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Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Research Article

Regulatory Effect of Adipose-Derived Mesenchymal Stem Cells and/ or Acitretin on Adam10 Gene in Alzheimer's Disease Rat Model

Author(s): Noha O. Abu Nasra, Emad M. Elzayat, Kamal M. Dawood, Naglaa M. Hagag, Manal M. Yehya and Mohamed Hosney*

Volume 17, Issue 4, 2022

Published on: 29 April, 2022

Page: [370 - 388] Pages: 19

DOI: 10.2174/1574888X17666220302154618

Price: $65

Abstract

Background: Alzheimer's disease (AD) is a progressive neurodegenerative disease characterized by progressive cognitive deterioration. All recent therapeutic strategies tend to inhibit the generation of the Aβ peptide. These approaches tend to mediate both α - and γ -secretases to undergo the nonamyloidogenic pathway. ADAM10 is the main α-secretase that cleaves APP, and it is regulated by the metabolic product of vitamin A (retinoic acid), which is being widely used recently in AD research as a target for treatment. Mesenchymal stem cells (MSCs) are also used recently as a promising regenerative therapy for AD.

Objectives: The present study aimed to: (1) study the effect of MSCs with/without acitretin on the regulation of Adam10 gene expression in AlCl3-induced AD rat model, and (2) validate the hypothesis that AD is a time-dependent progressive disease that spreads spontaneously even after the stopping of exposure to AlCl3.

Methods: The experimental work has been designed to include three successive phases; AlCl3 induction phase (I), AlCl3 withdrawal phase (W), and therapeutic phase (T). Forty-five male albino Wistar rats were randomly divided into 2 main groups: the control (C) group (15 rats) and AD group (30 rats). The therapeutic potential of MSCs with/without acitretin has been evaluated at behavioral, physiological, molecular, and histopathological levels.

Results: Among the three therapeutic groups, combined administration of both MSC and acitretin showed the best compensatory effects on most of the measured parameters.

Conclusion: The present study approved that AD is a time-dependent progressive disease which spreads spontaneously without more AlCl3 exposure.

Keywords: Alzheimer's disease, neurodegeneration, mesenchymal stem cells, acitretin, adam10, β-amyloid.

