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Current Stem Cell Research & Therapy

Editor-in-Chief

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

Mini-Review Article

Stem Cells as a Potential Therapeutic Option for Treating Neurodegenerative Diseases

Author(s): L Aishwarya, Dharmarajan Arun and Suresh Kannan

Volume 17, Issue 7, 2022

Published on: 10 August, 2021

Page: [590 - 605] Pages: 16

DOI: 10.2174/1574888X16666210810105136

Price: $65

Abstract

In future, neurodegenerative diseases will take over cancer's place and become the major cause of death in the world, especially in developed countries. Advancements in the medical field and its facilities have led to an increase in the old age population, and thus contributing to the increase in number of people suffering from neurodegenerative diseases. Economically it is a great burden to society and the affected family. No current treatment aims to replace, protect, and regenerate lost neurons; instead, it alleviates the symptoms, extends the life span by a few months and creates severe side effects. Moreover, people who are affected are physically dependent for performing their basic activities, which makes their life miserable. There is an urgent need for therapy that could be able to overcome the deficits of conventional therapy for neurodegenerative diseases. Stem cells, the unspecialized cells with the properties of self-renewing and potency to differentiate into various cells types, can become a potent therapeutic option for neurodegenerative diseases. Stem cells have been widely used in clinical trials to evaluate their potential in curing different types of ailments. In this review, we discuss the various types of stem cells and their potential use in the treatment of neurodegenerative diseases-plural based on published preclinical and clinical studies.

Keywords: Stem cells, neurodegenerative diseases, conventional therapy, regeneration, stem cell treatment, preclinical and clinical trial.

