castelo-Branco M, Soares I, Lopes DV, Buongusto F, Martinusso CA, Jr A, et al. Intraperitoneal but not intravenous cryopreserved mesenchymal stromal cells home to the inflamed colon and ameliorate experimental colitis. PLoS One 2012; 7:1-12.
34
35. Guo W, Liu B, Yin Y, Kan X, Gong Q, Li Y, et al. Licochalcone A protects the blood-milk barrier integrity and relieves the inflammatory response in LPS-induced mastitis. Front Immunol 2019; 10:287-301.
35
36. Li M, Zhang YX, Zhang Z, Zhou XY, Zuo XL, Cong Y, et al. Endomicroscopy will track injected mesenchymal stem cells in rat colitis models. Inflamm Bowel Dis 2015; 21:2068-2077.
36
37. Dave M, Hayashi Y, Gajdos GB, Smyrk TC, Svingen PA, Kvasha SM, et al. Stem cells for murine interstitial cells of cajal suppress cellular immunity and colitis via prostaglandin E2 secretion. Gastroenterology 2015; 148:978-990.
37
38. Chen QQ, Yan L, Wang CZ, Wang WH, Shi H, Su BB, et al. Mesenchymal stem cells alleviate TNBS-induced colitis by modulating inflammatory and autoimmune responses. World J Gastroenterol 2013; 19:4702-4717.
38
39. Kang SK, Shin IS, Ko MS, Jo JY, Ra JC. Journey of mesenchymal stem cells for homing: strategies to enhance efficacy and safety of stem cell therapy. Stem Cells Int 2012; 2012:342968-342979.
39
40. Sun X, Wei L, Chen Q, Terek RM. CXCR4/SDF1 mediate hypoxia induced chondrosarcoma cell invasion through ERK signaling and increased MMP1 expression. Mol Cancer 2010; 9:17-28.
40
41. Chen Z, Chen Q, Du H, Xu L, Wan J. Mesenchymal stem cells and CXC chemokine receptor 4 overexpression improved the therapeutic effect on colitis via mucosa repair. Exp Ther Med 2018; 16:821-829.
41
42. Liu H, Liu S, Li Y, Wang X, Xue W, Ge G, et al. The role of SDF-1-CXCR4/CXCR7 axis in the therapeutic effects of hypoxia-preconditioned mesenchymal stem cells for renal ischemia/reperfusion injury. PLoS One 2012; 7:1-13.
42
43. Yang JX, Zhang N, Wang HW, Gao P, Yang QP, Wen QP. CXCR4 receptor overexpression in mesenchymal stem cells facilitates treatment of acute lung injury in rats. J Biol Chem 2015; 290:1994-2006.
43
ORIGINAL_ARTICLE
Potential secondary metabolite from Indonesian Actinobacteria (InaCC A758) against Mycobacterium tuberculosis
Objective(s): This study explored Indonesian Actinobacteria which were isolated from Curcuma zedoaria endophytic microbes and mangrove ecosystem for new antimycobacterial compounds. Materials and Methods: Antimycobacterial activity test was carried out against Mycobacterium tuberculosis H37Rv. Chemical profiling of secondary metabolite using Gas Chromatography-Mass Spectroscopy (GC-MS) and High Resolution-Mass Spectroscopy (HR-MS) was done to the ethyl acetate extract of active strain InaCC A758. Molecular taxonomy analysis based on 16S rRNA gene and biosynthetic gene clusters analysis of polyketide synthase (PKS) and non-ribosomal peptide synthetase (NRPS) from InaCC A758 have been carried out. Bioassay guided isolation of ethyl acetate extract was done, then structural elucidation of active compound was performed using UV-Vis, FT-IR, and NMR spectroscopy methods. Results: The chemical profiling using HR-MS revealed that InaCC A758 has the potential to produce new antimycobacterial compounds. The 16S rRNA gene sequencing showed that InaCC A758 has the closest homology to Streptomyces parvus strain NBRC 14599 (99.64%). In addition, InaCC A758 has NRPS gene and related to S. parvulus (92% of similarity), and also PKS gene related to PKS-type borrelidin of S. rochei and S. parvulus (74% of similarity). Two compounds with potential antimycobacterial were predicted as 1) Compound 1, similar to dimethenamid (C12H18ClNO2S; MW 275.0723), with MIC value of 100 µg/ml, and 2) Compound 2, actinomycin D (C62H86N12O16; MW 1254.6285), with MIC value of 0.78 µg/ml. Conclusion: Actinomycin D has been reported to have antimycobacterial activity, however the compound has been predicted to resemble dimethenamid had not been reported to have similar activity.
https://ijbms.mums.ac.ir/article_18406_40b8758455d5cf7df7d17c47236517ca.pdf
2021-08-01
1058
1068
10.22038/ijbms.2021.56468.12601
Actinobacteria
Dactinomycin
Dimethenamid
Mass spectrometry
Mycobacterium tuberculosis
Peptide synthases RNA
Ribosomal
16S Streptomyces
Maya
Rakhmawatie
mayapriambodo83@gmail.com
1
Doctoral Program in Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta 55281, Indonesia
AUTHOR
Tri
Wibawa
twibawa@ugm.ac.id
2
Department of Microbiology, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta 55281, Indonesia
AUTHOR
Puspita
Lisdiyanti
puspita.lisdiyanti@bioteknologi.lipi.go.id
3
Research Center for Biotechnology, Indonesian Institute of Sciences, Kabupaten Bogor, West Java 16911, Indonesia
AUTHOR
Woro
Pratiwi
woro.rukmi@ugm.ac.id
4
Department of Pharmacology and Therapy, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta 55281, Indonesia
AUTHOR
Ema
Damayanti
emadamayanti80@gmail.com
5
Research Division of Natural Product Technology, Indonesian Institute of Sciences, Yogyakarta 55861, Indonesia
AUTHOR
Mustofa
Mustofa
mustofafk@ugm.ac.id
6
Department of Pharmacology and Therapy, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta 55281, Indonesia
LEAD_AUTHOR
1. Miggiano R, Rizzi M, and Ferraris DM. Mycobacterium tuberculosis pathogenesis, infection prevention and treatment. Pathogens 2020; 9:10–13.
1
2. WHO. Global tuberculosis report 2019. Geneva; 2019.
2
3. Nahid P, Mase SR, Migliori GB, Sotgiu G, Bothamley GH, Brozek JL, et al. Treatment of drug-resistant tuberculosis. Am J Respir Crit Care Med 2019; 200:1208–1218.
3
4. Cox E and Laessig K. FDA approval of bedaquiline-The benefif-risk balance for drug-resistant tuberculosis. N Engl J Med 2014; 371:689–691.
4
5. Shen B. A new golden age of natural products drug discovery. Cell 2015; 163:1297–1300.
5
6. Lahlou M. The success of natural products in drug discovery. Pharmacol Pharm 2013; 4:17–31.
6
7. Lee H and Suh JW. Anti-tuberculosis lead molecules from natural products targeting Mycobacterium tuberculosis ClpC1. J Ind Microbiol Biotechnol 2016; 43:205–212.
7
8. Chen C, Wang J, Guo H, Hou W, Yang N, Ren B, et al. Three antimycobacterial metabolites identified from a marine-derived Streptomyces sp. MS100061. Appl Microbiol Biotechnol 2013; 97:3885–3892.
8
9. Wardani IGAAK, Andayani DGS, Sukandar U, Sukandar EY, and Adnyana IK. Study on antimicrobial activity of Nocardia sp. strain TP1 isolated from Tangkuban Perahu Soil, West Java, Indonesia. Int J Pharm Pharm Sci 2013; 5:713–716.
9
10. Muharni, Fitrya, Oktaruliza M, and Elfita. Antibacterial and anti-oxidant activity testing of pyranon derivated compound from endophytic fungi Penicillium sp of kunyit putih (Curcuma zedoaria (Berg) Roscoe). Tradit Med J 2014; 19:107–112.
10
11. Retnowati Y, Moeljopawiro S, Djohan TS, and Soetarto ES. Antimicrobial activities of actinomycete isolates from rhizospheric soils in different mangrove forests of Torosiaje, Gorontalo, Indonesia. Biodiversitas 2018; 19:2196–2203.
11
12. Jiang ZK, Tuo L, Huang DL, Osterman IA, Tyurin AP, Liu SW, et al. Diversity, novelty, and antimicrobial activity of endophytic actinobacteria from mangrove plants in Beilun Estuary National Nature Reserve of Guangxi, China. Front Microbiol 2018; 9:1–11.
12
13. Sulistiyani TR, Lisdiyanti P, and Lestari Y. Population and diversity of endophytic bacteria associated with medicinal plant Curcuma zedoaria. Microbiol Indones 2014; 8:65–72.
13
14. Baskaran R, Mohan PM, Sivakumar K, Kumar A. Antimicrobial activity and phylogenetic analysis of Streptomyces parvulus DOSMB-D105 isolated from the mangrove sediments of Andaman Islands. Acta Microbiol Immunol Hung 2016; 63:27–46.
14
15. George TK, Devadasan D, and Jisha MS. Chemotaxonomic profiling of Penicillium setosum using high-resolution mass spectrometry (LC-Q-ToF-MS). Heliyon 2019; 5:1–9.
15
16. Franzblau SG, Degroote MA, Cho SH, Andries K, Nuermberger E, Orme IM, et al. Comprehensive analysis of methods used for the evaluation of compounds against Mycobacterium tuberculosis. Tuberculosis 2012; 92:453–488.
16
17. Wang X, Huang L, Kang Z, Buchenauer H, and Gao X. Optimization of the fermentation process of actinomycete strain Hhs.015(T). J Biomed Biotechnol 2010; 2010:1–10.
17
18. Sengupta S, Pramanik A, Ghosh A, Bhattacharyya M. Antimicrobial activities of actinomycetes isolated from unexplored regions of Sundarbans mangrove ecosystem. BMC Microbiol 2015; 15:1–16.
18
19. Rakhmawatie MD, Wibawa T, Lisdiyanti P, Pratiwi WR, Mustofa. Evaluation of crystal violet decolorization assay and resazurin microplate assay for antimycobacterial screening. Heliyon 2019; 5:e02263.
19
20. Gontang EA, Gaudêncio SP, Fenical W, Jensen PR. Sequence-based analysis of secondary-metabolite biosynthesis in marine actinobacteria. Appl Environ Microbiol 2010; 76:2487–2499.
20
21. Ayuso-Sacido A, Genilloud O. New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: Detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 2005; 49:10–24.
21
22. Kumar S, Stecher G, and Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874.
22
23. Ahsan T, Chen J, Wu Y, Irfan M, Shafi J. Screening, identification, optimization of fermentation conditions, and extraction of secondary metabolites for the biocontrol of Rhizoctonia Solani AG-3. Biotechnol Biotechnol Equip 2017; 31:91–98.
23
24. Saitou N and Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425.
24
25. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution (N Y) 1985; 39:783–791.
25
26. Tamura K and Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526.
26
27. Abd-Elnaby H, Abo-Elala G, Abdel-Raouf U, Abd-Elwahab A, and Hamed M. Antibacterial and anticancer activity of marine Streptomyces parvus: Optimization and application. Biotechnol Biotechnol Equip 2016; 30:180–191.
27
28. Gonzalez-Pimentel JL, Jurado V, Laiz L, and Saiz-Jimenez C. Draft genome sequence of a granaticin-producing strain of Streptomyces parvus isolated from a Roman Tomb in the Necropolis of Carmona, Spain. Microbiol Resour Announc 2019; 8:4–5.
28
29. Schoenian I, Spiteller M, Ghaste M, Wirth R, Herz H, Spiteller D. Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc Natl Acad Sci U S A 2011; 108:1955–1960.
29
30. Hu D, Chen Y, Sun C, Jin T, Fan G, Liao Q, et al. Genome guided investigation of antibiotics producing actinomycetales strain isolated from a Macau mangrove ecosystem. Sci Rep 2018; 8:1–12.
30
31. Shetty PR, Buddana SK, Tatipamula VB, Naga YVV, and Ahmad J. Production of polypeptide antibiotic from Streptomyces parvulus and its antibacterial activity. Brazilian J Microbiol 2014; 45:303–312.
31
32. Rahman MM, Ahmad SH, Mohamed MTM, and Ab Rahman MZ. Antimicrobial compounds from leaf extracts of Jatropha curcas, Psidium guajava, and Andrographis paniculata. Sci World J 2014; 2014:1–8.
32
33. Yu M, Li Y, Banakar SP, Liu L, Shao C, Li Z, et al. New metabolites from the co-culture of marine-derived actinomycete Streptomyces rochei MB037 and fungus Rhinocladiella similis35. Front Microbiol 2019; 10:1–11.
33
34. Olano C. Hutchinson’s legacy: Keeping on polyketide biosynthesis. J Antibiot (Tokyo) 2011; 64:51–57.
34
35. Altameme H, Hameed IH, Kareem M. Analysis of alkaloid phytochemical compounds in the ethanolic extract of Datura stramonium and evaluation of antimicrobial activity. African J Biotechnol 2015; 14:1668–1674.
35
36. Isnaeni I, Kusumawati I, Suwito MF, Darmawati A, Mertaniasih NM. Antimicrobial activity of Streptomyces spp. isolated from vegetable plantation soil. J Biol Res 2016; 21:69–74.
36
37. Morbidoni HR, Vilchèze C, Kremer L, Bittman R, Sacchettini JC, Jacobs WR. Dual inhibition of mycobacterial fatty acid biosynthesis and degradation by 2-alkynoic acids. Chem Biol 2006; 13:297–307.
37
38. Zhao WY, Zhu TJ, Fan GT, Liu HB, Fang YC, Gu QQ, et al. Three new dioxopiperazine metabolites from a marine-derived fungus Aspergillus fumigatus Fres. Nat Prod Res 2010; 24:953–957.
38
39. Reina JC, Pérez-Victoria I, Martín J, and Llamas I. A quorum-sensing inhibitor strain of vibrio alginolyticus blocks Qs-controlled phenotypes in Chromobacterium violaceum and Pseudomonas aeruginosa. Mar Drugs 2019; 17:1–18.
39
40. Nuñez A, Sapozhnikova Y, and Lehotay SJ. Characterization of MS/MS product ions for the differentiation of structurally isomeric pesticides by high-resolution mass spectrometry. Toxics 2018; 6:1–12.
40
41. Kottege J. Evaluation of the active dimethenamid – P in the product frontier – P herbicide. Canberra; 2007.
41
42. Rhee KH. Isolation and characterization of Streptomyces sp. KH-614 producing anti-VRE (vancomycin-resistant enterococci) antibiotics. J Gen Appl Microbiol 2002; 48:321–327.
42
43. Kresge N, Simoni RD, and Hill RL. Selman Waksman: The father of antibiotics. J Biol Chem 2004; 279:101–103.
43
44. Khieu TN, Liu MJ, Nimaichand S, Quach NT, Chu-Ky S, Phi QT, et al. Characterization and evaluation of antimicrobial and cytotoxic effects of Streptomyces sp. HUST012 isolated from medicinal plant Dracaena cochinchinensis Lour. Front Microbiol 2015; 6:1–9.
44
45. Hurwitz J, Furth JJ, Malamy M, and Alexander M. The role of deoxyribonucleic acid in ribonucleic acid synthesis. III. The inhibition of the enzymatic synthesis of ribonucleic acid and deoxyribonucleic acid by actinomycin D and proflavin. Proc Natl Acad Sci U S A 1962; 48:1222–1230.
45
46. Ciulli A, Scott DE, Ando M, and Reyes F. Inhibition of Mycobacterium tuberculosis pantothenate synthetase by analogues of the reaction intermediate. ChemBioChem 2015; 9:2606–2611.
46
47. Yang Y, Gao P, Liu Y, Ji X, Gan M, Guan Y, et al. A discovery of novel Mycobacterium tuberculosis pantothenate synthetase inhibitors based on the molecular mechanism of actinomycin D inhibition. Bioorganic Med Chem Lett 2011; 21:3943–3946.
47
48. Munir MU, Ahmed A, Usman M, and Salman S. Recent advances in nanotechnology-aided materials in combating microbial resistance and functioning as antibiotics substitutes. Int J Nanomedicine 2020; 15:7329–7358.
48
49. Khameneh B, Iranshahy M, Vahdati-Mashhadian N, Sahebkar A, and Fazly Bazzaz BS. Non-antibiotic adjunctive therapy: A promising approach to fight tuberculosis. Pharmacol Res 2019; 146:1–12.
49
50. Barka EA, Vatsa P, Sanchez L, Nathalie Gaveau-Vaillant CJ, Klenk H-P, Clément C, et al. Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 2016; 80:1–43.
50
51. Schmitzer PR, Graupner PR, Chapin EL, Fields SC, Gilbert JR, Gray JA, et al. Ribofuranosyl triazolone: A natural product herbicide with activity on adenylosuccinate synthetase following phosphorylation. J Nat Prod 2000; 63:777–781.
51
52. Õmura S and Crump A. The life and times of ivermectin - A success story. Nat Rev Microbiol 2004; 2:984–989.
52
53. Singh V and Tripathi CK. Isolation and characterization of actinomycin V and D from a new isolate of Streptomyces sp. In: International Conference and Exhibition on Pharmacognosy, Phytochemistry, and Natural Products. Hyderabad; 2013; 261.
53
54. Chandrakar S, Gupta AK. Actinomycin-Producing Endophytic Streptomyces parvulus Associated with Root of Aloe vera and Optimization of Conditions for Antibiotic Production. Probiotics Antimicrob Proteins 2019; 11:1055–1069.
54
55. Zhang X, Ye X, Chai W, Lian XY, Zhang Z. New metabolites and bioactive actinomycins from marine-derived Streptomyces sp. ZZ338. Mar Drugs 2016; 14:1–9.
55
56. Praveen V and Tripathi CKM. Studies on the production of actinomycin-D by Streptomyces griseoruber - A novel source. Lett Appl Microbiol 2009; 49:450–455.
56
57. Srinu M, Kumar MMK, and Shankar GG. Actinomycin D from marine sediment associated Streptomyces capillispiralis MTCC10471. Asian J Pharm Res Heal Care 2013; 5:16–23.
57
ORIGINAL_ARTICLE
Expression of SR-B1 receptor in breast cancer cell lines, MDA-MB-468 and MCF-7: Effect on cell proliferation and apoptosis
Objective(s): High-density lipoprotein (HDL) is necessary for proliferation of several cells. The growth of many kinds of cells, such as breast cancer cells (BCC) is motivated by HDL. Cellular uptake of cholesterol from HDL which increases cell growth is facilitated by scavenger receptors of the B class (SR-BI). The proliferative effect of HDL might be mediated by this receptor. It is also believed that HDL has an anti-apoptotic effect on various cell types and promotes cell growth. This study was designed to investigate SR-BI expression, proliferation and apoptotic effect of HDL on human BCC lines, MCF-7 and MDA-MB-468.Materials and Methods: Real-time-PCR method was used to evaluate expression of SR-BI, and cholesterol concentration was measured using a cholesterol assay kits (Pars AZ moon, Karaj, Iran). Cell viability was assessed using the MTT test. To identify cell apoptosis, the annexin V-FITC staining test and caspase-9 activity assay were applied.Results: Treatment of both cell lines (MCF-7, MDA-MB-468) with HDL results in augmentation of SR-BI mRNA expression and also elevation of the intracellular cholesterol (p <0.01). HDL induced cell proliferation, cell cycle progression, and prevented activation of caspase-9 (p <0.05). We also demonstrated that inhibition of SR-B1 by BLT-1 could reduce cell proliferation, and induction of SR-B1 receptor by quercetin increased HDL-induced proliferation in both cell lines (p <0.05).Conclusion: It can be concluded that alteration in HDL levels by SR-B1 activator (Quercetin) or inhibitor (BLT-1) may affect BCC growth and apoptosis induction.
https://ijbms.mums.ac.ir/article_18424_f1bad8ca504ff3a4b6d92d341e7a2ea6.pdf
2021-08-01
1069
1077
10.22038/ijbms.2021.56752.12674
BC BLT
1 HDL MCF
7 MDA
MB
468 SR
B1
Neamat
Karimi
karimi.neamat@gmail.com
1
Department of Clinical Biochemistry, Cancer Research Laboratory, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
AUTHOR
Fatemeh
Karami-Tehrani
karamitf@modares.ac.ir
2
Department of Clinical Biochemistry, Cancer Research Laboratory, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
LEAD_AUTHOR
1. Saha S, Singh BK, Singh K, Khanna R, Meena RN. Analysis of serum level of 25-hydroxycholecalciferol, calcium and lipid profile in carcinoma breast. Int Surgery J. 2019;6:3204-3210
1
2. Martin SS, Blumenthal RS, Miller M. LDL cholesterol: the lower the better. Med Clin. 2012;96:13-26.
2
3. Gaard M, Tretli S, Urdal P. Risk of breast cancer in relation to blood lipids: a prospective study of 31,209 Norwegian women. Cancer Causes Control. 1994;5:501-509.
3
4. Mady EA. Association between estradiol, estrogen receptors, total lipids, triglycerides, and cholesterol in patients with benign and malignant breast tumors. J Steroid Biochem Mol Biol. 2000;75:323-328.
4
5. Bani I, Williams CM, Boulter P, Dickerson J. Plasma lipids and prolactin in patients with breast cancer. Br J Cancer. 1986;54:439-446.