Graphical Abstract

[1]
Nalivaeva NN, Turner AJ. The amyloid precursor protein: A biochemical enigma in brain development, function and disease. FEBS Lett 2013; 587(13): 2046-54.
[http://dx.doi.org/10.1016/j.febslet.2013.05.010] [PMID: 23684647]
[2]
Oh SJ, Lee HJ, Jeong YJ, et al. Evaluation of the neuroprotective effect of taurine in Alzheimer’s disease using functional molecular imag-ing. Sci Rep 2020; 10(1): 15551.
[http://dx.doi.org/10.1038/s41598-020-72755-4] [PMID: 32968166]
[3]
Eftekharzadeh M, Simorgh S, Doshmanziari M, Hassanzadeh L, Shariatpanahi M. Human adipose-derived stem cells reduce receptor-interacting protein 1, receptor-interacting protein 3, and mixed lineage kinase domain-like pseudokinase as necroptotic markers in rat model of Alzheimer’s disease. Indian J Pharmacol 2020; 52(5): 392-401.
[http://dx.doi.org/10.4103/ijp.IJP_545_19] [PMID: 33283771]
[4]
Johnson VJ, Kim SH, Sharma RP. Aluminum-maltolate induces apoptosis and necrosis in neuro-2a cells: potential role for p53 signaling. Toxicol Sci 2005; 83(2): 329-39.
[http://dx.doi.org/10.1093/toxsci/kfi028] [PMID: 15537749]
[5]
Shaw CA, Tomljenovic L. Aluminum in the central nervous system (CNS): toxicity in humans and animals, vaccine adjuvants, and auto-immunity. Immunol Res 2013; 56(2-3): 304-16.
[http://dx.doi.org/10.1007/s12026-013-8403-1] [PMID: 23609067]
[6]
Ali AA, Ahmed HI, Abu-Elfotuh K. Modeling stages mimic Alzheimer’s disease induced by different doses of aluminum in rats: focus on progression of the disease in response to time. J Alzheimer’s Parkinsonism Dementia 2016; 1: 1-11.
[7]
MacLeod R, Hillert EK, Cameron RT, Baillie GS. The role and therapeutic targeting of α-, β- and γ-secretase in Alzheimer’s disease. Future Sci OA 2015; 1(3): FSO11.
[http://dx.doi.org/10.4155/fso.15.9] [PMID: 28031886]
[8]
De Strooper B, Vassar R, Golde T. The secretases: enzymes with therapeutic potential in Alzheimer disease. Nat Rev Neurol 2010; 6(2): 99-107.
[http://dx.doi.org/10.1038/nrneurol.2009.218] [PMID: 20139999]
[9]
Chow VW, Mattson MP, Wong PC, Gleichmann M. An overview of APP processing enzymes and products. Neuromolecular Med 2010; 12(1): 1-12.
[http://dx.doi.org/10.1007/s12017-009-8104-z] [PMID: 20232515]
[10]
Peron R, Vatanabe IP, Manzine PR, Camins A, Cominetti MR. Alpha-secretase ADAM10 regulation: insights into Alzheimer’s disease treatment. Pharmaceuticals (Basel) 2018; 11(1): E12.
[http://dx.doi.org/10.3390/ph11010012] [PMID: 29382156]
[11]
Tippmann F, Hundt J, Schneider A, Endres K, Fahrenholz F. Up-regulation of the alpha-secretase ADAM10 by retinoic acid receptors and acitretin. FASEB J 2009; 23(6): 1643-54.
[http://dx.doi.org/10.1096/fj.08-121392] [PMID: 19144697]
[12]
Freese C, Reinhardt S, Hefner G, Unger RE, Kirkpatrick CJ, Endres K. A novel blood-brain barrier co-culture system for drug targeting of Alzheimer’s disease: establishment by using acitretin as a model drug. PLoS One 2014; 9(3): e91003.
[http://dx.doi.org/10.1371/journal.pone.0091003] [PMID: 24608847]
[13]
Li M, Guo K, Ikehara S. Stem cell treatment for Alzheimer’s disease. Int J Mol Sci 2014; 15(10): 19226-38.
[http://dx.doi.org/10.3390/ijms151019226] [PMID: 25342318]
[14]
Duma C, Kopyov O, Kopyov A, et al. Human intracerebroventricular (ICV) injection of autologous, non-engineered, adipose-derived stromal vascular fraction (ADSVF) for neurodegenerative disorders: results of a 3-year phase 1 study of 113 injections in 31 patients. Mol Biol Rep 2019; 46(5): 5257-72.
[http://dx.doi.org/10.1007/s11033-019-04983-5] [PMID: 31327120]
[15]
