In search of elixir: Pharmacological agents against stem cell senescence

Document Type : Review Article

Authors

1 Vice-chancellery of Food and Drug,Shahroud University of Medical Sciences, Shahroud, Iran

2 Targeted Drug Delivery Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran

3 Department of Pharmacodynamics and Toxicology, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran

4 Pharmaceutical Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran

Abstract

Stem cell senescence causes different complications. In addition to the aging phenomenon, stem cell senescence has been investigated in various concepts such as cancer, adverse drug effects, and as a limiting factor in cell therapy. This manuscript examines protective medicines and supplements which are capable of hindering stem cell senescence. We searched the databases such as EMBASE, PubMed, and Web of Science with the keywords “stem cell,” “progenitor cell,” “satellite,” “senescence” and excluded the keywords “cancer,” “tumor,” “malignancy” and “carcinoma” until June 2020. Among these results, we chose 47 relevant studies. Our investigation indicates that most of these studies examined endothelial progenitor cells, hematopoietic stem cells, mesenchymal stem cells, adipose-derived stem cells, and a few others were about less-discussed types of stem cells such as cardiac stem cells, myeloblasts, and induced pluripotent stem cells. From another aspect, 17β-Estradiol, melatonin, metformin, rapamycin, coenzyme Q10, N-acetyl cysteine, and vitamin C were the most studied agents, while the main protective mechanism was through telomerase activity enhancement or oxidative damage ablation.
Although many of these studies are in vitro, they are still worthwhile. Stem cell senescence in the in vitro expansion stage is an essential concern in clinical procedures of cell therapy. Moreover, in vitro studies are the first step for further in vivo and clinical studies. It is noteworthy to mention the fact that these protective agents have been used in the clinical setting for various purposes for a long time. Given that, we only need to examine their systemic anti-senescence effects and effective dosages.

Keywords

References

1. Mohammadi E, Mehri S, Badie Bostan H, Hosseinzadeh H. Protective effect of crocin against d-galactose-induced aging in mice. Avicenna J Phytomed 2018; 8:14-23.
2. Rodier F, Campisi J. Four faces of cellular senescence. J Cell Biol 2011; 192:547-556.
3. Sharpless NE, DePinho RA. Telomeres, stem cells, senescence, and cancer. J Clin Invest 2004; 113:160-168.
4. Flach J, Bakker ST, Mohrin M, Conroy PC, Pietras EM, Reynaud D, et al. Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells. Nature 2014; 512:198-202.
5. Signer RAJ, Morrison SJ. Mechanisms that Regulate Stem Cell Aging and Life Span. Cell Stem Cell 2013; 12:152-165.
6. Lee AC, Fenster BE, Ito H, Takeda K, Bae NS, Hirai T, et al. Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. J Biol Chem 1999; 274:7936-7940.
7. Shin DH, Lee SJ, Kim JS, Ryu JH, Kim JS. Synergistic effect of immunoliposomal gemcitabine and bevacizumab in glioblastoma stem cell-targeted therapy. J Biomed Nanotechnol 2015; 11:1989-2002.
8. Childs BG, Durik M, Baker DJ, van Deursen JM. Cellular senescence in aging and age-related disease: from mechanisms to therapy. Nat Med 2015; 21:1424-1435.
9. Korski KI, Kubli DA, Wang BJ, Khalafalla FG, Monsanto MM, Firouzi F, et al. Hypoxia prevents mitochondrial dysfunction and senescence in human c-Kit(+) cardiac progenitor cells. Stem Cells 2019; 37:555-567.
10. Liu S, Mahairaki V, Bai H, Ding Z, Li J, Witwer KW, et al. Highly purified human extracellular vesicles produced by stem cells alleviate aging cellular phenotypes of senescent human cells. Stem Cells 2019; 37:779-790.
11. Rao VV, Vu MK, Ma H, Killaars AR, Anseth KS. Rescuing mesenchymal stem cell regenerative properties on hydrogel substrates post serial expansion. Bioeng Transl Med 2019; 4:51-60.