5
6. Basu T, Williams D. Plasma and body lipids in patients with carcinoma of the breast. Oncology. 1975;31:172-176.
6
7. Alexopoulos C, Blatsios B, Avgerinos A. Serum lipids and lipoprotein disorders in cancer patients. Cancer. 1987;60:3065-3070.
7
8. Chang S-J, Hou M-F, Tsai S-M, Wu S-H, Hou LA, Ma H, et al. The association between lipid profiles and breast cancer among Taiwanese women. 2007;45:1219-1223.
8
9. Gerber M, Cavallo F, Marubini E, Richardson S, Barbieri A, Capitelli E, et al. Liposoluble vitamins and lipid parameters in breast cancer. A joint study in northern Italy and southern France. Int J Cancer. 1988;42:489-494.
9
10. Kökoǧlu E, Karaarslan I, Karaarslan HM, Baloǧlu H. Alterations of serum lipids and lipoproteins in breast cancer. Cancer lett. 1994;82:175-178.
10
11. Goodwin PJ, Boyd NF, Hanna W, Hartwick W, Murray D, Qizilbash A, et al. Elevated levels of plasma triglycerides are associated with histologically defined piemenopausal breast cancer risk.Nutr Cancer. 1997;27:282-292.
11
12. Rössner S, Wallgren A. Serum lipoproteins and proteins after breast cancer surgery and effects of tamoxifen. Atherosclerosis. 1984;52:339-346.
12
13. Cao WM, Murao K, Imachi H, Yu X, Abe H, Yamauchi A, et al. A mutant high-density lipoprotein receptor inhibits proliferation of human breast cancer cells. Cancer Res. 2004;64:1515-1521.
13
14. Murao K, Imachi H, Cao W, Yu X, Li J, Yoshida K, et al. High-density lipoprotein is a potential growth factor for adrenocortical cells. Biochem Biophys Res Commun. 2006;344:226-232.
14
15. Al-Jarallah A, Chen X, González L, Trigatti BL. High density lipoprotein stimulated migration of macrophages depends on the scavenger receptor class B, type I, PDZK1 and Akt1 and is blocked by sphingosine 1 phosphate receptor antagonists. PLoS ONE. 2014;9:e106487.
15
16. Gao M, Zhao D, Schouteden S, Sorci-Thomas MG, Van Veldhoven PP, Eggermont K, et al. Regulation of high-density lipoprotein on hematopoietic stem/progenitor cells in atherosclerosis requires scavenger receptor type BI expression. Arteriosclerosis Thromb Vas Biol.2014;34:1900-1909.
16
17. Brian J, Jacques genest. High-density lipoproteins and endothelial function. Circulation. 2001; 104:1978-1983.
17
18. Nofer J-R, Assmann G. Atheroprotective effects of high-density lipoprotein-associated lysosphingolipids. Trends cardiovasc Med. 2005;15:265-271.
18
19. Guo C, Luttrell LM, Price DT. Mitogenic signaling in androgen sensitive and insensitive prostate cancer cell lines. J Urol. 2000;163:1027-1032.
19
20. Kane LP, Mollenauer MN, Xu Z, Turck CW, Weiss A. Akt-dependent phosphorylation specifically regulates Cot induction of NF-κB-dependent transcription. Mol Cell Biol. 2002;22:5962-5974.
20
21. Grewal T, de Diego I, Kirchhoff MF, Tebar F, Heeren J, Rinninger F, et al. High density lipoprotein-induced signaling of the MAPK pathway involves scavenger receptor type BI-mediated activation of Ras. J Biol Chem. 2003;278:16478-16481.
21
22. Yuan B, Wu C, Wang X, Wang D, Liu H, Guo L, et al. High scavenger receptor class B type I expression is related to tumor aggressiveness and poor prognosis in breast cancer. Tumor Biol. 2016;37:3581-3588.
22
23. Mooberry LK, Nair M, Paranjape S, McConathy WJ, Lacko AG. Receptor mediated uptake of paclitaxel from a synthetic high density lipoprotein nanocarrier. J Drug Target. 2010;18:53-58.
23
24. Ren K, Jiang T, Zhao G-J. Quercetin induces the selective uptake of HDL-cholesterol via promoting SR-BI expression and the activation of the PPARγ/LXRα pathway. Food funct. 2018;9:624-635.
24
25. Nieland TJ, Penman M, Dori L, Krieger M, Kirchhausen T. Discovery of chemical inhibitors of the selective transfer of lipids mediated by the HDL receptor SR-BI. Proc Natl Acad Sci. 2002;99:15422-15427.
25
26. Yu M, Romer KA, Nieland TJ, Xu S, Saenz-Vash V, Penman M, et al. Exoplasmic cysteine Cys384 of the HDL receptor SR-BI is critical for its sensitivity to a small-molecule inhibitor and normal lipid transport activity. Proc Natl Acad Sci. 2011;108:12243-12248.
26
27. Danilo C, Gutierrez-Pajares JL, Mainieri MA, Mercier I, Lisanti MP, Frank PG. Scavenger receptor class B type I regulates cellular cholesterol metabolism and cell signaling associated with breast cancer development. Breast Cancer Res. 2013;15:1-13.
27
28. Llaverias G, Danilo C, Mercier I, Daumer K, Capozza F, Williams TM, et al. Role of cholesterol in the development and progression of breast cancer. Am J pathol. 2011;178:402-412.
28
29. Nofer J-R, Levkau B, Wolinska I, Junker R, Fobker M, von Eckardstein A, et al. Suppression of endothelial cell apoptosis by high density lipoproteins (HDL) and HDL-associated lysosphingolipids. J Biol Chem. 2001;276:34480-34485.
29
30. Yang J-T, Li Z-L, Wu J-Y, Lu F-J, Chen C-H. An oxidative stress mechanism of shikonin in human glioma cells. PLoS ONE. 2014;9:e94180.
30
31. MacLellan DL, Steen H, Adam RM, Garlick M, Zurakowski D, Gygi SP, et al. A quantitative proteomic analysis of growth factor‐induced compositional changes in lipid rafts of human smooth muscle cells. Proteomics. 2005;5:4733-4742.
31
32. Zuchermann MJ, Ipsen JH, Mouritsen OG. Cholesterol in membrane models. CRC press; 1992:223-259.
32
33. Shahzad MM, Mangala LS, Han HD, Lu C, Bottsford-Miller J, Nishimura M, et al. Targeted delivery of small interfering RNA using reconstituted high-density lipoprotein nanoparticles. Neoplasia. 2011;13:309-319.
33
34. Su F, Kozak KR, Imaizumi S, Gao F, Amneus MW, Grijalva V, et al. Apolipoprotein AI (apoA-I) and apoA-I mimetic peptides inhibit tumor development in a mouse model of ovarian cancer. Proc Natl Acad Sci. 2010;107:19997-20002.
34
35. Witt W, Kolleck I, Fechner H, Sinha P, Rüstow B. Regulation by vitamin E of the scavenger receptor BI in rat liver and HepG2 cells. J lipid Res. 2000;41:2009-2016.
35
36. Suc I, Escargueil-Blanc I, Troly M, Salvayre R, Nègre-Salvayre A. HDL and apoA prevent cell death of endothelial cells induced by oxidized LDL. Arteriosclerosis Thromb Vas Biol. 1997;17:2158-2166.
36
37. Seetharam D, Mineo C, Gormley AK, Gibson LL, Vongpatanasin W, Chambliss KL, et al. High-density lipoprotein promotes endothelial cell migration and reendothelialization via scavenger receptor-B type I. Circ Res. 2006;98:63-72.
37
38. Sekine Y, Demosky SJ, Stonik JA, Furuya Y, Koike H, Suzuki K, et al. High-density lipoprotein induces proliferation and migration of human prostate androgen–independent cancer cells by an ABCA1-dependent mechanism. Mol Cancer Res. 2010;8:1284-1294.
38
39. Martin G, Pilon A, Albert C, Vallé M, Hum DW, Fruchart JC, et al. Comparison of expression and regulation of the high‐density lipoprotein receptor SR‐BI and the low‐density lipoprotein receptor in human adrenocortical carcinoma NCI‐H295 cells. Eur J Biochem. 1999;261:481-491.
39
40. Exon JH, South EH, Taruscio TG, Clifton GD, Fariss MW. Chemopreventive effect of dietary d-α-tocopheryl succinate supplementation on precancer colon aberrant crypt formation and vitamin E analogue levels in young and old rats. Nutr Cancer. 2004;49:72-80.
40
41. Twiddy AL, Cox ME, Wasan KM. Knockdown of scavenger receptor class B type I reduces prostate specific antigen secretion and viability of prostate cancer cells. Prostate. 2012;72:955-965.
41
42. Gospodarowicz D, Lui G-M, Gonzalez R. High-density lipoproteins and the proliferation of human tumor cells maintained on extracellular matrix-coated dishes and exposed to defined medium. Cancer Res. 1982;42:3704-3713.
42
43. Michalides R. Cell cycle regulators: mechanisms and their role in aetiology, prognosis, and treatment of cancer. J Clin Pathol. 1999;52:555-568.
43
44. Nofer J-R, Junker R, Pulawski E, Fobker M, Levkau B, von Eckardstein A, et al. High density lipoproteins induce cell cycle entry in vascular smooth muscle cells via mitogen activated protein kinase-dependent pathway.J Thromb Haemost. 2001;85:730-735.
44
45. Nofer J-R. Signal transduction by HDL: agonists, receptors, and signaling cascades. High density Lipoproteins. 2015:229-256.
45
46. Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. New Engl J Med. 2006;354:270-282.
46
47. Wakeling A, Newboult E, Peters S. Effects of antioestrogens on the proliferation of MCF-7 human breast cancer cells. J Mol Endocrinol. 1989;2:225-234.
47
48. George KS, Wu S. Lipid raft: A floating island of death or survival. Toxicol Appl Pharmacol. 2012;259:311-319.
48
49. Murai T. The role of lipid rafts in cancer cell adhesion and migration. Int J Cell Biol. 2012;2012.
49
50. Phillips MC. Molecular mechanisms of cellular cholesterol efflux. J Biol Chem. 2014;289:24020-24029.
50
51. Paillasse MR, de Medina P, Amouroux G, Mhamdi L, Poirot M, Silvente-Poirot S. Signaling through cholesterol esterification: a new pathway for the cholecystokinin 2 receptor involved in cell growth and invasion. J lipid Res. 2009;50:2203-2211.
51
52. De medina P, Boubekeur N, Balaguer P, Favre G, Silvente-Poirot S, Poirot M. The prototypical inhibitor of cholesterol esterification, Sah 58-035 [3-[decyldimethylsilyl]-n-[2-(4-methylphenyl)-1-phenylethyl] propanamide], is an agonist of estrogen receptors. J Pharmacol Exp Ther. 2006;319:139-149.
52
53. De medina P, Genovese S, Paillasse MR, Mazaheri M, Caze-Subra S, Bystricky K, et al. Auraptene is an inhibitor of cholesterol esterification and a modulator of estrogen receptors. Mol Pharmacol. 2010;78:827-836.
53
54. Uda S, Accossu S, Spolitu S, Collu M, Angius F, Sanna F, et al. A lipoprotein source of cholesteryl esters is essential for proliferation of CEM-CCRF lymphoblastic cell line. Tumor Biol. 2012;33:443-453.
54
55. Pan B, Ren H, He Y, Lv X, Ma Y, Li J, et al. HDL of patients with type 2 diabetes mellitus elevates the capability of promoting breast cancer metastasis. Clin Cancer Res. 2012;18:1246-1256.
55
56. Lu C-W, Lo Y-H, Chen C-H, Lin C-Y, Tsai C-H, Chen P-J, et al. VLDL and LDL, but not HDL, promote breast cancer cell proliferation, metastasis and angiogenesis. Cancer lett. 2017;388:130-138.
56
57. Rotheneder M, Kostner GM. Effects of low‐and high‐density lipoproteins on the proliferation of human breast cancer cells In vitro: Differences between hormone‐dependent and hormone‐independent cell lines. Int J cancer. 1989;43:875-879.
57
58. Cust AE, Kaaks R, Friedenreich C, Bonnet F, Laville M, Tjønneland A, et al. Metabolic syndrome, plasma lipid, lipoprotein and glucose levels, and endometrial cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC). Endocr-Relat cancer. 2007;14:755-767.
58
59. Jürgens G, Xu Q, Huber L, Böck G, Howanietz H, Wick G, et al. Promotion of lymphocyte growth by high density lipoproteins (HDL): physiological significance of the HDL binding site. J Biol Chem. 1989;264:8549-8556.
59
60. Xu J, Qian J, Xie X, Lin L, Ma J, Huang Z, et al. High density lipoprotein cholesterol promotes the proliferation of bone-derived mesenchymal stem cells via binding scavenger receptor-B type I and activation of PI3K/Akt, MAPK/ERK1/2 pathways. Mol Cell Biochem. 2012;371:55-64.
60
ORIGINAL_ARTICLE
Interaction of miR-146a-5p with oxidative stress and inflammation in complications of type 2 diabetes mellitus in male rats: antioxidant and anti-inflammatory protection strategies in type 2 diabetic retinopathy
Objective(s): This study aimed to evaluate the role of miR-146a-5p in the pathogenesis of diabetic retinopathy and its interaction with oxidative stress and inflammation in the ocular tissue of rats with type 2 diabetes mellitus (T2DM). Materials and Methods: Twenty adult male Sprague Dawley rats (220 ±20 g) were randomly assigned to control and diabetic groups. A high-fat diet was used for three months to induce T2DM which was confirmed by the HOMA-IR index. After that, the levels of glucose and insulin in serum, HOMA-IR as an indicator of insulin resistance, the ocular level of oxidative markers, TNF‐α, IL-1β, MIPs, and MCP-1 along with ocular gene expression of NF-κB, Nrf2, and miR-146a-5p were evaluated.Results: The level of lipid peroxidation along with metabolic and inflammatory factors significantly increased and the antioxidant enzyme activity significantly decreased in diabetic rats (p <0.05). The ocular expression of NF-κB and TNF-α increased and Nrf2, HO-1, and miR-146a-5p expression decreased in diabetic rats (p <0.05). In addition, a negative correlation between miR-146a-5p expression with NF-κB and HOMA-IR and a positive correlation between miR-146a-5p with Nrf2 were observed.Conclusion: It can be concluded that miR-146a-5p may regulate Nrf2 and NF-κB expression and inflammation and oxidative stress in the ocular tissue of diabetic rats.
https://ijbms.mums.ac.ir/article_18494_a3b4f2452194e78bc32ed2baa6a28679.pdf
2021-08-01
1078
1086
10.22038/ijbms.2021.56958.12706
Diabetic retinopathy
Inflammation
MicroRNA
Oxidative stress
Type 2 diabetes
Seyed Ahmad
Rasoulinejad
rasolisa2@gmail.com
1
Department of Ophthalmology, Ayatollah Rouhani Hospital, Babol University of Medical Sciences, Babol, Iran
AUTHOR
Abolfazl
Akbari
akbariabolfazl@gmail.com
2
Department of Physiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran
LEAD_AUTHOR
Khadijeh
Nasiri
kh.nasiri@umz.ac.ir
3
Department of Exercise Physiology, Faculty of Sport Sciences, University of Mazandaran, Babolsar, Iran
AUTHOR
1. Wu Y, Ding Y, Tanaka Y, Zhang W. Risk factors contributing to type 2 diabetes and recent advances in the treatment and prevention. Int J Med Sci 2014;11:1185-1200.
1
2. Jelkmann W. Regulation of erythropoietin production. J Physiol 2011;589:1251-1258.
2
3. Prattichizzo F, Giuliani A, Ceka A, Rippo MR, Bonfigli AR, Testa R, et al. Epigenetic mechanisms of endothelial dysfunction in type 2 diabetes. Clin Epigenetics 2015;7:56-68.
3
4. Rajasekar P, O’Neill CL, Eeles L, Stitt AW, Medina RJ. Epigenetic changes in endothelial progenitors as a possible cellular basis for glycemic memory in diabetic vascular complications. J Int J Diabetes Res 2015;2015:436879-896.
4
5. Kato M, Natarajan R. Epigenetics and epigenomics in diabetic kidney disease and metabolic memory. Nat Rev Nephrol 2019;15:327-345.
5
6. Zaiou M. circRNAs signature as potential diagnostic and prognostic biomarker for diabetes mellitus and related cardiovascular complications. Cells. 2020;9:659-678.
6
7. Barutta F, Bellini S, Mastrocola R, Bruno G, Gruden G. MicroRNA and microvascular complications of diabetes. Int J Endocrinol 2018;2018 :6890501-6890521.
7
8. Markopoulos GS, Roupakia E, Tokamani M, Alabasi G, Sandaltzopoulos R, Marcu KB, et al. Roles of NF-κB signaling
8
in the regulation of miRNAs impacting on inflammation in cancer. Biomedicines 2018;6:40-59.
9
9. Olivieri F, Lazzarini R, Recchioni R, Marcheselli F, Rippo MR, Di Nuzzo S, et al. MiR-146a as marker of senescenceassociated pro-inflammatory status in cells involved in vascular remodelling. Age 2013;35:1157-1172.
10
10. Li B, Liu S, Miao L, Cai L. Prevention of diabetic complications by activation of Nrf2: Diabetic cardiomyopathy and nephropathy. Exp Diabetes Res 2012;2012 :216512-216519.
11
11. da Costa RM, Rodrigues D, Pereira CA, Silva JF, Alves JV, Lobato NS, et al. Nrf2 as a potential mediator of cardiovascular
12
risk in metabolic diseases. Front Pharmacol 2019;10:382-394.
13
12. Shi L, Kim AJ, Chang RC, Chang JY, Ying W, Ko ML, et al. Deletion of miR-150 exacerbates retinal vascular overgrowth in high-fat-diet induced diabetic mice. PLoS One 2016;11:e0157543.
14
13. Nasiri K, Akbari A, Nimrouzi M, Ruyvaran M, Mohamadian A. Safflower seed oil improves steroidogenesis and spermatogenesis in rats with type II diabetes mellitus by modulating the genes expression involved in steroidogenesis,
15
inflammation and oxidative stress. J Ethnopharmacol 2021;275:114139-114152.
16
14. Nimrouzi M, Ruyvaran M, Zamani A, Nasiri K, Akbari A. Oil and extract of safflower seed improve fructose induced metabolic syndrome through modulating the homeostasis of trace elements, TNF-α, and fatty acids metabolism. J Ethnopharmacol 2020;254:112721-112733.
17
15. Kim AJ, Chang JYA, Shi L, Chang RCA, Ko ML, Ko GYP. The Effects of Metformin on Obesity-Induced Dysfunctional Retinas. Invest Ophthalmol Vis Sci 2017;58:106-118.
18
16. Clarkson-Townsend DA, Douglass AJ, Singh A, Allen RS, Uwaifo IN, Pardue MT. Impacts of high fat diet on ocular outcomes in rodent models of visual disease. Exp Eye Res 2021;204:108440-108455.
19
17. Wan RJ, Li YH. MicroRNA‑146a/NAPDH oxidase4 decreases reactive oxygen species generation and inflammation in a diabetic nephropathy model. Mol Med Rep 2018;17:4759-4766.
20
18. Chang RC, Shi L, Huang CC, Kim AJ, Ko ML, Zhou B, et al. High-fat diet-induced retinal dysfunction. Invest Ophthalmol Vis Sci. 2015;56:2367-2380.
21
19. Aebi H. [13] Catalase in vitro. Methods Enzymol 1984;105:121-126.
22
20. Zal F, Mostafavi‐Pour Z, Vessal M. Comparison of the effects of vitamin e and/or quercetin in attenuating chronic cyclosporine a‐induced nephrotoxicity in male rats. Clin Exp Pharmacol Physiol 2007;34:720-724.
23
21. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
24
22. Wei J, Wang J, Zhou Y, Yan S, Li K, Lin H. MicroRNA-146a contributes to SCI recovery via regulating TRAF6 and IRAK1 expression. Biomed Res Int 2016;2016: : 4013487-4013495.
25
23. Nimrouzi M, Abolghasemi J, Sharifi MH, Nasiri K, Akbari A. Thyme oxymel by improving of inflammation, oxidative stress, dyslipidemia and homeostasis of some trace elements ameliorates obesity induced by high-fructose/fat diet in male rat. Biomed Pharmacother 2020;126:110079-110092.
26
24. Echeverría F, Valenzuela R, Espinosa A, Bustamante A, Álvarez D, Gonzalez-Mañan D, et al. Reduction of high-fat dietinduced liver proinflammatory state by eicosapentaenoic acid plus hydroxytyrosol supplementation: Involvement of resolvins RvE1/2 and RvD1/2. J Nutr Biochem 2019;63:35-43.
27
25. de Faria JBL, Silva KC, de Faria JML. The contribution of hypertension to diabetic nephropathy and retinopathy: The role of inflammation and oxidative stress. Hypertens Res 2011;34:413-422.
28
26. Wu MY, Yiang GT, Lai TT, Li CJ. The oxidative stress and mitochondrial dysfunction during the pathogenesis of diabetic
29
retinopathy. Oxid Med Cell Longev 2018;2018:3420187- 3420199.
30
27. Pickering RJ, Rosado CJ, Sharma A, Buksh S, Tate M, de Haan JB. Recent novel approaches to limit oxidative stress and inflammation in diabetic complications. Clin Transl Immunology 2018;7:e1016.
31
28. Chaar LJ, Coelho A, Silva NM, Festuccia WL, Antunes VR. High-fat diet-induced hypertension and autonomic imbalance
32
are associated with an upregulation of CART in the dorsomedial hypothalamus of mice. Physiol Rep 2016;4:e12811.