Li X, Fok KL, Guo J, et al. Retinoic acid promotes stem cell differentiation and embryonic development by transcriptionally activating CFTR. Biochim Biophys Acta Mol Cell Res 2018; 1865(4): 605-15.
[http://dx.doi.org/10.1016/j.bbamcr.2018.01.005] [PMID: 29326073]
[16]
Mishra S, Kelly KK, Rumian NL, Siegenthaler JA. Retinoic acid is required for neural stem and progenitor cell proliferation in the adult hippocampus. Stem Cell Reports 2018; 10(6): 1705-20.
[http://dx.doi.org/10.1016/j.stemcr.2018.04.024] [PMID: 29805108]
[17]
Justin Thenmozhi A, Raja TR, Janakiraman U, Manivasagam T. Neuroprotective effect of hesperidin on aluminium chloride induced Alzheimer’s disease in Wistar rats. Neurochem Res 2015; 40(4): 767-76.
[http://dx.doi.org/10.1007/s11064-015-1525-1] [PMID: 25630717]
[18]
Zimcikova E, Simko J, Karesova I, Kremlacek J, Malakova J. Behavioral effects of antiepileptic drugs in rats: Are the effects on mood and behavior detectable in open-field test? Seizure 2017; 52: 35-40.
[http://dx.doi.org/10.1016/j.seizure.2017.09.015] [PMID: 28957723]
[19]
Deacon RMJ, Rawlins JNP. T-maze alternation in the rodent. Nat Protoc 2006; 1(1): 7-12.
[http://dx.doi.org/10.1038/nprot.2006.2] [PMID: 17406205]
[20]
Abbasi-Oshaghi E, Mirzaei F, Pourjafar M. NLRP3 inflammasome, oxidative stress, and apoptosis induced in the intestine and liver of rats treated with titanium dioxide nanoparticles: In vivo and in vitro study. Int J Nanomedicine 2019; 14: 1919-36.
[http://dx.doi.org/10.2147/IJN.S192382] [PMID: 30936694]
[21]
Mohamed AS, Hosney M, Bassiony H, et al. Sodium pentobarbital dosages for exsanguination affect biochemical, molecular and histolog-ical measurements in rats. Sci Rep 2020; 10(1): 378.
[http://dx.doi.org/10.1038/s41598-019-57252-7] [PMID: 31942001]
[22]
Cao Z, Wang F, Xiu C, Zhang J, Li Y. Hypericum perforatum extract attenuates behavioral, biochemical, and neurochemical abnormalities in Aluminum chloride-induced Alzheimer’s disease rats. Biomed Pharmacother 2017; 91: 931-7.
[http://dx.doi.org/10.1016/j.biopha.2017.05.022] [PMID: 28514831]
[23]
Choi SS, Lee SR, Kim SU, Lee HJ. Alzheimer’s disease and stem cell therapy. Exp Neurobiol 2014; 23(1): 45-52.
[http://dx.doi.org/10.5607/en.2014.23.1.45] [PMID: 24737939]
[24]
Keskin AO, Durmaz N, Uncu G, et al. Future treatment of Alzheimer disease 2019.
[http://dx.doi.org/10.5772/intechopen.85096]
[25]
Munoz JR, Stoutenger BR, Robinson AP, Spees JL, Prockop DJ. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci USA 2005; 102(50): 18171-6.
[http://dx.doi.org/10.1073/pnas.0508945102] [PMID: 16330757]
[26]
Maltman DJ, Hardy SA, Przyborski SA. Role of mesenchymal stem cells in neurogenesis and nervous system repair. Neurochem Int 2011; 59(3): 347-56.
[http://dx.doi.org/10.1016/j.neuint.2011.06.008] [PMID: 21718735]
[27]
Ma T, Gong K, Ao Q, et al. Intracerebral transplantation of adipose-derived mesenchymal stem cells alternatively activates microglia and ameliorates neuropathological deficits in Alzheimer’s disease mice. Cell Transplant 2013; 22(Suppl. 1): S113-26.
[http://dx.doi.org/10.3727/096368913X672181] [PMID: 24070198]
[28]
Misra S, Chopra K, Saikia UN, et al. Effect of mesenchymal stem cells and galantamine nanoparticles in rat model of Alzheimer’s disease. Regen Med 2016; 11(7): 629-46.
[http://dx.doi.org/10.2217/rme-2016-0032] [PMID: 27582416]
[29]
Lee CS, Koo J. A review of acitretin, a systemic retinoid for the treatment of psoriasis. Expert Opin Pharmacother 2005; 6(10): 1725-34.
[http://dx.doi.org/10.1517/14656566.6.10.1725] [PMID: 16086658]
[30]
