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CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Review Article

Neural Basis of Dental Pulp Stem Cells and its Potential Application in Parkinson’s Disease

Author(s): Yogita Sharma, K Shobha, Mata Sundeep, Venkata Bharatkumar Pinnelli, Shagufta Parveen and Anandh Dhanushkodi*

Volume 21, Issue 1, 2022

Published on: 11 March, 2021

Page: [62 - 76] Pages: 15

DOI: 10.2174/1871527320666210311122921

Price: $65

Abstract

Parkinson’s Disease (PD) is the second most common neurodegenerative disease after Alzheimer’s disease. Though significant insights into the molecular-biochemical-cellular-behavioral basis of PD have been understood, there is no appreciable treatment available till date. Current therapies provide symptomatic relief without any influence on the progression of the disease. Stem cell therapy has been vigorously explored to treat PD. In this comprehensive review, we analyze various stem cell candidates for treating PD and discuss the possible mechanisms. We advocate the advantage of using neural crest originated Dental Pulp Stem Cells (DPSC) due to their predisposition towards neural differentiation and their potential to regenerate neurons far better than commonly used bone marrow derived mesenchymal stem cells (BM-MSCs). Eventually, we highlight the current challenges in the field and the strategies, which may be used for overcoming the impediments.

Keywords: Parkinson’s disease, stem cells, Dental Pulp, neuroprotection, exosomes, BM-MSC.

Graphical Abstract
[1]
Dorsey ER, Constantinescu R, Thompson JP, et al. Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 2007; 68(5): 384-6.
[http://dx.doi.org/10.1212/01.wnl.0000247740.47667.03] [PMID: 17082464]
[2]
Elbaz A, Carcaillon L, Kab S, Moisan F. Epidemiology of Parkinson’s disease. Rev Neurol (Paris) 2016; 172(1): 14-26.
[http://dx.doi.org/10.1016/j.neurol.2015.09.012] [PMID: 26718594]
[3]
Pringsheim T, Jette N, Frolkis A, Steeves TD. The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 2014; 29(13): 1583-90.
[http://dx.doi.org/10.1002/mds.25945] [PMID: 24976103]
[4]
Moisan F, Kab S, Mohamed F, et al. Parkinson disease male-to-female ratios increase with age: French nationwide study and meta-analysis. J Neurol Neurosurg Psychiatry 2016; 87(9): 952-7.
[http://dx.doi.org/10.1136/jnnp-2015-312283] [PMID: 26701996]
[5]
Horowski R, Horowski L, Vogel S, Poewe W, Kielhorn FW. An essay on Wilhelm von Humboldt and the shaking palsy: first comprehensive description of Parkinson’s disease by a patient. Neurology 1995; 45(3 Pt 1): 565-8.
[http://dx.doi.org/10.1212/WNL.45.3.565] [PMID: 7898719]
[6]
Maïga B, Koné A, Landouré G, et al. Non-motor signs in patients with Parkinson’s disease at the University Hospital of Point “G”, Mali. eNeurologicalSci 2016; 3: 35-6.
[http://dx.doi.org/10.1016/j.ensci.2016.02.001] [PMID: 29430533]
[7]
Prashanth LK, Fox S, Meissner WG. l-Dopa-induced dyskinesia- clinical presentation, genetics, and treatment. Int Rev Neurobiol 2011; 98: 31-54.
[http://dx.doi.org/10.1016/B978-0-12-381328-2.00002-X] [PMID: 21907082]
[8]
Lozano AM, Lipsman N, Bergman H, et al. Deep brain stimulation: current challenges and future directions. Nat Rev Neurol 2019; 15(3): 148-60.
[http://dx.doi.org/10.1038/s41582-018-0128-2] [PMID: 30683913]
[9]
Campos FL, Carvalho MM, Cristovão AC, et al. Rodent models of Parkinson’s disease: beyond the motor symptomatology. Front Behav Neurosci 2013; 7: 175.
[http://dx.doi.org/10.3389/fnbeh.2013.00175] [PMID: 24324416]
[10]
Sedelis M, Schwarting RK, Huston JP. Behavioral phenotyping of the MPTP mouse model of Parkinson’s disease. Behav Brain Res 2001; 125(1-2): 109-25.
[http://dx.doi.org/10.1016/S0166-4328(01)00309-6] [PMID: 11682102]
[11]
Bové J, Perier C. Neurotoxin-based models of Parkinson’s disease. Neuroscience 2012; 211: 51-76.
[http://dx.doi.org/10.1016/j.neuroscience.2011.10.057] [PMID: 22108613]
[12]
Grow DA, McCarrey JR, Navara CS. Advantages of nonhuman primates as preclinical models for evaluating stem cell-based therapies for Parkinson’s disease. Stem Cell Res (Amst) 2016; 17(2): 352-66.
[http://dx.doi.org/10.1016/j.scr.2016.08.013] [PMID: 27622596]
[13]
West RJ, Furmston R, Williams CA, Elliott CJ. Neurophysiology of Drosophila models of Parkinson’s disease. Parkinsons Dis 2015; 2015: 381281.