33
29. Kolluru GK, Bir SC, Kevil CG. Endothelial Dysfunction and Diabetes: Effects on angiogenesis, vascular remodeling, and wound healing. Int J Vasc Med 2012;2012:918267-Last page.
34
30. Barrett EJ, Liu Z, Khamaisi M, King GL, Klein R, Klein BEK, et al. Diabetic Microvascular Disease: An endocrine society scientific statement. J Clin Endocrinol Metab 2017;102:4343-4410.
35
31. Rohowetz LJ, Kraus JG, Koulen P. Reactive oxygen speciesmediated damage of retinal neurons: Drug development
36
targets for therapies of chronic neurodegeneration of the retina. Int J Mol Sci 2018;19: 3362-3392.
37
32. Suryavanshi SV, Kulkarni YA. NF-κβ: A potential target in the management of vascular complications of diabetes. Front
38
Pharmacol 2017;8:798-810.
39
33. Huang H, Gandhi JK, Zhong X, Wei Y, Gong J, Duh EJ, et al. TNFα is required for late BRB breakdown in diabetic retinopathy, and its inhibition prevents leukostasis and protects vessels and neurons from apoptosis. Invest Ophthalmol Vis Sci 2011;52:1336-1344.
40
34. Semeraro F, Cancarini A, Rezzola S, Romano MR, Costagliola C. Diabetic retinopathy: vascular and inflammatory disease. J Diabetes Res 2015;2015:582060-582076.
41
35. Bhavsar I, Miller CS, Al-Sabbagh M. Macrophage inflammatory protein-1 alpha (MIP-1 alpha)/CCL3: As a biomarker. eneral Methods in Biomarker Research and their Applications. 2015:223-249.
42
36. Rübsam A, Parikh S, Fort PE. Role of inflammation in diabetic retinopathy. Int J Mol Sci 2018;19:942-973.
43
37. Patel JI, Saleh GM, Hykin PG, Gregor ZJ, Cree IA. Concentration of haemodynamic and inflammatory related cytokines in diabetic retinopathy. Eye 2008;22:223-228.
44
38. Tashimo A, Mitamura Y, Nagai S, Nakamura Y, Ohtsuka K, Mizue Y, et al. Aqueous levels of macrophage migration inhibitory factor and monocyte chemotactic protein‐1 in patients with diabetic retinopathy. Diabet Med 2004;21:1292-
45
39. Zhang W, Liu H, Al-Shabrawey M, Caldwell RW, Caldwell RB. Inflammation and diabetic retinal microvascular complications. J Cardiovasc Dis Res 2011;2:96-103.
46
40. Batliwala S, Xavier C, Liu Y, Wu H, Pang IH. Involvement of Nrf2 in ocular diseases. Oxid Med Cell Longev 2017;2017::1703810- 1703828.
47
41. David JA, Rifkin WJ, Rabbani PS, Ceradini DJ. The Nrf2/Keap1/ARE pathway and oxidative stress as a therapeutic target in type II diabetes mellitus. J Diabetes Res 2017;2017:4826724-4826739.
48
42. Jiménez-Osorio AS, Picazo A, González-Reyes S, Barrera-Oviedo D, Rodríguez-Arellano ME, Pedraza-Chaverri J. Nrf2 and redox status in prediabetic and diabetic patients. Int J Mol Sci 2014;15:20290-20305.
49
43. Ahmed SMU, Luo L, Namani A, Wang XJ, Tang X. Nrf2 signaling pathway: Pivotal roles in inflammation. BBA Molecular Basis of Disease 2017;186:585-597.
50
44. Li L, Pan H, Wang H, Li X, Bu X, Wang Q, et al. Interplay between VEGF and Nrf2 regulates angiogenesis due to intracranial venous hypertension. Sci Rep 2016;6:1-11.
51
45. Uno K, Prow TW, Bhutto IA, Yerrapureddy A, McLeod DS, Yamamoto M, et al. Role of Nrf2 in retinal vascular development and the vaso-obliterative phase of oxygen-induced retinopathy. Exp Eye Res 2010;90:493-500.
52
46. Lenin R, Sankaramoorthy A, Mohan V, Balasubramanyam M. Altered immunometabolism at the interface of increased endoplasmic reticulum (ER) stress in patients with type 2 diabetes. J Leukoc Biol 2015;98:615-622.
53
47. Karolina DS, Armugam A, Tavintharan S, Wong MTK, Lim SC, Sum CF, et al. MicroRNA 144 impairs insulin signaling by inhibiting the expression of insulin receptor substrate 1 in type 2 diabetes mellitus. PLoS One 2011;6:e22839.
54
48. Alipoor B, Ghaedi H, Meshkani R, Torkamandi S, Saffari S, Iranpour M, et al. Association of MiR-146a expression and type 2 diabetes mellitus: A meta-analysis. Int J Mol Cell Med 2017;6:156-163.
55
49. Saba R, Sorensen DL, Booth SA. MicroRNA-146a: A dominant, negative regulator of the innate immune response.
56
Front Immunol 2014;5:578-589.
57
50. Li K, Zhao B, Wei D, Wang W, Cui Y, Qian L, et al. miR‑146a improves hepatic lipid and glucose metabolism by targeting MED1. Int J Mol Med 2020;45:543-555.
58
51. Park K, Steffes M, Lee DH, Himes JH, Jacobs DR, Jr. Association of inflammation with worsening HOMA-insulin resistance. Diabetologia 2009;52:2337-2344.
59
52. Park K, Gross M, Lee D-H, Holvoet P, Himes JH, Shikany JM, et al. Oxidative stress and insulin resistance: The coronary artery risk development in young adults study. Diabetes Care 2009;32:1302-1307.
60
53. Rajamani U, Jialal I. Hyperglycemia induces Tolllike receptor-2 and-4 expression and activity in human microvascular retinal endothelial cells: Implications for diabetic retinopathy. J Diabetes Res 2014; 2014 :790902-790928.
61
54. Morcos M, Schlotterer A, Sayed AAR, Kukudov G, Oikomonou D, Ibrahim Y, et al. Rosiglitazone reduces angiotensin II and advanced glycation end product-dependent sustained nuclear factor-κB activation in cultured human proximal tubular epithelial cells. Horm Metab Re 2008;40:752-759.
62
55. Xie Y, Chu A, Feng Y, Chen L, Shao Y, Luo Q, et al. MicroRNA- 146a: A comprehensive indicator of inflammation and oxidative stress status induced in the brain of chronic t2dm rats. Front Pharmacol 2018;9:478-489.
63
56. Mann M, Mehta A, Zhao JL, Lee K, Marinov GK, Garcia-Flores Y, et al. An NF-κB-microRNA regulatory network tunes macrophage inflammatory responses. Nat Commun 2017;8:851-864.
64
57. Ma X, Becker Buscaglia LE, Barker JR, Li Y. MicroRNAs in NF-kappaB signaling. J Mol Cell Biol 2011;3:159-166.
65
58. Lo WY, Peng CT, Wang HJ. MicroRNA-146a-5p mediates high glucose-induced endothelial inflammation via targeting
66
interleukin-1 receptor-associated kinase 1 expression. Front Physiol 2017;8:551-561.
67
59. Luo Q, Ren Z, Zhu L, Shao Y, Xie Y, Feng Y, et al. Involvement of microRNA-146a in the inflammatory response of s tatus epilepticus rats. CNS Neurol Disord Drug Targets 2017;16:686-693.
68
60. Xu J, Zgheib C, Liechty KW. miRNAs in bone marrow–derived mesenchymal stem cells. MicroRNA in regenerative medicine: Elsevier; 2015;111-136.
69
61. Li S, Yue Y, Xu W, Xiong S. MicroRNA-146a represses mycobacteria-induced inflammatory response and facilitates
70
bacterial replication via targeting IRAK-1 and TRAF-6. PLoS One 2013;8:e81438.
71
62. He X, Jing Z, Cheng G. MicroRNAs: New regulators of toll-like receptor signalling pathways. BioMed Res Int 2014;2014:945169-9451783.
72
63. Kamali K, Korjan ES, Eftekhar E, Malekzadeh K, Soufi FG. The role of miR-146a on NF-κB expression level in human umbilical vein endothelial cells under hyperglycemic condition. Bratisl Lek Listy 2016;117:376-380.
73
64. Qu X, Wang N, Cheng W, Xue Y, Chen W, Qi M. MicroRNA‑146a protects against intracerebral hemorrhage by inhibiting inflammation and oxidative stress. Exp Ther Med 2019;18:3920-3928.
74
65. Yu M, Li H, Liu Q, Liu F, Tang L, Li C, et al. Nuclear factor p65 interacts with Keap1 to repress the Nrf2-ARE pathway. Cell Signal 2011;23:883-892.
75
66. Hirotsu Y, Katsuoka F, Funayama R, Nagashima T, Nishida Y, Nakayama K, et al. Nrf2-MafG heterodimers contribute globally to anti-oxidant and metabolic networks. Nucleic Acids Res 2012;40:10228-10239.
76
67. Rada P, Rojo AI, Chowdhry S, McMahon M, Hayes JD, Cuadrado A. SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol
77
2011;31:1121-1133.
78
ORIGINAL_ARTICLE
Attenuation of tacrolimus induced oxidative stress, mitochondrial damage, and cell cycle arrest by Boerhavia diffusa root fraction in mdck cell lines
Objective(s): The protective effect of ethyl acetate fraction (EAF) of Boerhavia diffusa roots against Tacrolimus (TAC) induced nephrotoxicity was studied using MDCK cell lines.Materials and Methods: Ethanolic root extract of B. diffusa was fractionated using the liquid-liquid partition method. The cytotoxic effect of TAC and protective effect of EAF co-treatment were studied in MDCK cell lines by measuring ROS, LPO, and NO levels; collagen accumulation, effect on mitochondrial membrane integrity and cell cycle analysis were studied. The active component in EAF was quantified by HPLC analysis.Results: TAC induced toxicity, leading to apoptosis and necrosis, was significantly reduced (p <0.001) in EAF co-treatment, with reversal of cell cycle arrest and reduced cell population at sub G0/G1 phase. Further, ROS (p <0.05), LPO and NO (p <0.001), were significantly reduced with EAF co-treatment compared with TAC individually treated cells. TAC induced mitochondrial membrane integrity loss was found to be significantly reduced in co-treated cells, as measured by rhodamine123 (p <0.05) and translocation of cytochrome c (p <0.001) from nucleus to cytoplasm, and caspase 3 release (p <0.001). The same was confirmed through annexin-FITC and PI staining (p <0.05) with reduced apoptotic and necrotic death in co-treated population. Interestingly, EAF co-treatment decreased collagen accumulation (p <0.001) with significant increase in the cell survival of tubular epithelial cells. HPLC analysis showed the presence of Quercetin (87.5 mg/g) in EAF, which may be responsible for the nephroprotective role. Conclusion: Thus, these results provide sound evidence that EAF may be an effective adjuvant therapy to prevent nephrotoxicity induced by TAC.
https://ijbms.mums.ac.ir/article_18416_93bb5b1f670859ea8ae9f02379f5c487.pdf
2021-08-01
1087
1097
10.22038/ijbms.2021.56519.12618
Apoptosis
Boerhavia diffusa
Caspase 3
Cell cycle
HPLC
Nephrotoxicity
Quercetin
Reactive Oxygen Species
Kalaivani
M.K.
kvani.mk@gmail.com
1
Department of Biomedical Sciences, Sri Ramachandra Institute of Higher Education and Research (DU), Porur, Chennai 6000116, India
AUTHOR
Cordelia
John
cordeliajohn7@gmail.com
2
Department of Biomedical Sciences, Sri Ramachandra Institute of Higher Education and Research (DU), Porur, Chennai 6000116, India
AUTHOR
Bhavana
Jonnagaladda
bhavana1489@gmail.com
3
Department of Biomedical Sciences, Sri Ramachandra Institute of Higher Education and Research (DU), Porur, Chennai 6000116, India
AUTHOR
Akila
Kesavan
k.akila07@gmail.com
4
Department of Human Genetics, Sri Ramachandra Institute of Higher Education and Research (DU), Porur, Chennai, 600116, India
AUTHOR
Sumathy
Arockiasamy
sumathyjoseph04@sriramachandra.edu.in
5
Department of Biomedical Sciences, Sri Ramachandra Institute of Higher Education and Research (DU), Porur, Chennai 6000116, India
LEAD_AUTHOR
1. Naesens M, Kuypers DR, Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009; 4:481-508.
1
2. Zhou X, Yang G, Davis CA, Doi SQ, Hirszel P, Wingo CS, et al. Hydrogen peroxide mediates FK506-induced cytotoxicity in renal cells. Kidney Int 2004; 65:139-147.
2
3. Matas AJ, Smith JM, Skeans MA, Lamb KE, Gustafson SK, Samana CJ, et al. OPTN/SRTR 2011 annual data report: Kidney. Am J Transplant 2013; 13 Suppl 1:11-46.
3
4. Hošková L, Málek I, Kautzner J, Honsová E, van Dokkum RPE, Husková Z, et al. Tacrolimus-induced hypertension and nephrotoxicity in Fawn-Hooded rats are attenuated by dual inhibition of renin–angiotensin system. Hypertens Res 2014; 37:724-732.
4
5. Khanna AK, Pieper GM. NADPH oxidase subunits (NOX-1, p22phox, Rac-1) and tacrolimus-induced nephrotoxicity in a rat renal transplant model. Nephrol Dial Transplant 2006; 22:376-385.
5
6. Ara C, Dirican A, Unal B, Bay Karabulut A, Piskin T. The effect of melatonin against fk506-induced renal oxidative stress in rats. Surg Innov 2011; 18:34-38.
6
7. Hisamura F, Kojima-Yuasa A, Kennedy DO, Matsui-Yuasa I. Protective effect of green tea extract and tea polyphenols against fk506-induced cytotoxicity in renal cells. Basic Clin Pharmacol Toxicol 2006; 98:192-196.
7
8. Li X, Zhuang S. Recent advances in renal interstitial fibrosis and tubular atrophy after kidney transplantation. Fibrogenesis & Tissue Repair 2014; 7:1-11.
8
9. Butani L, Afshinnik A, Johnson J, Javaheri D, Peck S, German JB, et al. Amelioration of tacrolimus-induced nephrotoxicity in rats using juniper oil. Transplantation 2003; 76:306-311.
9
10. Suman S, Hayagreeva Dinakar Y, Suhas reddy P V, Sai Sudha Yadav B, Venkateshwar Reddy V. Ameliorative effect of Cubeba Officinalis dried fruits against Tacrolimus induced nephrotoxicity in Wistar albino rats.Int. J Res Pharm Sci 2020; 11:596-602.
10
11. Oyouni A, Saggu S, Tousson E, Mohan A, Farasani A. Mitochondrial nephrotoxicity induced by tacrolimus (FK-506) and modulatory effects of Bacopa monnieri (Farafakh) of Tabuk Region. Pharmacognosy Res 2019; 11:20-24.
11
12. Oyouni AAA, Saggu S, Tousson E, Rehman H. Immunosuppressant drug tacrolimus induced mitochondrial nephrotoxicity, modified PCNA and Bcl-2 expression attenuated by Ocimum basilicum L. in CD1 mice. Toxicol Rep 2018; 5:687-694.
12
13. Jegan N, editor. Effect of Hydroalcoholic Extract of Boerhaavia Diffusa Linn against Cisplatin Induced Nephrotoxicity2015; 10:17-22.
13
14. Padmini P. An experimental study of biochemical and histopathological study on gentamycin induced renal failure in albino rat and the effectiveness of punarnava (Boerhaevia Diffusa) on reversal of renal damage. IOSR JDMS 2013; 9:17-21.
14
15. Sawardekar S, Patel T. Evaluation of the effects of boerhaavia diffusa on gentamicin induced nephrotoxicity in rats. J Ayurveda Integr Med 2015; 6:95-103.
15
16. Yadav HN, Sharma US, Singh S, Gupta YK. Effect of combination of Tribulus terrestris, Boerhavia diffusa and Terminalia chebula reverses mercuric chloride-induced nephrotoxicity and renal accumulation of mercury in rat. Orient Pharm Exp Med 2019; 19:497-507.
16
17. Karwasra R, Kalra P, Nag T, Gupta Y, Singh S, Panwar A. Safety assessment and attenuation of cisplatin induced nephrotoxicity by tuberous roots of Boerhaavia diffusa. Regul Toxicol Pharm 2016; 81:341-352.
17
18. Indhumathi T, Shipa K, Mohandass S. Evaluation of nephroprotective role of Boerhaavea diffusa leaves against mercuric chloride induced toxicity in experimental rats. J Pharm Res 2011; 4:1848-1850.
18
19. M.K K, Soundararajan P, Vasanthi HR, Arockiasamy S. In vitro nephroprotective role of ethanolic root extract of boerhaavia diffusa against cisplatin induced nephrotoxicity. Int J Phytomed 2015;7: 388-395.
19
20. Bowlekar PB, Gadgoli CH. Amelioration of cisplatin induced nephrotoxicity by standardized methanolic extract of roots of boerhaavia diffusa. Nat Prod J 2014; 4:217-223.
20
21. Kalaivani M, Arockiasamy S, John C, Vasanthi H, Soundararajan P. Therapeutic potential of Boerhavia diffusa L. against cyclosporine A-Induced mitochondrial dysfunction and apoptosis in madin–Darby canine kidney cells. Pharmacogn Mag 2018; 14:132-140.
21
22. Erdogan S, Doganlar O, Doganlar ZB, Turkekul K. Naringin sensitizes human prostate cancer cells to paclitaxel therapy. Prostate Int 2018; 6:126-135.
22
23. Repetto G, del Peso A, Zurita JL. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 2008; 3:1125-1131.
23
24. Elumalai P, Gunadharini DN, Senthilkumar K, Banudevi S, Arunkumar R, Benson CS, et al. Induction of apoptosis in human breast cancer cells by nimbolide through extrinsic and intrinsic pathway. Toxicol Lett 2012; 215:131-142.
24
25. Servais H, Ortiz A, Devuyst O, Denamur S, Tulkens PM, Mingeot-Leclercq MP. Renal cell apoptosis induced by nephrotoxic drugs: cellular and molecular mechanisms and potential approaches to modulation. Apoptosis 2008; 13:11-32.
25
26. Ligasová A, Koberna K. Quantification of fixed adherent cells using a strong enhancer of the fluorescence of DNA dyes. Sci. Rep 2019; 9:8701.
26
27. Balaji C, Muthukumaran J, Vinothkumar R, Nalini N. Anticancer effects of sinapic acid on human colon cancer cell lines HT-29 and SW480. Int J Pharm Biol Arch 2014; 5: 176-183.
27
28. Hsieh C-Y, Chen C-L, Yang K-C, Ma C-T, Choi P-C, Lin C-F. Detection of reactive oxygen species during the cell cycle under normal culture conditions using a modified fixed-sample staining method. Immunoassay Immunochem 2015; 36:149-161.
28
29. Filipkowski RK, Hetman M, Kaminka B, Kaczmarek L. DNA fragmentation in rat brain after intraperitoneal administration of kainate. Neuroreport 1994; 5:1538-1540.
29
30. Satoh M, Kashihara N, Fujimoto S, Horike H, Tokura T, Namikoshi T, et al. A novel free radical scavenger, edarabone, protects against cisplatin-induced acute renal damage in vitro and in vivo. J Pharmacol Exp Ther 2003; 305:1183-1190.
30
31. Hortelano S, López-Collazo E, Boscá L. Protective effect of cyclosporin A and FK506 from nitric oxide-dependent apoptosis in activated macrophages. Br J Pharmacol 1999; 126:1139-1146.
31
32. Taso OV, Philippou A, Moustogiannis A, Zevolis E, Koutsilieris M. Lipid peroxidation products and their role in neurodegenerative diseases. Ann Res Hosp 2019; 3:2-10.
32
33. Zhong Z, Connor HD, Li X, Mason RP, Forman DT, Lemasters JJ, et al. Reduction of ciclosporin and tacrolimus nephrotoxicity by plant polyphenols. J Pharm Pharmacol 2006; 58:1533-1543.
33
34. Mishra S, Aeri V, Gaur PK, Jachak SM. Phytochemical, therapeutic, and ethnopharmacological overview for a traditionally important herb: Boerhavia diffusa linn. BioMed Research International 2014; 2014:1-19.
34
35. Ortiz A, Lorz C, Catalán M, Ortiz A, Coca S, Egido J. Cyclosporine A induces apoptosis in murine tubular epithelial cells: Role of caspases. Kidney Int 1998; 54:S25-S29.
35
36. Ali AS, Almalki AS, Alharthy BT. Effect of kaempferol on tacrolimus-induced nephrotoxicity and calcineurin B1 expression level in animal model. J Exp Pharmacol 2020; 12:397-407.
36
37. Park C, Kwon DH, Hwang SJ, Han MH, Jeong J-W, Hong SH, et al. Protective effects of nargenicin a1 against tacrolimus-induced oxidative stress in hirame natural embryo cells. International journal of environmental research and public health 2019; 16:1-13.
37
38. Kim ES, Lee JS, Akram M, Kim KA, Shin YJ, Yu JH, et al. Protective activity of dendropanax morbifera against cisplatin-induced acute kidney injury. Kidney Blood Press. Res 2015; 40:1-12.