Postina R, Schroeder A, Dewachter I, et al. A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J Clin Invest 2004; 113(10): 1456-64.
[http://dx.doi.org/10.1172/JCI20864] [PMID: 15146243]
[31]
Kaur A, Gill KD. Possible peripheral markers for chronic aluminium toxicity in Wistar rats. Toxicol Ind Health 2006; 22(1): 39-46.
[http://dx.doi.org/10.1191/0748233706th242oa] [PMID: 16572710]
[32]
Singh NA, Bhardwaj V, Ravi C, Ramesh N, Mandal AKA, Khan ZA. EGCG nanoparticles attenuate aluminum chloride induced neurobe-havioral deficits, beta amyloid and tau pathology in a rat model of Alzheimer’s disease. Front Aging Neurosci 2018; 10: 244.
[http://dx.doi.org/10.3389/fnagi.2018.00244] [PMID: 30150930]
[33]
Chen TJ, Hung HS, Wang DC, Chen SS. The protective effect of Rho-associated kinase inhibitor on aluminum-induced neurotoxicity in rat cortical neurons. Toxicol Sci 2010; 116(1): 264-72.
[http://dx.doi.org/10.1093/toxsci/kfq114] [PMID: 20395307]
[34]
Belaïd-Nouira Y, Bakhta H, Bouaziz M, Flehi-Slim I, Haouas Z, Ben Cheikh H. Study of lipid profile and parieto-temporal lipid peroxida-tion in AlCl3 mediated neurotoxicity. Modulatory effect of fenugreek seeds. Lipids Health Dis 2012; 11: 16.
[http://dx.doi.org/10.1186/1476-511X-11-16] [PMID: 22280491]
[35]
Abd-Elhady RM, Elsheikh AM, Khalifa AE. Anti-amnestic properties of Ginkgo biloba extract on impaired memory function induced by aluminum in rats. Int J Dev Neurosci 2013; 31(7): 598-607.
[http://dx.doi.org/10.1016/j.ijdevneu.2013.07.006] [PMID: 23933390]
[36]
Khan KA, Kumar N, Nayak PG, et al. Impact of caffeic acid on aluminium chloride-induced dementia in rats. J Pharm Pharmacol 2013; 65(12): 1745-52.
[http://dx.doi.org/10.1111/jphp.12126] [PMID: 24236984]
[37]
Taïr K, Kharoubi O, Taïr OA, Hellal N, Benyettou I, Aoues A. Aluminium-induced acute neurotoxicity in rats: treatment with aqueous extract of Arthrophytum (Hammada scoparia). J Acute Dis 2016; 5(6): 470-82.
[http://dx.doi.org/10.1016/j.joad.2016.08.028]
[38]
Ankarcrona M, Winblad B. Biomarkers for apoptosis in Alzheimer’s disease. Int J Geriatr Psychiatry 2005; 20(2): 101-5.
[http://dx.doi.org/10.1002/gps.1260] [PMID: 15660410]
[39]
Ghenimi N, Beauvieux MC, Biran M, Pallet V, Higueret P, Gallis JL. Vitamin A deficiency in rats induces anatomic and metabolic changes comparable with those of neurodegenerative disorders. J Nutr 2009; 139(4): 696-702.
[http://dx.doi.org/10.3945/jn.108.102988] [PMID: 19193816]
[40]
Kalueff AV, Stewart AM, Song C, Berridge KC, Graybiel AM, Fentress JC. Neurobiology of rodent self-grooming and its value for transla-tional neuroscience. Nat Rev Neurosci 2016; 17(1): 45-59.
[http://dx.doi.org/10.1038/nrn.2015.8] [PMID: 26675822]
[41]
Fernández-Teruel A, Estanislau C. Meanings of self-grooming depend on an inverted U-shaped function with aversiveness. Nat Rev Neurosci 2016; 17(9): 591.
[http://dx.doi.org/10.1038/nrn.2016.102] [PMID: 27466142]
[42]
Rojas-Carvajal M, Fornaguera J, Mora-Gallegos A, Brenes JC. Testing experience and environmental enrichment potentiated open-field habituation and grooming behaviour in rats. Anim Behav 2018; 137: 225-35.
[http://dx.doi.org/10.1016/j.anbehav.2018.01.018]
[43]
Pavlik VN, Doody RS, Massman PJ, Chan W. Influence of premorbid IQ and education on progression of Alzheimer’s disease. Dement Geriatr Cogn Disord 2006; 22(4): 367-77.
[http://dx.doi.org/10.1159/000095640] [PMID: 16954693]
[44]
Bertuzzi L, Rosa A, Ourique A, et al. Stem cell’s behavioral effects in rats in a model of Alzheimer’s disease. Adv Stem Cells 2014; 2014: 1-13.
[45]