Graphical Abstract
[1]
Gammon K. Neurodegenerative disease: Brain windfall. Nature 2014; 515(7526): 299-300.
[http://dx.doi.org/10.1038/nj7526-299a] [PMID: 25396246]
[2]
Wilcock GK, Esiri MM. Plaques, tangles and dementia. A quantitative study. J Neurol Sci 1982; 56(2-3): 343-56.
[http://dx.doi.org/10.1016/0022-510X(82)90155-1] [PMID: 7175555]
[3]
Sonntag KC, Pruszak J, Yoshizaki T, van Arensbergen J, Sanchez-Pernaute R, Isacson O. Enhanced yield of neuroepithelial precursors and midbrain-like dopaminergic neurons from human embryonic stem cells using the bone morphogenic protein antagonist noggin. Stem Cells 2007; 25(2): 411-8.
[http://dx.doi.org/10.1634/stemcells.2006-0380] [PMID: 17038668]
[4]
Sawa A, Tomoda T, Bae BI. Mechanisms of neuronal cell death in Huntington’s disease. Cytogenet Genome Res 2003; 100(1-4): 287-95.
[http://dx.doi.org/10.1159/000072864] [PMID: 14526190]
[5]
Walling AD. Amyotrophic lateral sclerosis: Lou Gehrig’s disease. Am Fam Physician 1999; 59(6): 1489-96.
[PMID: 10193591]
[6]
Da Cruz S, Cleveland DW. Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Curr Opin Neurobiol 2011; 21(6): 904-19.
[http://dx.doi.org/10.1016/j.conb.2011.05.029] [PMID: 21813273]
[7]
Compston A, Coles A. Multiple sclerosis. Lancet 2008; 372(9648): 1502-17.
[http://dx.doi.org/10.1016/S0140-6736(08)61620-7] [PMID: 18970977]
[8]
Dong F, Caplan AI. Cell transplantation as an initiator of endogenous stem cell-based tissue repair. Curr Opin Organ Transplant 2012; 17(6): 670-4.
[http://dx.doi.org/10.1097/MOT.0b013e328359a617] [PMID: 23111645]
[9]
Choi SS, Lee S-R, 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]
[10]
Nayak MS, Kim Y-S, Goldman M, Keirstead HS, Kerr DA. Cellular therapies in motor neuron diseases. Biochim Biophys Acta 2006; 1762(11-12): 1128-38.
[http://dx.doi.org/10.1016/j.bbadis.2006.06.004] [PMID: 16872810]
[11]
Weiss ML, Troyer DL. Stem cells in the umbilical cord. Stem Cell Rev 2006; 2(2): 155-62.
[http://dx.doi.org/10.1007/s12015-006-0022-y] [PMID: 17237554]
[12]
Thomson JA. Embryonic stem cell lines derived from human blastocysts. Science (80- ) 1998; 282: 1145-7.
[13]
Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat Biotechnol 2000; 18(4): 399-404.
[http://dx.doi.org/10.1038/74447] [PMID: 10748519]
[14]
Zhang S-C, Wernig M, Duncan ID, Brüstle O, Thomson JA. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 2001; 19(12): 1129-33.
[http://dx.doi.org/10.1038/nbt1201-1129] [PMID: 11731781]
[15]
Acharya MM, Christie LA, Lan ML, et al. Rescue of radiation-induced cognitive impairment through cranial transplantation of human embryonic stem cells. Proc Natl Acad Sci USA 2009; 106(45): 19150-5.
[http://dx.doi.org/10.1073/pnas.0909293106] [PMID: 19901336]
[16]
Tang J, Xu H, Fan X, et al. Embryonic stem cell-derived neural precursor cells improve memory dysfunction in Abeta(1-40) injured rats. Neurosci Res 2008; 62(2): 86-96.
[http://dx.doi.org/10.1016/j.neures.2008.06.005] [PMID: 18634835]
[17]
Moghadam FH, Alaie H, Karbalaie K, Tanhaei S, Nasr Esfahani MH, Baharvand H. Transplantation of primed or unprimed mouse embryonic stem cell-derived neural precursor cells improves cognitive function in Alzheimerian rats. Differentiation 2009; 78(2-3): 59-68.
[http://dx.doi.org/10.1016/j.diff.2009.06.005] [PMID: 19616885]
[18]
Yue W, Li Y, Zhang T, et al. ESC-derived basal forebrain cholinergic neurons ameliorate the cognitive symptoms associated with alzheimer’s disease in mouse models. Stem Cell Reports 2015; 5(5): 776-90.
[http://dx.doi.org/10.1016/j.stemcr.2015.09.010] [PMID: 26489896]
[19]
Sanchez-Pernaute R, Lee H, Patterson M, et al. Parthenogenetic dopamine neurons from primate embryonic stem cells restore function in experimental Parkinson’s disease. Brain 2008; 131(Pt 8): 2127-39.
[http://dx.doi.org/10.1093/brain/awn144] [PMID: 18669499]
[20]
Kim J-H, Auerbach JM, Rodríguez-Gómez JA, et al. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson’s disease. Nature 2002; 418(6893): 50-6.
[http://dx.doi.org/10.1038/nature00900] [PMID: 12077607]
[21]
Gantner CW, de Luzy IR, Kauhausen JA, et al. Viral delivery of gdnf promotes functional integration of human stem cell grafts in Parkinson’s disease. Cell Stem Cell 2020; 26(4): 511-526.e5.
[http://dx.doi.org/10.1016/j.stem.2020.01.010] [PMID: 32059808]
[22]
Kirkeby A, Grealish S, Wolf DA, et al. Generation of regionally specified neural progenitors and functional neurons from human embryonic stem cells under defined conditions. Cell Rep 2012; 1(6): 703-14.
[http://dx.doi.org/10.1016/j.celrep.2012.04.009] [PMID: 22813745]
[23]
Kriks S, Shim JW, Piao J, et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson’s disease. Nature 2011; 480(7378): 547-51.
[http://dx.doi.org/10.1038/nature10648] [PMID: 22056989]
[24]
Steinbeck JA, Choi SJ, Mrejeru A, et al. Optogenetics enables functional analysis of human embryonic stem cell-derived grafts in a Parkinson’s disease model. Nat Biotechnol 2015; 33(2): 204-9.
[http://dx.doi.org/10.1038/nbt.3124] [PMID: 25580598]
[25]
Daadi MM, Grueter BA, Malenka RC, Redmond DE Jr, Steinberg GK. Dopaminergic neurons from midbrain-specified human embryonic stem cell-derived neural stem cells engrafted in a monkey model of Parkinson’s disease. PLoS One 2012; 7(7): e41120.
[http://dx.doi.org/10.1371/journal.pone.0041120] [PMID: 22815935]
[26]
Wang YK, Zhu WW, Wu MH, et al. Human clinical-grade parthenogenetic esc-derived dopaminergic neurons recover locomotive defects of nonhuman primate models of Parkinson’s disease. Stem Cell Reports 2018; 11(1): 171-82.
[http://dx.doi.org/10.1016/j.stemcr.2018.05.010] [PMID: 29910127]
[27]
Aubry L, Bugi A, Lefort N, Rousseau F, Peschanski M, Perrier AL. Striatal progenitors derived from human ES cells mature into DARPP32 neurons in vitro and in quinolinic acid-lesioned rats. Proc Natl Acad Sci USA 2008; 105(43): 16707-12.
[http://dx.doi.org/10.1073/pnas.0808488105] [PMID: 18922775]
[28]