[http://dx.doi.org/10.1155/2015/381281] [PMID: 25960916]
[14]
Martinez BA, Caldwell KA, Caldwell GA. C. elegans as a model system to accelerate discovery for Parkinson disease. Curr Opin Genet Dev 2017; 44: 102-9.
[http://dx.doi.org/10.1016/j.gde.2017.02.011] [PMID: 28242493]
[15]
Backlund EO. Adrenal-to-brain transplants and Parkinson’s disease. JAMA 1987; 258(14): 1891.
[http://dx.doi.org/10.1001/jama.1987.03400140053013] [PMID: 3656595]
[16]
Spencer DD, Robbins RJ, Naftolin F, et al. Unilateral transplantation of human fetal mesencephalic tissue into the caudate nucleus of patients with Parkinson’s disease. N Engl J Med 1992; 327(22): 1541-8.
[http://dx.doi.org/10.1056/NEJM199211263272201] [PMID: 1435880]
[17]
Freed CR, Breeze RE, Rosenberg NL, et al. Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson’s disease. N Engl J Med 1992; 327(22): 1549-55.
[http://dx.doi.org/10.1056/NEJM199211263272202] [PMID: 1435881]
[18]
Kordower JH, Freeman TB, Snow BJ, et al. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson’s disease. N Engl J Med 1995; 332(17): 1118-24.
[http://dx.doi.org/10.1056/NEJM199504273321702] [PMID: 7700284]
[19]
Piccini P, Brooks DJ, Björklund A, et al. Dopamine release from nigral transplants visualized in vivo in a Parkinson’s patient. Nat Neurosci 1999; 2(12): 1137-40.
[http://dx.doi.org/10.1038/16060] [PMID: 10570493]
[20]
Bjorklund A. Cell therapy for Parkinson's disease: problems and prospects. Novartis Foundation symposium 2005; 265: 174-86.
[http://dx.doi.org/10.1002/0470091452.ch14]
[21]
Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292(5819): 154-6.
[http://dx.doi.org/10.1038/292154a0] [PMID: 7242681]
[22]
Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981; 78(12): 7634-8.
[http://dx.doi.org/10.1073/pnas.78.12.7634] [PMID: 6950406]
[23]
Thomson JA, Kalishman J, Golos TG, et al. Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci USA 1995; 92(17): 7844-8.
[http://dx.doi.org/10.1073/pnas.92.17.7844] [PMID: 7544005]
[24]
Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Hearn JP. Pluripotent cell lines derived from common marmoset (Callithrix jacchus) blastocysts. Biol Reprod 1996; 55(2): 254-9.
[http://dx.doi.org/10.1095/biolreprod55.2.254] [PMID: 8828827]
[25]
Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282(5391): 1145-7.
[http://dx.doi.org/10.1126/science.282.5391.1145] [PMID: 9804556]
[26]
Bain G, Ray WJ, Yao M, Gottlieb DI. Retinoic acid promotes neural and represses mesodermal gene expression in mouse embryonic stem cells in culture. Biochem Biophys Res Commun 1996; 223(3): 691-4.
[http://dx.doi.org/10.1006/bbrc.1996.0957] [PMID: 8687458]
[27]
Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI. Embryonic stem cells express neuronal properties in vitro. Dev Biol 1995; 168(2): 342-57.
[http://dx.doi.org/10.1006/dbio.1995.1085] [PMID: 7729574]
[28]
Deacon T, Dinsmore J, Costantini LC, Ratliff J, Isacson O. Blastula-stage stem cells can differentiate into dopaminergic and serotonergic neurons after transplantation. Exp Neurol 1998; 149(1): 28-41.
[http://dx.doi.org/10.1006/exnr.1997.6674] [PMID: 9454612]
[29]
Bjorklund LM, Sánchez-Pernaute R, Chung S, et al. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci USA 2002; 99(4): 2344-9.
[http://dx.doi.org/10.1073/pnas.022438099] [PMID: 11782534]
[30]
Wurst W, Bally-Cuif L. Neural plate patterning: upstream and downstream of the isthmic organizer. Nat Rev Neurosci 2001; 2(2): 99-108.
[http://dx.doi.org/10.1038/35053516] [PMID: 11253000]
[31]
Lee SH, Lumelsky N, Studer L, Auerbach JM, McKay RD. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol 2000; 18(6): 675-9.
[http://dx.doi.org/10.1038/76536] [PMID: 10835609]
[32]
Chung S, Sonntag KC, Andersson T, et al. Genetic engineering of mouse embryonic stem cells by Nurr1 enhances differentiation and maturation into dopaminergic neurons. Eur J Neurosci 2002; 16(10): 1829-38.
[http://dx.doi.org/10.1046/j.1460-9568.2002.02255.x] [PMID: 12453046]
[33]
Kim JH, 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]
[34]
Takagi Y, Takahashi J, Saiki H, et al. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 2005; 115(1): 102-9.
[http://dx.doi.org/10.1172/JCI21137] [PMID: 15630449]
[35]
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]
[36]
Wernig M, Zhao JP, 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]
[37]
Cooper O, Hargus G, Deleidi M, et al. Differentiation of human ES and Parkinson’s disease iPS cells into ventral midbrain dopaminergic neurons requires a high activity form of SHH, FGF8a and specific regionalization by retinoic acid. Mol Cell Neurosci 2010; 45(3): 258-66.