Safar MM, Arab HH, Rizk SM, El-Maraghy SA. Bone marrow-derived endothelial progenitor cells protect against scopolamine-induced Alzheimer-like pathological aberrations. Mol Neurobiol 2016; 53(3): 1403-18.
[http://dx.doi.org/10.1007/s12035-014-9051-8] [PMID: 25526861]
[46]
Schwerk A, Altschüler J, Roch M, et al. Adipose-derived human mesenchymal stem cells induce long-term neurogenic and anti-inflammatory effects and improve cognitive but not motor performance in a rat model of Parkinson’s disease. Regen Med 2015; 10(4): 431-46.
[http://dx.doi.org/10.2217/rme.15.17] [PMID: 26022763]
[47]
Dos Santos Guilherme M, Stoye NM, Rose-John S, Garbers C, Fellgiebel A, Endres K. The synthetic retinoid acitretin increases IL-6 in the central nervous system of Alzheimer disease model mice and human patients. Front Aging Neurosci 2019; 11: 182.
[http://dx.doi.org/10.3389/fnagi.2019.00182] [PMID: 31396076]
[48]
Sodhi RK, Singh N. All-trans retinoic acid rescues memory deficits and neuropathological changes in mouse model of streptozotocin-induced dementia of Alzheimer’s type. Prog Neuropsychopharmacol Biol Psychiatry 2013; 40: 38-46.
[http://dx.doi.org/10.1016/j.pnpbp.2012.09.012] [PMID: 23044340]
[49]
Behairi N, Belkhelfa M, Rafa H, et al. All-trans retinoic acid (ATRA) prevents lipopolysaccharide-induced neuroinflammation, amyloido-genesis and memory impairment in aged rats. J Neuroimmunol 2016; 300: 21-9.
[http://dx.doi.org/10.1016/j.jneuroim.2016.10.004] [PMID: 27806872]
[50]
O’Reilly KC, Shumake J, Gonzalez-Lima F, Lane MA, Bailey SJ. Chronic administration of 13-cis-retinoic acid increases depression-related behavior in mice. Neuropsychopharmacology 2006; 31(9): 1919-27.
[http://dx.doi.org/10.1038/sj.npp.1300998] [PMID: 16395305]
[51]
Goncalves MB, Clarke E, Hobbs C, et al. Amyloid β inhibits retinoic acid synthesis exacerbating Alzheimer disease pathology which can be attenuated by an retinoic acid receptor α agonist. Eur J Neurosci 2013; 37(7): 1182-92.
[http://dx.doi.org/10.1111/ejn.12142] [PMID: 23379615]
[52]
Etchamendy N, Enderlin V, Marighetto A, et al. Alleviation of a selective age-related relational memory deficit in mice by pharmacologi-cally induced normalization of brain retinoid signaling. J Neurosci 2001; 21(16): 6423-9.
[http://dx.doi.org/10.1523/JNEUROSCI.21-16-06423.2001] [PMID: 11487666]
[53]
Malik MA, Blusztajn JK, Greenwood CE. Nutrients as trophic factors in neurons and the central nervous system: role of retinoic acid. J Nutr Biochem 2000; 11(1): 2-13.
[http://dx.doi.org/10.1016/S0955-2863(99)00066-2] [PMID: 15539337]
[54]
Fathi F, Altiraihi T, Mowla SJ, Movahedin M. Transplantation of retinoic acid treated murine embryonic stem cells & behavioural deficit in Parkinsonian rats. Indian J Med Res 2010; 131: 536-44.
[PMID: 20424305]
[55]
Crandall J, Sakai Y, Zhang J, et al. 13-cis-retinoic acid suppresses hippocampal cell division and hippocampal-dependent learning in mice. Proc Natl Acad Sci USA 2004; 101(14): 5111-6.
[http://dx.doi.org/10.1073/pnas.0306336101] [PMID: 15051884]
[56]
Maden M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci 2007; 8(10): 755-65.
[http://dx.doi.org/10.1038/nrn2212] [PMID: 17882253]
[57]
Bonnet E, Touyarot K, Alfos S, Pallet V, Higueret P, Abrous DN. Retinoic acid restores adult hippocampal neurogenesis and reverses spatial memory deficit in vitamin A deprived rats. PLoS One 2008; 3(10): e3487.
[http://dx.doi.org/10.1371/journal.pone.0003487] [PMID: 18941534]
[58]
Agostinho P, Pliássova A, Oliveira CR, Cunha RA. Localization and trafficking of amyloid-beta protein precursor and secretases: impact on Alzheimer’s disease. J Alzheimers Dis 2015; 45(2): 329-47.