Delli Carri A, Onorati M, Lelos MJ, et al. Developmentally coordinated extrinsic signals drive human pluripotent stem cell differentiation toward authentic DARPP-32+ medium-sized spiny neurons. Development 2013; 140(2): 301-12.
[http://dx.doi.org/10.1242/dev.084608] [PMID: 23250204]
[29]
Ma L, Hu B, Liu Y, et al. Human embryonic stem cell-derived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice. Cell Stem Cell 2012; 10(4): 455-64.
[http://dx.doi.org/10.1016/j.stem.2012.01.021] [PMID: 22424902]
[30]
Aharonowiz M, Einstein O, Fainstein N, Lassmann H, Reubinoff B, Ben-Hur T. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS One 2008; 3(9): e3145.
[http://dx.doi.org/10.1371/journal.pone.0003145] [PMID: 18773082]
[31]
Wang X, Kimbrel EA, Ijichi K, et al. Human ESC-derived MSCs outperform bone marrow MSCs in the treatment of an EAE model of multiple sclerosis. Stem Cell Reports 2014; 3(1): 115-30.
[http://dx.doi.org/10.1016/j.stemcr.2014.04.020] [PMID: 25068126]
[32]
Yan L, Jiang B, Niu Y, et al. Intrathecal delivery of human ESC-derived mesenchymal stem cell spheres promotes recovery of a primate multiple sclerosis model. Cell Death Discov 2018; 4: 28.
[http://dx.doi.org/10.1038/s41420-018-0091-0] [PMID: 30131877]
[33]
Li X-J, Du Z-W, Zarnowska ED, et al. Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 2005; 23(2): 215-21.
[http://dx.doi.org/10.1038/nbt1063] [PMID: 15685164]
[34]
Wyatt TJ, Rossi SL, Siegenthaler MM, et al. Human motor neuron progenitor transplantation leads to endogenous neuronal sparing in 3 models of motor neuron loss. Stem Cells Int 2011; 2011: 207230.
[35]
Izrael M, Slutsky SG, Admoni T, et al. Safety and efficacy of human embryonic stem cell-derived astrocytes following intrathecal transplantation in SOD1G93A and NSG animal models. Stem Cell Res Ther 2018; 9(1): 152.
[http://dx.doi.org/10.1186/s13287-018-0890-5] [PMID: 29871694]
[36]
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-76.
[http://dx.doi.org/10.1016/j.cell.2006.07.024] [PMID: 16904174]
[37]
Tang J. How close is the stem cell cure to the alzheimer’s disease: Future and beyond? Neural Regen Res 2012; 7(1): 66-71.
[PMID: 25806061]
[38]
Pang ZP, Yang N, Vierbuchen T, et al. Induction of human neuronal cells by defined transcription factors. Nature 2011; 476(7359): 220-3.
[http://dx.doi.org/10.1038/nature10202] [PMID: 21617644]
[39]
Wernig M, Zhao J-P, Pruszak J, et al. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson’s disease. Proc Natl Acad Sci USA 2008; 105(15): 5856-61.
[http://dx.doi.org/10.1073/pnas.0801677105] [PMID: 18391196]
[40]
Matsumoto T, Fujimori K, Andoh-Noda T, et al. Functional neurons generated from t cell-derived induced pluripotent stem cells for neurological disease modeling. Stem Cell Reports 2016; 6(3): 422-35.
[http://dx.doi.org/10.1016/j.stemcr.2016.01.010] [PMID: 26905201]
[41]
Nguyen HN, Byers B, Cord B, et al. LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 2011; 8(3): 267-80.
[http://dx.doi.org/10.1016/j.stem.2011.01.013] [PMID: 21362567]
[42]
Gunhanlar N, Shpak G, van der Kroeg M, et al. A simplified protocol for differentiation of electrophysiologically mature neuronal networks from human induced pluripotent stem cells. Mol Psychiatry 2018; 23(5): 1336-44.
[http://dx.doi.org/10.1038/mp.2017.56] [PMID: 28416807]
[43]
Fujiwara N, Shimizu J, Takai K, et al. Restoration of spatial memory dysfunction of human APP transgenic mice by transplantation of neuronal precursors derived from human iPS cells. Neurosci Lett 2013; 557(Pt B): 129-34.
[http://dx.doi.org/10.1016/j.neulet.2013.10.043] [PMID: 24466594]
[44]
Cha M-Y, Kwon Y-W, Ahn H-S, et al. Protein-induced pluripotent stem cells ameliorate cognitive dysfunction and reduce aβ deposition in a mouse model of alzheimer’s disease. Stem Cells Transl Med 2017; 6(1): 293-305.
[http://dx.doi.org/10.5966/sctm.2016-0081] [PMID: 28170178]
[45]
Takamatsu K, Ikeda T, Haruta M, et al. Degradation of amyloid beta by human induced pluripotent stem cell-derived macrophages expressing Neprilysin-2. Stem Cell Res 2014; 13(3 Pt A): 442-53.
[http://dx.doi.org/10.1016/j.scr.2014.10.001] [PMID: 25460605]
[46]
Doi D, Magotani H, Kikuchi T, et al. Pre-clinical study of induced pluripotent stem cell-derived dopaminergic progenitor cells for Parkinson’s disease. Nat Commun 2020; 11(1): 3369.
[http://dx.doi.org/10.1038/s41467-020-17165-w] [PMID: 32632153]
[47]
Rhee YH, Ko JY, Chang MY, et al. Protein-based human iPS cells efficiently generate functional dopamine neurons and can treat a rat model of Parkinson disease. J Clin Invest 2011; 121(6): 2326-35.
[http://dx.doi.org/10.1172/JCI45794] [PMID: 21576821]
[48]
Kikuchi T, Morizane A, Doi D, et al. Survival of human induced pluripotent stem cell-derived midbrain dopaminergic neurons in the brain of a primate model of Parkinson’s disease. J Parkinsons Dis 2011; 1(4): 395-412.
[http://dx.doi.org/10.3233/JPD-2011-11070] [PMID: 23933658]
[49]
Hargus G, Cooper O, Deleidi M, et al. Differentiated Parkinson patient-derived induced pluripotent stem cells grow in the adult rodent brain and reduce motor asymmetry in Parkinsonian rats. Proc Natl Acad Sci USA 2010; 107(36): 15921-6.
[http://dx.doi.org/10.1073/pnas.1010209107] [PMID: 20798034]
[50]
Morizane A, Kikuchi T, Hayashi T, et al. MHC matching improves engraftment of iPSC-derived neurons in non-human primates. Nat Commun 2017; 8(1): 385.
[http://dx.doi.org/10.1038/s41467-017-00926-5] [PMID: 28855509]
[51]
Kikuchi T, Morizane A, Doi D, et al. Human iPS cell-derived dopaminergic neurons function in a primate Parkinson’s disease model. Nature 2017; 548(7669): 592-6.
[http://dx.doi.org/10.1038/nature23664] [PMID: 28858313]
[52]
Jeon I, Choi C, Lee N, et al. In vivo roles of a patient-derived induced pluripotent stem cell line (hd72-ipsc) in the yac128 model of Huntington’s disease. Int J Stem Cells 2014; 7(1): 43-7.
[http://dx.doi.org/10.15283/ijsc.2014.7.1.43] [PMID: 24921027]
[53]