38
39. Farris AB, Colvin RB. Renal interstitial fibrosis: Mechanisms and evaluation in: Current opinion in nephrology and hypertension. Curr Opin Nephrol Hypertens 2012; 21:289-300.
39
40. Zhu Q, Hu J, Meng H, Shen Y, Zhou J, Zhu Z. S-Phase cell cycle arrest, apoptosis, and molecular mechanisms of aplasia ras homolog member i–induced human ovarian cancer skov3 cell lines. Int J Gynecol Cancer 2014; 24:629-634.
40
41. Prathapan A, Vineetha VP, Raghu KG. Protective effect of Boerhaavia diffusa L. against mitochondrial dysfunction in angiotensin II induced hypertrophy in H9c2 cardiomyoblast cells. PLoS One 2014; 9:e96220.
41
42. Chaudhary S, Ganjoo P, Raiusddin S, Parvez S. Nephroprotective activities of quercetin with potential relevance to oxidative stress induced by valproic acid. Protoplasma 2015; 252:209-217.
42
43. Lim SW, Shin YJ, Luo K, Quan Y, Cui S, Ko EJ, et al. Ginseng increases Klotho expression by FoxO3-mediated manganese superoxide dismutase in a mouse model of tacrolimus-induced renal injury. Aging 2019; 11:5548-5569.
43
44. Abdel-Aziz A-A, El-Din M, Balah A, Akool E-S. Molecular mechanisms of the modulatory effect of vitamin E on tacrolimus (FK506)-induced renal injury in rats. Br J Pharm Res 2016; 9:1-9.
44
45. Wongmekiat O, Leelarugrayub N, Thamprasert K. Beneficial effect of shallot (Allium ascalonicum L.) extract on cyclosporine nephrotoxicity in rats. Food and chemical toxicology: An international journal published for the British Industrial Biological Research Association 2008; 46:1844-1850.
45
46. Hisamura F, Kojima-Yuasa A, Huang X, Kennedy DO, Matsui-Yuasa I. Synergistic effect of green tea polyphenols on their protection against FK506-induced cytotoxicity in renal cells. Am J Chin Med 2008; 36:615-624.
46
47. Jeon SH, Park HM, Kim SJ, Lee MY, Kim GB, Rahman MM, et al. Taurine reduces FK506-induced generation of ROS and activation of JNK and Bax in Madin Darby canine kidney cells. Hum Exp Toxicol 2010; 29:627-633.
47
48. Mehrotra S, Mishra KP, Maurya R, Srimal RC, Singh VK. Immunomodulation by ethanolic extract of Boerhaavia diffusa roots. Int Immunopharmacol 2002; 2:987-996.
48
49. Athira KV, Madhana RM, Lahkar M. Flavonoids, the emerging dietary supplement against cisplatin-induced nephrotoxicity. Chem Biol Interact 2016; 248:18-20.
49
50. Vargas F, Romecín P, García-Guillén AI, Wangesteen R, Vargas-Tendero P, Paredes MD, et al. Flavonoids in kidney health and disease. Front Physiol 2018; 9:1-12.
50
51. Zal F, Mostafavi-Pour Z, Vessal M. Comparison of the effects of vitamin E and/or quercetin in attenuating chronic cyclosporine A-induced nephrotoxicity in male rats. Clin Exp Pharmacol Physiol 2007; 34:720-724.
51
ORIGINAL_ARTICLE
Type1 and 3 fimbriae phenotype and genotype as suitable markers for uropathogenic bacterial pathogenesis via attachment, cell surface hydrophobicity, and biofilm formation in catheter-associated urinary tract infections (CAUTIs)
Objective(s): Catheters are one of the factors for complicated urinary tract infections. Uropathogenic bacteria can attach to the catheter via cell surface hydrophobicity (CSH), form biofilms, and remain in urinary tract. The study was evaluated phenotypic and genotypic characteristics of fimbriae in Klebsiella pneumoniae and uropathogenic Escherichia coli (UPEC) isolates from patients with catheter-associated urinary tract infections (CAUTIs) and their association with biofilm formation. Materials and Methods: Urine specimens were collected through catheters in patients with CAUTIs. Sixty bacterial isolates were identified by biochemical tests. For determination of biofilm formation a tissue culture plate was used. Microbial adhesion to hydrocarbons (MATH) was conducted for CSH determination. The mannose-sensitive haemagglutination (MSHA) and mannose-resistant haemagglutination (MRHA) were determined for type 1 and type 3 fimbriae. Finally, the presence of genes encoding fimbriae was determined by PCR.Results: All isolates showed strong CSH, biofilm capacity and MRHA phenotype. The results showed that 20% of UPEC and 23% of K. pneumoniae isolates contained MSHA phenotypes. There was a significant association between biofilm formation and MSHA phenotype in UPEC isolates. The frequency of fimA (80%) and fimH (96.6%) in K. pneumoniae isolates was higher than UPEC isolates. Both types of bacterial isolates with MSHA phenotypes harbored the fimH gene. Conclusion: The phenotypic and genotypic characteristics of two bacterial species were highly similar. Also, the type of fimbriae affected bacterial biofilm formation through catheterization. It seems that fimH and mrk gene cluster subunits are suitable markers for identifying bacterial pathogenesis.
https://ijbms.mums.ac.ir/article_18493_d4d95965ffb8a73f59c23135c98642bd.pdf
2021-08-01
1098
1106
10.22038/ijbms.2021.53691.12079
Biofilm
Catheterization
Fimbriae
Urinary tract infections
Uropathogenic
Fatemeh
Mohammad Zadeh
1
Department of Microbiology, Varamin-Pishva Branch, Islamic Azad University, Varamin, Iran
AUTHOR
Hamed
Zarei
h.zarei@iautmu.ac.ir
2
Department of Biology, Faculty of Basic science, Central Tehran Branch, Islamic Azad University, Tehran, Iran
LEAD_AUTHOR
Sahar
Honarmand Jahromy
sahar_hj2@yahoo.com
3
Department of Microbiology, Varamin-Pishva Branch, Islamic Azad University, Varamin, Iran
AUTHOR
1. Tarchouna M, Ferjani A, Ben-Selma W, Boukadida J. Distribution of uropathogenic virulence genes in Escherichia coli isolated from patients with urinary tract infection. Int J Infect Dis 2013:17:e450-e3.
1
2. Foxman B. Urinary tract infection syndromes: occurrence, recurrence, bacteriology, risk factors, and disease burden. Infect Dis Clin North Am 2013:28:1-13.
2
3. Gould CV, Umscheid CA, Agarwal RK, Kuntz G, Pegues DA.Committee HICPA. Guideline for prevention of catheter-associated urinary tract infections 2009. Infect Control Hosp Epidemiol 2010:31:319-26.
3
4. Lobdell KW, Stamou S, Sanchez JA. Hospital-acquired infections. Surg Clin North Am 2012: 92:65-77.
4
5. Jordan R P C, Malic S, Waters MG, Stickler D J, Williams DW. “Development of an antimicrobial urinary catheter to inhibit urinary catheter encrustation .Microbiol.Dis 2015: 3:1-7.
5
6. Chatterjee S, Maiti PK, Dey R, Kundu Ak , Dey Rk .“Biofilms on indwelling urologic devices: microbes and antimicrobial management prospect.” Ann Med Health Sci Res 2014: 4:100-104.
6
7. Ndejiko MJ, Abubakar BM, Hindatu Y, Sulaiman M, Saidu H, Idris A, et al. Bacterial biofilm: a major challenge of catheterization. J Microbiol Res 2013:3:213-23.
7
8. Pelling H, Nzakizwanayo J, Milo S, Denham EL , MacFarlane WM, Bock LJ, et al. BV.Bacterial biofilm formation on indwelling urethral catheters. Lett Appl Microbiol 2019: 68: 277-293.
8
9. Donlan R, Costerton J. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002: 15: 167–193.
9
10. Heilmann C. Adhesion mechanisms of staphylococci. Bacterial adhesion: Adv Exp Med Biol 2011:715:105-23.
10
11. Terlizzi ME, Gribaudo G, Maffe ME. UroPathogenic Escherichia coli (UPEC) Infections: Virulence Factors, Bladder Responses, Antibiotic, and Non-antibiotic Antimicrobial Strategies. Front Microbiol 2017:15:1-22.
11
12. Ronald A, Nicolle L, Stamm E, Krieger J, Warren J, Schaeffer A, et al. Urinary tract infection in adults: research priorities and strategies. Int J Antimicrob Agents 2001:17:343-348.
12
13. Gerlach GF, Clegg S, Allen BL. Identification and characterization of the genes encoding the type 3 and type 1 fimbrial adhesins of Klebsiella pneumoniae. J bacteriol 1989:171:1262-1270.
13
14. Ottow J. Ecology, physiology, and genetics of fimbriae and pili. Annu Rev Microbiol 1975:29:79-108.
14
15. Barnhart MM, Sauer FG, Pinkner JS, Hultgren SJ. Chaperone-subunit-usher interactions required for donor strand exchange during bacterial pilus assembly. J bacteriol 2003:185:2723-2730.
15
16. Brinton Jr CC. The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. Trans N Y Acad Sci 1965:27:1003-1054.
16
17. Schroll C, Barken KB, Krogfelt KA, Struve C. Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formation. BMC microbiol 2010:10:179-189
17
18. Cheryl-lynn YO, Beatson SA, Totsika M, Forestier C, McEwan AG, Schembri MA. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC microbiol 2010:10:183-195
18
19. Stahlhut SG, Struve C, Krogfelt KA, Reisner A. Biofilm formation of Klebsiella pneumoniae on urethral catheters requires either type 1 or type 3 fimbriae. FEMS Immunol Med Microbiol 2012: 65: 350-359.
19
20. Bergqvist D, Brönnestam R, Hedelin H, Ståhl A. The relevance of urinary sampling methods in patients with indwelling Foley catheters. Br J Urol 1980:52:92-95.
20
21. Stark RP, Maki DG. Bacteriuria in the catheterized patient: what quantitative level of bacteriuria is relevant? N Engl J Med 1984:311:560-564.
21
22. Stepanović S, Vuković D, Hola V, Bonaventura GD, Djukić S, Ćirković I, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Apmis 2007:115:891-899.
22
23. Collee J, Fraser A, Marmino B, Simons A. Mackin and McCartney, Practical Medical Microbiology. The Churchill Livingstone. Inc USA 1996.
23
24. Rosenberg M. Bacterial adherence to hydrocarbons: a useful technique for studying cell surface hydrophobicity. FEMS Microbiol Lett 1984:22:289-295.
24
25.Nwanyanwu C, Abu G. Influence of growth media on hydrophobicity of phenol-utilizing bacteria found in petroleum refinery effluent. Int Res J Biol Sci 2013:2:6-11.
25
26. Kadam T, Rupa L, Balhal D, Totewad N, Gyananath G. Determination of the degree of hydrophobicity–A technique to assess bacterial colonization on leaf surface and root region of lotus plant. Asian J Exp Sci 2009:23:135-139.
26
27. Qadri F, Haque A, Faruque SM, Bettelheim KA, Robins-Browne R, Albert MJ. Hemagglutinating properties of enteroaggregative Escherichia coli. J clin microbiol. 1994:32:510-514.
27
28. Old D, Tavendale A, Senior B. A comparative study of the type-3 fimbriae of Klebsiella species. J med microbiol 1985: 20:203-214.
28
29. Narayanan A, Nair MS, Muyyarikkandy MS, Amalaradjou MA. Inhibition and inactivation of uropathogenic Escherichia coli biofilms on urinary catheters by sodium selenite. Inter J Mol sci 2018:19:1703-1716.
29
30. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015:13:269-284.
30
31. Niveditha S, Pramodhini S, Umadevi S, Kumar S, Stephen S. The isolation and the biofilm formation of uropathogens in the patients with catheter associated urinary tract infections (UTIs). J clin diagn res 2012:6:1478-1482.
31
32. Shah C, Baral R, Bartaula B, Shrestha LB. Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance. BMC microbiol. 2019: 19:204-210.
32
33. Karam MRA, Habibi M, Bouzari S. Relationships between virulence factors and antimicrobial resistance among Escherichia coli isolated from urinary tract infections and commensal isolates in Tehran, Iran. Osong Public Health Res Perspect 2018:9:217-224.
33
34. Fattahi S, Kafil HS, Nahai MR, Asgharzadeh M, Nori R, Aghazadeh M. Relationship of biofilm formation and different virulence genes in uropathogenic Escherichia coli isolates from Northwest Iran. GMS Hyg Infect Control 2015:10:1-10.
34
35. Krasowska A, Sigler K. How microorganisms use hydrophobicity and what does this mean for human needs? Front Cell Infect Microbiol 2014:4:112-119.
35
36.Gogra AB , Yao J, Sandy EH , Zheng SH , Zaray G , Koroma BM , Hui Z. Cell surface hydrophobicity (CSH) of Escherichia coli, Staphylococcus aureus and Aspergillus niger and the biodegradation of Diethyl Phthalate (DEP) via Microcalorimetry. J Am Sci 2010:6:78-88.
36
37. Mirani ZA, Fatima A, Urooj S, Aziz M, Khan MN, Abbas T. Relationship of cell surface hydrophobicity with biofilm formation and growth rate: A study on Pseudomonas aeruginosa, Staphylococcus aureus, and Escherichia coli. Iran J Basic Med Sci 2018:21:760-769.
37
38. Schwan WR. Regulation of fim genes in uropathogenic Escherichia coli. World J Clin Infect Dis 2011:1:17-25.
38
39. Burmølle M, Bahl MI, Jensen LB, Sørensen SJ, Hansen LH. Type 3 fimbriae, encoded by the conjugative plasmid pOLA52, enhance biofilm formation and transfer frequencies in Enterobacteriaceae strains. Microbiol 2008:154:187-95.
39
40. Wang X, Lünsdorf H, Ehrén I, Brauner A, Römling U. Characteristics of biofilms from urinary tract catheters and presence of biofilm-related components in Escherichia coli. Curr Microbiol 2010:60:446-53.
40
41. Ulett GC, Mabbett AN, Fung KC, Webb RI, Schembri MA. The role of F9 fimbriae of uropathogenic Escherichia coli in biofilm formation. Microbiol 2007:153:2321-2331.
41
42. Murphy CN, Mortensen MS, Krogfelt KA, Clegg S. Role of Klebsiella pneumoniae type 1 and type 3 fimbriae in colonizing silicone tubes implanted into the bladders of mice as a model of catheter-associated urinary tract infections. Infect Immun 2013:81:3009-3017.
42
43. Stærk K, Khandige S, Kolmos HJ, Møller-Jensen J, Andersen TE. Uropathogenic Escherichia coli express type 1 fimbriae only in surface adherent populations under physiological growth conditions. J Infect Dis 2016:213:386-94.
43
44. Caitlin N. Murphy, Martin S. Mortensen, Karen A. Krogfelt, Steven Clegg Role of Klebsiella pneumoniae Type 1 and Type 3 Fimbriae in Colonizing Silicone Tubes Implanted into the Bladders of Mice as a Model of Catheter-Associated Urinary Tract Infections. Infect Immun 2013:81: 3009–3017.
44
45. Mahmood MT, Abdullah BA. The relationship between biofilm formation and presence of fimH and mrkD genes among Escherichia coli and K. pneumoniae isolated from patients in Mosul. Mosul J Nurs 2015:3:34-42.
45
ylococcus aureusand Aspergillus nigerand the biodegradation of Diethyl Phthalate (DEP) via Microcalorimetry. Journal of American Science. 2010;6(7)
46
37. Mirani ZA, Fatima A, Urooj S, Aziz M, Khan MN, Abbas T. Relationship of cell surface hydrophobicity with biofilm formation and growth rate: A study on Pseudomonas aeruginosa, Staphylococcus aureus, and Escherichia coli. Iranian journal of basic medical sciences. 2018;21(7):760.
47
38. Schwan WR. Regulation of fim genes in uropathogenic Escherichia coli. World journal of clinical infectious diseases. 2011;1(1):17.
48
39. Burmølle M, Bahl MI, Jensen LB, Sørensen SJ, Hansen LH. Type 3 fimbriae, encoded by the conjugative plasmid pOLA52, enhance biofilm formation and transfer frequencies in Enterobacteriaceae strains. Microbiology. 2008;154(1):187-95.
49
40. Wang X, Lünsdorf H, Ehrén I, Brauner A, Römling U. Characteristics of biofilms from urinary tract catheters and presence of biofilm-related components in Escherichia coli. Current microbiology. 2010;60(6):446-53.
50
41. Ulett GC, Mabbett AN, Fung KC, Webb RI, Schembri MA. The role of F9 fimbriae of uropathogenic Escherichia coli in biofilm formation. Microbiology. 2007;153(7):2321-31.
51
42. Murphy CN, Mortensen MS, Krogfelt KA, Clegg S. Role of Klebsiella pneumoniae type 1 and type 3 fimbriae in colonizing silicone tubes implanted into the bladders of mice as a model of catheter-associated urinary tract infections. Infection and immunity. 2013;81(8):3009-17.
52
43. Stærk K, Khandige S, Kolmos HJ, Møller-Jensen J, Andersen TE. Uropathogenic Escherichia coli express type 1 fimbriae only in surface adherent populations under physiological growth conditions. The Journal of infectious diseases. 2016;213(3):386-94.
53
44. Schroll C, Barken KB, Krogfelt KA, Struve C. Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formation. BMC Microbiology. 2010, 10:179.
54
45. Caitlin N. Murphy, Martin S. Mortensen, Karen A. Krogfelt, Steven Clegg Role of Klebsiella pneumoniae Type 1 and Type 3 Fimbriae in Colonizing Silicone Tubes Implanted into the Bladders of Mice as a Model of Catheter-Associated Urinary Tract Infections. Infection and Immunity .2013;81(8): 3009–3017.
55
46. Mahmood MT, Abdullah BA. The relationship between biofilm formation and presence of fimH and mrkD genes among E. coli and K. pneumoniae isolated from patients in Mosul. Mosul Journal of Nursing. 2015;3(1):34-42.
56
ORIGINAL_ARTICLE
Alpha-lipoic acid could attenuate the effect of chemerin-induced diabetic nephropathy progression
Objective(s): Chemerin is associated with insulin resistance, obesity, and metabolic syndrome. α-lipoic acid (α-LA) is a potent antioxidant involved in the reduction of diabetic symptoms. This study aimed to investigate the relationship between chemerin and P38 MAPK in the progression of diabetic nephropathy (DN) and examine the effects of α-LA on chemerin-treated human mesangial cells (HMCs). Materials and Methods: HMCs were transfected with a chemerin-overexpressing plasmid. HMCs were also treated with high-glucose, chemerin, α-LA, PDTC (pyrrolidine dithiocarbamate ammonium, NF-κB p65 inhibitor), and/or SB203580 (P38 MAPK inhibitor). Cell proliferation was tested using the Cell Counting Kit-8 assay. Collagen type IV and laminin were tested by ELISA. Chemerin expression was detected by qRT-PCR. The chemerin receptor was detected by immunohistochemistry. Interleukin-6 (IL-6), tumor necrosis factor-a (TNF-α), nuclear factor-κBp-p65 (NF-κB p-p65), transforming growth factor-β (TGF-β), and p-P38 mitogen-activated protein kinase (p-P38 MAPK) were evaluated by western blot.Results: High-glucose culture increased the expression of the chemerin receptor. α-LA inhibited HMC proliferation. Chemerin overexpression increased collagen type IV and laminin expression. P38 MAPK signaling was activated by chemerin, resulting in up-regulation of IL-6, TNF-α, NF-κB p-p65, and TGF-β. SB203580, PDTC, and α-LA reversed the effects of chemerin, reducing IL-6, TNF-α, NF-κB p-p65, and TGF-β expression. Conclusion: Chemerin might be involved in the occurrence and development of DN. α-LA might prevent the effects of chemerin on the progression of DN, possibly via the P38 MAPK pathway.
https://ijbms.mums.ac.ir/article_18413_b2a04ae398dbd7f8bb42b60841d369b9.pdf
2021-08-01
1107
1116
10.22038/ijbms.2021.50792.11570
Alpha
lipoic acid Chemerin Diabetic nephropathy Nuclear factor
kappa
B P38 mitogen
activated
protein kinases
Hong
Zhang
1014842045@qq.com
1
Department of Endocrinology, First Affiliated Hospital of Harbin Medical University, Harbin, China
AUTHOR
Jiawei
Mu
mujiawei1790@sina.com
2
Department of Endocrinology, First Affiliated Hospital of Harbin Medical University, Harbin, China
AUTHOR
Jinqiu
Du
2524740516@qq.com
3
Department of Endocrinology, First Affiliated Hospital of Harbin Medical University, Harbin, China
AUTHOR
Ying
Feng
923299326@qq.com
4
Department of Endocrinology, First Affiliated Hospital of Harbin Medical University, Harbin, China
AUTHOR
Wenhui
Xu
1545189411@qq.com
5
Department of Endocrinology, First Affiliated Hospital of Harbin Medical University, Harbin, China
AUTHOR
Mengmeng
Bai
408168542@qq.com
6
Department of Endocrinology, First Affiliated Hospital of Harbin Medical University, Harbin, China
AUTHOR
Huijuan
Zhang
hydzhj@126.com
7
Department of Endocrinology, First Affiliated Hospital of Harbin Medical University, Harbin, China
LEAD_AUTHOR
1. Uwaezuoke SN. The role of novel biomarkers in predicting diabetic nephropathy: A review. Int J Nephrol Renovasc Dis 2017;10:221-231
1
2. American Diabetes A. Standards of medical care in diabetes-2016 abridged for primary care providers. Clin Diabetes 2016;34:3-21.
