Effect of mesenchymal stem cells and polyvinyl alcohol-coated selenium nanoparticles on rats with Alzheimer-like phenotypes

Articles in Press

Document Type : Original Article

Authors

1 Neurophysiology Research Center, Hamadan University of Medical Sciences, Hamadan, Iran

2 Department of Anatomy, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran

3 Department of Chemistry, Faculty of Science, University of Zabol, Zabol, Iran

4 School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran

10.22038/ijbms.2024.76242.16495

Abstract

Objective(s): Mesenchymal stem cell (MSC) transplantation represents a promising approach for treating Alzheimer’s disease (AD). These stem cells, however, have a short lifespan following transplantation into recipient animals. Selenium nanoparticles, due to their size, aid in drug delivery for brain disorders. This study investigated the therapeutic effect of MSCs and polyvinyl alcohol (PVA)-coated selenium nanoparticles (SeNPs) in a rat model of AD.
Materials and Methods: An Alzheimer-like phenotype was induced through intracerebroventricular (ICV) administration of streptozotocin (STZ).  Rats were assigned to five groups: control, Alz (STZ; 3 mg/kg, 10 μl, ICV), Alz+stem cell (ICV transplantation), Alz+SeNP (0.4 mg/kg, orally), and Alz+stem cell+SeNPs. The ICV administration of STZ mimicked some aspects of AD in the Alz groups. SeNPs were administrated for 30 days following STZ administration. The novel object recognition (NOR) and passive avoidance learning (PAL) tests were used to evaluate cognition and memory. Oxidative stress biomarkers and brain-derived neurotrophic factor (BDNF) were assessed by biochemical analysis, ELISA kits, and Congo red staining, respectively. 
Results: The combined therapy of PVA-coated SeNPs and MSC transplantation was more effective in enhancing memory reacquisition compared to either SeNPs or MSCs alone. The use of stem cells in conjunction with PVA-coated SeNPs significantly boosted anti-oxidant capacity.
Conclusion: The results suggest that the joint treatment with PVA-coated SeNPs and MSCs offers considerable neuroprotection against AD in animal models.