Fink KD, Crane AT, Lévêque X, et al. Intrastriatal transplantation of adenovirus-generated induced pluripotent stem cells for treating neuropathological and functional deficits in a rodent model of Huntington’s disease. Stem Cells Transl Med 2014; 3(5): 620-31.
[http://dx.doi.org/10.5966/sctm.2013-0151] [PMID: 24657963]
[54]
Mu S, Wang J, Zhou G, et al. Transplantation of induced pluripotent stem cells improves functional recovery in Huntington’s disease rat model. PLoS One 2014; 9(7): e101185.
[http://dx.doi.org/10.1371/journal.pone.0101185] [PMID: 25054283]
[55]
Al-Gharaibeh A, Culver R, Stewart AN, et al. Induced pluripotent stem cell-derived neural stem cell transplantations reduced behavioral deficits and ameliorated neuropathological changes in yac128 mouse model of Huntington’s disease. Front Neurosci 2017; 11: 628.
[http://dx.doi.org/10.3389/fnins.2017.00628] [PMID: 29209158]
[56]
Cho IK, Hunter CE, Ye S, Pongos AL, Chan AWS. Combination of stem cell and gene therapy ameliorates symptoms in Huntington’s disease mice. NPJ Regen Med 2019; 4: 7.
[http://dx.doi.org/10.1038/s41536-019-0066-7] [PMID: 30937182]
[57]
Laterza C, Merlini A, De Feo D, et al. iPSC-derived neural precursors exert a neuroprotective role in immune-mediated demyelination via the secretion of LIF. Nat Commun 2013; 4: 2597.
[http://dx.doi.org/10.1038/ncomms3597] [PMID: 24169527]
[58]
Wang S, Bates J, Li X, et al. Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 2013; 12(2): 252-64.
[http://dx.doi.org/10.1016/j.stem.2012.12.002] [PMID: 23395447]
[59]
Douvaras P, Wang J, Zimmer M, et al. Efficient generation of myelinating oligodendrocytes from primary progressive multiple sclerosis patients by induced pluripotent stem cells. Stem Cell Reports 2014; 3(2): 250-9.
[http://dx.doi.org/10.1016/j.stemcr.2014.06.012] [PMID: 25254339]
[60]
Zhang C, Cao J, Li X, et al. Treatment of multiple sclerosis by transplantation of neural stem cells derived from induced pluripotent stem cells. Sci China Life Sci 2016; 59(9): 950-7.
[http://dx.doi.org/10.1007/s11427-016-0114-9] [PMID: 27233903]
[61]
Nizzardo M, Simone C, Rizzo F, et al. Minimally invasive transplantation of iPSC-derived ALDHhiSSCloVLA4+ neural stem cells effectively improves the phenotype of an amyotrophic lateral sclerosis model. Hum Mol Genet 2014; 23(2): 342-54.
[http://dx.doi.org/10.1093/hmg/ddt425] [PMID: 24006477]
[62]
Kondo T, Funayama M, Tsukita K, et al. Focal transplantation of human iPSC-derived glial-rich neural progenitors improves lifespan of ALS mice. Stem Cell Reports 2014; 3(2): 242-9.
[http://dx.doi.org/10.1016/j.stemcr.2014.05.017] [PMID: 25254338]
[63]
McBride JL, Behrstock SP, Chen EY, et al. Human neural stem cell transplants improve motor function in a rat model of Huntington’s disease. J Comp Neurol 2004; 475(2): 211-9.
[http://dx.doi.org/10.1002/cne.20176] [PMID: 15211462]
[64]
Pirhajati Mahabadi V, Movahedin M, Semnanian S, Mirnajafi-Zadeh J, Faizi M. In vitro differentiation of neural stem cells into noradrenergic-like cells. Int J Mol Cell Med 2015; 4(1): 22-31.
[PMID: 25815279]
[65]
Wang L, Martin DR, Baker HJ, et al. Neural progenitor cell transplantation and imaging in a large animal model. Neurosci Res 2007; 59(3): 327-40.
[http://dx.doi.org/10.1016/j.neures.2007.08.011] [PMID: 17897743]
[66]
Alizadeh R, Hassanzadeh G, Joghataei MT, et al. In vitro differentiation of neural stem cells derived from human olfactory bulb into dopaminergic-like neurons. Eur J Neurosci 2017; 45(6): 773-84.
[http://dx.doi.org/10.1111/ejn.13504] [PMID: 27987378]
[67]
Zhu J, Zhou L, XingWu F. Tracking neural stem cells in patients with brain trauma. N Engl J Med 2006; 355(22): 2376-8.
[http://dx.doi.org/10.1056/NEJMc055304] [PMID: 17135597]
[68]
Blurton-Jones M, Kitazawa M, Martinez-Coria H, et al. Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci USA 2009; 106(32): 13594-9.
[http://dx.doi.org/10.1073/pnas.0901402106] [PMID: 19633196]
[69]
Park D, Yang YH, Bae DK, et al. Improvement of cognitive function and physical activity of aging mice by human neural stem cells over-expressing choline acetyltransferase. Neurobiol Aging 2013; 34(11): 2639-46.
[http://dx.doi.org/10.1016/j.neurobiolaging.2013.04.026] [PMID: 23731954]
[70]
Blurton-Jones M, Spencer B, Michael S, et al. Neural stem cells genetically-modified to express neprilysin reduce pathology in Alzheimer transgenic models. Stem Cell Res Ther 2014; 5(2): 46.
[http://dx.doi.org/10.1186/scrt440] [PMID: 25022790]
[71]
ON K. Peri-hippocampal stem cell transplantation rescues cognitive decline in alzheimer’s disease. Proceedings of the congress of neurological surgeons annual meeting; 2014. Boston, MA, USA.
[72]
McGinley LM, Kashlan ON, Bruno ES, et al. Human neural stem cell transplantation improves cognition in a murine model of Alzheimer’s disease. Sci Rep 2018; 8(1): 14776.
[http://dx.doi.org/10.1038/s41598-018-33017-6] [PMID: 30283042]
[73]
Li B, Liu J, Gu G, Han X, Zhang Q, Zhang W. Impact of neural stem cell-derived extracellular vesicles on mitochondrial dysfunction, sirtuin 1 level, and synaptic deficits in Alzheimer’s disease. J Neurochem 2020; 154(5): 502-18.
[http://dx.doi.org/10.1111/jnc.15001] [PMID: 32145065]
[74]
Marsh SE, Yeung ST, Torres M, et al. HuCNs-sc human nscs fail to differentiate, form ectopic clusters, and provide no cognitive benefits in a transgenic model of Alzheimer’s disease. Stem Cell Reports 2017; 8(2): 235-48.
[http://dx.doi.org/10.1016/j.stemcr.2016.12.019] [PMID: 28199828]
[75]
Madhavan L, Daley BF, Paumier KL, Collier TJ. Transplantation of subventricular zone neural precursors induces an endogenous precursor cell response in a rat model of Parkinson’s disease. J Comp Neurol 2009; 515(1): 102-15.
[http://dx.doi.org/10.1002/cne.22033] [PMID: 19399899]
[76]
Deng X, Liang Y, Lu H, et al. Co-transplantation of GDNF-overexpressing neural stem cells and fetal dopaminergic neurons mitigates motor symptoms in a rat model of Parkinson’s disease. PLoS One 2013; 8(12): e80880.