12. Qi L, Wang R, Shi Q, Yuan M, Jin M, Li D. Umbilical cord mesenchymal stem cell conditioned medium restored the expression of collagen II and aggrecan in nucleus pulposus mesenchymal stem cells exposed to high glucose. J Bone Miner Metab 2019; 37:455-466.
13. Vono R, Jover Garcia E, Spinetti G, Madeddu P. Oxidative stress in mesenchymal stem cell senescence: Regulation by coding and noncoding RNAs. Antioxid Redox Signal 2018; 29:864-879.
14. Khatiwala RV, Zhang S, Li X, Devejian N, Bennett E, Cai C. Inhibition of p16(INK4A) to rejuvenate aging human cardiac progenitor cells via the upregulation of anti-oxidant and NFkappaB signal pathways. Stem Cell Rev Rep 2018; 14:612-625.
15. Tousian H, Razavi BM, Hosseinzadeh H. Looking for immortality: Review of phytotherapy for stem cell senescence. Iran J Basic Med Sci 2020; 23:154-166.
16. Arbab AS, Bashaw LA, Miller BR, Jordan EK, Bulte JW, Frank JA. Intracytoplasmic tagging of cells with ferumoxides and transfection agent for cellular magnetic resonance imaging after cell transplantation: methods and techniques. Transplantation 2003; 76:1123-1130.
17. Hristov M, Weber C. Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J Cell Mol Med 2004; 8:498-508.
18. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 2003; 348:593-600.
19. Tobler K, Freudenthaler A, Baumgartner-Parzer SM, Wolzt M, Ludvik B, Nansalmaa E, et al. Reduction of both number and proliferative activity of human endothelial progenitor cells in obesity. Int J Obes (Lond) 2010; 34:687-700.
20. Scheubel RJ, Zorn H, Silber RE, Kuss O, Morawietz H, Holtz J, et al. Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J Am Coll Cardiol 2003; 42:2073-2080.
21. Lee ST, Chu K, Jung KH, Kim DH, Kim EH, Choe VN, et al. Decreased number and function of endothelial progenitor cells in patients with migraine. Neurology 2008; 70:1510-1517.
22. Kobayashi K, Imanishi T, Akasaka T. Endothelial progenitor cell differentiation and senescence in an angiotensin II-infusion rat model. Hypertens Res 2006; 29:449-455.
23. De Falco E, Carnevale R, Pagano F, Chimenti I, Fianchini L, Bordin A, et al. Role of NOX2 in mediating doxorubicin-induced senescence in human endothelial progenitor cells. Mech Ageing Dev 2016; 159:37-43.
24. Sugawara J, Mitsui-Saito M, Hayashi C, Hoshiai T, Senoo M, Chisaka H, et al. Decrease and senescence of endothelial progenitor cells in patients with preeclampsia. J Clin Endocrinol Metab 2005; 90:5329-5332.
25. Hu Z, Zhang F, Yang Z, Zhang J, Zhang D, Yang N, et al. Low-dose aspirin promotes endothelial progenitor cell migration and adhesion and prevents senescence. Cell Biol Int 2008; 32:761-768.
26. Tsai H-Y, Lin C-P, Huang P-H, Li S-Y, Chen J-S, Lin F-Y, et al. Coenzyme Q10 attenuates high glucose-induced endothelial progenitor cell dysfunction through AMP-Activated protein kinase pathways. J Diabetes Res 2016; 2016:6384759.
27. Zhu JH, Chen JZ, Wang XX, Xie XD, Sun J, Zhang FR. Homocysteine accelerates senescence and reduces proliferation of endothelial progenitor cells. J Mol Cell Cardiol 2006; 40:648-652.
28. Assmus B, Urbich C, Aicher A, Hofmann WK, Haendeler J, Rossig L, et al. HMG-CoA reductase inhibitors reduce senescence and increase proliferation of endothelial progenitor cells via regulation of cell cycle regulatory genes. Circ Res 2003; 92:1049-1055.
29. Zhao L, Cao F, Yin T, Sun D, Cheng K, Zhang J, et al. Moderate dose insulin promotes function of endothelial progenitor cells. Cell Biol Int 2011; 35:215-220.