2
3. Chamberlain JJ, Rhinehart AS, Shaefer CF, Jr, Neuman A. Diagnosis and management of diabetes: synopsis of the 2016 american diabetes association standards of medical care in diabetes. Ann Intern Med 2016;164:542-552.
3
4. Bakris GL. Recognition, pathogenesis, and treatment of different stages of nephropathy in patients with type 2 diabetes mellitus. Mayo Clin Proc 2011;86:444-56.
4
5. Ma J, Sun F, Wang J, Jiang H, Lu J, Wang X, et al. Effects of aldosterone on chemerin expression and secretion in 3t3-l1 adipocytes. Exp Clin Endocrinol Diabetes 2018;126:187-193.
5
6. Weng C, Shen Z, Li X, Jiang W, Peng L, Yuan H, et al. Effects of chemerin/CMKLR1 in obesity-induced hypertension and potential mechanism. Am J Transl Res 2017;9:3096-3104.
6
7. Zylla S, Rettig R, Völzke H, Endlich K, Nauck M, Friedrich N. Serum chemerin levels are inversely associated with renal function in a general population. Clin Endocrinol (Oxf). 2018;88:146-153.
7
8. Namazi N, Larijani B, Azadbakht L. Alpha-lipoic acid supplement in obesity treatment: A systematic review and meta-analysis of clinical trials. Clin Nutr 2018;37:419-428.
8
9. Saleh HM, El-Sayed YS, Naser SM, Eltahawy AS, Onoda A, Umezawa M. Efficacy of α-lipoic acid against cadmium toxicity on metal ion and oxidative imbalance, and expression of metallothionein and anti-oxidant genes in rabbit brain. Environ Sci Pollut Res Int 2017;24:24593-25601.
9
10. Zhang J, McCullough PA. Lipoic acid in the prevention of acute kidney injury. Nephron 2016;134:133-140.
10
11. Gomes MB, Negrato CA. Alpha-lipoic acid as a pleiotropic compound with potential therapeutic use in diabetes and other chronic diseases. Diabetol Metab Syndr 2014;6:80-120.
11
12. Dong K, Hao P, Xu S, Liu S, Zhou W, Yue X, et al. Alpha-lipoic acid alleviates high-glucose suppressed osteogenic differentiation of MC3T3-E1 cells via anti-oxidant effect and pi3k/akt signaling pathway. Cell Physiol Biochem 2017;42:1897-1906.
12
13. Sun Y, Yang P-P, Song Z-Y, Feng Y, Hu D-M, Hu J, et al. α-lipoic acid suppresses neuronal excitability and attenuates colonic hypersensitivity to colorectal distention in diabetic rats. J Pain Res 2017;10:1645-1655.
13
14. Jurisic-Erzen D, Starcevic-Klasan G, Ivanac D, Peharec S, Girotto D, Jerkovic R. The effects of alpha-lipoic acid on diabetic myopathy. J Endocrinol Invest 2018;41:203-209.
14
15. Adhikary L, Chow F, Nikolic-Paterson DJ, Stambe C, Dowling J, Atkins RC, et al. Abnormal p38 mitogen-activated protein kinase signalling in human and experimental diabetic nephropathy. Diabetologia 2004;47:1210-1222.
15
16. Pang Y, Zhu H, Xu J, Yang L, Liu L, Li J. β-arrestin-2 is involved in irisin induced glucose metabolism in type 2 diabetes via p38 MAPK signaling. Exp Cell Res 2017;360:199-204.
16
17. Dhanya R, Arya AD, Nisha P, Jayamurthy P. Quercetin, a lead compound against type 2 diabetes ameliorates glucose uptake via ampk pathway in skeletal muscle cell line. Front Pharmacol 2017;8:336-51.
17
18. Guo S, Meng X-W, Yang X-S, Liu X-F, Ou-Yang C-H, Liu C. Curcumin administration suppresses collagen synthesis in the hearts of rats with experimental diabetes. Acta Pharmacol Sin 2018;39:195-204.
18
19. Yeda X, Shaoqing L, Yayi H, Bo Z, Huaxin W, Hong C, et al. Dexmedetomidine protects against renal ischemia and reperfusion injury by inhibiting the P38-MAPK/TXNIP signaling activation in streptozotocin induced diabetic rats. Acta Cir Bras 2017;32:429-439.
19
20. Zhang X, Wang L, Shang J, Ning LN, Zhao J, Dou Y, et al. Chemerin/ChemR23 promotes high glucose-induced IL-6 and TNF-α expressions in glomerular endothelial cells via p38 MAPK. Chinese Journal of Nephrology 2017;33:524-530.
20
21. Shang J, Wang L, Zhang Y, Zhang S, Ning L, Zhao J, et al. Chemerin/ChemR23 axis promotes inflammation of glomerular endothelial cells in diabetic nephropathy. J Cell Mol Med. 2019;23:3417-3428.
21
22. El Dayem SM, Battah AA, El Bohy Ael M, El Shehaby A, El Ghaffar EA. Relationship of plasma level of chemerin and vaspin to early atherosclerotic changes and cardiac autonomic neuropathy in adolescent type 1 diabetic patients. J Pediatr Endocrinol Metab 2015;28:265-273.
22
23. Bozaoglu K, Bolton K, McMillan J, Zimmet P, Jowett J, Collier G, et al. Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology 2007;148:4687-4694.
23
24. Gu P, Wang W, Yao Y, Xu Y, Wang L, Zang P, et al. Increased circulating chemerin in relation to chronic microvascular complications in patients with type 2 diabetes. Int J Endocrinol 2019;2019:8693516.
24
25. Hu W, Feng P. Elevated serum chemerin concentrations are associated with renal dysfunction in type 2 diabetic patients. Diabetes Res Clin Pract 2011;91:159-163.
25
26. Hu W, Yu Q, Zhang J, Liu D. Rosiglitazone ameliorates diabetic nephropathy by reducing the expression of Chemerin and ChemR23 in the kidney of streptozotocin-induced diabetic rats. Inflammation 2012;35:1287-1293.
26
27. Salama FE, Anass QA, Abdelrahman AA, Saeed EB. Chemerin: A biomarker for cardiovascular disease in diabetic chronic kidney disease patients. Saudi J Kidney Dis Transpl 2016;27:977-984.
27
28. Bartkoski S, Day M. Alpha-lipoic acid for treatment of diabetic peripheral neuropathy. Am Fam Physician 2016;93:786.
28
29. Wang X, Lin H, Xu S, Jin Y, Zhang R. Alpha lipoic acid combined with epalrestat: A therapeutic option for patients with diabetic peripheral neuropathy. Drug Des Devel Ther 2018;12:2827-2840.
29
30. Rochette L, Ghibu S, Muresan A, Vergely C. Alpha-lipoic acid: Molecular mechanisms and therapeutic potential in diabetes. Can J Physiol Pharmacol 2015;93:1021-1027.
30
31. Han Y, Wang M, Shen J, Zhang Z, Zhao M, Huang J, et al. Differential efficacy of methylcobalamin and alpha-lipoic acid treatment on symptoms of diabetic peripheral neuropathy. Minerva Endocrinol 2018;43:11-18.
31
32. Papanas N, Ziegler D. Efficacy of alpha-lipoic acid in diabetic neuropathy. Expert Opin Pharmacother 2014;15:2721-2731.
32
33. Shay KP, Moreau RF, Smith EJ, Smith AR, Hagen TM. Alpha-lipoic acid as a dietary supplement: molecular mechanisms and therapeutic potential. Biochim Biophys Acta 2009;1790:1149-1160.
33
34. Sadeghiyan Galeshkalami N, Abdollahi M, Najafi R, Baeeri M, Jamshidzade A, Falak R, et al. Alpha-lipoic acid and coenzyme Q10 combination ameliorates experimental diabetic neuropathy by modulating oxidative stress and apoptosis. Life Sci 2019;216:101-110.
34
35. Chukanova EI, Chukanova AS. [Alpha-lipoic acid in the treatment of diabetic polyneuropathy]. Zh Nevrol Psikhiatr Im S S Korsakova 2018;118:103-109.
35
36. Agathos E, Tentolouris A, Eleftheriadou I, Katsaouni P, Nemtzas I, Petrou A, et al. Effect of alpha-lipoic acid on symptoms and quality of life in patients with painful diabetic neuropathy. J Int Med Res 2018;46:1779-1790.
36
37. Cakici N, Fakkel TM, van Neck JW, Verhagen AP, Coert JH. Systematic review of treatments for diabetic peripheral neuropathy. Diabet Med 2016;33:1466-1476.
37
38. Varkonyi T, Korei A, Putz Z, Martos T, Keresztes K, Lengyel C, et al. Advances in the management of diabetic neuropathy. Minerva Med 2017;108:419-437.
38
39. Salehi B, Berkay Yilmaz Y, Antika G, Boyunegmez Tumer T, Fawzi Mahomoodally M, Lobine D, et al. Insights on the Use of alpha-Lipoic Acid for Therapeutic Purposes. Biomolecules 2019;9:356.
39
40. Ibrahimpasic K. Alpha lipoic acid and glycaemic control in diabetic neuropathies at type 2 diabetes treatment. Med Arch 2013;67:7-9.
40
41. Gomes MB, Negrato CA. Alpha-lipoic acid as a pleiotropic compound with potential therapeutic use in diabetes and other chronic diseases. Diabetol Metab Syndr 2014;6:80-120.
41
42. Nguyen N, Takemoto JK. a case for alpha-lipoic acid as an alternative treatment for diabetic polyneuropathy. J Pharm Pharm Sci 2018;21:177s-191s.
42
43. Snyder MJ, Gibbs LM, Lindsay TJ. Treating painful diabetic peripheral neuropathy: an update. Am Fam Physician. 2016;94:227-234.
43
44. Vallianou N, Evangelopoulos A, Koutalas P. Alpha-lipoic acid and diabetic neuropathy. Rev Diabet Stud 2009;6:230-236.
44
45. Seyit DA, Degirmenci E, Oguzhanoglu A. Evaluation of electrophysiological effects of melatonin and alpha lipoic acid in rats with streptozotocine induced diabetic neuropathy. Exp Clin Endocrinol Diabetes 2016;124:300-306.
45
46. Won JC, Kwon HS, Moon SS, Chun SW, Kim CH, Park IB, et al. Gamma-linolenic acid versus alpha-lipoic acid for treating painful diabetic neuropathy in adults: A 12-week, double-placebo, randomized, noninferiority trial. Diabetes Metab J 2020;44:542-54.
46
47. Ziegler D, Low PA, Litchy WJ, Boulton AJ, Vinik AI, Freeman R, et al. Efficacy and safety of anti-oxidant treatment with alpha-lipoic acid over 4 years in diabetic polyneuropathy: the NATHAN 1 trial. Diabetes Care 2011;34:2054-2060.
47
48. Feng B, Yan XF, Xue JL, Xu L, Wang H. The protective effects of alpha-lipoic acid on kidneys in type 2 diabetic Goto-Kakisaki rats via reducing oxidative stress. Int J Mol Sci 2013;14:6746-6756.
48
49. Yi X, Xu L, Hiller S, Kim HS, Nickeleit V, James LR, et al. Reduced expression of lipoic acid synthase accelerates diabetic nephropathy. J Am Soc Nephrol 2012;23:103-111.
49
50. Xu L, Hiller S, Simington S, Nickeleit V, Maeda N, James LR, et al. Influence of different levels of lipoic acid synthase gene expression on diabetic nephropathy. PLoS One 2016;11:e0163208.
50
51. Zabel BA, Silverio AM, Butcher EC. Chemokine-like receptor 1 expression and chemerin-directed chemotaxis distinguish plasmacytoid from myeloid dendritic cells in human blood. J Immunol 2005;174:244-251.
51
52. Hu W, Feng P. Elevated serum chemerin concentrations are associated with renal dysfunction in type 2 diabetic patients. Diabetes Res Clin Pract 2011;91:159-163.
52
53. Hu W, Yu Q, Zhang J, Liu D. Rosiglitazone ameliorates diabetic nephropathy by reducing the expression of Chemerin and ChemR23 in the kidney of streptozotocin-induced diabetic rats. Inflammation 2012;35:1287-1293.
53
54. Wang Y, Liu L, Peng W, Liu H, Liang L, Zhang X, et al. Ski-related novel protein suppresses the development of diabetic nephropathy by modulating transforming growth factor-beta signaling and microRNA-21 expression. J Cell Physiol 2019;234:17925-17936.
54
55. Ding H, Xu Y, Jiang N. Upregulation of miR-101a suppresses chronic renal fibrosis by regulating KDM3A via blockade of the YAP-TGF-beta-smad signaling pathway. Mol Ther Nucleic Acids 2020;19:1276-1289.
55
56. He X, Cheng R, Huang C, Takahashi Y, Yang Y, Benyajati S, et al. A novel role of LRP5 in tubulointerstitial fibrosis through activating TGF-beta/Smad signaling. Signal Transduct Target Ther 2020;5:45-63.
56
57. Komers R, Lindsley JN, Oyama TT, Cohen DM, Anderson S. Renal p38 MAP kinase activity in experimental diabetes. Lab Invest 2007;87:548-558.
57
58. Kang SW, Adler SG, Lapage J, Natarajan R. p38 MAPK and MAPK kinase 3/6 mRNA and activities are increased in early diabetic glomeruli. Kidney Int 2001;60:543-552.
58
59. Kim SI, Kwak JH, Zachariah M, He Y, Wang L, Choi ME. TGF-beta-activated kinase 1 and TAK1-binding protein 1 cooperate to mediate TGF-beta1-induced MKK3-p38 MAPK activation and stimulation of type I collagen. Am J Physiol Renal Physiol 2007;292:F1471-F1478.
59
60. Hills CE, Squires PE. TGF-beta1-induced epithelial-to-mesenchymal transition and therapeutic intervention in diabetic nephropathy. Am J Nephrol 2010;31:68-74.
60
61. Yeh CH, Sturgis L, Haidacher J, Zhang XN, Sherwood SJ, Bjercke RJ, et al. Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-kappaB transcriptional activation and cytokine secretion. Diabetes 2001;50:1495-1504.
61
62. Kaneko K, Miyabe Y, Takayasu A, Fukuda S, Miyabe C, Ebisawa M, et al. Chemerin activates fibroblast-like synoviocytes in patients with rheumatoid arthritis. Arthritis Res Ther 2011;13:R158.
62
63. Sell H, Laurencikiene J, Taube A, Eckardt K, Cramer A, Horrighs A, et al. Chemerin is a novel adipocyte-derived factor inducing insulin resistance in primary human skeletal muscle cells. Diabetes 2009;58:2731-2740.
63
64. Kaur J, Adya R, Tan BK, Chen J, Randeva HS. Identification of chemerin receptor (ChemR23) in human endothelial cells: Chemerin-induced endothelial angiogenesis. Biochem Biophys Res Commun 2010;391:1762-1768.
64
65. Yi X, Xu L, Hiller S, Kim H-S, Nickeleit V, James LR, et al. Reduced expression of lipoic acid synthase accelerates diabetic nephropathy. J Am Soc Nephrol 2012;23:103-111.
65
66. Feng B, Yan X-F, Xue J-L, Xu L, Wang H. The protective effects of α-lipoic acid on kidneys in type 2 diabetic Goto-Kakisaki rats via reducing oxidative stress. Int J Mol Sci 2013;14:6746-6756.
66
67. Yi X, Nickeleit V, James LR, Maeda N. α-Lipoic acid protects diabetic apolipoprotein E-deficient mice from nephropathy. J Diabetes Complications 2011;25:193-201.
67
68. Lee SJ, Kang JG, Ryu OH, Kim CS, Ihm S-H, Choi MG, et al. Effects of alpha-lipoic acid on transforming growth factor beta1-p38 mitogen-activated protein kinase-fibronectin pathway in diabetic nephropathy. Metabolism. 2009;58:616-623.
68
69. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010;140:883-899.
69
70. Kim J, Bhattacharjee R, Dayyat E, Snow AB, Kheirandish-Gozal L, Goldman JL, et al. Increased cellular proliferation and inflammatory cytokines in tonsils derived from children with obstructive sleep apnea. Pediatr Res 2009;66:423-428.
70
71. Chen L, Deng H, Cui H, Fang J, Zuo Z, Deng J, et al. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget 2018;9:7204-7218.
71
72. Moens U, Kostenko S, Sveinbjornsson B. The role of mitogen-activated protein kinase-activated protein kinases (mapkapks) in inflammation. Genes 2013;4:101-133.
72
73. Lu N, Malemud CJ. Extracellular signal-regulated kinase: A regulator of cell growth, inflammation, chondrocyte and bone cell receptor-mediated gene expression. Int J Mol Sci 2019;20:3792-3823.
73
ORIGINAL_ARTICLE
Prevalence of bacteriocin genes in Lactobacillus strains isolated from fecal samples of healthy individuals and their inhibitory effect against foodborne pathogens
Objective(s): Foodborne diseases are considered as an important public health issue. The purpose of the current study was to isolate Lactobacillus spp. strains from fecal samples, investigate their antimicrobial properties, and assess the expression of genes encoding bacteriocin in co-culture of Lactobacillus with enteric pathogens. Materials and Methods: Fecal samples of healthy people were collected. Human colon adenocarcinoma cell line Caco-2 was used to examine Lactobacillus strains adherence capacity. Quantitative real-time reverse transcription PCR (qRT-PCR) was used to determine bacteriocin-encoding genes expression in co-culture of the selected Lactobacillus strain with Salmonella, Shigella, and two diarrheagenic Escherichia coli serotypes during 4, 6, and 24 hr of incubation. Results: The selected L. plantarum strain was able to inhibit four foodborne pathogens in both methods. L. plantarum No.14 exhibited the highest ability to adhere to Caco-2 cells. In this study, pln F, sak P, pln I, pln B, and pln J genes of L. plantarum No.14 were upregulated in co-culture of L. plantarum No.14 with diarrheagenic E. coli serotypes. In addition, acd, Lactacin F, sak P, pln J, pln EF, and pln NC8 genes as well as pln NC8 and pln A genes mRNA levels were significantly increased in co-culture of L. plantarum No.14 with Shigella dysenteriae, and Salmonella typhi, respectively, during 24 hrs of incubation. Conclusion: Other studied genes were down-regulated during the incubation time. The selected L. plantarum strains could be served as alternative antimicrobial agents against pathogens which could contaminate foodstuffs and are responsible for human diseases.
https://ijbms.mums.ac.ir/article_18495_8bc20a83035540b422d8ae87386d5fdb.pdf
2021-08-01
1117
1125
10.22038/ijbms.2021.53299.11998
Bacteriocin Caco
2 cells Escherichia coli Foodborne disease Gene expression Lactobacillus plantarum
Atieh
Darbandi
atiehdarbandi86@gmail.com
1
Department of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Roya
Ghanavati
ghanavati.r@iums.ac.ir
2
Behbahan Faculty of Medical Science, Behbahan, Iran
AUTHOR
arezoo
asadi
arezoo_asadi1364@yahoo.com
3
Department of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Shiva
Mirklantari
mirklantari.s@iums.ac.ir
4
Department of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Meysam
Hasannejad Bibalan
meysam_hasannejad@yahoo.com
5
Department of Microbiology, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran
AUTHOR
Vahid
Lohrasbi
vahidlohrasbi@yahoo.com
6
Department of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Behrooz
Sadeghi Kalani
sadeghi.b@iums.ac.ir
7
Department of Microbiology, Faculty of Medicine, Ilam University of Medical Sciences, Ilam, Iran
AUTHOR
Mahdi
Rohani
m_rohani@pasteur.ac.ir
8
Department of Microbiology, Pasteur Institute of Iran, Tehran, Iran
AUTHOR
Malihe
Talebi
talebi.m@iums.ac.ir
9
Microbial Biotechnology Research Centre, Iran University of Medical Sciences, Tehran, Iran
AUTHOR
Mohammad
Pourshafie
lohrasbi.v@iums.ac.ir
10
Department of Microbiology, Pasteur Institute of Iran, Tehran, Iran
LEAD_AUTHOR
1. Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, et al. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS medicine 2015;12:e1001923.
1
2. Faour-Klingbeil D, C. D. Todd E. Prevention and control of foodborne diseases in middle-east north african countries: Review of national control systems. Int J Environ Res Public Health 2020;17:70.
2
3. Uçar A, Yilmaz MV. Food safety–problems and solutions. Significance, Prev Control Food Relat Dis 2016:3-15.
3
4. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998;11:142-201.
4
5. Organization WH. WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007-2015. WHO; 2015.
5
6. Zweifel C, Stephan R. Spices and herbs as source of Salmonella-related foodborne diseases. Int Food Res J 2012;45:765-769.
6
7. Yang S-C, Lin C-H, Sung CT, Fang J-Y. Antibacterial activities of bacteriocins: application in foods and pharmaceuticals. Front Microbiol 2014;5:241.
7
8. Kerry RG, Patra JK, Gouda S, Park Y, Shin H-S, Das G. Benefaction of probiotics for human health: A review. J FOOD DRUG ANAL 2018;26:927-39.
8
9. Zielińska D, Kolożyn-Krajewska D. Food-origin lactic acid bacteria may exhibit probiotic properties. J Food Drug Anal 2018.