[http://dx.doi.org/10.1371/journal.pone.0080880] [PMID: 24312503]
[77]
Yasuhara T, Matsukawa N, Hara K, et al. Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson’s disease. J Neurosci 2006; 26(48): 12497-511.
[http://dx.doi.org/10.1523/JNEUROSCI.3719-06.2006] [PMID: 17135412]
[78]
Redmond DE Jr, Bjugstad KB, Teng YD, et al. Behavioral improvement in a primate Parkinson’s model is associated with multiple homeostatic effects of human neural stem cells. Proc Natl Acad Sci USA 2007; 104(29): 12175-80.
[http://dx.doi.org/10.1073/pnas.0704091104] [PMID: 17586681]
[79]
Armstrong RJE, Watts C, Svendsen CN, Dunnett SB, Rosser AE. Survival, neuronal differentiation, and fiber outgrowth of propagated human neural precursor grafts in an animal model of Huntington’s disease. Cell Transplant 2000; 9(1): 55-64.
[http://dx.doi.org/10.1177/096368970000900108] [PMID: 10784067]
[80]
Lee ST, Chu K, Park JE, et al. Intravenous administration of human neural stem cells induces functional recovery in Huntington’s disease rat model. Neurosci Res 2005; 52(3): 243-9.
[http://dx.doi.org/10.1016/j.neures.2005.03.016] [PMID: 15896865]
[81]
Pluchino S, Zanotti L, Rossi B, et al. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005; 436(7048): 266-71.
[http://dx.doi.org/10.1038/nature03889] [PMID: 16015332]
[82]
Einstein O, Friedman-Levi Y, Grigoriadis N, Ben-Hur T. Development/plasticity/repair transplanted neural precursors enhance host brain-derived myelin regeneration. J Neurosci 2009; 29(50): 15694-702.
[83]
Lee YE, An J, Lee KH, et al. The synergistic local immunosuppressive effects of neural stem cells expressing indoleamine 2,3-dioxygenase (ido) in an experimental autoimmune encephalomyelitis (eae) animal model. PLoS One 2015; 10(12): e0144298.
[http://dx.doi.org/10.1371/journal.pone.0144298] [PMID: 26636969]
[84]
Li X, Zhang Y, Yan Y, et al. Neural stem cells engineered to express three therapeutic factors mediate recovery from chronic stage cns autoimmunity. Mol Ther 2016; 24(8): 1456-69.
[http://dx.doi.org/10.1038/mt.2016.104] [PMID: 27203442]
[85]
Corti S, Locatelli F, Papadimitriou D, et al. Neural stem cells LewisX+ CXCR4+ modify disease progression in an amyotrophic lateral sclerosis model. Brain 2007; 130(Pt 5): 1289-305.
[http://dx.doi.org/10.1093/brain/awm043] [PMID: 17439986]
[86]
Xu L, Yan J, Chen D, et al. Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 2006; 82(7): 865-75.
[http://dx.doi.org/10.1097/01.tp.0000235532.00920.7a] [PMID: 17038899]
[87]
Zalfa C, Rota Nodari L, Vacchi E, et al. Transplantation of clinical-grade human neural stem cells reduces neuroinflammation, prolongs survival and delays disease progression in the SOD1 rats. Cell Death Dis 2019; 10(5): 345.
[http://dx.doi.org/10.1038/s41419-019-1582-5] [PMID: 31024007]
[88]
Hwang DH, Lee HJ, Park IH, et al. Intrathecal transplantation of human neural stem cells overexpressing VEGF provide behavioral improvement, disease onset delay and survival extension in transgenic ALS mice. Gene Ther 2009; 16(10): 1234-44.
[http://dx.doi.org/10.1038/gt.2009.80] [PMID: 19626053]
[89]
Ryan JM, Barry FP, Murphy JM, Mahon BP. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm 2005; 2: 8.
[90]
Trzaska KA, King CC, Li KY, et al. Brain-derived neurotrophic factor facilitates maturation of mesenchymal stem cell-derived dopamine progenitors to functional neurons. J Neurochem 2009; 110(3): 1058-69.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06201.x] [PMID: 19493166]
[91]
Balasubramanian S, Thej C, Venugopal P, et al. Higher propensity of Wharton’s jelly derived mesenchymal stromal cells towards neuronal lineage in comparison to those derived from adipose and bone marrow. Cell Biol Int 2013; 37(5): 507-15.
[http://dx.doi.org/10.1002/cbin.10056] [PMID: 23418097]
[92]
Hosseini SM, Vasaghi A, Nakhlparvar N, Roshanravan R, Talaei-Khozani T, Razi Z. Differentiation of Wharton’s jelly mesenchymal stem cells into neurons in alginate scaffold. Neural Regen Res 2015; 10(8): 1312-6.
[http://dx.doi.org/10.4103/1673-5374.162768] [PMID: 26487861]
[93]
Mitchell KE, Weiss ML, Mitchell BM, et al. Matrix cells from Wharton’s jelly form neurons and glia. Stem Cells 2003; 21: 50-60.
[94]
Mu MW, Zhao ZY, Li CG. Comparative study of neural differentiation of bone marrow mesenchymal stem cells by different induction methods. Genet Mol Res 2015; 14(4): 14169-76.
[http://dx.doi.org/10.4238/2015.October.29.39] [PMID: 26535734]
[95]
Zeng R, Wang L-W, Hu Z-B, et al. Differentiation of human bone marrow mesenchymal stem cells into neuron-like cells in vitro. Spine 2011; 36(13): 997-1005.
[http://dx.doi.org/10.1097/BRS.0b013e3181eab764] [PMID: 21270716]
[96]
Kan I, Barhum Y, Melamed E, Offen D. Mesenchymal stem cells stimulate endogenous neurogenesis in the subventricular zone of adult mice. Stem Cell Rev Rep 2011; 7(2): 404-12.
[http://dx.doi.org/10.1007/s12015-010-9190-x] [PMID: 20830611]
[97]
Volkman R, Offen D. Concise review: Mesenchymal stem cells in neurodegenerative diseases. Stem Cells 2017; 35(8): 1867-80.
[http://dx.doi.org/10.1002/stem.2651] [PMID: 28589621]
[98]
Staff NP, Jones DT, Singer W. Mesenchymal stromal cell therapies for neurodegenerative diseases. Mayo Clin Proc 2019; 94(5): 892-905.
[http://dx.doi.org/10.1016/j.mayocp.2019.01.001] [PMID: 31054608]
[99]
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]
[100]
Park HJ, Shin JY, Lee BR, Kim HO, Lee PH. Mesenchymal stem cells augment neurogenesis in the subventricular zone and enhance differentiation of neural precursor cells into dopaminergic neurons in the substantia nigra of a Parkinsonian model. Cell Transplant 2012; 21(8): 1629-40.
[http://dx.doi.org/10.3727/096368912X640556] [PMID: 22546197]
[101]
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(2): 329-43.
[PMID: 20014009]
[102]
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]
[103]
Yokokawa K, Iwahara N, Hisahara S, et al. Transplantation of mesenchymal stem cells improves amyloid-β pathology by modifying microglial function and suppressing oxidative stress. J Alzheimers Dis 2019; 72(3): 867-84.