30. Imanishi T, Kobayashi K, Kuroi A, Ikejima H, Akasaka T. Pioglitazone inhibits angiotensin II-induced senescence of endothelial progenitor cell. Hypertens Res 2008; 31:757-765.
31. Shen X, Wang M, Bi X, Zhang J, Wen S, Fu G, et al. Resveratrol prevents endothelial progenitor cells from senescence and reduces the oxidative reaction via PPARgamma/HO1 pathways. Mol Med Rep 2016; 14:5528-5534.
32. Alhurani RE, Chahal CAA, Ahmed AT, Mohamed EA, Miller VM. Sex hormone therapy and progression of cardiovascular disease in menopausal women. Clin Sci (Lond) 2016; 130:1065-1074.
33. Imanishi T, Hano T, Nishio I. Estrogen reduces angiotensin II-induced acceleration of senescence in endothelial progenitor cells. Hypertens Res 2005; 28:263-271.
34. Tormos AM, Talens-Visconti R, Nebreda AR, Sastre J. p38 MAPK: a dual role in hepatocyte proliferation through reactive oxygen species. Free Radic Res 2013; 47:905-916.
35. Imanishi T, Hano T, Nishio I. Estrogen reduces endothelial progenitor cell senescence through augmentation of telomerase activity. J Hypertens 2005; 23:1699-1706.
36. D'Apolito M, Colia AL, Lasalvia M, Capozzi V, Falcone MP, Pettoello-Mantovani M, et al. Urea-induced ROS accelerate senescence in endothelial progenitor cells. Atherosclerosis 2017; 263:127-136.
37. Ramirez R, Carracedo J, Nogueras S, Buendia P, Merino A, Canadillas S, et al. Carbamylated darbepoetin derivative prevents endothelial progenitor cell damage with no effect on angiogenesis. J Mol Cell Cardiol 2009; 47:781-788.
38. Junhui Z, Xiaojing H, Binquan Z, Xudong X, Junzhu C, Guosheng F. Nicotine-reduced endothelial progenitor cell senescence through augmentation of telomerase activity via the PI3K/Akt pathway. Cytotherapy 2009; 11:485-491.
39. You J, Sun J, Ma T, Yang Z, Wang X, Zhang Z, et al. Curcumin induces therapeutic angiogenesis in a diabetic mouse hindlimb ischemia model via modulating the function of endothelial progenitor cells. Stem Cell Res Ther 2017; 8:182.
40. Makino N, Oyama J, Maeda T, Koyanagi M, Higuchi Y, Shimokawa I, et al. FoxO1 signaling plays a pivotal role in the cardiac telomere biology responses to calorie restriction. Mol Cell Biochem 2016; 412:119-130.
41. Yao E-H, Fukuda N, Matsumoto T, Katakawa M, Yamamoto C, Han Y, et al. Effects of the antioxidative β-Blocker celiprolol on endothelial progenitor cells in hypertensive rats. Am J Hypertens 2008; 21:1062-1068.
42. Wu VC, Young GH, Huang PH, Lo SC, Wang KC, Sun CY, et al. In acute kidney injury, indoxyl sulfate impairs human endothelial progenitor cells: modulation by statin. Angiogenesis 2013; 16:609-624.
43. Li Y, Xu X, Wang L, Liu G, Li Y, Wu X, et al. Senescent mesenchymal stem cells promote colorectal cancer cells growth via galectin-3 expression. Cell Biosci 2015; 5:21.
44. Thum T, Hoeber S, Froese S, Klink I, Stichtenoth DO, Galuppo P, et al. Age-dependent impairment of endothelial progenitor cells is corrected by growth-hormone-mediated increase of insulin-like growth-factor-1. Circ Res 2007; 100:434-443.
45. Rossi L, Challen GA, Sirin O, Lin KK-Y, Goodell MA. Hematopoietic stem cell characterization and isolation. Methods Mol Biol 2011; 750:47-59.
46. Vanikar AV, Trivedi HL, Kumar A, Gopal SC, Patel HV, Gumber MR, et al. Co-infusion of donor adipose tissue-derived mesenchymal and hematopoietic stem cells helps safe minimization of immunosuppression in renal transplantation - single center experience. Ren Fail 2014; 36:1376-1384.