[http://dx.doi.org/10.1016/j.mcn.2010.06.017] [PMID: 20603216]
[38]
Emborg ME, Liu Y, Xi J, et al. Induced pluripotent stem cell-derived neural cells survive and mature in the nonhuman primate brain. Cell Rep 2013; 3(3): 646-50.
[http://dx.doi.org/10.1016/j.celrep.2013.02.016] [PMID: 23499447]
[39]
Wang S, Zou C, Fu L, et al. Autologous iPSC-derived dopamine neuron transplantation in a nonhuman primate Parkinson’s disease model. Cell Discov 2015; 1: 15012.
[http://dx.doi.org/10.1038/celldisc.2015.12] [PMID: 27462412]
[40]
Hallett PJ, Deleidi M, Astradsson A, et al. Successful function of autologous iPSC-derived dopamine neurons following transplantation in a non-human primate model of Parkinson’s disease. Cell Stem Cell 2015; 16(3): 269-74.
[http://dx.doi.org/10.1016/j.stem.2015.01.018] [PMID: 25732245]
[41]
Soldner F, Hockemeyer D, Beard C, et al. Parkinson’s disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 2009; 136(5): 964-77.
[http://dx.doi.org/10.1016/j.cell.2009.02.013] [PMID: 19269371]
[42]
Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 1970; 3(4): 393-403.
[http://dx.doi.org/10.1111/j.1365-2184.1970.tb00347.x] [PMID: 5523063]
[43]
Venugopal C, Chandanala S, Prasad HC, Nayeem D, Bhonde RR, Dhanushkodi A. Regenerative therapy for hippocampal degenerative diseases: lessons from preclinical studies. J Tissue Eng Regen Med 2017; 11(2): 321-33.
[http://dx.doi.org/10.1002/term.2052] [PMID: 26118731]
[44]
Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.
[http://dx.doi.org/10.1080/14653240600855905] [PMID: 16923606]
[45]
Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats-similarities to astrocyte grafts. Proc Natl Acad Sci USA 1998; 95(7): 3908-13.
[http://dx.doi.org/10.1073/pnas.95.7.3908] [PMID: 9520466]
[46]
Hou LL, Zheng M, Wang DM, et al. Migration and differentiation of human bone marrow mesenchymal stem cells in the rat brain. Sheng li xue bao : [Acta physiologica Sinica] 2003; 55(2): 153-9.
[47]
Dezawa M, Kanno H, Hoshino M, et al. Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J Clin Invest 2004; 113(12): 1701-10.
[http://dx.doi.org/10.1172/JCI200420935] [PMID: 15199405]
[48]
Blandini F, Cova L, Armentero MT, et al. Transplantation of undifferentiated human mesenchymal stem cells protects against 6-hydroxydopamine neurotoxicity in the rat. Cell Transplant 2010; 19(2): 203-17.
[http://dx.doi.org/10.3727/096368909X479839] [PMID: 19906332]
[49]
Cova L, Armentero MT, Zennaro E, et al. Multiple neurogenic and neurorescue effects of human mesenchymal stem cell after transplantation in an experimental model of Parkinson’s disease. Brain Res 2010; 1311: 12-27.
[http://dx.doi.org/10.1016/j.brainres.2009.11.041] [PMID: 19945443]
[50]
Chen D, Fu W, Zhuang W, Lv C, Li F, Wang X. Therapeutic effects of intranigral transplantation of mesenchymal stem cells in rat models of Parkinson’s disease. J Neurosci Res 2017; 95(3): 907-17.
[http://dx.doi.org/10.1002/jnr.23879] [PMID: 27617772]
[51]
Park HJ, Lee PH, Bang OY, Lee G, Ahn YH. Mesenchymal stem cells therapy exerts neuroprotection in a progressive animal model of Parkinson’s disease. J Neurochem 2008; 107(1): 141-51.
[http://dx.doi.org/10.1111/j.1471-4159.2008.05589.x] [PMID: 18665911]
[52]
Hellmann MA, Panet H, Barhum Y, Melamed E, Offen D. Increased survival and migration of engrafted mesenchymal bone marrow stem cells in 6-hydroxydopamine-lesioned rodents. Neurosci Lett 2006; 395(2): 124-8.
[http://dx.doi.org/10.1016/j.neulet.2005.10.097] [PMID: 16359791]
[53]
Wang Z, Lin Y, Ye H, Chen W, Shang J, Wei T. Over-expression of CXCR4 promotes homing and proliferation of mouse bone marrow mesenchymal stem cells. Xi bao yu fen zi mian yi xue za zhi = Chinese journal of cellular and molecular immunology 2019; 35(5): 393-8.
[54]
Yu Y, Wu RX, Gao LN, Xia Y, Tang HN, Chen FM. Stromal cell-derived factor-1-directed bone marrow mesenchymal stem cell migration in response to inflammatory and/or hypoxic stimuli. Cell Adhes Migr 2016; 10(4): 342-59.
[http://dx.doi.org/10.1080/19336918.2016.1139287] [PMID: 26745021]
[55]
Somoza R, Juri C, Baes M, Wyneken U, Rubio FJ. Intranigral transplantation of epigenetically induced BDNF-secreting human mesenchymal stem cells: implications for cell-based therapies in Parkinson's disease. Biol Blood Marrow Transplant 2010; 16(11): 1530-40.