[http://dx.doi.org/10.3233/JAD-190817] [PMID: 31640102]
[104]
Wei Y, Xie Z, Bi J, Zhu Z. Anti-inflammatory effects of bone marrow mesenchymal stem cells on mice with Alzheimer’s disease. Exp Ther Med 2018; 16(6): 5015-20.
[http://dx.doi.org/10.3892/etm.2018.6857] [PMID: 30542456]
[105]
Lykhmus O, Koval L, Voytenko L, et al. Intravenously injected mesenchymal stem cells penetrate the brain and treat inflammation-induced brain damage and memory impairment in mice. Front Pharmacol 2019; 10: 355.
[http://dx.doi.org/10.3389/fphar.2019.00355] [PMID: 31057400]
[106]
Wang X, Ma S, Yang B, et al. Resveratrol promotes hUC-MSCs engraftment and neural repair in a mouse model of Alzheimer’s disease. Behav Brain Res 2018; 339: 297-304.
[http://dx.doi.org/10.1016/j.bbr.2017.10.032] [PMID: 29102593]
[107]
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.
[http://dx.doi.org/10.1016/j.brainres.2018.12.034] [PMID: 30586546]
[108]
Reza-Zaldivar EE, Hernández-Sapiéns MA, Gutiérrez-Mercado YK, et al. Mesenchymal stem cell-derived exosomes promote neurogenesis and cognitive function recovery in a mouse model of Alzheimer’s disease. Neural Regen Res 2019; 14(9): 1626-34.
[http://dx.doi.org/10.4103/1673-5374.255978] [PMID: 31089063]
[109]
Losurdo M, Pedrazzoli M, D’Agostino C, et al. Intranasal delivery of mesenchymal stem cell-derived extracellular vesicles exerts immunomodulatory and neuroprotective effects in a 3xTg model of Alzheimer’s disease. Stem Cells Transl Med 2020; 9(9): 1068-84.
[http://dx.doi.org/10.1002/sctm.19-0327] [PMID: 32496649]
[110]
Chi K, Fu R-H, Huang Y-C, et al. Adipose-derived stem cells stimulated with n-butylidenephthalide exhibit therapeutic effects in a mouse model of Parkinson’s disease. Cell Transplant 2018; 27(3): 456-70.
[http://dx.doi.org/10.1177/0963689718757408] [PMID: 29756519]
[111]
Glavaski-Joksimovic A, Virag T, Mangatu TA, McGrogan M, Wang XS, Bohn MC. Glial cell line-derived neurotrophic factor-secreting genetically modified human bone marrow-derived mesenchymal stem cells promote recovery in a rat model of Parkinson’s disease. J Neurosci Res 2010; 88(12): 2669-81.
[http://dx.doi.org/10.1002/jnr.22435] [PMID: 20544825]
[112]
Park HJ, Oh SH, Kim HN, Jung YJ, Lee PH. Mesenchymal stem cells enhance α-synuclein clearance via M2 microglia polarization in experimental and human Parkinsonian disorder. Acta Neuropathol 2016; 132(5): 685-701.
[http://dx.doi.org/10.1007/s00401-016-1605-6] [PMID: 27497943]
[113]
Wang YL, Liu XS, Wang SS, et al. Curcumin-activated mesenchymal stem cells derived from human umbilical cord and their effects on MPTP-mouse model of Parkinson’s disease: A new biological therapy for Parkinson’s disease. Stem Cells Int 2020; 2020: 4636397.
[114]
Mendes-Pinheiro B, Anjo SI, Manadas B, et al. Bone marrow mesenchymal stem cells’ secretome exerts neuroprotective effects in a Parkinson’s disease rat model. Front Bioeng Biotechnol 2019; 7: 294.
[http://dx.doi.org/10.3389/fbioe.2019.00294] [PMID: 31737616]
[115]
Li Q, Wang Z, Xing H, Wang Y, Guo Y. Exosomes derived from miR-188-3p-modified adipose-derived mesenchymal stem cells protect Parkinson’s disease. Mol Ther Nucleic Acids 2021; 23: 1334-44.
[http://dx.doi.org/10.1016/j.omtn.2021.01.022] [PMID: 33717653]
[116]
Pollock K, Dahlenburg H, Nelson H, et al. Human mesenchymal stem cells genetically engineered to overexpress brain-derived neurotrophic factor improve outcomes in Huntington’s disease mouse models. Mol Ther 2016; 24(5): 965-77.
[http://dx.doi.org/10.1038/mt.2016.12] [PMID: 26765769]
[117]
Fink KD, Rossignol J, Crane AT, et al. Transplantation of umbilical cord-derived mesenchymal stem cells into the striata of R6/2 mice: Behavioral and neuropathological analysis. Stem Cell Res Ther 2013; 4(5): 130.
[http://dx.doi.org/10.1186/scrt341] [PMID: 24456799]
[118]
Rossignol J, Fink KD, Crane AT, et al. Reductions in behavioral deficits and neuropathology in the R6/2 mouse model of Huntington’s disease following transplantation of bone-marrow-derived mesenchymal stem cells is dependent on passage number. Stem Cell Res Ther 2015; 6: 9.
[http://dx.doi.org/10.1186/scrt545] [PMID: 25971780]
[119]
Ebrahimi MJ, Aliaghaei A, Boroujeni ME, et al. Human umbilical cord matrix stem cells reverse oxidative stress-induced cell death and ameliorate motor function and striatal atrophy in rat model of Huntington disease. Neurotox Res 2018; 34(2): 273-84.
[http://dx.doi.org/10.1007/s12640-018-9884-4] [PMID: 29520722]
[120]
Hosseini M, Moghadas M, Edalatmanesh MA, Hashemzadeh MR. Xenotransplantation of human adipose derived mesenchymal stem cells in a rodent model of Huntington’s disease: Motor and non-motor outcomes. Neurol Res 2015; 37(4): 309-19.
[http://dx.doi.org/10.1179/1743132814Y.0000000456] [PMID: 25376132]
[121]
Kim KS, Lee HJ, An J, et al. Transplantation of human adipose tissue-derived stem cells delays clinical onset and prolongs life span in ALS mouse model. Cell Transplant 2014; 23(12): 1585-97.
[http://dx.doi.org/10.3727/096368913X673450] [PMID: 24070071]
[122]
Kim H, Kim HY, Choi MR, et al. Dose-dependent efficacy of ALS-human mesenchymal stem cells transplantation into cisterna magna in SOD1-G93A ALS mice. Neurosci Lett 2010; 468(3): 190-4.
[http://dx.doi.org/10.1016/j.neulet.2009.10.074] [PMID: 19879334]
[123]
Krakora D, Mulcrone P, Meyer M, et al. Synergistic effects of GDNF and VEGF on lifespan and disease progression in a familial ALS rat model. Mol Ther 2013; 21(8): 1602-10.
[http://dx.doi.org/10.1038/mt.2013.108] [PMID: 23712039]
[124]
Řehořová M, Vargová I, Forostyak S, et al. A combination of intrathecal and intramuscular application of human mesenchymal stem cells partly reduces the activation of necroptosis in the spinal cord of SOD1g93a rats. Stem Cells Transl Med 2019; 8(6): 535-47.
[http://dx.doi.org/10.1002/sctm.18-0223] [PMID: 30802001]
[125]