47. Verburg RJ, Kruize AA, van den Hoogen FH, Fibbe WE, Petersen EJ, Preijers F, et al.. High-dose chemotherapy and autologous hematopoietic stem cell transplantation in patients with rheumatoid arthritis: results of an open study to assess feasibility, safety, and efficacy. Arthritis Rheum 2001; 44:754-760.
48. Thakkar UG, Trivedi HL, Vanikar AV, Dave SD. Insulin-secreting adipose-derived mesenchymal stromal cells with bone marrow-derived hematopoietic stem cells from autologous and allogenic sources for type 1 diabetes mellitus. Cytotherapy 2015; 17:940-947.
49. Liu J, Jia DY, Cai SZ, Li CP, Zhang MS, Zhang YY, et al.. Mitochondria defects are involved in lead-acetate-induced adult hematopoietic stem cell decline. Toxicol Lett 2015; 235:37-44.
50. Zhang XP, Zhang GH, Wang YY, Liu J, Wei Q, Xu CY, et al. Oxidized low-density lipoprotein induces hematopoietic stem cell senescence. Cell Biol Int 2013; 37:940-948.
51. Mancardi GL, Sormani MP, Gualandi F, Saiz A, Carreras E, Merelli E, et al. Autologous hematopoietic stem cell transplantation in multiple sclerosis: a phase II trial. Neurology 2015; 84:981-988.
52. Chen J. Hematopoietic stem cell development, aging and functional failure. Int J Hematol 2011; 94:3-10.
53. Luo Y, Li L, Zou P, Wang J, Shao L, Zhou D, et al. Rapamycin enhances long-term hematopoietic reconstitution of ex vivo expanded mouse hematopoietic stem cells by inhibiting senescence. Transplantation 2014; 97:20-29.
54. Molofsky AV, He S, Bydon M, Morrison SJ, Pardal R. Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16(Ink4a) and p19(Arf) senescence pathways. Genes Dev 2005; 19:1432-1437.
55. Xu S, Cai Y, Wei Y. mTOR Signaling from Cellular Senescence to Organismal Aging. Aging Dis 2014; 5:263-273.
56. Xu G, Wu H, Zhang J, Li D, Wang Y, Wang Y, et al. Metformin ameliorates ionizing irradiation-induced long-term hematopoietic stem cell injury in mice. Free Radic Biol Med 2015; 87:15-25.
57. Stewart MC, Stewart AA. Mesenchymal stem cells: characteristics, sources, and mechanisms of action. Vet Clin North Am Equine Pract 2011; 27:243-261.
58. Jo CH, Lee YG, Shin WH, Kim H, Chai JW, Jeong EC, et al. Intra-articular injection of mesenchymal stem cells for the treatment of osteoarthritis of the knee: a proof-of-concept clinical trial. Stem Cells 2014; 32:1254-1266.
59. Zheng G, Huang L, Tong H, Shu Q, Hu Y, Ge M, et al. Treatment of acute respiratory distress syndrome with allogeneic adipose-derived mesenchymal stem cells: a randomized, placebo-controlled pilot study. Respir Res 2014; 15:39.
60. Panes J, Garcia-Olmo D, Van Assche G, Colombel JF, Reinisch W, Baumgart DC, et al. Expanded allogeneic adipose-derived mesenchymal stem cells (Cx601) for complex perianal fistulas in Crohn's disease: a phase 3 randomised, double-blind controlled trial. Lancet 2016; 388:1281-1290.
61. Qin HL, Zhu XH, Zhang B, Zhou L, Wang WY. Clinical evaluation of human umbilical cord mesenchymal stem cell transplantation after angioplasty for diabetic foot. Exp Clin Endocrinol Diabetes 2016; 124:497-503.
62. Rushkevich YN, Kosmacheva SM, Zabrodets GV, Ignatenko SI, Goncharova NV, Severin IN, et al. The use of autologous mesenchymal stem cells for cell therapy of patients with amyotrophic lateral sclerosis in belarus. Bull Exp Biol Med 2015; 159:576-581.
63. Gao LR, Chen Y, Zhang NK, Yang XL, Liu HL, Wang ZG, et al. Intracoronary infusion of Wharton's jelly-derived mesenchymal stem cells in acute myocardial infarction: double-blind, randomized controlled trial. BMC Med 2015; 13:162.