[http://dx.doi.org/10.3233/JAD-142730] [PMID: 25589722]
[59]
Wang L, Hu J, Zhao Y, Lu X, Zhang Q, Niu Q. Effects of aluminium on β-amyloid (1-42) and secretases (APP-cleaving enzymes) in rat brain. Neurochem Res 2014; 39(7): 1338-45.
[http://dx.doi.org/10.1007/s11064-014-1317-z] [PMID: 24792732]
[60]
Finder VH, Vodopivec I, Nitsch RM, Glockshuber R. The recombinant amyloid-beta peptide Abeta1-42 aggregates faster and is more neurotoxic than synthetic Abeta1-42. J Mol Biol 2010; 396(1): 9-18.
[http://dx.doi.org/10.1016/j.jmb.2009.12.016] [PMID: 20026079]
[61]
Verdurand M, Chauveau F, Daoust A, et al. Differential effects of amyloid-beta 1-40 and 1-42 fibrils on 5-HT1A serotonin receptors in rat brain. Neurobiol Aging 2016; 40: 11-21.
[http://dx.doi.org/10.1016/j.neurobiolaging.2015.12.008] [PMID: 26973100]
[62]
Selkoe DJ, Hardy J. The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol Med 2016; 8(6): 595-608.
[http://dx.doi.org/10.15252/emmm.201606210] [PMID: 27025652]
[63]
Praticò D, Uryu K, Sung S, Tang S, Trojanowski JQ, Lee VM. Aluminum modulates brain amyloidosis through oxidative stress in APP transgenic mice. FASEB J 2002; 16(9): 1138-40.
[http://dx.doi.org/10.1096/fj.02-0012fje] [PMID: 12039845]
[64]
Yumoto S, Kakimi S, Ohsaki A, Ishikawa A. Demonstration of aluminum in amyloid fibers in the cores of senile plaques in the brains of patients with Alzheimer’s disease. J Inorg Biochem 2009; 103(11): 1579-84.
[http://dx.doi.org/10.1016/j.jinorgbio.2009.07.023] [PMID: 19744735]
[65]
Harach T, Jammes F, Muller C, et al. Administrations of human adult ischemia-tolerant mesenchymal stem cells and factors reduce amy-loid beta pathology in a mouse model of Alzheimer’s disease. Neurobiol Aging 2017; 51: 83-96.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.11.009] [PMID: 28056358]
[66]
Cui Y, Ma S, Zhang C, et al. Human umbilical cord mesenchymal stem cells transplantation improves cognitive function in Alzheimer’s disease mice by decreasing oxidative stress and promoting hippocampal neurogenesis. Behav Brain Res 2017; 320: 291-301.
[http://dx.doi.org/10.1016/j.bbr.2016.12.021] [PMID: 28007537]
[67]
Kawahara K, Suenobu M, Ohtsuka H, et al. Cooperative therapeutic action of retinoic acid receptor and retinoid x receptor agonists in a mouse model of Alzheimer’s disease. J Alzheimers Dis 2014; 42(2): 587-605.
[http://dx.doi.org/10.3233/JAD-132720] [PMID: 24916544]
[68]
Zhang Q, Zhang F, Ni Y, Kokot S. Effects of aluminum on amyloid-beta aggregation in the context of Alzheimer’s disease. Arab J Chem 2019; 12(8): 2897-904.
[http://dx.doi.org/10.1016/j.arabjc.2015.06.019]
[69]
Kawahara M, Kato-Negishi M. Link between aluminum and the pathogenesis of Alzheimer’s disease: the integration of the aluminum and amyloid cascade hypotheses. Int J Alzheimers Dis 2011; 2011: 276393.
[http://dx.doi.org/10.4061/2011/276393] [PMID: 21423554]
[70]
Ghribi O, Herman MM, DeWitt DA, Forbes MS, Savory J. Abeta(1-42) and aluminum induce stress in the endoplasmic reticulum in rabbit hippocampus, involving nuclear translocation of gadd 153 and NF-kappaB. Brain Res Mol Brain Res 2001; 96(1-2): 30-8.
[http://dx.doi.org/10.1016/S0169-328X(01)00256-X] [PMID: 11731006]
[71]
Mrass P, Rendl M, Mildner M, et al. Retinoic acid increases the expression of p53 and proapoptotic caspases and sensitizes keratinocytes to apoptosis: a possible explanation for tumor preventive action of retinoids. Cancer Res 2004; 64(18): 6542-8.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-1129] [PMID: 15374966]