Walker CL, Meadows RM, Merfeld-Clauss S, Du Y, March KL, Jones KJ. Adipose-derived stem cell conditioned medium impacts asymptomatic peripheral neuromuscular denervation in the mutant superoxide dismutase (G93A) transgenic mouse model of amyotrophic lateral sclerosis. Restor Neurol Neurosci 2018; 36(5): 621-7.
[http://dx.doi.org/10.3233/RNN-180820] [PMID: 30010155]
[126]
Sun H, Hou Z, Yang H, et al. Multiple systemic transplantations of human amniotic mesenchymal stem cells exert therapeutic effects in an ALS mouse model. Cell Tissue Res 2014; 357(3): 571-82.
[http://dx.doi.org/10.1007/s00441-014-1903-z] [PMID: 24906288]
[127]
Sironi F, Vallarola A, Violatto MB, et al. Multiple intracerebroventricular injections of human umbilical cord mesenchymal stem cells delay motor neurons loss but not disease progression of SOD1G93A mice. Stem Cell Res 2017; 25: 166-78.
[http://dx.doi.org/10.1016/j.scr.2017.11.005] [PMID: 29154076]
[128]
Bai L, Lennon DP, Eaton V, et al. Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 2009; 57(11): 1192-203.
[http://dx.doi.org/10.1002/glia.20841] [PMID: 19191336]
[129]
Shiri E, Pasbakhsh P, Borhani-Haghighi M, et al. Mesenchymal stem cells ameliorate cuprizone-induced demyelination by targeting oxidative stress and mitochondrial dysfunction. Cell Mol Neurobiol 2020. Epub ahead of print.
[http://dx.doi.org/10.1007/s10571-020-00910-6] [PMID: 32594382]
[130]
Liu Y, Ma Y, Du B, Wang Y, Yang GY, Bi X. Mesenchymal stem cells attenuated blood-brain barrier disruption via downregulation of aquaporin-4 expression in EAE mice. Mol Neurobiol 2020; 57(9): 3891-901.
[http://dx.doi.org/10.1007/s12035-020-01998-z] [PMID: 32613467]
[131]
Gramlich OW, Brown AJ, Godwin CR, et al. Systemic mesenchymal stem cell treatment mitigates structural and functional retinal ganglion cell degeneration in a mouse model of multiple sclerosis. Transl Vis Sci Technol 2020; 9(8): 16.
[http://dx.doi.org/10.1167/tvst.9.8.16] [PMID: 32855863]
[132]
Wang YL, Xue P, Xu CY, et al. SPK1-transfected UCMSC has better therapeutic activity than UCMSC in the treatment of experimental autoimmune encephalomyelitis model of Multiple sclerosis. Sci Rep 2018; 8(1): 1756.
[http://dx.doi.org/10.1038/s41598-018-19703-5] [PMID: 29379030]
[133]
Zhang L, Wang X, Lu X, et al. Tetramethylpyrazine enhanced the therapeutic effects of human umbilical cord mesenchymal stem cells in experimental autoimmune encephalomyelitis mice through Nrf2/HO-1 signaling pathway. Stem Cell Res Ther 2020; 11(1): 186.
[http://dx.doi.org/10.1186/s13287-020-01700-z] [PMID: 32430010]
[134]
Zhou X, Liu X, Liu L, et al. Transplantation of ifn-γ primed hucmscs significantly improved outcomes of experimental autoimmune encephalomyelitis in a mouse model. Neurochem Res 2020; 45(7): 1510-7.
[http://dx.doi.org/10.1007/s11064-020-03009-y] [PMID: 32172400]
[135]
Heidari Barchi Nezhad R, Asadi F, Abtahi Froushani SM, et al. The effects of transplanted mesenchymal stem cells treated with 17-b estradiol on experimental autoimmune encephalomyelitis. Mol Biol Rep 2019; 46(6): 6135-46.
[http://dx.doi.org/10.1007/s11033-019-05048-3] [PMID: 31555971]
[136]
Constantin G, Marconi S, Rossi B, et al. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 2009; 27(10): 2624-35.
[http://dx.doi.org/10.1002/stem.194] [PMID: 19676124]
[137]
Shalaby SM, Sabbah NA, Saber T, Abdel Hamid RA. Adipose-derived mesenchymal stem cells modulate the immune response in chronic experimental autoimmune encephalomyelitis model. IUBMB Life 2016; 68(2): 106-15.
[http://dx.doi.org/10.1002/iub.1469] [PMID: 26757144]
[138]
Rando A, Pastor D, Viso-León MC, et al. Intramuscular transplantation of bone marrow cells prolongs the lifespan of SOD1G93A mice and modulates expression of prognosis biomarkers of the disease. Stem Cell Res Ther 2018; 9(1): 90.
[http://dx.doi.org/10.1186/s13287-018-0843-z] [PMID: 29625589]
[139]
Yousefi F, Ebtekar M, Soudi S, Soleimani M, Hashemi SM. In vivo immunomodulatory effects of adipose-derived mesenchymal stem cells conditioned medium in experimental autoimmune encephalomyelitis. Immunol Lett 2016; 172: 94-105.
[http://dx.doi.org/10.1016/j.imlet.2016.02.016] [PMID: 26930038]
[140]
Clark K, Zhang S, Barthe S, et al. Placental mesenchymal stem cell-derived extracellular vesicles promote myelin regeneration in an animal model of multiple sclerosis. Cells 2019; 8(12): 8.
[http://dx.doi.org/10.3390/cells8121497] [PMID: 31771176]
[141]
Jafarinia M, Alsahebfosoul F, Salehi H, et al. Therapeutic effects of extracellular vesicles from human adipose-derived mesenchymal stem cells on chronic experimental autoimmune encephalomyelitis. J Cell Physiol 2020; 235(11): 8779-90.
[http://dx.doi.org/10.1002/jcp.29721] [PMID: 32329062]
[142]
Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000; 61(4): 364-70.
[http://dx.doi.org/10.1002/1097-4547(20000815)61:4<364::AID-JNR2>3.0.CO;2-C] [PMID: 10931522]
[143]
Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 2002; 297(5590): 2256-9.
[144]
Roybon L, Ma Z, Asztely F, et al. Failure of transdifferentiation of adult hematopoietic stem cells into neurons. Stem Cells 2006; 24(6): 1594-604.
[http://dx.doi.org/10.1634/stemcells.2005-0548] [PMID: 16556707]
[145]
Corey S, Lippert T, Borlongan CV. Translational lab-to-clinic hurdles in stem cell therapy. Chinese Neurosurg J 2016; 2: 41.
[http://dx.doi.org/10.1186/s41016-016-0058-z]
[146]
George B. Regulations and guidelines governing stem cell based products: Clinical considerations. Perspect Clin Res 2011; 2(3): 94-9.
[http://dx.doi.org/10.4103/2229-3485.83228] [PMID: 21897884]
[147]
Kim HJ, Seo SW, Chang JW, et al. Stereotactic brain injection of human umbilical cord blood mesenchymal stem cells in patients with Alzheimer’s disease dementia: A phase 1 clinical trial. Alzheimers Dement (N Y) 2015; 1(2): 95-102.
[http://dx.doi.org/10.1016/j.trci.2015.06.007] [PMID: 29854930]
[148]
Oliva AA, Baumel B, Brody M, et al. Clinical evaluation of allogeneic mesenchymal stem cells for Alzheimer’s disease. Alzheimers Dement 2020; 16: 1.