9
10. Dadfarma N, Nowroozi J, Kazemi B, Bandehpour M. Identification of the effects of acid-resistant Lactobacillus caseimetallopeptidase gene under colon-specific promoter on the colorectal and breast cancer cell lines. Iran J Basic Med Sci 2021;24:506-13.
10
11. Vieco-Saiz N, Belguesmia Y, Raspoet R, Auclair E, Gancel F, Kempf I, et al. Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Front Microbiol. 2019;10.
11
12. Fathizadeh H, Saffari M, Esmaeili D, Moniri R, Salimian M. Evaluation of antibacterial activity of enterocin A-colicin E1 fusion peptide. Iran J Basic Med Sci 2020;23 :1471-1479.
12
13. Simons A, Alhanout K, Duval RE. Bacteriocins, antimicrobial peptides from bacterial origin: Overview of their biology and their impact against multidrug-resistant. Bacteria Microorganisms 2020;8.
13
14. Heng NC, Tagg JR. What’s in a name? Class distinction for bacteriocins. Nat Rev Microbiol 2006;4:160.
14
15. Netz DJA, Sahl H-G, Marcolino R, dos Santos Nascimento Jn, de Oliveira SS, Soares MB, et al. Molecular characterisation of aureocin A70, a multi-peptide bacteriocin isolated from Staphylococcus aureus. J Mol Biol 2001;311:939-949.
15
16. Rohani M, Noohi N, Talebi M, Katouli M, Pourshafie MR. Highly heterogeneous probiotic Lactobacillus species in healthy iranians with low functional activities. PLoS One 2015;10: e0144467.
16
17. Kwon H-S, Yang E-H, Yeon S-W, Kang B-H, Kim T-Y. Rapid identification of probiotic Lactobacillus species by multiplex PCR using species-specific primers based on the region extending from 16S rRNA through 23S rRNA. FEMS Microbiol Lett 2004;239:267-275.
17
18. Macwana SJ, Muriana PM. A ‘bacteriocin PCR array’for identification of bacteriocin-related structural genes in lactic acid bacteria. J Microbiol Methods 2012;88:197-204.
18
19. Noohi N, Ebrahimipour G, Rohani M, Talebi M, Pourshafie MR. Phenotypic characteristics and probiotic potentials of Lactobacillus spp. isolated from poultry. Jundishapur J Microbiol 2014;7.
19
20. Lebeer S, Verhoeven TL, Vélez MP, Vanderleyden J, De Keersmaecker SC. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 2007;73:6768-6775.
20
21. Hernandez D, Cardell E, Zarate V. Antimicrobial activity of lactic acid bacteria isolated from Tenerife cheese: initial characterization of plantaricin TF711, a bacteriocin‐like substance produced by Lactobacillus plantarum TF711. J Appl Microbiol 2005;99:77-84.
21
22. Toba T, Samant S, Itoh T. Assay system for detecting bacteriocin in microdilution wells. Lett Appl Microbiol 1991;13:102-104.
22
23. Jacobsen CN, Nielsen VR, Hayford A, Møller PL, Michaelsen K, Paerregaard A, et al. Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 1999;65:4949-4956.
23
24. Drago L, Gismondo MR, Lombardi A, De Haën C, Gozzini L. Inhibition of in vitro growth of enteropathogens by new Lactobacillus isolates of human intestinal origin. FEMS Microbiol Lett 1997;153:455-463.
24
25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 2001;25:402-408.
25
26. Scallan E, Griffin PM, Angulo FJ, Tauxe RV, Hoekstra RM. Foodborne illness acquired in the United States—unspecified agents. Emerg Infect Dis 2011;17:16.
26
27. Zahedi Bialvaei A, Sheikhalizadeh V, Mojathedi A, Irajian G. Epidemiological burden of Listeria monocytogenes in Iran. Iran J Basic Med Sci 2018;21:770-780.
27
28. Murphree R, Garman K, Phan Q, Everstine K, Gould LH, Jones TF. Characteristics of foodborne disease outbreak investigations conducted by Foodborne Diseases Active Surveillance Network (FoodNet) sites, 2003–2008. Arch Clin Infect Dis 2012;54:498-503.
28
29. Zhang L, Wei Q, Han Q, Chen Q, Tai W, Zhang J, et al. Detection of Shigella in milk and clinical samples by magnetic immunocaptured-loop-mediated isothermal amplification assay. Front microbiol 2018;9:94.
29
30. Terpou A, Papadaki A, Lappa IK, Kachrimanidou V, Bosnea LA, Kopsahelis N. Probiotics in food systems: Significance and emerging strategies towards improved viability and delivery of enhanced beneficial value. Nutrients 2019;11:1591.
30
31. Michail S, Abernathy F. Lactobacillus plantarum reduces the in vitro secretory response of intestinal epithelial cells to enteropathogenic Escherichia coli infection. J Pediatr Gastroenterol Nutr 2002;35:350-355.
31
32. Lievin-Le Moal V, Amsellem R, Servin A, Coconnier M. Lactobacillus acidophilus (strain LB) from the resident adult human gastrointestinal microflora exerts activity against brush border damage promoted by a diarrhoeagenic Escherichia coli in human enterocyte-like cells. Gut 2002;50 :803-811.
32
33. Sherman PM, Johnson-Henry KC, Yeung HP, Ngo PS, Goulet J, Tompkins TA. Probiotics reduce enterohemorrhagic Escherichia coli O157: H7-and enteropathogenic E. coli O127: H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect Immun 2005;73:5183-5188.
33
34. Davoodabadi A, Dallal MMS, Lashani E, Ebrahimi MT. Antimicrobial activity of Lactobacillus spp. isolated from fecal flora of healthy breast-fed infants against diarrheagenic Escherichia coli. Jundishapur J Microbiol 2015;8.
34
35. Perez RH, Zendo T, Sonomoto K, editors. Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications. Microb Cell Fact;13:1-3.
35
36. Silva CC, Silva SP, Ribeiro SC. Application of bacteriocins and protective cultures in dairy food preservation. Front Microbiol 2018;9:594.
36
37. Abbasiliasi S, Tan JS, Ibrahim TAT, Bashokouh F, Ramakrishnan NR, Mustafa S, et al. Fermentation factors influencing the production of bacteriocins by lactic acid bacteria: A review. RSC Adv 2017;7:29395-29420.
37
38. Mokoena MP. Lactic acid bacteria and their bacteriocins: classification, biosynthesis and applications against uropathogens: a mini-review. Molecules 2017;22:1255.
38
39. Chanos P, Mygind T. Co-culture-inducible bacteriocin production in lactic acid bacteria. Appl Microbiol Biotechnol 2016;100:4297-308.
39
40. Gobbetti M, De Angelis M, Di Cagno R, Minervini F, Limitone A. Cell–cell communication in food related bacteria. Int J Food Microbiol 2007;120:34-45.
40
41. Diep DB, Straume D, Kjos M, Torres C, Nes IF. An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides 2009;30:1562-1574.
41
42. Acedo JZ, Chiorean S, Vederas JC, van Belkum MJ. The expanding structural variety among bacteriocins from Gram-positive bacteria. FEMS Microbiol Rev 2018;42:805-828.
42
43. Maldonado-Barragán A, West SA. The cost and benefit of quorum sensing-controlled bacteriocin production in Lactobacillus plantarum. J Evol Biol 2020;33:101-111.
43
44. Collins B, Guinane CM, Cotter PD, Hill C, Ross RP. Assessing the contributions of the LiaS histidine kinase to the innate resistance of Listeria monocytogenes to nisin, cephalosporins, and disinfectants. Appl Environ Microbiol 2012;78:2923-2929.
44
45. Maldonado A, Ruiz-Barba JL, Jiménez-Díaz R. Purification and genetic characterization of plantaricin NC8, a novel coculture-inducible two-peptide bacteriocin from Lactobacillus plantarum NC8. Appl Environ Microbiol 2003;69:383-389.
45
46. Diep DB, Johnsborg O, Risøen PA, Nes IF. Evidence for dual functionality of the operon plnABCD in the regulation of bacteriocin production in Lactobacillus plantarum. Mol Microbiol 2001;41:633-644.
46
47. Stoyancheva G, Marzotto M, Dellaglio F, Torriani S. Bacteriocin production and gene sequencing analysis from vaginal Lactobacillus strains. Arch Microbiol 2014;196 :645-653.
47
48. Majhenič A, Venema K, Allison G, Matijašić B, Rogelj I, Klaenhammer T. DNA analysis of the genes encoding acidocin LF221 A and acidocin LF221 B, two bacteriocins produced by Lactobacillus gasseri LF221. Appl Microbiol Biotechnol 2004;63:705-714
48
49. Omar NB, Abriouel H, Lucas R, Martínez-Cañamero M, Guyot J-P, Gálvez A. Isolation of bacteriocinogenic Lactobacillus plantarum strains from ben saalga, a traditional fermented gruel from Burkina Faso. Int J Food Microbiol 2006;112:44-50.
49
50. Kawai Y, Saitoh B, Takahashi O, Kitazawa H, Saito T, Nakajima H, et al. Primary amino acid and DNA sequences of gassericin T, a lactacin F-family bacteriocin produced by Lactobacillus gasseri SBT2055. Biosci Biotechnol Biochem 2000;64:2201-2208.
50
51. Holo H, Jeknic Z, Daeschel M, Stevanovic S, Nes IF. Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology 2001;147:643-651.
51
52. Hata T, Tanaka R, Ohmomo S. Isolation and characterization of plantaricin ASM1: a new bacteriocin produced by Lactobacillus plantarum A-1. Int J Food Microbiol 2010;137:94-99.
52
53. Omar NB, Abriouel H, Keleke S, Valenzuela AS, Martínez-Cañamero M, López RL, et al. Bacteriocin-producing Lactobacillus strains isolated from poto poto, a Congolese fermented maize product, and genetic fingerprinting of their plantaricin operons. Int J Food Microbiol 2008;127:18-25.
53
54. Maldonado-Barragán A, Caballero-Guerrero B, Lucena-Padrós H, Ruiz-Barba JL. Induction of bacteriocin production by coculture is widespread among plantaricin-producing Lactobacillus plantarum strains with different regulatory operons. Food Microbiol 2013;33:40-47.
54
55. Rojo-Bezares B, Saenz Y, Navarro L, Zarazaga M, Ruiz-Larrea F, Torres C. Coculture-inducible bacteriocin activity of Lactobacillus plantarum strain J23 isolated from grape must. Food Microbiol 2007;24:482-491.
55
56. Tichaczek PS, Nissen-Meyer J, Nes IF, Vogel RF, Hammes WP. Characterization of the bacteriocins curvacin A from Lactobacillus curvatus LTH1174 and sakacin P from L. sake LTH673. Syst Appl Microbiol 1992;15:460-468.
56
ORIGINAL_ARTICLE
Intranasal administration of immunogenic poly-epitope from influenza H1N1 and H3N2 viruses adjuvanted with chitin and chitosan microparticles in BALB/c mice
Objective(s): Prevalence of influenza virus, creates the need to achieve an efficient vaccine against it. We examined whether the predicted antigenic epitopes of HA, NP, and M2 proteins of the influenza H1N1 and H3N2 viruses accompanied by chitin and chitosan biopolymers might be relevant to the induction of effective proper mucosal responses. Materials and Methods: The construct was prepared using B and T cell predicted epitopes of HA, NP, and M2 proteins from the influenza H1N1 and H3N2 viruses by considering haplotype “d” as a dominant allele in the BALB/c mice. Intranasal immunization with purified LPS free recombinant protein together with chitin and chitosan microparticles as adjuvants was administered at an interval of 2 weeks in thirty-five BALB/c female mice which were divided into seven groups. Ten days after the last immunization, humoral and cellular immune responses were examined. Results: Elevated systemic IgG2a, IgA, and mucosal IgA revealed a humoral response to the construct. An increase in the number of IFN-γ-producing cells in re-stimulation of splenocytes in the culture medium by poly-tope as well as rise in the concentrations of IL-6, IL-17, and TNF-α along with the regulatory response of IL-10, presented the capacity of the designed protein to provoke significant immune responses. The neutralization test ultimately confirmed the high efficacy of the protein in inhibiting the virus. Conclusion: The results support the fact that immunogenic poly-tope protein in the presence of chitin and chitosan microparticles as mucosal adjuvants is able to induce humoral and cell-mediated responses in BALB/c mice.
https://ijbms.mums.ac.ir/article_18497_fb389047ebed8c53be3c733deddc42c7.pdf
2021-08-01
1126
1137
10.22038/ijbms.2021.58087.12909
Chitin microparticles
Chitosan microparticles
Influenza H1N1 virus
Influenza H3N2 virus
Inhaled vaccine
Sahar
Sadeghi
sadeghis@sbmu.ac.ir
1
Department of Medical Biotechnology, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
AUTHOR
Mojgan
Bandehpour
bandehpour@gmail.com
2
Department of Medical Biotechnology, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
LEAD_AUTHOR
Mostafa
Haji Molla Hoseini
m.mollahoseni@sbmu.ac.ir
3
Department of Immunology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
AUTHOR
Zarin
Sharifnia
zarin.sharifnia@gmail.com
4
Cellular and Molecular Biology Research Center, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
AUTHOR
1. Haji Molla Hoseini M, Sadeghi S, Azizi M, Pouriran R. Immunomodulatory activities of chitin and chitosan microparticles. In: Gopi S, Thomas S, Pius A, editors. Handbook of chitin and chitosan: Chitin- and chitosan-based polymer materials for various applications. 1st ed. Elsevier Inc; 2020. p. 609–639.
1
2. Ichinohe T, Nagata N, Strong P, Tamura S, Takahashi H, Ninomiya A, et al. Prophylactic effects of chitin microparticles on highly pathogenic H5N1 Influenza virus. J Med Virol 2007;79:811–819.
2
3. Fang L, Wolmarans B, Kang M, Jeong KC, Wright AC. Application of chitosan microparticles for reduction of vibrio species in seawater and live oysters (Crassostrea virginica). Appl Environ Microbiol 2015;81:640–647.
3
4. Hasegawa H, Ichinohe T, Strong P, Watanabe I, Ito S, Tamura S, et al. Protection against Influenza virus infection by intranasal administration of hemagglutinin vaccine with chitin microparticles as an adjuvant. J Med Virol 2005;75:130–136.
4
5. Baaten BJG, Clarke B, Strong P, Hou S. Nasal mucosal administration of chitin microparticles boosts innate immunity against Influenza A virus in the local pulmonary tissue. Vaccine 2010;28:4130–4137.
5
6. Muzzarelli R. Chitins and Chitosans as immunoadjuvants and non-allergenic drug carriers. Mar Drugs 2010;8:292–312.
6
7. Ahire VJ, Sawant KK, Doshi JB, Ravetkar SD. Chitosan microparticles as oral delivery system for tetanus toxoid. Drug Dev Ind Pharm 2007;33:1112–1124.
7
8. Wang X, Zhang W, Liu F, Zheng M, Zheng D, Zhang T, et al. Intranasal immunization with live attenuated influenza vaccine plus chitosan as an adjuvant protects mice against homologous and heterologous virus challenge. Arch Virol 2012;157:1451–1461.
8
9. Mann AJ, Noulin N, Catchpole A, Stittelaar KJ, de Waal L, Veldhuis Kroeze EJB, et al. Intranasal H5N1 Vaccines, adjuvanted with chitosan derivatives, protect ferrets against highly pathogenic influenza intranasal and intratracheal challenge. PLoS One 2014 ;9:e93761.
9
10. Elieh-Ali-Komi D, Hamblin MR. Chitin and Chitosan: Production and application of versatile biomedical nanomaterials. Int J Adv Res 2016;4:411–427.
10
11. Qiu X, Duvvuri VR, Bahl J. Computational approaches and challenges to developing universal influenza vaccines. Vaccines 2019;7:45.
11
12. He L, Zhu J. Computational tools for epitope vaccine design and evaluation. Curr Opin Virol 2015;11:103–112.
12
13. Correia BE, Bates JT, Loomis RJ, Baneyx G, Carrico C, Jardine JG, et al. Proof of principle for epitope-focused vaccine design. Nature 2014;507:201–206.
13
14. Bouvier NM, Palese P. The biology of influenza viruses. Vaccine 2008;26:D49–53.
14
15. Sautto GA, Kirchenbaum GA, Ross TM. Towards a universal influenza vaccine: different approaches for one goal. Virol J 2018;15:17.
15
16. Krammer F, Palese P. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 2015;14:167–182.
16
17. Ben-Yedidia T, Arnon R. Epitope-based vaccine against influenza. Expert Rev Vaccines. 2007;6:939–948.
17
18. Chen J-R, Liu Y-M, Tseng Y-C, Ma C. Better influenza vaccines: an industry perspective. J Biomed Sci 2020;27:33.
18
19. Cohen J. Why is the flu vaccine so mediocre? Science 2017;357:1222–1223.
19
20. Ichihashi T, Yoshida R, Sugimoto C, Takada A, Kajino K. Cross-protective peptide vaccine against Influenza A viruses developed in HLA-A*2402 human immunity model. PLoS One 2011;6:e24626.
20
21. Grohskopf LA, Sokolow LZ, Broder KR, Olsen SJ, Karron RA, Jernigan DB, et al. Prevention and control of seasonal influenza with vaccines. MMWR Recomm Rep 2016;65:1–54.
21
22. Cheung Y-K, Cheng SC-S, Ke Y, Xie Y. Two novel HLA-A*0201 T-cell epitopes in avian H5N1 viral nucleoprotein induced specific immune responses in HHD mice. Vet Res 2010;41:24.
22
23. Wang M, Larsen M V., Nielsen M, Harndahl M, Justesen S, Dziegiel MH, et al. HLA class I binding 9mer peptides from Influenza A virus induce CD4+ T cell responses. PLoS One 2010;5:e10533.
23
24. Li W, Joshi M, Singhania S, Ramsey K, Murthy A. Peptide vaccine: Progress and challenges. Vaccines 2014;2:515–536.
24
25. Xia Y, Fan Q, Hao D, Wu J, Ma G, Su Z. Chitosan-based mucosal adjuvants: Sunrise on the ocean. Vaccine 2015;33:5997–6010.
25
26. Skwarczynski M, Toth I. Non-invasive mucosal vaccine delivery: Advantages, challenges and the future. Expert Opin Drug Deliv 2020;17:435–437.
26
27. Marasini N, Skwarczynski M, Toth I. Intranasal delivery of nanoparticle-based vaccines. Ther Deliv 2017;8:151–167.
27
28. Jin Z, Gao S, Cui X, Sun D, Zhao K. Adjuvants and delivery systems based on polymeric nanoparticles for mucosal vaccines. Int J Pharm 2019;572:118731.
28
29. Hashemi H, Pouyanfard S, Bandehpour M, Noroozbabaei Z, Kazemi B, Saelens X, et al. Immunization with M2e-displaying T7 bacteriophage nanoparticles protects against influenza A virus challenge. PLoS One 2012;7: e45765.
29
30. Bello M, Campos-Rodriguez R, Rojas-Hernandez S, Contis-Montes de Oca A, Correa-Basurto J. Predicting peptide vaccine candidates against H1N1 influenza virus through theoretical approaches. Immunol Res 2015;62:3–15.
30
31. Lee Y-TYY-J, Kim K-H, Ko E, Kim M, Kwon Y, Tang Y, et al. New vaccines against influenza virus. Clin Exp Vaccine Res 2014;3:12–28.
31
32. Ekiert DC, Bhabha G, Elsliger M-A, Friesen RHE, Jongeneelen M, Throsby M, et al. Antibody recognition of a highly conserved Influenza virus epitope. Science 2009 ;324:246–251.
32
33. Wu KW, Chien CY, Li SW, King CC, Chang CH. Highly conserved influenza A virus epitope sequences as candidates of H3N2 flu vaccine targets. Genomics 2012;100:102–109.
33
34. Fleri Ward, Paul Sinu, Dhanda Sandeep Kumar, Mahajan Swapnil, Xu Xiaojun, Peters Bjoern and Sette Alessandro. The immune epitope database and analysis resource in epitope discovery and synthetic vaccine design. Front Immunol 2017; 8: 278.
34
35. Klein JS, Jiang S, Galimidi RP, Keeffe JR, Bjorkman PJ. Design and characterization of structured protein linkers with differing flexibilities. Protein Eng Des Sel. 2014;27:325-330.
35
36. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 2015;10: 845-858.
36
37. Grote A, Hiller K, Scheer M, Münch R, Nörtemann B, Hempel DC, Jahn D. JCat: A novel tool to adapt codon usage of a target gene to its potential expression host. Nucleic Acids Res 2005 ;33: W526-31.
37
38. Saadat M, Gandomkar M, Bahrenipour A, Bandehpour M, Kazemi B, Mosaffa N. Evaluation of the designed multi-epitope protein of Brucella melitensis in guinea pigs. Iran J Basic Med Sci 2021; 24: 833-841.
38
39. Verma A, Prasad KN, Singh AK, Nyati KK, Gupta RK, Paliwal VK. Evaluation of the MTT lymphocyte proliferation assay for the diagnosis of neurocysticercosis. J Microbiol Methods 2010;81:175–178.
39
40. Cui LM, Zhang K, Ma DJ, Liu SP, Zhang XW. Protein expression under sustained activation of signal transducer and activator of transcription-3 in diethylnitrosamine-induced rat liver carcinogenesis. Oncol Lett 2014;8:608–614.