64. Soeder Y, Loss M, Johnson CL, Hutchinson JA, Haarer J, Ahrens N, et al. First-in-human case study: Multipotent adult progenitor cells for immunomodulation after liver transplantation. Stem Cells Transl Med 2015; 4:899-904.
65. Zhao XF, Xu Y, Zhu ZY, Gao CY, Shi YN. Clinical observation of umbilical cord mesenchymal stem cell treatment of severe systolic heart failure. Genet Mol Res 2015; 14:3010-3017.
66. Kong D, Zhuang X, Wang D, Qu H, Jiang Y, Li X, et al. Umbilical cord mesenchymal stem cell transfusion ameliorated hyperglycemia in patients with type 2 diabetes mellitus. Clin Lab 2014; 60:1969-1976.
67. Llufriu S, Sepulveda M, Blanco Y, Marin P, Moreno B, Berenguer J, et al. Randomized placebo-controlled phase II trial of autologous mesenchymal stem cells in multiple sclerosis. PLoS One 2014; 9:e113936.
68. Zhou S, Greenberger JS, Epperly MW, Goff JP, Adler C, Leboff MS, et al. Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts. Aging Cell 2008; 7:335-343.
69. Lee JK, Jin HK, Endo S, Schuchman EH, Carter JE, Bae JS. Intracerebral transplantation of bone marrow-derived mesenchymal stem cells reduces amyloid-beta deposition and rescues memory deficits in Alzheimer's disease mice by modulation of immune responses. Stem Cells 2010; 28:329-343.
70. Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 1997; 64:295-312.
71. Izadpanah R, Schachtele DJ, Pfnur AB, Lin D, Slakey DP, Kadowitz PJ, et al. The impact of statins on biological characteristics of stem cells provides a novel explanation for their pleiotropic beneficial and adverse clinical effects. Am J Physiol Cell Physiol 2015; 309:C522-531.
72. Ling L, Camilleri ET, Helledie T, Samsonraj RM, Titmarsh DM, Chua RJ, et al. Effect of heparin on the biological properties and molecular signature of human mesenchymal stem cells. Gene 2016; 576:292-303.
73. Liu Q, Zhu H, Dong J, Li H, Zhang H. Defective proliferative potential of MSCs from pediatric myelodysplastic syndrome patients is associated with cell senescence. Int J Clin Exp Pathol 2015; 8:13059-13066.
74. Klinkhammer BM, Kramann R, Mallau M, Makowska A, van Roeyen CR, Rong S, et al. Mesenchymal stem cells from rats with chronic kidney disease exhibit premature senescence and loss of regenerative potential. PLoS One 2014; 9:e92115.
75. Zhang D, Lu H, Chen Z, Wang Y, Lin J, Xu S, et al. High glucose induces the aging of mesenchymal stem cells via Akt/mTOR signaling. Mol Med Rep 2017; 16:1685-1690.
76. Wang Y, Han ZB, Song YP, Han ZC. Safety of mesenchymal stem cells for clinical application. Stem Cells Int 2012; 2012:652034.
77. Despars G, Carbonneau CL, Bardeau P, Coutu DL, Beauséjour CM. Loss of the osteogenic differentiation potential during senescence is limited to bone progenitor cells and is dependent on p53. PLoS One 2013; 8.
78. Di GH, Liu Y, Lu Y, Liu J, Wu C, Duan HF. IL-6 secreted from senescent mesenchymal stem cells promotes proliferation and migration of breast cancer cells. PLoS One 2014; 9:e113572.
79. Xu J, Huang Z, Lin L, Fu M, Song Y, Shen Y, et al. miRNA-130b is required for the ERK/FOXM1 pathway activation-mediated protective effects of isosorbide dinitrate against mesenchymal stem cell senescence induced by high glucose. Int J Mol Med 2015; 35:59-71.
80. Gu Z, Tan W, Ji J, Feng G, Meng Y, Da Z, et al. Rapamycin reverses the senescent phenotype and improves immuno-regulation of mesenchymal stem cells from MRL/lpr mice and systemic lupus erythematosus patients through inhibition of the mTOR signaling pathway. Aging (Albany NY) 2016; 8:1102-1114.