[72]
Wang GH, Liu Y, Wu XB, et al. Neuroprotective effects of human umbilical cord-derived mesenchymal stromal cells combined with ni-modipine against radiation-induced brain injury through inhibition of apoptosis. Cytotherapy 2016; 18(1): 53-64.
[http://dx.doi.org/10.1016/j.jcyt.2015.10.006] [PMID: 26719199]
[73]
Rafat A, Mohammadi Roushandeh A, Alizadeh A, Hashemi-Firouzi N, Golipoor Z. Comparison of the melatonin preconditioning efficacy between bone marrow and adipose-derived mesenchymal stem cells. Cell J 2019; 20(4): 450-8.
[PMID: 30123990]
[74]
Wang Q, Zhang L, Yuan X, et al. The relationship between the Bcl-2/Bax proteins and the mitochondria-mediated apoptosis pathway in the differentiation of adipose-derived stromal cells into neurons. PLoS One 2016; 11(10): e0163327.
[http://dx.doi.org/10.1371/journal.pone.0163327] [PMID: 27706181]
[75]
Liu T, Lee M, Ban JJ, Im W, Mook-Jung I, Kim M. Cytosolic extract of human adipose stem cells reverses the amyloid beta-induced mito-chondrial apoptosis via P53/Foxo3a pathway. PLoS One 2017; 12(1): e0168859.
[http://dx.doi.org/10.1371/journal.pone.0168859] [PMID: 28046000]
[76]
Sodhi RK, Singh N. Retinoids as potential targets for Alzheimer’s disease. Pharmacol Biochem Behav 2014; 120: 117-23.
[http://dx.doi.org/10.1016/j.pbb.2014.02.016] [PMID: 24582848]
[77]
Behairi N, Belkhelfa M, Mesbah-Amroun H, et al. All-trans-retinoic acid modulates nitric oxide and interleukin-17A production by pe-ripheral blood mononuclear cells from patients with Alzheimer’s disease. Neuroimmunomodulation 2015; 22(6): 385-93.
[http://dx.doi.org/10.1159/000435885] [PMID: 26278415]
[78]
Kim S, Chang KA, Kim Ja, et al. The preventive and therapeutic effects of intravenous human adipose-derived stem cells in Alzheimer’s disease mice. PLoS One 2012; 7(9): e45757.
[http://dx.doi.org/10.1371/journal.pone.0045757] [PMID: 23049854]
[79]
Ha S, Ahn S, Kim S, et al. In vivo imaging of human adipose-derived stem cells in Alzheimer’s disease animal model. J Biomed Opt 2014; 19(5): 051206.
[http://dx.doi.org/10.1117/1.JBO.19.5.051206] [PMID: 24297061]
[80]
Kalinin S, Gavrilyuk V, Polak PE, et al. Noradrenaline deficiency in brain increases beta-amyloid plaque burden in an animal model of Alzheimer’s disease. Neurobiol Aging 2007; 28(8): 1206-14.
[http://dx.doi.org/10.1016/j.neurobiolaging.2006.06.003] [PMID: 16837104]
[81]
Khakpai F, Nasehi M, Haeri-Rohani A, Eidi A, Zarrindast MR. Septo-hippocampo-septal loop and memory formation. Basic Clin Neurosci 2013; 4(1): 5-23.
[PMID: 25337323]
[82]
Sun ZZ, Chen ZB, Jiang H, Li LL, Li EG, Xu Y. Alteration of Aβ metabolism-related molecules in predementia induced by AlCl3 and D-galactose. Age (Dordr) 2009; 31(4): 277-84.
[http://dx.doi.org/10.1007/s11357-009-9099-y] [PMID: 19468866]
[83]
Auti ST, Kulkarni YA. Neuroprotective effect of cardamom oil against aluminum induced neurotoxicity in rats. Front Neurol 2019; 10: 399.
[http://dx.doi.org/10.3389/fneur.2019.00399] [PMID: 31114535]
[84]
Kaizer RR, Corrêa MC, Spanevello RM, et al. Acetylcholinesterase activation and enhanced lipid peroxidation after long-term exposure to low levels of aluminum on different mouse brain regions. J Inorg Biochem 2005; 99(9): 1865-70.
[http://dx.doi.org/10.1016/j.jinorgbio.2005.06.015] [PMID: 16055195]
[85]
Prakash D, Sudhandiran G. Dietary flavonoid fisetin regulates aluminium chloride-induced neuronal apoptosis in cortex and hippocampus of mice brain. J Nutr Biochem 2015; 26(12): 1527-39.
[http://dx.doi.org/10.1016/j.jnutbio.2015.07.017] [PMID: 26411262]
[86]