[56]
Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 2000; 97(25): 13625-30.
[http://dx.doi.org/10.1073/pnas.240309797] [PMID: 11087820]
[57]
Govindasamy V, Abdullah AN, Ronald VS, et al. Inherent differential propensity of dental pulp stem cells derived from human deciduous and permanent teeth. J Endod 2010; 36(9): 1504-15.
[http://dx.doi.org/10.1016/j.joen.2010.05.006] [PMID: 20728718]
[58]
Ibarretxe G, Crende O, Aurrekoetxea M, García-Murga V, Etxaniz J, Unda F. Neural crest stem cells from dental tissues: a new hope for dental and neural regeneration. Stem Cells Int 2012; 2012: 103503.
[http://dx.doi.org/10.1155/2012/103503] [PMID: 23093977]
[59]
Karaöz E, Demircan PC, Sağlam O, Aksoy A, Kaymaz F, Duruksu G. Human dental pulp stem cells demonstrate better neural and epithelial stem cell properties than bone marrow-derived mesenchymal stem cells. Histochem Cell Biol 2011; 136(4): 455-73.
[http://dx.doi.org/10.1007/s00418-011-0858-3] [PMID: 21879347]
[60]
Mead B, Logan A, Berry M, Leadbeater W, Scheven BA. Concise review: dental pulp stem cells: a novel cell therapy for retinal and central nervous system repair. Stem Cells 2017; 35(1): 61-7.
[http://dx.doi.org/10.1002/stem.2398] [PMID: 27273755]
[61]
Venugopal C, K S, Rai KS, Pinnelli VB, Kutty BM, Dhanushkodi A. Neuroprotection by human dental pulp mesenchymal stem cells: from billions to nano. Curr Gene Ther 2018; 18(5): 307-23.
[http://dx.doi.org/10.2174/1566523218666180913152615] [PMID: 30209999]
[62]
Davidson RM. Neural form of voltage-dependent sodium current in human cultured dental pulp cells. Arch Oral Biol 1994; 39(7): 613-20.
[http://dx.doi.org/10.1016/0003-9969(94)90137-6] [PMID: 7945020]
[63]
Sakai K, Yamamoto A, Matsubara K, et al. Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. J Clin Invest 2012; 122(1): 80-90.
[PMID: 22133879]
[64]
Foudah D, Monfrini M, Donzelli E, et al. Expression of neural markers by undifferentiated mesenchymal-like stem cells from different sources. J Immunol Res 2014; 2014: 987678.
[http://dx.doi.org/10.1155/2014/987678] [PMID: 24741639]
[65]
Martens W, Wolfs E, Struys T, Politis C, Bronckaers A, Lambrichts I. Expression pattern of basal markers in human dental pulp stem cells and tissue. Cells Tissues Organs 2012; 196(6): 490-500.
[http://dx.doi.org/10.1159/000338654] [PMID: 22739146]
[66]
Karaöz E, Doğan BN, Aksoy A, et al. Isolation and in vitro characterisation of dental pulp stem cells from natal teeth. Histochem Cell Biol 2010; 133(1): 95-112.
[http://dx.doi.org/10.1007/s00418-009-0646-5] [PMID: 19816704]
[67]
Arthur A, Rychkov G, Shi S, Koblar SA, Gronthos S. Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells 2008; 26(7): 1787-95.
[http://dx.doi.org/10.1634/stemcells.2007-0979] [PMID: 18499892]
[68]
Osathanon T, Sawangmake C, Nowwarote N, Pavasant P. Neurogenic differentiation of human dental pulp stem cells using different induction protocols. Oral Dis 2014; 20(4): 352-8.
[http://dx.doi.org/10.1111/odi.12119] [PMID: 23651465]
[69]
Gervois P, Struys T, Hilkens P, et al. Neurogenic maturation of human dental pulp stem cells following neurosphere generation induces morphological and electrophysiological characteristics of functional neurons. Stem Cells Dev 2015; 24(3): 296-311.
[http://dx.doi.org/10.1089/scd.2014.0117] [PMID: 25203005]
[70]
Király M, Porcsalmy B, Pataki A, et al. Simultaneous PKC and cAMP activation induces differentiation of human dental pulp stem cells into functionally active neurons. Neurochem Int 2009; 55(5): 323-32.
[http://dx.doi.org/10.1016/j.neuint.2009.03.017] [PMID: 19576521]
[71]
Heng BC, Jiang S, Yi B, Gong T, Lim LW, Zhang C. Small molecules enhance neurogenic differentiation of dental-derived adult stem cells. Arch Oral Biol 2019; 102: 26-38.
[http://dx.doi.org/10.1016/j.archoralbio.2019.03.024] [PMID: 30954806]
[72]
Heng BC, Lim LW, Wu W, Zhang C. An overview of protocols for the neural induction of dental and oral stem cells in vitro. Tissue Eng Part B Rev 2016; 22(3): 220-50.
[http://dx.doi.org/10.1089/ten.teb.2015.0488] [PMID: 26757369]
[73]
Heng BC, Gong T, Xu J, Lim LW, Zhang C. EphrinB2 signalling modulates the neural differentiation of human dental pulp stem cells. Biomed Rep 2018; 9(2): 161-8.