81. Zhang D, Yan B, Yu S, Zhang C, Wang B, Wang Y, et al. Coenzyme Q10 inhibits the aging of mesenchymal stem cells induced by D-galactose through Akt/mTOR signaling. Oxid Med Cell Longev 2015; 2015:867293.
82. Zhang J, Zhang J, Li T, Zhang N, Tang S, Tao Z, et al. Effect of idebenone on bone marrow mesenchymal stem cells in vitro. Mol Med Rep 2018; 17:5376-5383.
83. Yang M, Teng S, Ma C, Yu Y, Wang P, Yi C. Ascorbic acid inhibits senescence in mesenchymal stem cells through ROS and AKT/mTOR signaling. Cytotechnology 2018; 70:1301-1313.
84. Klotz B, Mentrup B, Regensburger M, Zeck S, Schneidereit J, Schupp N, et al. 1,25-dihydroxyvitamin D3 treatment delays cellular aging in human mesenchymal stem cells while maintaining their multipotent capacity. PLoS One 2012; 7:e29959.
85. Lee WJ, Lee SC, Lee JH, Rho GJ, Lee SL. Differential regulation of senescence and in vitro differentiation by 17beta-estradiol between mesenchymal stem cells derived from male and female mini-pigs. J Vet Sci 2016; 17:159-170.
86. Breu A, Sprinzing B, Merkl K, Bechmann V, Kujat R, Jenei-Lanzl Z, et al. Estrogen reduces cellular aging in human mesenchymal stem cells and chondrocytes. J Orthop Res 2011; 29:1563-1571.
87. Kong Y, Song Y, Tang FF, Zhao HY, Chen YH, Han W, et al. N-acetyl-L-cysteine improves mesenchymal stem cell function in prolonged isolated thrombocytopenia post-allotransplant. Br J Haematol 2018; 180:863-878.
88. Han YS, Kim SM, Lee JH, Jung SK, Noh H, Lee SH. Melatonin protects chronic kidney disease mesenchymal stem cells against senescence via PrP(C) -dependent enhancement of the mitochondrial function. J Pineal Res 2019; 66:e12535.
89. Yang F, Yang L, Li Y, Yan G, Feng C, Liu T, et al. Melatonin protects bone marrow mesenchymal stem cells against iron overload-induced aberrant differentiation and senescence. J Pineal Res 2017; 63.
90. Ok JS, Song SB, Hwang ES. Enhancement of replication and differentiation potential of human bone marrow stem cells by nicotinamide treatment. Int J Stem Cells 2018; 11:13-25.
91. Hernandez-Vallejo SJ, Beaupere C, Larghero J, Capeau J, Lagathu C. HIV protease inhibitors induce senescence and alter osteoblastic potential of human bone marrow mesenchymal stem cells: beneficial effect of pravastatin. Aging Cell 2013; 12:955-965.
92. Meza-Zepeda LA, Noer A, Dahl JA, Micci F, Myklebost O, Collas P. High-resolution analysis of genetic stability of human adipose tissue stem cells cultured to senescence. J Cell Mol Med 2008; 12:553-563.
93. Gm C, El L, Jj C, Mr B, Ge DC, Ma S, et al. Direct comparison of progenitor cells derived from adipose, muscle, and bone marrow from wild-type or craniosynostotic rabbits. Plast Reconstr Surg 2011; 127:88-97.
94. Burrow KL, Hoyland JA, Richardson SM. Human adipose-derived stem cells exhibit enhanced proliferative capacity and retain multipotency longer than donor-matched bone marrow mesenchymal stem cells during expansion in vitro. Stem Cells Int 2017; 2017:2541275.
95. Sun Z, Gou W, Kim DS, Dong X, Strange C, Tan Y, et al. Adipose stem cell therapy mitigates chronic pancreatitis via differentiation into acinar-like cells in mice. Mol Ther 2017.
96. Numan MT, Kamdar A, Young J, Butler IJ. Autologous adipose stem cell therapy for autonomic nervous system dysfunction in two young patients. Stem Cells Dev 2017; 26:391-393.