[149]
Schiess M, Suescun J, Doursout MF, et al. Allogeneic bone marrow-derived mesenchymal stem cell safety in idiopathic Parkinson’s disease. Mov Disord 2021.
[http://dx.doi.org/10.1002/mds.28582] [PMID: 33772873]
[150]
Venkataramana NK, Kumar SKV, Balaraju S, et al. Open-labeled study of unilateral autologous bone-marrow-derived mesenchymal stem cell transplantation in Parkinson’s disease. Transl Res 2010; 155(2): 62-70.
[http://dx.doi.org/10.1016/j.trsl.2009.07.006] [PMID: 20129486]
[151]
Garitaonandia I, Gonzalez R, Sherman G, Semechkin A, Evans A, Kern R. Novel approach to stem cell therapy in Parkinson’s disease. Stem Cells Dev 2018; 27(14): 951-7.
[http://dx.doi.org/10.1089/scd.2018.0001] [PMID: 29882481]
[152]
Lige L, Zengmin T. Transplantation of neural precursor cells in the treatment of Parkinson disease: An efficacy and safety analysis. Turk Neurosurg 2016; 26(3): 378-83.
[PMID: 27161464]
[153]
Shroff G, Hopf-Seidel P. Use of human embryonic stem cells in the treatment of Parkinson’s disease: A case report. Int J Emerg Ment Health 2015; 17: 661-3.
[154]
Bachoud-Lévi AC, Gaura V, Brugières P, et al. Effect of fetal neural transplants in patients with Huntington’s disease 6 years after surgery: A long-term follow-up study. Lancet Neurol 2006; 5(4): 303-9.
[http://dx.doi.org/10.1016/S1474-4422(06)70381-7] [PMID: 16545746]
[155]
Burt RK, Burns W, Hess A. Bone marrow transplantation for multiple sclerosis. Bone Marrow Transplant 1995; 16(1): 1-6.
[http://dx.doi.org/10.1038/sj.bmt.1703081] [PMID: 7581107]
[156]
Cohen JA, Imrey PB, Planchon SM, et al. Pilot trial of intravenous autologous culture-expanded mesenchymal stem cell transplantation in multiple sclerosis. Mult Scler J 2018; 24: 501-11.
[157]
Fernández O, Izquierdo G, Fernández V, et al. Adipose-derived mesenchymal stem cells (AdMSC) for the treatment of secondary-progressive multiple sclerosis: A triple blinded, placebo controlled, randomized phase I/II safety and feasibility study. PLoS One 2018; 13(5): e0195891.
[http://dx.doi.org/10.1371/journal.pone.0195891] [PMID: 29768414]
[158]
Li J-F, Zhang D-J, Geng T, et al. The potential of human umbilical cord-derived mesenchymal stem cells as a novel cellular therapy for multiple sclerosis. Cell Transplant 2014; 23(Suppl. 1): S113-22.
[http://dx.doi.org/10.3727/096368914X685005] [PMID: 25385295]
[159]
Shroff G. Human embryonic stem cell for the treatment of multiple sclerosis: A case report. Case Reports Int 2015; 4: 38-42.
[http://dx.doi.org/10.5348/crint-2015-15-CR-10]
[160]
Shroff G. Transplantation of human embryonic stem cells in patients with multiple sclerosis and lyme disease. Am J Case Rep 2016; 17: 944-9.
[http://dx.doi.org/10.12659/AJCR.899745] [PMID: 27956736]
[161]
Meng M, Liu Y, Wang W, et al. Umbilical cord mesenchymal stem cell transplantation in the treatment of multiple sclerosis. 2018; 10(1): p. 212.
[162]
Burt RK, Balabanov R, Burman J, et al. Effect of nonmyeloablative hematopoietic stem cell transplantation vs continued disease-modifying therapy on disease progression in patients with relapsing-remitting multiple sclerosis: A randomized clinical trial. JAMA 2019; 321(2): 165-74.
[http://dx.doi.org/10.1001/jama.2018.18743] [PMID: 30644983]
[163]
Glass JD, Boulis NM, Johe K, et al. Lumbar intraspinal injection of neural stem cells in patients with amyotrophic lateral sclerosis: Results of a phase I trial in 12 patients. Stem Cells 2012; 30(6): 1144-51.
[http://dx.doi.org/10.1002/stem.1079] [PMID: 22415942]
[164]
Prabhakar S, Marwaha N, Lal V, Sharma RR, Rajan R, Khandelwal N. Autologous bone marrow-derived stem cells in amyotrophic lateral sclerosis: A pilot study. Neurol India 2012; 60(5): 465-9.
[http://dx.doi.org/10.4103/0028-3886.103185] [PMID: 23135021]
[165]
Petrou P, Gothelf Y, Argov Z, et al. Safety and clinical effects of mesenchymal stem cells secreting neurotrophic factor transplantation in patients with amyotrophic lateral sclerosis: Results of Phase 1/2 and 2a clinical trials. JAMA Neurol 2016; 73(3): 337-44.
[http://dx.doi.org/10.1001/jamaneurol.2015.4321] [PMID: 26751635]
[166]
Mazzini L, Gelati M, Profico DC, et al. Results from phase I clinical trial with intraspinal injection of neural stem cells in amyotrophic lateral sclerosis: A long-term outcome. Stem Cells Transl Med 2019; 8(9): 887-97.
[http://dx.doi.org/10.1002/sctm.18-0154] [PMID: 31104357]
[167]
Pawlukowska W, Baumert B, Gołąb-Janowska M, et al. Articulation recovery in ALS patients after lineage-negative adjuvant cell therapy-preliminary report. Int J Med Sci 2020; 17(13): 1927-35.
[http://dx.doi.org/10.7150/ijms.47002] [PMID: 32788871]
[168]
Kolli N, Lu M, Maiti P, Rossignol J, Dunbar GL. Application of the gene editing tool, CRISPR-Cas9, for treating neurodegenerative diseases. Neurochem Int 2018; 112: 187-96.
[http://dx.doi.org/10.1016/j.neuint.2017.07.007] [PMID: 28732771]
[169]
Riordan NH, Morales I, Fernández G, et al. Clinical feasibility of umbilical cord tissue-derived mesenchymal stem cells in the treatment of multiple sclerosis. J Transl Med 2018; 16(1): 57.
[http://dx.doi.org/10.1186/s12967-018-1433-7] [PMID: 29523171]
[170]
Mazzini L, Gelati M, Profico DC, Sgaravizzi G, Projetti Pensi M, Muzi G, et al. Human neural stem cell transplantation in ALS: Initial results from a phase I trial. J Transl Med 2015; 13: 17.
[171]
Oh K-W, Moon C, Kim HY, et al. Phase I trial of repeated intrathecal autologous bone marrow-derived mesenchymal stromal cells in amyotrophic lateral sclerosis. Stem Cells Transl Med 2015; 4(6): 590-7.
[http://dx.doi.org/10.5966/sctm.2014-0212] [PMID: 25934946]
[172]
Barczewska M, Grudniak M, Maksymowicz S, et al. Safety of intrathecal injection of Wharton’s jelly-derived mesenchymal stem cells in amyotrophic lateral sclerosis therapy. Neural Regen Res 2019; 14(2): 313-8.
[http://dx.doi.org/10.4103/1673-5374.243723] [PMID: 30531015]

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