[http://dx.doi.org/10.3892/br.2018.1108] [PMID: 29963307]
[74]
Li D, Zou XY, El-Ayachi I, et al. Human dental pulp stem cells and gingival mesenchymal stem cells display action potential capacity in vitro after neuronogenic differentiation. Stem Cell Rev Rep 2019; 15(1): 67-81.
[http://dx.doi.org/10.1007/s12015-018-9854-5]
[75]
Wang J, Wang X, Sun Z, et al. Stem cells from human-exfoliated deciduous teeth can differentiate into dopaminergic neuron-like cells. Stem Cells Dev 2010; 19(9): 1375-83.
[http://dx.doi.org/10.1089/scd.2009.0258] [PMID: 20131979]
[76]
Chang CC, Chang KC, Tsai SJ, Chang HH, Lin CP. Neurogenic differentiation of dental pulp stem cells to neuron-like cells in dopaminergic and motor neuronal inductive media. J Formos Med Assoc 2014; 113(12): 956-65.
[77]
Singh M, Kakkar A, Sharma R, et al. Synergistic effect of bdnf and fgf2 in efficient generation of functional dopaminergic neurons from human mesenchymal stem cells. Sci Rep 2017; 7(1): 10378.
[http://dx.doi.org/10.1038/s41598-017-11028-z] [PMID: 28871128]
[78]
Gnanasegaran N, Govindasamy V, Kathirvaloo P, Musa S, Abu Kasim NH. Effects of cell cycle phases on the induction of dental pulp stem cells toward dopaminergic-like cells. J Tissue Eng Regen Med 2018; 12(2): e881-93.
[http://dx.doi.org/10.1002/term.2401] [PMID: 28079995]
[79]
Gnanasegaran N, Govindasamy V, Abu Kasim NH. Differentiation of stem cells derived from carious teeth into dopaminergic- like cells. Int Endod J 2016; 49(10): 937-49.
[http://dx.doi.org/10.1111/iej.12545] [PMID: 26354006]
[80]
Kang YH, Shivakumar SB, Son YB, et al. Comparative analysis of three different protocols for cholinergic neuron differentiation in vitro using mesenchymal stem cells from human dental pulp. Anim Cells Syst (Seoul) 2019; 23(4): 275-87.
[http://dx.doi.org/10.1080/19768354.2019.1626280] [PMID: 31489249]
[81]
Ellis KM, O’Carroll DC, Lewis MD, Rychkov GY, Koblar SA. Neurogenic potential of dental pulp stem cells isolated from murine incisors. Stem Cell Res Ther 2014; 5(1): 30.
[http://dx.doi.org/10.1186/scrt419] [PMID: 24572146]
[82]
Cho YA, Kim DS, Song M, Bae WJ, Lee S, Kim EC. Protein Interacting with Never in Mitosis A-1 Induces Glutamatergic and GABAergic Neuronal Differentiation in Human Dental Pulp Stem Cells. J Endod 2016; 42(7): 1055-61.
[http://dx.doi.org/10.1016/j.joen.2016.04.004] [PMID: 27178251]
[83]
Sanen K, Martens W, Georgiou M, Ameloot M, Lambrichts I, Phillips J. Engineered neural tissue with Schwann cell differentiated human dental pulp stem cells: potential for peripheral nerve repair? J Tissue Eng Regen Med 2017; 11(12): 3362-72.
[http://dx.doi.org/10.1002/term.2249] [PMID: 28052540]
[84]
Lambrichts I, Driesen RB, Dillen Y, et al. Dental pulp stem cells: their potential in reinnervation and angiogenesis by using scaffolds. J Endod 2017; 43(9S): S12-6.
[http://dx.doi.org/10.1016/j.joen.2017.06.001] [PMID: 28781091]
[85]
Kerkis I, Kerkis A, Dozortsev D, et al. Isolation and characterization of a population of immature dental pulp stem cells expressing OCT-4 and other embryonic stem cell markers. Cells Tissues Organs 2006; 184(3-4): 105-16.
[http://dx.doi.org/10.1159/000099617] [PMID: 17409736]
[86]
Chang YC, Li WC, Twu NF, et al. Induction of dental pulp-derived induced pluripotent stem cells in the absence of c-Myc for differentiation into neuron-like cells. J Chin Med Assoc 2014; 77(12): 618-25.
[http://dx.doi.org/10.1016/j.jcma.2014.08.009] [PMID: 25441769]
[87]
El Ayachi I, Zhang J, Zou XY, et al. Human dental stem cell derived transgene-free iPSCs generate functional neurons via embryoid body-mediated and direct induction methods. J Tissue Eng Regen Med 2018; 12(4): e1836-51.
[http://dx.doi.org/10.1002/term.2615] [PMID: 29139614]
[88]
Tamaoki N, Takahashi K, Tanaka T, et al. Dental pulp cells for induced pluripotent stem cell banking. J Dent Res 2010; 89(8): 773-8.