97. Stepien A, Dabrowska NL, Maciagowska M, Macoch RP, Zolocinska A, Mazur S, et al. Clinical application of autologous adipose stem cells in patients with multiple sclerosis: preliminary results. Mediators Inflamm 2016; 2016:5302120.
98. Schweitzer KS, Johnstone BH, Garrison J, Rush NI, Cooper S, Traktuev DO, et al. Adipose stem cell treatment in mice attenuates lung and systemic injury induced by cigarette smoking. Am J Respir Crit Care Med 2011; 183:215-225.
99. Rajashekhar G, Ramadan A, Abburi C, Callaghan B, Traktuev DO, Evans-Molina C, et al. Regenerative therapeutic potential of adipose stromal cells in early stage diabetic retinopathy. PLoS One 2014; 9:e84671.
100. Yu HS, Park MK, Kang SA, Cho KS, Mun SJ, Roh HJ. Culture supernatant of adipose stem cells can ameliorate allergic airway inflammation via recruitment of CD4+CD25+Foxp3 T cells. Stem Cell Res Ther 2017; 8:8.
101. Zhao J, Hu L, Liu J, Gong N, Chen L. The effects of cytokines in adipose stem cell-conditioned medium on the migration and proliferation of skin fibroblasts in vitro. Biomed Res Int 2013; 2013:578479.
102. Mantovani C, Terenghi G, Magnaghi V. Senescence in adipose-derived stem cells and its implications in nerve regeneration. Neural Regen Res 2014; 9:10-15.
103. Minamino T, Orimo M, Shimizu I, Kunieda T, Yokoyama M, Ito T, et al. A crucial role for adipose tissue p53 in the regulation of insulin resistance. Nat Med 2009; 15:1082-1087.
104. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993; 259:87-91.
105. Orjalo AV, Bhaumik D, Gengler BK, Scott GK, Campisi J. Cell surface-bound IL-1alpha is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Proc Natl Acad Sci U S A 2009; 106:17031-17036.
106. Wei C, Liu X, Tao J, Wu R, Zhang P, Bian Y, et al. Effects of vitamin C on characteristics retaining of in vitro-cultured mouse adipose-derived stem cells. In Vitro Cell Dev Biol Anim 2014; 50:75-86.
107. Mobarak H, Fathi E, Farahzadi R, Zarghami N, Javanmardi S. L-carnitine significantly decreased aging of rat adipose tissue-derived mesenchymal stem cells. Vet Res Commun 2017; 41:41-47.
108. Fathi E, Farahzadi R, Rahbarghazi R, Samadi Kafil H, Yolmeh R. Rat adipose-derived mesenchymal stem cells aging reduction by zinc sulfate under extremely low frequency electromagnetic field exposure is associated with increased telomerase reverse transcriptase gene expression. Vet Res Forum 2017; 8:89-96.
109. Yun SP, Han YS, Lee JH, Kim SM, Lee SH. Melatonin rescues mesenchymal stem cells from senescence induced by the uremic toxin p-cresol via inhibiting mTOR-dependent autophagy. Biomol Ther (Seoul) 2017.
110. Liao N, Shi Y, Zhang C, Zheng Y, Wang Y, Zhao B, et al. Anti-oxidants inhibit cell senescence and preserve stemness of adipose tissue-derived stem cells by reducing ROS generation during long-term in vitro expansion. Stem Cell Res Ther 2019; 10:306.
111. Marycz K, Tomaszewski KA, Kornicka K, Henry BM, Wronski S, Tarasiuk J, et al. Metformin decreases reactive oxygen species, enhances osteogenic properties of adipose-derived multipotent mesenchymal stem cells in vitro, and increases bone density in vivo. Oxid Med Cell Longev 2016; 2016:9785890.
112. Hickson LJ, Langhi Prata LGP, Bobart SA, Evans TK, Giorgadze N, Hashmi SK, et al. Senolytics decrease senescent cells in humans: Preliminary report from a clinical trial of Dasatinib plus Quercetin in individuals with diabetic kidney disease. EBioMedicine 2019; 47:446-456.