40
41. Bahrami AA, Bandehpour M, Khalesi B, Kazemi B. Computational design and analysis of a poly-epitope fusion protein: A new vaccine candidate for Hepatitis and Poliovirus. Int J Pep Res Ther 2020;26:389-403.
41
42. Shibata Y, Foster LA, Metzger WJ, Myrvik QN. Alveolar macrophage priming by intravenous administration of chitin particles, polymers of N-acetyl-D-glucosamine, in mice. Infect Immun 1997;65:1734–1741.
42
43. Hamajima K, Kojima Y, Matsui K, Toda Y, Jounai N, Ozaki T, et al. Chitin micro-particles (CMP): A useful adjuvant for inducing viral specific immunity when delivered intranasally with an hiv-dna vaccine. Viral Immunol 2003;16:541–547.
43
44. Da Silva CA, Chalouni C, Williams A, Hartl D, Lee CG, Elias JA. Chitin is a size-dependent regulator of macrophage TNF and IL-10 production. J Immunol 2009;182:3573–3582.
44
45. Bueter CL, Lee CK, Rathinam VAK, Healy GJ, Taron CH, Specht CA, et al. Chitosan but not chitin activates the inflammasome by a mechanism dependent upon phagocytosis. J Biol Chem 2011;286:35447–35455.
45
46. Da Silva CA, Pochard P, Lee CG, Elias JA. Chitin particles are multifaceted immune adjuvants. Am J Respir Crit Care Med 2010;182:1482–1491.
46
47. Zygmunt BM, Rharbaoui F, Groebe L, Guzman CA. Intranasal immunization promotes Th17 immune responses. J Immunol 2009;183:6933–6938.
47
48. Da Silva CA, Hartl D, Liu W, Lee CG, Elias JA. TLR-2 and IL-17A in chitin-induced macrophage activation and acute inflammation. J Immunol 2008;181:4279–86.
48
49. Jaffar Z, Ferrini ME, Herritt LA, Roberts K. Cutting Edge: Lung mucosal Th17-mediated responses induce polymeric Ig receptor expression by the airway epithelium and elevate secretory IgA levels. J Immunol 2009;182:4507–4511.
49
50. Li M, Wang Y, Sun Y, Cui H, Zhu SJ, Qiu H-J. Mucosal vaccines: Strategies and challenges. Immunol Lett 2020;217:116–125.
50
51. van Baalen CA, Jeeninga RE, Penders GHWM, van Gent B, van Beek R, Koopmans MPG, et al. ViroSpot microneutralization assay for antigenic characterization of human influenza viruses. Vaccine 2017;35:46–52.
51
52. Mosafer J, Sabbaghi AH, Badiee A, Dehghan S, Tafaghodi M. Preparation, characterization and in vivo evaluation of alginate-coated chitosan and trimethylchitosan nanoparticles loaded with PR8 influenza virus for nasal immunization. Asian J Pharm Sci 2019;14:216–221.
52
53. Lebre F, Bento D, Jesus S, Borges O. Chitosan-based nanoparticles as a hepatitis b antigen delivery system. Methods Enzymol. 2012;509:127–142.
53
54. Kerch G. The potential of chitosan and its derivatives in prevention and treatment of age-related diseases. Mar Drugs 2015;13:2158–2182.
54
55. Aranaz I, Mengibar M, Harris R, Panos I, Miralles B, Acosta N, et al. Functional characterization of chitin and chitosan. Curr Chem Biol 2009;3:203–230.
55
ORIGINAL_ARTICLE
Ginkgo biloba leaf extract (EGb-761) elicits neuroprotection against cerebral ischemia/reperfusion injury by enhancement of autophagy flux in neurons in the penumbra
Objective(s): Ginkgo biloba leaf extract (EGb-761) injection has been widely used as adjuvant therapy for cerebral stroke in China. However, its underlying pharmacological mechanism is not completely understood. The present study aimed to investigate whether the therapeutic effects of EGb-761 are exerted by modulating autophagy flux. Materials and Methods: Ischemic cerebral stroke was prepared in male Sprague-Dawley rats by middle cerebral artery occlusion (MCAO) followed by reperfusion. The MCAO/reperfusion rats were then treated with EGb-761 injection once daily for 7 days. Thereafter, the brain tissues in the ischemic penumbra were obtained to detect the key proteins in the autophagic/lysosomal pathway with Beclin1, LC3, (SQSTM1)/p62, ubiquitin, LAMP-1, cathepsin B, and cathepsin D antibodies by western blot and immunofluorescence. Meanwhile, the infarct volume, neurological deficits, and neuronal apoptosis were assessed to evaluate the therapeutic outcomes.Results: The results illustrated that EGb-761 treatment was not only able to promote the autophagic activities of Beclin1 and LC3-II in neurons, but also could enhance the autophagic clearance, as indicated by reinforced lysosomal activities of LAMP-1, cathepsin B, and cathepsin D, as well as alleviating autophagic accumulation of ubiquitin and insoluble p62 in the MCAO+EGb-761 group, compared with those in the MCAO+saline group. Meanwhile, cerebral ischemia-induced neurological deficits, infarct volume, and neuronal apoptosis were significantly attenuated by 7 days of EGb-761 therapy. Conclusion: Our data suggest that EGb-761 injection can elicit a neuroprotective efficacy against MCAO/reperfusion injury, and this neuroprotection may be exerted by enhancement of autophagy flux in neurons in the ischemic penumbra.
https://ijbms.mums.ac.ir/article_18496_89b119a2312b2f37daf5481014fc8307.pdf
2021-08-01
1138
1145
10.22038/ijbms.2021.46318.10694
Autophagy
Enhancement
Ginkgo biloba
Ischemic stroke
Neuroprotection
Deng
Yihao
827821533@qq.com
1
Department of Basic Medicine, Medical School, Kunming University of Science and Technology, Kunming 650500, China
AUTHOR
Guo
Tao
475612496@qq.com
2
Department of Basic Medicine, Medical School, Kunming University of Science and Technology, Kunming 650500, China
AUTHOR
Wu
Zhiyuan
1131014322@qq.com
3
Department of Basic Medicine, Medical School, Kunming University of Science and Technology, Kunming 650500, China
AUTHOR
Zhao
Xiaoming
974464177@qq.com
4
Department of Basic Medicine, Medical School, Kunming University of Science and Technology, Kunming 650500, China
AUTHOR
Dong
Lingling
1213679564@qq.com
5
Department of Basic Medicine, Medical School, Kunming University of Science and Technology, Kunming 650500, China
AUTHOR
He
Hongyun
18487158200@163.com
6
Department of Basic Medicine, Medical School, Kunming University of Science and Technology, Kunming 650500, China
LEAD_AUTHOR
1. Feigin VL, Vos T. Global burden of neurological disorders: from global burden of disease estimates to actions. Neuroepidemiology 2019;52:1-2.
1
2. Meschia JF, Brott T. Ischemic stroke. Eur J Neurol 2018;25:35-40.
2
3. Sun H, Zou X, Liu L. Epidemiological factors of stroke: A survey of the current status in China. J Stroke. 2013;15:109-114.
3
4. Bano D, Ankarcrona M. Beyond the critical point: An overview of excitotoxicity, calcium overload and the downstream consequences. Neurosci Lett. 2018;663:79-85.
4
5. Radak D, Katsiki N, Resanovic I, Jovanovic A, Sudar-Milovanovic E, Zafirovic S, et al. Apoptosis and acute brain ischemia in ischemic stroke. Curr Vasc Pharmacol 2017;15:115-122.
5
6. Khoshnam SE, Winlow W, Farzaneh M, Farbood Y, Moghaddam HF. Pathogenic mechanisms following ischemic stroke. Neurol Sci 2017;38:1167-1186.
6
7. Leng T, Xiong ZG. Treatment for ischemic stroke: From thrombolysis to thrombectomy and remaining challenges. Brain Circ 2019;5:8-11.
7
8. Yuh WT, Alexander MD, Ueda T, Maeda M, Taoka T, Yamada K, et al. Revisiting current goldens rules in managing scute ischemic stroke: evaluation of new dtrategies to further improve treatment selection and outcome. AJR Am Roentgenol 2017;208:32-41.
8
9. Nash KM, Shah ZA. Current perspectives on the beneficial role of Ginkgo biloba in neurological and cerebrovascular disorders. Integr Med Insights 2015;10:1-9.
9
10. Chau FT, Chan HY, Cheung CY, Xu CJ, Liang Y, Kvalheim OM. Recipe for uncovering the bioactive components in herbal medicine. Anal Chem 2009;81:7217-7225.
10
11. Van Beek TA, Montoro P. Chemical analysis and quality control of Ginkgo biloba leaves, extracts, and phytopharmaceuticals. J Chromatoqr A 2009;1216:2002-2032.
11
12. Mohanta TK, Tamboli Y, Zubaidha PK. Phytochemical and medicinal importance of Ginkgo biloba L. Nat Prod Res 2014;28:746-752.
12
13. Liu H, Ye M, Guo H. An updated review of randomized clinical trials testing the improvement of cognitive function of Ginkgo biloba extract in healthy people and alzheimer’s patients. Front Pharmacol. 2020;10:1688.
13
14. Savaskan E, Mueller H, Hoerr R, von Gunten A, Gauthier S. Treatment effects of Ginkgo biloba extract EGb 761® on the spectrum of behavioral and psychological symptoms of dementia: meta-analysis of randomized controlled trials. Int Psychogeriatr 2018;30:285-293.
14
15. Hosseini-Sharifabad M, Anvari M. Effects of Ginkgo biloba extract on the structure of Cornu Ammonis in aged rat: a morphometric study. Iran J Basic Med Sci 2015;18:932–937.
15
16. Zhou X, Qi Y, Chen T. Long-term pre-treatment of anti-oxidant Ginkgo biloba extract EGb-761 attenuates cerebral ischemia-induced neuronal damage in aged mice. Biomed Pharmacother 2017;85:256-263.
16
17. Chandrasekaran K, Mehrabian Z, Spinnewyn B, Chinopoulos C, Drieu K, Fiskum G. Neuroprotective effects of bilobalide, a component of Ginkgo biloba extract (Egb 761) in global brain ischemia and in excitotoxicity-induced neuronal death. Pharmacopsychiatry 2003;36:89-94.
17
18. Liu Y, Wu X, Yu Z. Ginkgo leaf extract and dipyridamole injection as adjuvant treatment for acute cerebral infarction: Protocol for systemic review and meta-analysis of randomized controlled trials. Medicine (Baltimore). 2019;98:e14643.
18
19. Oskouei DS1, Rikhtegar R, Hashemilar M, Sadeghi-Bazargani H, Sharifi-Bonab M, Sadeghi-Hokmabadi E, et al. The effect of Ginkgo biloba on functional outcome of patients with acute ischemic stroke: a double-blind, placebo-controlled, randomized clinical trial. J Stroke Cerebrovasc Dis 2013;22:e557-563.
19
20. Doherty J, Baehrecke EH. Life, death and autophagy. Nat Cell Biol 2018;20:1110-1117.
20
21. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol 2010;221:3-12.
21
22. Hou K, Xu D, Chen S. The progress of neuronal autophagy in cerebral ischemia stroke: Mechanisms, roles and research methods. J Neurol Sci 2019;400:72-82.
22
23. Chen W, Sun Y, Liu K, Sun X. Autophagy: A double-edged sword for neuronal survival after cerebral ischemia. Neural Regen Res 2014;9:1210-1216.
23
24. Beard DJ, Hadley G, Thurley N, Howells DW, Sutherland BA, Buchan AM. The effect of rapamycin treatment on cerebral ischemia: A systematic review and meta-analysis of animal model studies. Int J Stroke 2019;14:137-145.
24
25. Ni Y, Gu WW, Liu ZH, Zhu YM, Rong JG, Kent TA, et al. RIP1K contributes to neuronal and astrocytic cell death in ischemic stroke via activating autophagic-lysosomal pathway. Neuroscience 2018;371:60-74.
25
26. Zhi X, Feng W, Rong Y, Liu R. Anatomy of autophagy: from the beginning to the end. Cell Mol Life Sci. 2018;75:815-831.
26
27. Lahiri V, Hawkins WD, Klionsky DJ. Watch what you (self-) eat: Autophagic mechanisms that modulate metabolism. Cell Metab 2019;29:803-826.
27
28. Yu L, Chen Y, Tooze SA. Autophagy pathway: Cellular and molecular mechanisms. Autophagy 2018;14:207-215.
28
29. Liu Y, Xue X, Zhang H, Che X, Luo J, Wang P, et al. Neuronal-targeted TFEB rescues dysfunction of the autophagy-lysosomal pathway and alleviates ischemic injury in permenent cerebral ishcemia. Autophagy 2019;15:493-509.
29
30. He HY, Ren L, Guo T, Deng YH. Neuronal autophagy aggravates microglia inflammatory injury by downregulating CX3CL1/fractalkine after ischemic stroke. Neural Regen Res 2019;14:280-288.
30
31. Zheng Y, Wu Z, Yi F, Orange M, Yao M, Yang B, et al. By Activating Akt/eNOS Bilobalide B inhibits autophagy and promotes angiogenesis following focal cerebral ischemia reperfusion. Cell Physio Biochem 2018;47:604-616.
31
32. Chen XP, Zhang X, Liao WJ, Wang Q. Effect of physical and social components of enriched environment on astrocytes proliferation in rats after cerebral ischaemia/reperfusion injury. Neurochem Res 2017;42:1308-1316.
32
33. Li MZ, Zhang Y, Zou HY, Ouyang JY, Zhang Y, Yang L, et al. Investigation of Ginkgo biloba extract (Egb 761) promotes neurovascular restoration and axonal remodeling after embolic stroke in rat using magnetic resonance imaging and histopathological analysis. Biomed Pharmacother 2018;103:989-1001.
33
34. Zeng GR, Zhou SD, Shao YJ, Zhang MH, Dong LM, Lv JW, et al. Effect of Ginkgo biloba extract-761 on motor functions in permanent middle cerebral artery occlusion rats. Phytomedicine 2018;48:94-103.
34
35. Yin B, Xu Y, Wei R, Luo B. Ginkgo biloba on focal cerebral ischemia: a systematic review and meta-analysis. Am J Chin Med 2014;42:769-783.
35
36. Li S, Zhang X, Fang Q, Zhou J, Zhang M, Wang H, et al. Ginkgo biloba extract improved cognitive and neurological functions of acute ischemic stroke: a randomised controlled trial. Stroke Vasc Neurol 2017;2:189-197.
36
37. Chong PZ, Ng HY, Tai JT, Lee SWH. Efficacy and safety of Ginkgo biloba in patients with acute ischemic stroke: A systematic review and meta-analysis. Am J Chin Med 2020;48:513-534.
37
38. Liang ZH, Jia YB, Wang ML, Li ZR, Li M, Yun YL, et al. Efficacy of ginkgo biloba extract as augmentation of venlafaxine in treating post-stroke depression. Neuropsychiatr Dis Treat 2019;15:2551-2557.
38
39. Wolf MS, Bayir H, Kochanek PM, Clark RSB. The role of autophagy in acute brain injury: A state of flux? Neurobiol Dis 2019;122:9-15.
39
40. Sun Y, Zhu Y, Zhong X, Chen X, Wang J, Ying G, et al. Crosstalk between autophagy and cerebral ischemia. Front Neurosci 2019;12:1022.
40
41. Zhang X, Yan H, Yuan Y, Gao J, Shen Z, Cheng Y, et al. Cerebral ischemia-reperfusion-induced autophagy protects against neuronal injury by mitochondrial clearance. Autophagy 2013;9:1321-1333.
41
42. Morselli E, Tasdemir E, Maiuri MC, Galluzzi L, Kepp O, Criollo A, et al. Mutant p53 protein localized in the cytoplasm inhibits autophagy. Cell Cycle 2008;7:3056-3061.
42
43. Mo Y, Sun YY, Liu KY. Autophagy and inflammation in ischemic stroke. Neural Regen Res 2020;15:1388-1396.
43
44. Parzych KR, Klionsky DJ. An overview of autophagy: morphology, mechanism, and regulation. Anti-oxid Redox Signal 2014;20:460-473.
44
45. Dai S, Xu Q, Liu S, Yu B, Liu J, Tang J. Role of autophagy and its signaling pathways in ischemia/reperfusion injury. Am J Transl Res 2017;9:4470-4480.
45
46. Eskelinen EL. Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol Aspects Med 2006;27:495-502.
46
47. Kaminskyy V, Zhivotovsky B. Proteases in autophagy. Biochim Biophys Acta 2012;1824: 44-50.
47
48. Wang T, Zhao N, Peng L, Li Y, Huang X, Zhu J, et al. DJ-1 regulates microglial polarization through P62-mediated TRAF6/IRF5 signaling in cerebral ischemia-reperfusion. Front Cell Dev Biol 2020;8:593890.
48
49. Hochrainer K. Protein modifications with ubiquitin as response to rerebral ischemia-reperfusion injury. Transl Stroke Res 2018;9:157-173.
49
50. Cui DR, Sun DW, Wang XT, Yi LY, Kulikowicz E, Reyes M, et al. Impaired autophagyosome clearance contributes to neuronal death in a piglet model of neonatal hypoxic-ischemic encephalopathy. Cell Death Dis 2017;8:e2919.
50
51. Zhang Y, Liu J, Yang B, Zheng Y, Yao M, Sun M, et al. Ginkgo biloba extract inhibits astrocytic lipocalin-2 expression and alleviates neuroinflammatory injury via the JAKS/STAT3 pathway after ischemic brain stroke. Front Pharmacol 2018;9:518.
51
52. Demarin V, BasicKes V, Trkanjec Z, Budisic M, Bosniak Pasic M, CmacP, et al. Efficacy and safety of Ginkgo biloba standardized extract in the treatment of vascular cognitive impairment: a randomized, double-blind, placebo-controlled clinical trial. Neuropsychiatr Dis Treat 2017;13:483-490.
52
ORIGINAL_ARTICLE
Combination of s-methyl cysteine and protocatechuic acid provided greater lipid-lowering and anti-inflammatory effects in mice liver against chronic alcohol consumption
Objective(s): Protective effects of s-methyl cysteine (SMC) alone, protocatechuic acid (PCA) alone, and SMC plus PCA against chronic ethanol consumption induced hepatic steatosis and inflammation were investigated. Materials and Methods: Mice were divided into six groups: normal diet (ND) group, Lieber-DeCarli liquid diet without ethanol (LD diet) group, LD diet with ethanol (LED diet) group, SMC group (LED diet plus 0.25% SMC), PCA group (LED diet plus 0.25% PCA), and SMC+PCA group (LED diet plus 0.125% SMC + 0.125% PCA). After 8 weeks of supplementation, blood and liver were used for analysis. Results: Biochemical and histological data showed that SMC plus PCA led to a greater reduction in lipid droplets in the liver than SMC or PCA treatment alone. SMC plus PCA resulted in greater suppression in hepatic mRNA expression of peroxisome proliferator-activated receptor-gamma, sterol regulatory element-binding protein 1c, stearoyl-CoA desaturase-1, cyclooxygenase-2, and myeloperoxidase than SMC or PCA treatment alone. SMC plus PCA led to a greater decrease in hepatic reactive oxygen species and inflammatory cytokine levels than SMC or PCA treatment alone. Conclusion: These novel findings suggest that the combination of SMC and PCA was a potent remedy for alcoholic liver disorders.
https://ijbms.mums.ac.ir/article_18418_c699e09113f50fe8aede6f14678c9688.pdf
2021-08-01
1146
1152
10.22038/ijbms.2021.56705.12660
Ethanol Hepatic steatosis Myeloperoxidase Protocatechuic acid S
methyl cysteine
Chun-Che
Lin
d83949@mail.cmuh.org.tw
1
Center for Digestive Medicine, China Medical University Hospital, China Medical University, Taichung, Taiwan
AUTHOR
Ya-Chen
Yang
yachenyang@asia.edu.tw
2
Department of Food Nutrition and Health Biotechnology, Asia University, Taichung, Taiwan
AUTHOR
Chia-Yu
Chen
d00207@auh.org.tw
3
Department of Gastroenterology, Asia University Hospital, Taichung, Taiwan
AUTHOR
Mei-Chin
Yin
mcyin@hotmail.com.tw
4
Department of Food Nutrition and Health Biotechnology, Asia University, Taichung, Taiwan
LEAD_AUTHOR
1. Purohit V, Gao B, Song BJ. Molecular mechanisms of alcoholic fatty liver. Alcohol Clin Exp Res 2009; 33:191-205.
1
2. Wang Z, Yao T, Song Z. Chronic alcohol consumption disrupted cholesterol homeostasis in rats: Down-regulation of low-density lipoprotein receptor and enhancement of cholesterol biosynthesis pathway in the liver. Alcohol Clin Exp Res 2010; 34:471-478.
2
3. van Rooy MJ, Pretorius E. Obesity, hypertension and hypercholesterolemia as risk factors for atherosclerosis leading to ischemic events. Curr Med Chem 2014; 21:2121-2129.
3
4. Boyle M, Masson S, Anstee QM. The bidirectional impacts of alcohol consumption and the metabolic syndrome: Cofactors for progressive fatty liver disease. J Hepatol 2018; 68:251-267.
4
5. Lopes PC, Fuhrmann A, Sereno J, Espinoza DO, Pereira MJ, Eriksson JW, et al. Short and long term in vivo effects of cyclosporine A and sirolimus on genes and proteins involved in lipid metabolism in Wistar rats. Metabolism 2014; 63:702-715.