[http://dx.doi.org/10.1177/0022034510366846] [PMID: 20554890]
[89]
Kawano E, Toriumi T, Iguchi S, Suzuki D, Sato S, Honda M. Induction of neural crest cells from human dental pulp-derived induced pluripotent stem cells. Biomed Res (Aligarh) 2017; 38(2): 135-47.
[http://dx.doi.org/10.2220/biomedres.38.135] [PMID: 28442664]
[90]
Chen J, Lin M, Foxe JJ, et al. Transcriptome comparison of human neurons generated using induced pluripotent stem cells derived from dental pulp and skin fibroblasts. PLoS One 2013; 8(10): e75682.
[http://dx.doi.org/10.1371/journal.pone.0075682] [PMID: 24098394]
[91]
Kumar A, Kumar V, Rattan V, Jha V, Bhattacharyya S. Secretome cues modulate the neurogenic potential of bone marrow and dental stem cells. Mol Neurobiol 2017; 54(6): 4672-82.
[http://dx.doi.org/10.1007/s12035-016-0011-3] [PMID: 27422132]
[92]
Mead B, Logan A, Berry M, Leadbeater W, Scheven BA. Dental pulp stem cells, a paracrine-mediated therapy for the retina. Neural Regen Res 2014; 9(6): 577-8.
[http://dx.doi.org/10.4103/1673-5374.130089] [PMID: 25206857]
[93]
Stolzing A, Jones E, McGonagle D, Scutt A. Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 2008; 129(3): 163-73.
[http://dx.doi.org/10.1016/j.mad.2007.12.002] [PMID: 18241911]
[94]
Shi S, Robey PG, Gronthos S. Comparison of human dental pulp and bone marrow stromal stem cells by cDNA microarray analysis. Bone 2001; 29(6): 532-9.
[http://dx.doi.org/10.1016/S8756-3282(01)00612-3] [PMID: 11728923]
[95]
Huang AH, Snyder BR, Cheng PH, Chan AW. Putative dental pulp-derived stem/stromal cells promote proliferation and differentiation of endogenous neural cells in the hippocampus of mice. Stem Cells 2008; 26(10): 2654-63.
[http://dx.doi.org/10.1634/stemcells.2008-0285] [PMID: 18687995]
[96]
Mead B, Hill LJ, Blanch RJ, et al. Mesenchymal stromal cell-mediated neuroprotection and functional preservation of retinal ganglion cells in a rodent model of glaucoma. Cytotherapy 2016; 18(4): 487-96.
[http://dx.doi.org/10.1016/j.jcyt.2015.12.002] [PMID: 26897559]
[97]
Mead B, Logan A, Berry M, Leadbeater W, Scheven BA. Intravitreally transplanted dental pulp stem cells promote neuroprotection and axon regeneration of retinal ganglion cells after optic nerve injury. Invest Ophthalmol Vis Sci 2013; 54(12): 7544-56.
[http://dx.doi.org/10.1167/iovs.13-13045] [PMID: 24150755]
[98]
Mead B, Logan A, Berry M, Leadbeater W, Scheven BA. Paracrine-mediated neuroprotection and neuritogenesis of axotomised retinal ganglion cells by human dental pulp stem cells: comparison with human bone marrow and adipose-derived mesenchymal stem cells. PLoS One 2014; 9(10): e109305.
[http://dx.doi.org/10.1371/journal.pone.0109305] [PMID: 25290916]
[99]
Ishizaka R, Hayashi Y, Iohara K, et al. Stimulation of angiogenesis, neurogenesis and regeneration by side population cells from dental pulp. Biomaterials 2013; 34(8): 1888-97.
[http://dx.doi.org/10.1016/j.biomaterials.2012.10.045] [PMID: 23245334]
[100]
Zhang Y, Xing Y, Jia L, et al. An in vitro comparative study of multisource derived human mesenchymal stem cells for bone tissue engineering. Stem Cells Dev 2018; 27(23): 1634-45.
[http://dx.doi.org/10.1089/scd.2018.0119] [PMID: 30234437]
[101]
Ahmed Nel-M, Murakami M, Hirose Y, Nakashima M. Therapeutic potential of dental pulp stem cell secretome for alzheimer’s disease treatment: an in vitro study. Stem Cells Int 2016; 2016: 8102478.
[http://dx.doi.org/10.1155/2016/8102478] [PMID: 27403169]
[102]
Nosrat IV, Smith CA, Mullally P, Olson L, Nosrat CA. Dental pulp cells provide neurotrophic support for dopaminergic neurons and differentiate into neurons in vitro; implications for tissue engineering and repair in the nervous system. Eur J Neurosci 2004; 19(9): 2388-98.
[http://dx.doi.org/10.1111/j.0953-816X.2004.03314.x] [PMID: 15128393]
[103]
Apel C, Forlenza OV, de Paula VJ, et al. The neuroprotective effect of dental pulp cells in models of Alzheimer’s and Parkinson’s disease. J Neural Transm (Vienna) 2009; 116(1): 71-8.
[http://dx.doi.org/10.1007/s00702-008-0135-3] [PMID: 18972063]
[104]
Nesti C, Pardini C, Barachini S, et al. Human dental pulp stem cells protect mouse dopaminergic neurons against MPP+ or rotenone. Brain Res 2011; 1367: 94-102.