Hyman BT, Yuan J. Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat Rev Neurosci 2012; 13(6): 395-406.
[http://dx.doi.org/10.1038/nrn3228] [PMID: 22595785]
[87]
Eikelenboom P, Bate C, Van Gool WA, et al. Neuroinflammation in Alzheimer’s disease and prion disease. Glia 2002; 40(2): 232-9.
[http://dx.doi.org/10.1002/glia.10146] [PMID: 12379910]
[88]
Millington C, Sonego S, Karunaweera N, et al. Chronic neuroinflammation in Alzheimer’s disease: new perspectives on animal models and promising candidate drugs. BioMed Res Int 2014; 2014: 309129.
[http://dx.doi.org/10.1155/2014/309129] [PMID: 25025046]
[89]
Xie SS, Wang X, Jiang N, et al. Multi-target tacrine-coumarin hybrids: cholinesterase and monoamine oxidase B inhibition properties against Alzheimer’s disease. Eur J Med Chem 2015; 95: 153-65.
[http://dx.doi.org/10.1016/j.ejmech.2015.03.040] [PMID: 25812965]
[90]
Wojtunik-Kulesza KA, Oniszczuk A, Oniszczuk T, Waksmundzka-Hajnos M. The influence of common free radicals and antioxidants on development of Alzheimer’s Disease. Biomed Pharmacother 2016; 78: 39-49.
[http://dx.doi.org/10.1016/j.biopha.2015.12.024] [PMID: 26898423]
[91]
Park D, Yang G, Bae DK, et al. Human adipose tissue-derived mesenchymal stem cells improve cognitive function and physical activity in ageing mice. J Neurosci Res 2013; 91(5): 660-70.
[http://dx.doi.org/10.1002/jnr.23182] [PMID: 23404260]
[92]
Shin JY, Park HJ, Kim HN, et al. Mesenchymal stem cells enhance autophagy and increase β-amyloid clearance in Alzheimer disease models. Autophagy 2014; 10(1): 32-44.
[http://dx.doi.org/10.4161/auto.26508] [PMID: 24149893]
[93]
Lee EY, Xia Y, Kim WS, et al. Hypoxia-enhanced wound-healing function of adipose-derived stem cells: increase in stem cell prolifera-tion and up-regulation of VEGF and bFGF. Wound Repair Regen 2009; 17(4): 540-7.
[http://dx.doi.org/10.1111/j.1524-475X.2009.00499.x] [PMID: 19614919]
[94]
Katsuda T, Tsuchiya R, Kosaka N, et al. Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exo-somes. Sci Rep 2013; 3: 1197.
[http://dx.doi.org/10.1038/srep01197] [PMID: 23378928]
[95]
Jiang L, Jones S, Jia X. Stem cell transplantation for peripheral nerve regeneration: current options and opportunities. Int J Mol Sci 2017; 18(1): E94.
[http://dx.doi.org/10.3390/ijms18010094] [PMID: 28067783]
[96]
Kazemiha M, Sarveazad A, Moradi F, et al. Histological and behavioral alterations following hADSCs intravenous administration in Alz-heimer’s rat model. Thrita 2020; 8(1): 99975.
[http://dx.doi.org/10.5812/thrita.99975]
[97]
Dheen ST, Jun Y, Yan Z, Tay SS, Ling EA. Retinoic acid inhibits expression of TNF-alpha and iNOS in activated rat microglia. Glia 2005; 50(1): 21-31.
[http://dx.doi.org/10.1002/glia.20153] [PMID: 15602748]
[98]
Ding Y, Qiao A, Wang Z, et al. Retinoic acid attenuates beta-amyloid deposition and rescues memory deficits in an Alzheimer’s disease transgenic mouse model. J Neurosci 2008; 28(45): 11622-34.
[http://dx.doi.org/10.1523/JNEUROSCI.3153-08.2008] [PMID: 18987198]
[99]
Gunes Bilgili S, Calka O, Akdeniz N, Bayram I, Metin A. The effects of retinoids on secondary wound healing: biometrical and histo-pathological study in rats. J Dermatolog Treat 2013; 24(4): 283-9.
[http://dx.doi.org/10.3109/09546634.2012.697985] [PMID: 22646471]
[100]
Hou L, Du Y, Zhao C, Wu Y. PAX2 may induce ADAM10 expression in renal tubular epithelial cells and contribute to epithelial-to-mesenchymal transition. Int Urol Nephrol 2018; 50(9): 1729-41.
[http://dx.doi.org/10.1007/s11255-018-1956-0] [PMID: 30117015]

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