Keywords

Main Subjects

References

1. Bali P, Lahiri DK, Banik A, Nehru B, Anand A. Potential for stem cells therapy in Alzheimer’s disease: Do neurotrophic factors play critical role? Curr Alzheimer Res 2017; 14:208-220.
2. Brown C, McKee C, Bakshi S, Walker K, Hakman E, Halassy S, et al. Mesenchymal stem cells: Cell therapy and regeneration potential. J Tissue Eng Regen Med 2019; 13:1738-1755.
3. Sweeney SK, Manzar GS, Zavazava N, Assouline JG. Tracking embryonic hematopoietic stem cells to the bone marrow: Nanoparticle options to evaluate transplantation efficiency. Stem Cell Res Ther 2018; 9:204-217.
4. Chia YC, Anjum CE, Yee HR, Kenisi Y, Chan MKS, Wong MBF, et al. Stem cell therapy for neurodegenerative diseases: How Do stem cells bypass the blood-brain barrier and home to the brain?  Stem Cells Int 2020; 2020:8889061.
5. Fleifel D, Rahmoon MA, AlOkda A, Nasr M, Elserafy M, El-Khamisy SF. Recent advances in stem cells therapy: A focus on cancer, Parkinson’s and Alzheimer’s. J Genet Eng Biotechnol 2018; 16:427-432.
6. Esmaeilzade B, Artimani T, Amiri I, Najafi R, Shahidi S, Sabec M, et al. Dimethyloxalylglycine preconditioning enhances protective effects of bone marrow-derived mesenchymal stem cells in Aβ- induced Alzheimer disease. Physiol Behav 2019; 199:265-272.
7. Igartúa DE, Martinez CS, Del VAS, Prieto MJ. Combined Therapy for Alzheimer’s disease: Tacrine and PAMAM dendrimers co-administration reduces the side effects of the drug without modifying its activity. AAPS PharmSciTech 2020; 21:110-114.
8. Hashemi-Firouzi N, Komaki A, Soleimani Asl S, Shahidi S. The effects of the 5-HT7 receptor on hippocampal long-term potentiation and apoptosis in a rat model of Alzheimer’s disease. Brain Res Bull 2017; 135:85-91.
9. Rojas-Gutierrez E, Muñoz-Arenas G, Treviño S, Espinosa B, Chavez R, Rojas K, et al. Alzheimer’s disease and metabolic syndrome: A link from oxidative stress and inflammation to neurodegeneration.  2017; 71:e21990.
10. Chakari-Khiavi F, Dolati S, Chakari-Khiavi A, Abbaszadeh H, Aghebati-Maleki L, Pourlak T, et al. Prospects for the application of mesenchymal stem cells in Alzheimer’s disease treatment. Life Sci 2019; 231:116564.
11. Mohammadzadeh M, Halabian R, Gharehbaghian A, Amirizadeh N, Jahanian-Najafabadi A, Roushandeh AM, et al. Nrf-2 overexpression in mesenchymal stem cells reduces oxidative stress-induced apoptosis and cytotoxicity. Cell Stress Chaperones 2012; 17:553-565.
12. Labak M, Foniok T, Kirk D, Rushforth D, Tomanek B, Jasiński A, et al. Metabolic changes in rat brain following intracerebroventricular injections of streptozotocin: A model of sporadic Alzheimer’s disease. Acta Neurochir Suppl 2010; 106:177-181.
13. Grieb P. Intracerebroventricular streptozotocin injections as a model of alzheimer’s disease: In search of a relevant mechanism. Mol Neurobiol 2016; 53:1741-1752.
14. Correia SC, Santos RX, Perry G, Zhu X, Moreira PI, Smith MA. Insulin-resistant brain state: the culprit in sporadic Alzheimer’s disease? Ageing Res Rev 2011; 10:264-273.
15. Kamat PK, Kalani A, Rai S, Tota SK, Kumar A, Ahmad AS. Streptozotocin intracerebroventricular-induced neurotoxicity and brain insulin resistance: a therapeutic intervention for treatment of sporadic Alzheimer’s disease (sAD)-like pathology. Mol Neurobiol 2016; 53:4548-4562.
16. Chen Y, Liang Z, Blanchard J, Dai CL, Sun S, Lee MH, et al. A non-transgenic mouse model (icv-STZ mouse) of Alzheimer’s disease: similarities to and differences from the transgenic model (3xTg-AD mouse). Mol Neurobiol 2013; 47:711-725.
17. Fan RF, Liu JX, Yan YX, Wang L, Wang ZY. Selenium relieves oxidative stress, inflammation, and apoptosis within spleen of chicken exposed to mercuric chloride. Poult Sci 2020; 99:5430-5439.
18. Zhang Y, Hu B, Wang M, Tong J, Pan J, Wang N, et al. Selenium protects against zearalenone-induced oxidative stress and apoptosis in the mouse kidney by inhibiting endoplasmic reticulum stress. Oxid Med Cell Longev 2020; 2020:6059058.
19. Hosnedlova B, Kepinska M, Skalickova S, Fernandez C, Ruttkay-Nedecky B, Peng Q, et al. Nano-selenium and its nanomedicine applications: a critical review. Int J Nanomedicine 2018; 13:2107-2128.
20. Kumar A, Prasad KS. Role of nano-selenium in health and environment. J Biotechnol 2021; 325:152-163.
21. Pinelli F, Perale G, Rossi F. Coating and functionalization strategies for nanogels and nanoparticles for selective drug delivery. Gels 2020;6:6-21.
22. Schubert J, Chanana M. Coating matters: Review on colloidal stability of nanoparticles with biocompatible coatings in biological media, living cells and organisms. Curr Med Chem 2018; 25:4553-4586.
23. Paxinos G. Watson C1998 The Rat Brain in Stereotaxic Coordinates. 4st ed. Academic Press; San Diego.1998.p.237.
24. Afshar S, Shahidi S. The effect of NAD-299 and TCB-2 on learning and memory, hippocampal BDNF levels and amyloid plaques in Streptozotocin-induced memory deficits in male rats. Psychopharmacology (Berl)  2018; 235:2809-2822.
25. Hashemi-Firouzi N, Shahidi S. 5-Hydroxytryptamine receptor 6 antagonist, SB258585 exerts neuroprotection in a rat model of Streptozotocin-induced Alzheimer’s disease. Metab Brain Dis 2018; 33:1243-1253.