[http://dx.doi.org/10.1016/j.brainres.2010.09.042] [PMID: 20854799]
[105]
Pierdomenico L, Bonsi L, Calvitti M, et al. Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 2005; 80(6): 836-42.
[http://dx.doi.org/10.1097/01.tp.0000173794.72151.88] [PMID: 16210973]
[106]
Gnanasegaran N, Govindasamy V, Mani V, Abu Kasim NH. Neuroimmunomodulatory properties of DPSCs in an in vitro model of Parkinson’s disease. IUBMB Life 2017; 69(9): 689-99.
[http://dx.doi.org/10.1002/iub.1655] [PMID: 28685937]
[107]
Zhang N, Lu X, Wu S, et al. Intrastriatal transplantation of stem cells from human exfoliated deciduous teeth reduces motor defects in Parkinsonian rats. Cytotherapy 2018; 20(5): 670-86.
[http://dx.doi.org/10.1016/j.jcyt.2018.02.371] [PMID: 29576501]
[108]
Gnanasegaran N, Govindasamy V, Simon C, et al. Effect of dental pulp stem cells in MPTP-induced old-aged mice model. Eur J Clin Invest 2017; 47(6): 403-14.
[http://dx.doi.org/10.1111/eci.12753] [PMID: 28369799]
[109]
Fujii H, Matsubara K, Sakai K, et al. Dopaminergic differentiation of stem cells from human deciduous teeth and their therapeutic benefits for Parkinsonian rats. Brain Res 2015; 1613: 59-72.
[http://dx.doi.org/10.1016/j.brainres.2015.04.001] [PMID: 25863132]
[110]
Jarmalaviciute A, Pivoriunas A. Exosomes as a potential novel therapeutic tools against neurodegenerative diseases. Pharmacological research 2016; 113(B): 816-22.
[111]
Kalani A, Tyagi N. Exosomes in neurological disease, neuroprotection, repair and therapeutics: problems and perspectives. Neural Regen Res 2015; 10(10): 1565-7.
[http://dx.doi.org/10.4103/1673-5374.165305] [PMID: 26692841]
[112]
Doeppner TR, Herz J, Görgens A, et al. Extracellular vesicles improve post-stroke neuroregeneration and prevent postischemic immunosuppression. Stem Cells Transl Med 2015; 4(10): 1131-43.
[http://dx.doi.org/10.5966/sctm.2015-0078] [PMID: 26339036]
[113]
Kalani A, Tyagi A, Tyagi N. Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics. Mol Neurobiol 2014; 49(1): 590-600.
[http://dx.doi.org/10.1007/s12035-013-8544-1] [PMID: 23999871]
[114]
Venugopal C, Shamir C, Senthilkumar S, et al. Dosage and passage dependent neuroprotective effects of exosomes derived from rat bone marrow mesenchymal stem cells: an in vitro analysis. Curr Gene Ther 2017; 17(5): 379-90.
[PMID: 29366415]
[115]
Jarmalavičiūtė A, Tunaitis V, Pivoraitė U, Venalis A, Pivoriūnas A. Exosomes from dental pulp stem cells rescue human dopaminergic neurons from 6-hydroxy-dopamine-induced apoptosis. Cytotherapy 2015; 17(7): 932-9.
[http://dx.doi.org/10.1016/j.jcyt.2014.07.013] [PMID: 25981557]
[116]
Zhuang X, Xiang X, Grizzle W, et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther 2011; 19(10): 1769-79.
[117]
Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 2011; 29(4): 341-5.
[http://dx.doi.org/10.1038/nbt.1807] [PMID: 21423189]
[118]
Shall G, Menosky M, Decker S, et al. Effects of passage number and differentiation protocol on the generation of dopaminergic neurons from rat bone marrow-derived mesenchymal stem cells. Int J Mol Sci 2018; 19(3): 720.
[http://dx.doi.org/10.3390/ijms19030720] [PMID: 29498713]
[119]
Hayashi T, Wakao S, Kitada M, et al. Autologous mesenchymal stem cell-derived dopaminergic neurons function in Parkinsonian macaques. J Clin Invest 2013; 123(1): 272-84.
[http://dx.doi.org/10.1172/JCI62516] [PMID: 23202734]
[120]
Ebrahimi V, Eskandarian Boroujeni M, Aliaghaei A, et al. Functional dopaminergic neurons derived from human chorionic mesenchymal stem cells ameliorate striatal atrophy and improve behavioral deficits in Parkinsonian rat model. Anat Rec (Hoboken) 2020; 303(8): 2274-89.
[http://dx.doi.org/10.1002/ar.24301] [PMID: 31642188]
[121]
Rad AA, Heidari MH, Aliaghaei A, Broujeni ME, Shojaei A, Abbaszadeh HA. In vitro differentiation of adipose derived stem cells into functional dopaminergic neurons. Biomed Pharmacol J 2017; 10(2): 595-605.
[http://dx.doi.org/10.13005/bpj/1146]
[122]
Wang TT, Tio M, Lee W, Beerheide W, Udolph G. Neural differentiation of mesenchymal-like stem cells from cord blood is mediated by PKA. Biochem Biophys Res Commun 2007; 357(4): 1021-7.