5
6. Chiu CY, Chan IL, Yang TH, Liu SH, Chiang MT. Supplementation of chitosan alleviates high-fat diet-enhanced lipogenesis in rats via adenosine monophosphate (AMP)-activated protein kinase activation and inhibition of lipogenesis-associated genes. J Agric Food Chem 2015; 63:2979-2988.
6
7. Araújo Júnior RF, Garcia VB, Leitão RF, Brito GA, Miguel Ede C, Guedes PM, et al. Carvedilol improves inflammatory response, oxidative stress and fibrosis in the alcohol-induced liver injury in rats by regulating kuppfer cells and hepatic stellate cells. PLoS One 2016; 11: e0148868.
7
8. Hasanein P, Seifi R. Beneficial effects of rosmarinic acid against alcohol-induced hepatotoxicity in rats. Can J Physiol Pharmacol 2018; 96:32-37.
8
9. Mehta AJ, Guidot DM. Alcohol abuse, the alveolar macrophage and pneumonia. Am J Med Sci 2012; 343:244-247.
9
10. Eid N, Ito Y, Otsuki Y. Ethanol-induced hepatic autophagy: Friend or foe? World J Hepatol 2015; 7:1154-1156.
10
11. Yan SL, Yin MC. Protective and alleviative effects from four cysteine-containing compounds on ethanol-induced acute liver injury through suppression of oxidation and inflammation. J Food Sci 2007; 72:511-515.
11
12. Lin CC, Yin MC. Effects of cysteine-containing compounds on biosynthesis of triacylglycerol and cholesterol and anti-oxidative protection in liver from mice consuming a high-fat diet. Br J Nutr 2008; 99:37-43.
12
13. Lin WL, Hsieh YJ, Chou FP, Wang CJ, Cheng MT, Tseng TH. Hibiscus protocatechuic acid inhibits lipopolysaccharide-induced rat hepatic damage. Arch Toxicol 2003; 77:42-47.
13
14. Yüksel M, Yıldar M, Başbuğ M, Çavdar F, Çıkman Ö, Akşit H, et al. Does protocatechuic acid, a natural anti-oxidant, reduce renal ischemia reperfusion injury in rats? Ulus Travma Acil Cerrahi Derg 2017; 23:1-6.
14
15. Liu WH, Lin CC. Wang ZH, Mong MC, Yin MC. Effects of protocatechuic acid on trans fat induced hepatic steatosis in mice. J Agric Food Chem 2010; 58:10247-10252.
15
16. Radhiga T, Sundaresan A, Viswanathan P, Pugalendi KV. Effect of protocatechuic acid on lipid profile and DNA damage in D-galactosamine-induced hepatotoxic rats. J Basic Clin Physiol Pharmacol 2016; 27:505-514.
16
17. Farombi EO, Adedara IA, Awoyemi OV, Njoku CR, Micah GO, Esogwa CU, et al. Dietary protocatechuic acid ameliorates dextran sulphate sodium-induced ulcerative colitis and hepatotoxicity in rats. Food Funct 2016; 7:913-921.
17
18. Kumral A, Giriş M, Soluk-Tekkeşin M, Olgaç V, Doğru-Abbasoğlu S, Türkoğlu Ü, et al. Beneficial effects of carnosine and carnosine plus vitamin E treatments on doxorubicin-induced oxidative stress and cardiac, hepatic, and renal toxicity in rats. Hum Exper Toxicol 2016; 35:635-643.
18
19. Chou IC, Mong MC, Lin CL, Yin MC. Greater protective potent of s-methyl cysteine and syringic acid combination for NGF-differentiated PC12 cells against kainic acid-induced injury. Int J Med Sci 2019; 16:1180-1187.
19
20. Motamedi Z, Amini SA, Raeisi E, Lemoigne Y, Heidarian E. Combined effects of protocatechuic acid and 5-fluorouracil on p53 gene expression and apoptosis in gastric adenocarcinoma cells. Turk J Pharm Sci 2020; 17:578-585.
20
21. Ren H, Wang D, Zhang L, Kang X, Li Y, Zhou X, et al. Catalpol induces autophagy and attenuates liver steatosis in ob/ob and high-fat diet-induced obese mice. Aging (Albany NY) 2019; 11:9461-9477.
21
22. da Silva-Santi LG, Antunes MM, Caparroz-Assef SM, Carbonera F, Masi LN, Curi R, et al. Liver fatty acid composition and inflammation in mice fed with high-carbohydrate diet or high-fat diet. Nutrients 2016; 2008:135625.
22
23. Wong T, Dang K, Ladhani S, Singal AK, Wong RJ. Prevalence of alcoholic fatty liver disease among adults in the United States, 2001-2016. JAMA 2019; 321:1723-1725.
23
24. Saito S, Kawabata J. Synergistic effects of thiols and amines on antiradical efficiency of protocatechuic acid. J Agric Food Chem 2014; 52: 8163-8168.
24
25. Lieber CS. Alcoholic fatty liver: its pathogenesis and mechanism of progression to inflammation and fibrosis. Alcohol 2004; 34:9-19.
25
26. Gu J, Zhang Y, Xu D, Zhao Z, Zhang Y, Pan Y, et al. Ethanol-induced hepatic steatosis is modulated by glycogen level in the liver. J Lipid Res 2015; 56:1329-1339.
26
27. Nan YM, Wang RQ, Fu N. Peroxisome proliferator-activated receptor alpha, a potential therapeutic target for alcoholic liver disease. World J Gastroenterol 2014; 20:8055-8060.
27
28. Gebhardt R. Metabolic zonation of the liver regulation and implications for liver function. Pharmacol Ther 1992; 53:275-354.
28
29. Braeuning A, Ittrich C, Köhle C, Hailfinger S, Bonin M, Buchmann A, et al. Differential gene expression in periportal and perivenous mouse hepatocytes. FEBS J 2006; 273:5051-5061.
29
30. Louvet A, Mathurin P. Alcoholic liver disease: mechanisms of injury and targeted treatment. Nat Rev Gastroenterol Hepatol 2015; 12:231-242.
30
31. Sim WC, Yin HQ, Choi HS, Choi YJ, Kwak HC, Kim SK, et al. L-serine supplementation attenuates alcoholic fatty liver by enhancing homocysteine metabolism in mice and rats. J Nutr 2015;145:260-267.
31
32. Thomas S, Senthilkumar GP, Sivaraman K, Bobby Z, Paneerselvam S, Harichandrakumar KT. Effect of s-methyl-L-cysteine on oxidative stress, inflammation and insulin resistance in male wistar rats fed with high fructose diet. Iran J Med Sci 2015; 40:45-50.
32
33. Safaeian L, Hajhashemi V, Haghjoo Javanmard S, Sanaye Naderi H. The effect of protocatechuic acid on blood pressure and oxidative stress in glucocorticoid-induced hypertension in rat. Iran J Pharm Res 2016; 15:83-91.
33
34. Albano E. Free radical mechanisms in immune reactions associated with alcoholic liver disease. Free Radical Biol Med 2002; 32:110-114.
34
35. Guo R, Xu X, Babcock SA, Zhang Y, Ren J. Aldehyde dedydrogenase-2 plays a beneficial role in ameliorating chronic alcohol-induced hepatic steatosis and inflammation through regulation of autophagy. J Hepatol 2015; 62:647-656.
35
36. Wang D, Gao Q, Wang T, Zhao G, Qian F, Huang J, et al. Green tea infusion protects against alcoholic liver injury by attenuating inflammation and regulating the PI3K/Akt/eNOS pathway in C57BL/6 mice. Food Funct 2017; 8:3165-3177.
36
37. Lee HP, Wu YC, Chen BC, Liu SC, Li TM, Huang WC, et al. Soya-cerebroside reduces interleukin production in human rheumatoid arthritis synovial fibroblasts by inhibiting the ERK, NF-kappa B and AP-1 signalling pathways. Food Agric Immunol 2020; 31:740-750.
37
38. Klebanoff SJ. Myeloperoxidase: friend and foe. J Leukoc Biol 2005; 77:598-625.
38
39. Loria V, Dato I, Graziani F, Biasucci L. Myeloperoxidase: A new biomarker of inflammation in ischemic heart disease and acute coronary syndromes. Mediat Inflamm 2008; 8:682.
39
40. Rezaee-Khorasany A, Razavi BM, Taghiabadi E, Tabatabaei Yazdi A, Hosseinzadeh H. Effect of crocin, an active saffron constituent, on ethanol toxicity in the rat: histopathological and biochemical studies. Iran J Basic Med Sci 2020; 23:51-62.
40
41. Hosseini SM, Taghiabadi E, Abnous K, Hariri AT, Pourbakhsh H, Hosseinzadeh H. Protective effect of thymoquinone, the active constituent of Nigella sativa fixed oil, against ethanol toxicity in rats. Iran J Basic Med Sci 2017; 20:927-939.
41
ORIGINAL_ARTICLE
Dystrophin gene editing by CRISPR/Cas9 system in human skeletal muscle cell line (HSkMC)
Objective(s): Duchene muscular dystrophy (DMD) is a progressive neuromuscular disease caused by mutations in the DMD gene, resulting in the absence of dystrophin expression leading to membrane fragility and myofibril necrosis in the muscle cells. Because of progressive weakness in the skeletal and cardiac muscles, premature death is inevitable. There is no curative treatment available for DMD. In recent years, advances in genetic engineering tools have made it possible to manipulate gene sequences and accurately modify disease-causing mutations. CRISPR/Cas9 technology is a promising tool for gene editing because of its ability to induce double-strand breaks in the DNA. Materials and Methods: In this study for the exon-skipping approach, we designed a new pair of guide RNAs (gRNA) to induce large deletion of exons 48 to 53 in the DMD gene in the human skeletal muscle cell line (HSkMC), in order to correct the frame of the gene.Results: Data showed successful editing of DMD gene by deletion of exons 48 to 53 and correction of the reading frame in edited cells. Despite a large deletion in the edited DMD gene, the data of real-time PCR, immune florescent staining demonstrated successful expression of truncated dystrophin in edited cells.Conclusion: This study demonstrated that the removal of exons 48-53 by the CRISPR / Cas9 system did not alter the expression of the DMD gene due to the preservation of the reading frame of the gene.
https://ijbms.mums.ac.ir/article_18498_d988ada858f045a656efe749ff211929.pdf
2021-08-01
1153
1158
10.22038/ijbms.2021.54711.12269
CRISPR/Cas9
DMD
Dystrophin
Gene editing
HSkMC
Mahintaj
Dara
dara.mahintaj@gmail.com
1
Department of Molecular Medicine, School of Advanced Medical Science and Technology, Shiraz University of Medical Science, Shiraz, Iran
AUTHOR
vahid
razban
razban_vahid@yahoo.com
2
Department of Molecular Medicine, School of Advanced Medical Science and Technology, Shiraz University of Medical Science, Shiraz, Iran
AUTHOR
Mohsen
Mazloomrezaei
mmrezaei@sums.ac.ir
3
Student Research Committee, Shiraz University of Medical Science, Shiraz, Iran
AUTHOR
Maryam
Ranjbar
maryamranjbar845@yahoo.com
4
Department of Medical Genetics, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
AUTHOR
Marjan
Nourigorji
mnourigorj@gmail.com
5
Department of Medical Genetics, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
AUTHOR
Mehdi
Dianatpour
darvak9@gmail.com
6
Department of Medical Genetics, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
LEAD_AUTHOR
1. Falzarano M, Scotton C, Passarelli C, Ferlini A. Duchenne muscular dystrophy: From diagnosis to therapy. J Molecules 2015; 20:18168-18184.
1
2. Ryder S, Leadley R, Armstrong N, Westwood M, De Kock S, Butt T, et al. The burden, epidemiology, costs and treatment for Duchenne muscular dystrophy: An evidence review. Orphanet J Rare Dis 2017; 12:1-21.
2
3. Aartsma-Rus A, Ginjaar IB, Bushby K. The importance of genetic diagnosis for Duchenne muscular dystrophy. World J Med Genet 2016; 53:145-151.
3
4. Walter MC, Reilich P. Recent developments in Duchenne muscular dystrophy: facts and numbers. J Cachexia Sarcopenia Muscle 2017; 8:681-685.
4
5. Garry DJ. Dystrophin-deficient cardiomyopathy. JACC CardioOncol 2016; 67: 2533-2546.
5
6. Birnkrant DJ, Bushby K, Bann CM, Alman BA, Apkon SD, Blackwell A, et al. Diagnosis and management of Duchenne muscular dystrophy, part 2: respiratory, cardiac, bone health, and orthopaedic management. Lancet Neurol 2018; 17:347-361.
6
7. Nelson CE, Gersbach CA. Genome editing for duchenne muscular dystrophy. Mus Gen Thera: Springer 2019; 2; 383-403.
7
8. Suthar R, Sankhyan N. Duchenne muscular dystrophy: A practice update. Indian J Pediatr 2018; 85: 276-281.
8
9. White S, Kalf M, Liu Q, Villerius M, Engelsma D, Kriek M, et al. Comprehensive detection of genomic duplications and deletions in the DMD gene, by use of multiplex amplifiable probe hybridization. Am J Hum Genet 2003; 71:365-371.
9
10. Hegde MR, Chin EL, Mulle JG, Okou DT, Warren ST, Zwick ME. Microarray‐based mutation detection in the dystrophin gene. Hum Mutat 2008; 29:1091-1099.
10
11. Andrews JG, Wahl RA. Duchenne and Becker muscular dystrophy in adolescents: current perspectives. Adolesc Health Med Ther 2018; 9:53-63.
11
12. Crone M, Mah JK. Current and emerging therapies for Duchenne muscular dystrophy. Curr Treat Options Neurol 2018; 20:1-17.
12
13. Shimizu-Motohashi Y, Komaki H, Motohashi N, Takeda Si, Yokota T, Aoki Y. Restoring dystrophin expression in Duchenne muscular dystrophy: current status of therapeutic approaches. J Pers Med 2019; 9:1-14.
13
14. Salmaninejad A, Valilou SF, Bayat H, Ebadi N, Daraei A, Yousefi M, et al. Duchenne muscular dystrophy: an updated review of common available therapies. Int J Neurosci 2018; 128:854-864.
14
15. Guiraud S, Chen H, Burns DT, Davies KE. Advances in genetic therapeutic strategies for Duchenne muscular dystrophy. Ex Physiol 2015; 100:1458-1467.
15
16. Jarmin S, Kymalainen H, Popplewell L, Dickson G. New developments in the use of gene therapy to treat Duchenne muscular dystrophy. Expert Opin Biol Ther 2014; 14:209-230.
16
17. Mendell JR, Rodino-Klapac LR. Duchenne muscular dystrophy: CRISPR/Cas9 treatment. Cell res 2016; 26:513-514.
17
18. Aartsma‐Rus A, Fokkema I, Verschuuren J, Ginjaar I, Van Deutekom J, van Ommen GJ, et al. Theoretic applicability of antisense‐mediated exon skipping for duchenne muscular dystrophy mutations. Hum Muta 2009; 30:293-299.
18
19. Xu L, Park KH, Zhao L, Xu J, El Refaey M, Gao Y, et al. CRISPR-mediated genome editing restores dystrophin expression and function in mdx mice. Mol Thera 2016; 24:564-569.
19
20. Gee P, Xu H, Hotta A. Cellular reprogramming, genome editing, and alternative CRISPR Cas9 technologies for precise gene therapy of Duchenne muscular dystrophy. Stem Cells Int 2017; 9:1-12.
20
21. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 2013; 8:2281-2308.
21
22. Terns MP, Terns RM. CRISPR-based adaptive immune systems. Curr Opin Microbiol 2011; 14:321-327.
22
23. Barrangou R. Cas9 targeting and the CRISPR revolution Sci 2014;344(6185):707-708.
23
24. Jiang F, Doudna JA. CRISPR–Cas9 structures and mechanisms. Annu Rev Biophys 2017; 46:505-529.
24
25. Thurtle‐Schmidt DM, Lo TW. Molecular biology at the cutting edge: A review on CRISPR/Cas9 gene editing for undergraduates. Biochem Mol Biol Educ 2018; 46:195-205.
25
26. Farboud B, Severson AF, Meyer BJ. Strategies for efficient genome editing using CRISPR-Cas9.J Genet 2019;211:431-457.
26
27. Lindahl T, Barnes D, editors. Repair of endogenous DNA damage. Cold Spring Harb Symp Quant Biol 2000: Cold Spring Harbor Laboratory Press.
27
28. Adli M. The CRISPR tool kit for genome editing and beyond. Nat Commun 2018;9: 1-13.
28
29. Frontera WR, Ochala J. Skeletal muscle: A brief review of structure and function. Calcif Tissue Int 2015; 96:183-195.
29
30. Hotta A. Genome editing gene therapy for duchenne muscular dystrophy. J Neuromuscul Dis 2015; 2:343-345.
30
31. Rando TA. Non-viral gene therapy for Duchenne muscular dystrophy: Progress and challenges. Biochim Biophys Acta Mol Basis Dis 2007; 1772:263-271.
31
32. Bertoni C, Morris GE, Rando TA. Strand bias in oligonucleotide-mediated dystrophin gene editing. Hum Mol Genet 2004; 14:221-233.
32
33. Ousterout DG, Kabadi AM, Thakore PI, Perez-Pinera P, Brown MT, Majoros WH, et al. Correction of dystrophin expression in cells from Duchenne muscular dystrophy patients through genomic excision of exon 51 by zinc finger nucleases. Mol Thera 2015; 23:523-532.
33
34. Ousterout DG, Perez-Pinera P, Thakore PI, Kabadi AM, Brown MT, Qin X, et al. Reading frame correction by targeted genome editing restores dystrophin expression in cells from Duchenne muscular dystrophy patients. Mol Thera 2013; 21:1718-1726.
34
35. Tabebordbar M, Zhu K, Cheng JK, Chew WL, Widrick JJ, Yan WX, et al. In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Sci 2016; 351:407-411.
35
36. Min Y-L, Li H, Rodriguez-Caycedo C, Mireault AA, Huang J, Shelton JM, et al. CRISPR-Cas9 corrects Duchenne muscular dystrophy exon 44 deletion mutations in mice and human cells. Sci adv 2019;5-3:324-336.
36
37. Young CS, Hicks MR, Ermolova NV, Nakano H, Jan M, Younesi S, et al. A single CRISPR-Cas9 deletion strategy that targets the majority of DMD patients restores dystrophin function in hiPSC-derived muscle cells. J Stem Cell 2016; 18:533-540.
37
38. Fortunato F, Rossi R, Falzarano MS, Ferlini A. Innovative Therapeutic Approaches for Duchenne Muscular Dystrophy. J Clin Med 2021; 10:820-841.
38
39. Babačić H, Mehta A, Merkel O, Schoser B. CRISPR-cas gene-editing as plausible treatment of neuromuscular and nucleotide-repeat-expansion diseases: A systematic review. PloS One 2019;14: e0212198.
39
40. Chemello F, Bassel-Duby R, Olson EN. Correction of muscular dystrophies by CRISPR gene editing. J Clin Invest 2020; 130:2766-2776.
40
41. Dara M, Razban V, Talebzadeh M, Moradi S, Dianatpour M. Using CRISPR/Cas9 system to knock out exon 48 in DMD gene. Avicenna J Med Biotechnol 2021; 13:54-57.
41
42. Salmaninejad A, Jafari Abarghan Y, Bozorg Qomi S, Bayat H, Yousefi M, Azhdari S, et al. Common therapeutic advances for Duchenne muscular dystrophy (DMD). Int J Neurosci 2020:1-20.
42
43. Dokholyan NV. Experimentally-driven protein structure
43
modeling. J Proteomics 2020; 220:103777-103800.
44
44. Hillary VE, Ceasar SA, Ignacimuthu S. Genome engineering in insects: focus on the CRISPR/Cas9 system. In: Genome engineering via CRISPR-Cas9 system: Academic Press 2020; 1:219-249.
45
45. Knott GJ, Doudna JA. CRISPR-Cas guides the future of genetic engineering. Science 2018; 361:866-869.
46
46. Koeks Z, Bladen CL, Salgado D, Van Zwet E, Pogoryelova O, McMacken G, et al. Clinical outcomes in duchenne muscular dystrophy: a study of 5345 patients from the treat-nmd dmd global database. J Neuromuscul Dis 2017; 4:293-306.
47
47. Manghwar H, Li B, Ding X, Hussain A, Lindsey K, Zhang X, et al. CRISPR/Cas systems in genome editing: methodologies and tools for sgRNA design, off‐target evaluation, and strategies to mitigate off‐target effects. Adv Sci 2020; 7:1902312-19002328.
48
48. Reinig AM, Mirzaei S, Berlau DJ. Advances in the treatment of duchenne muscular dystrophy: New and emerging pharmacotherapies. Pharmacotherapy: J Huma Pharmacol Drug Ther 2017; 37:492-499.
49
49. Mata López S, Balog-Alvarez C, Vitha S, Bettis AK, Canessa EH, Kornegay JN, et al. Challenges associated with homologous directed repair using CRISPR-Cas9 and TALEN to edit the DMD genetic mutation in canine Duchenne muscular dystrophy. PloS One 2020;15: e0228072.
50
50. Miyamoto M, Tochinai R, Sekizawa S-i, Shiga T, Uchida K, Tsuru Y, et al. Cardiac lesions in duchenne muscular dystrophy model rats with out-of-frame Dmd gene mutation mediated by CRISPR/Cas9 system. J Toxicol Pathol 2020; 33:227-236.
51