113. Kawakami Y, Hambright WS, Takayama K, Mu X, Lu A, Cummins JH, et al. Rapamycin rescues age-related changes in muscle-derived stem/progenitor cells from progeroid mice. Mol Ther Methods Clin Dev 2019; 14:64-76.
114. Galli R, Gritti A, Bonfanti L, Vescovi AL. Neural stem cells: an overview. Circ Res 2003; 92:598-608.
115. Velichkovska M, Surnar B, Nair M, Dhar S, Toborek M. Targeted mitochondrial COQ10 delivery attenuates antiretroviral-drug-induced senescence of neural progenitor cells. Mol Pharm 2019; 16:724-736.
116. Sakai D, Schol J. Cell therapy for intervertebral disc repair: Clinical perspective. J Orthop Translat 2017; 9:8-18.
117. Molinos M, Almeida CR, Caldeira J, Cunha C, Goncalves RM, Barbosa MA. Inflammation in intervertebral disc degeneration and regeneration. J R Soc Interface 2015; 12:20150429.
118. Han Y, Yuan F, Deng C, He F, Zhang Y, Shen H, et al. Metformin decreases LPS-induced inflammatory response in rabbit annulus fibrosus stem/progenitor cells by blocking HMGB1 release. Aging (Albany NY) 2019; 11:10252-10265.
119. Itzhaki-Alfia A, Leor J, Raanani E, Sternik L, Spiegelstein D, Netser S, et al. Patient characteristics and cell source determine the number of isolated human cardiac progenitor cells. Circulation 2009; 120:2559-2566.
120. Cai B, Ma W, Bi C, Yang F, Zhang L, Han Z, et al. Long noncoding RNA H19 mediates melatonin inhibition of premature senescence of c-kit(+) cardiac progenitor cells by promoting miR-675. J Pineal Res 2016; 61:82-95.
121. Saheera S, Potnuri AG, Nair R. Histamine-2 receptor antagonist famotidine modulates cardiac stem cell characteristics in hypertensive heart disease. PeerJ 2017; 5:e3882.
122.Saheera S, Potnuri AG, Nair RR. Modulation of cardiac stem cell characteristics by metoprolol in hypertensive heart disease. Hypertens Res 2018; 41:253-262.
123. Cantz T, Martin U. Induced pluripotent stem cells: characteristics and perspectives. Adv Biochem Eng Biotechnol 2010; 123:107-126.
124. Giorgetti A, Montserrat N, Rodriguez-Piza I, Azqueta C, Veiga A, Izpisua Belmonte JC. Generation of induced pluripotent stem cells from human cord blood cells with only two factors: Oct4 and Sox2. Nat Protoc 2010; 5:811-820.
125. Szabo E, Rampalli S, Risueno RM, Schnerch A, Mitchell R, Fiebig-Comyn A, et al. Direct conversion of human fibroblasts to multilineage blood progenitors. Nature 2010; 468:521-526.
126. Banito A, Rashid ST, Acosta JC, Li S, Pereira CF, Geti I, et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 2009; 23:2134-2139.
127. Berniakovich I, Laricchia-Robbio L, Izpisua Belmonte JC. N-acetylcysteine protects induced pluripotent stem cells from in vitro stress: impact on differentiation outcome. Int J Dev Biol 2012; 56:729-735.
128. Esteban MA, Wang T, Qin B, Yang J, Qin D, Cai J, et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 2010; 6:71-79.
129. Son MJ, Son MY, Seol B, Kim MJ, Yoo CH, Han MK, et al. Nicotinamide overcomes pluripotency deficits and reprogramming barriers. Stem Cells 2013; 31:1121-1135.
130. Schwartz SM, Benditt EP. Clustering of replicating cells in aortic endothelium. Proc Natl Acad Sci U S A 1976; 73:651-653.
131. Yun SP, Lee MY, Ryu JM, Song CH, Han HJ. Role of HIF-1alpha and VEGF in human mesenchymal stem cell proliferation by 17beta-estradiol: involvement of PKC, PI3K/Akt, and MAPKs. Am J Physiol Cell Physiol 2009; 296:C317-326.
Iranian Journal of Basic Medical Sciences
Volume 24, Issue 7
July 2021
Pages 868-880

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