26. Almasi A, Zarei M, Raoufi S, Sarihi A, Salehi I, Komaki A, et al. Influence of hippocampal GABA(B) receptor inhibition on memory in rats with acute β-amyloid toxicity. Metab Brain Dis 2018; 33:1859-1867.
27. Afshar S, Shahidi S, Rohani AH, Soleimani Asl S, Komaki A. Protective effects of 5-HT(1A) receptor antagonist and 5-HT(2A) receptor agonist on the biochemical and histological features in a rat model of Alzheimer’s disease. J Chem Neuroanat 2019; 96:140-147.
28. Witty CF, Gardella LP, Perez MC, Daniel JM. Short-term estradiol administration in aging ovariectomized rats provides lasting benefits for memory and the hippocampus: a role for insulin-like growth factor-I. Endocrinology 2013; 154:842-852.
29. Cevik B, Solmaz V, Yigitturk G, Cavusoğlu T, Peker G, Erbas O. Neuroprotective effects of erythropoietin on Alzheimer’s dementia model in rats. Adv Clin Exp Med 2017; 26:23-29.
30. Majkutewicz I, Kurowska E, Podlacha M, Myślińska D, Grembecka B, Ruciński J, et al. Dimethyl fumarate attenuates intracerebroventricular streptozotocin-induced spatial memory impairment and hippocampal neurodegeneration in rats. Behav Brain Res 2016; 308:24-37.
31. Poovaiah N, Davoudi Z, Peng H, Schlichtmann B, Mallapragada S, Narasimhan B, et al. Treatment of neurodegenerative disorders through the blood-brain barrier using nanocarriers. Nanoscale 2018; 10:16962-16983.
32. Yin T, Yang L, Liu Y, Zhou X, Sun J, Liu J. Sialic acid (SA)-modified selenium nanoparticles coated with a high blood-brain barrier permeability peptide-B6 peptide for potential use in Alzheimer’s disease. Acta Biomater 2015; 25:172-183.
33. Khurana A, Tekula S, Saifi MA, Venkatesh P, Godugu C. Therapeutic applications of selenium nanoparticles. Biomed Pharmacother 2019; 111:802-812.
34. Nazıroğlu M, Muhamad S, Pecze L. Nanoparticles as potential clinical therapeutic agents in Alzheimer’s disease: focus on selenium nanoparticles. Expert Rev Clin Pharmacol 2017; 10:773-782.
35. Huang T, Kumari S. Enhanced antibacterial activity of se nanoparticles upon coating with recombinant spider silk protein eADF4(κ16). Int J Nanomedicine 2020; 15:4275-4288.
36. Shah CP, Kumar M, Pushpa KK, Bajaj PN. Acrylonitrile-induced synthesis of polyvinyl alcohol-stabilized selenium nanoparticles. Cryst Growth Des 2008; 8:4159-4164.
37. Tran PA, O’Brien-Simpson N, Reynolds EC, Pantarat N, Biswas DP, O’Connor AJ. Low cytotoxic trace element selenium nanoparticles and their differential antimicrobial properties against Staphylococcus aureus and Escherichia coli. Nanotechnology 2016; 27:045101.
38. Godara S, Lather V, Kirthanashri SV, Awasthi R, Pandita D. Lipid-PLGA hybrid nanoparticles of paclitaxel: Preparation, characterization, in vitro and in vivo evaluation. Mater Sci Eng C Mater Biol Appl 2020; 109:110576.
39. Dkhil MA, Zrieq R, Al-Quraishy S, Abdel Moneim AE. Selenium nanoparticles attenuate oxidative stress and testicular damage in streptozotocin-induced diabetic rats. Molecules 2016; 21:1517.
40. Yuan X, Fu Z, Ji P, Guo L, Al-Ghamdy AO, Alkandiri A, et al. Selenium nanoparticles pre-treatment reverse behavioral, oxidative damage, neuronal loss and neurochemical alterations in pentylenetetrazole-induced epileptic seizures in mice. Int J Nanomedicine 2020; 15:6339-6353.
41. Bashir DW, Rashad MM, Ahmed YH, Drweesh EA, Elzahany EAM, Abou-El-Sherbini KS, et al. The ameliorative effect of nanoselenium on histopathological and biochemical alterations induced by melamine toxicity on the brain of adult male Albino rats. Neurotoxicology 2021; 86:37-51.
42. Abshenas R, Artimani T, Shahidi S, Ranjbar A, Komaki A, Salehi I, et al. Treadmill exercise enhances the promoting effects of preconditioned stem cells on memory and neurogenesis in Aβ-induced neurotoxicity in the rats. Life Sci 2020; 249:117482.
43. Hu W, Feng Z, Xu J, Jiang Z, Feng M. Brain-derived neurotrophic factor modified human umbilical cord mesenchymal stem cells-derived cholinergic-like neurons improve spatial learning and memory ability in Alzheimer’s disease rats. Brain Res 2019; 1710:61-73.
44. Potier E, Ferreira E, Meunier A, Sedel L, Logeart-Avramoglou D, Petite H. Prolonged hypoxia concomitant with serum deprivation induces massive human mesenchymal stem cell death. Tissue Eng 2007; 13:1325-1331.
45. Vissers C, Ming GL, Song H. Nanoparticle technology and stem cell therapy team up against neurodegenerative disorders. Adv Drug Deliv Rev 2019; 148:239-251.
46. Fatima S, Alfrayh R. Selenium nanoparticles by moderating oxidative stress promote differentiation of mesenchymal stem cells to osteoblasts. Int J Nanomedicine 2021; 16:331-343.
47. Blurton-Jones M, Kitazawa M, Martinez-Coria H, Castello NA, Müller FJ, Loring JF, et al. Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci U S A 2009; 106:13594-13599.
48. Nazarian S, Abdolmaleki Z. Mesenchymal stem cells with modafinil (gold nanoparticles) significantly improves neurological deficits in rats after middle cerebral artery occlusion. Exp Brain Res 2020; 238:2589-2601.

              
Iranian Journal of Basic Medical Sciences

Articles in Press, Accepted Manuscript
Available Online from 06 July 2024

Files

Share

How to cite

Statistics