[http://dx.doi.org/10.1016/j.bbrc.2007.04.046] [PMID: 17466951]
[123]
Lepski G, Jannes CE, Maciaczyk J, et al. Limited Ca2+ and PKA- pathway dependent neurogenic differentiation of human adult mesenchymal stem cells as compared to fetal neuronal stem cells. Exp Cell Res 2010; 316(2): 216-31.
[http://dx.doi.org/10.1016/j.yexcr.2009.08.006] [PMID: 19686736]
[124]
Lin X, Zhang Y, Dong J, et al. GM-CSF enhances neural differentiation of bone marrow stromal cells. Neuroreport 2007; 18(11): 1113-7.
[http://dx.doi.org/10.1097/WNR.0b013e3282010aff] [PMID: 17589309]
[125]
Khoo ML, Tao H, Meedeniya AC, Mackay-Sim A, Ma DD. Transplantation of neuronal-primed human bone marrow mesenchymal stem cells in hemiparkinsonian rodents. PLoS One 2011; 6(5): e19025.
[http://dx.doi.org/10.1371/journal.pone.0019025] [PMID: 21625433]
[126]
Nandy SB, Mohanty S, Singh M, Behari M, Airan B. Fibroblast Growth Factor-2 alone as an efficient inducer for differentiation of human bone marrow mesenchymal stem cells into dopaminergic neurons. J Biomed Sci 2014; 21(1): 83.
[http://dx.doi.org/10.1186/s12929-014-0083-1] [PMID: 25248378]
[127]
Berg J, Roch M, Altschüler J, et al. Human adipose-derived mesenchymal stem cells improve motor functions and are neuroprotective in the 6-hydroxydopamine-rat model for Parkinson’s disease when cultured in monolayer cultures but suppress hippocampal neurogenesis and hippocampal memory function when cultured in spheroids. Stem Cell Rev Rep 2015; 11(1): 133-49.
[http://dx.doi.org/10.1007/s12015-014-9551-y] [PMID: 25120226]
[128]
Suon S, Yang M, Iacovitti L. Adult human bone marrow stromal spheres express neuronal traits in vitro and in a rat model of Parkinson’s disease. Brain Res 2006; 1106(1): 46-51.
[http://dx.doi.org/10.1016/j.brainres.2006.05.109] [PMID: 16828720]
[129]
Zhang L, Seitz LC, Abramczyk AM, Liu L, Chan C. cAMP initiates early phase neuron-like morphology changes and late phase neural differentiation in mesenchymal stem cells. Cell Mol Life Sci 2011; 68(5): 863-76.
[http://dx.doi.org/10.1007/s00018-010-0497-1] [PMID: 20725762]
[130]
Rooney GE, Howard L, O’Brien T, Windebank AJ, Barry FP. Elevation of cAMP in mesenchymal stem cells transiently upregulates neural markers rather than inducing neural differentiation. Stem Cells Dev 2009; 18(3): 387-98.
[http://dx.doi.org/10.1089/scd.2008.0080] [PMID: 18554089]
[131]
Trzaska KA, Rameshwar P. Dopaminergic neuronal differentiation protocol for human mesenchymal stem cells. Mesenchymal stem cell assays and applications. Humana Press 2011; pp. 295-303.
[http://dx.doi.org/10.1007/978-1-60761-999-4_22]
[132]
Trzaska KA, Kuzhikandathil EV, Rameshwar P. Specification of a dopaminergic phenotype from adult human mesenchymal stem cells. Stem Cells 2007; 25(11): 2797-808.
[http://dx.doi.org/10.1634/stemcells.2007-0212] [PMID: 17656644]
[133]
Kondo T, Johnson SA, Yoder MC, Romand R, Hashino E. Sonic hedgehog and retinoic acid synergistically promote sensory fate specification from bone marrow-derived pluripotent stem cells. Proc Natl Acad Sci USA 2005; 102(13): 4789-94.
[http://dx.doi.org/10.1073/pnas.0408239102] [PMID: 15778294]
[134]
Liqing Y, Jia G, Jiqing C, et al. Directed differentiation of motor neuron cell-like cells from human adipose-derived stem cells in vitro. Neuroreport 2011; 22(8): 370-3.
[http://dx.doi.org/10.1097/WNR.0b013e3283469615] [PMID: 21532392]
[135]
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]
[136]
Ying C, Hu W, Cheng B, Zheng X, Li S. Neural differentiation of rat adipose-derived stem cells in vitro. Cell Mol Neurobiol 2012; 32(8): 1255-63.
[http://dx.doi.org/10.1007/s10571-012-9850-2] [PMID: 22569742]
[137]
Chun SY, Soker S, Jang YJ, Kwon TG, Yoo ES. Differentiation of human dental pulp stem cells into dopaminergic neuron-like cells in vitro. J Korean Med Sci 2016; 31(2): 171-7.
[http://dx.doi.org/10.3346/jkms.2016.31.2.171] [PMID: 26839468]
[138]
Fu YS, Cheng YC, Lin MY, et al. Conversion of human umbilical cord mesenchymal stem cells in Wharton’s jelly to dopaminergic neurons in vitro: potential therapeutic application for Parkinsonism. Stem Cells 2006; 24(1): 115-24.
[http://dx.doi.org/10.1634/stemcells.2005-0053] [PMID: 16099997]

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