Promising Role of Oral Cavity Mesenchymal Stem Cell-Derived Extracellular Vesicles in Neurodegenerative Diseases.

Exosomes Extracellular vesicles Neurodegenerative disease Oral cavity Regenerative medicine Stem cell therapy

Journal

Molecular neurobiology
ISSN: 1559-1182
Titre abrégé: Mol Neurobiol
Pays: United States
ID NLM: 8900963

Informations de publication

Date de publication:
Oct 2022
Historique:
received: 21 09 2021
accepted: 28 06 2022
pubmed: 23 7 2022
medline: 14 9 2022
entrez: 22 7 2022
Statut: ppublish

Résumé

Mesenchymal stem cells (MSCs) and mesenchymal stem cell-derived extracellular vesicles (MSC-EVs) have been regarded as the beneficial and available tools to treat various hereditary, multifactorial, acute, and chronic diseases. Mesenchymal stem cells can be extracted from numerous sources for clinical purposes while oral cavity-derived mesenchymal stem cells seem to be more effective in neuroregeneration than other sources due to their similar embryonic origins to neuronal tissues. In various studies and different neurodegenerative diseases (NDs), oral cavity mesenchymal stem cells have been applied to prove their promising capacities in disease improvement. Moreover, oral cavity mesenchymal stem cells' secretion is regarded as a novel and practical approach to neuroregeneration; hence, extracellular vesicles (EVs), especially exosomes, may provide promising results to improve CNS defects. This review article focuses on how oral cavity-derived stem cells and their extracellular vesicles can improve neurodegenerative conditions and tries to show which molecules are involved in the recovery process.

Identifiants

pubmed: 35867205
doi: 10.1007/s12035-022-02951-y
pii: 10.1007/s12035-022-02951-y
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

6125-6140

Subventions

Organisme : Shahid Beheshti University of Medical Sciences
ID : 29269 Hamtaparvari

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Williams A (2002) Defining neurodegenerative diseases: Disorders will be named after responsible rogue proteins and their solutions. Bmj 324(7352):1465–1466
Nooshabadi VT, Mardpour S, Yousefi-Ahmadipour A, Allahverdi A, Izadpanah M, Daneshimehr F, Ai J, Banafshe HR et al (2018) The extracellular vesicles-derived from mesenchymal stromal cells: a new therapeutic option in regenerative medicine. J Cell Biochem 119:8048–8073
pubmed: 29377241
Goldman S (2005) Stem and progenitor cell–based therapy of the human central nervous system. Nat Biotechnol 23:862–871
pubmed: 16003375
Maqsood M, Kang M, Wu X, Chen J, Teng L, Qiu L (2020) Adult mesenchymal stem cells and their exosomes: sources, characteristics, and application in regenerative medicine. Life Sci 256:118002
pubmed: 32585248
Ullah I, Subbarao RB, Rho GJ (2015) Human mesenchymal stem cells-current trends and future prospective. Biosci Rep 35(2):e00191
Pen A, Jensen U (2017) Current status of treating neurodegenerative disease with induced pluripotent stem cells. Acta Neurol Scand 135:57–72
pubmed: 26748435
Sugaya K, Vaidya M (2018) Stem cell therapies for neurodegenerative diseases. Adv Exp Med Biol 1056:61–84
Spagnuolo G, Codispoti B, Marrelli M, Rengo C, Rengo S, Tatullo M (2018) Commitment of oral-derived stem cells in dental and maxillofacial applications. Dent J 6:72
Becker AJ, McCulloch EA, Till JE (1963) Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197(4866):452–454
Mayo V, Sawatari Y, Huang C-YC, Garcia-Godoy F (2014) Neural crest-derived dental stem cells—where we are and where we are going. J Dent 42:1043–1051
pubmed: 24769107
Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci 97:13625–13630
pubmed: 11087820 pmcid: 17626
Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S (2003) SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci 100:5807–5812
pubmed: 12716973 pmcid: 156282
Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, Shi S, Huang GT-J (2008) Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 34:166–171
pubmed: 18215674 pmcid: 2714367
Rosa V, Dubey N, Islam I, Min KS, Nör JE (2016) Pluripotency of stem cells from human exfoliated deciduous teeth for tissue engineering. Stem Cells Int 2016:5957806
Akintoye SO, Lam T, Shi S, Brahim J, Collins MT, Robey PG (2006) Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. Bone 38:758–768. https://doi.org/10.1016/j.bone.2005.10.027
doi: 10.1016/j.bone.2005.10.027 pubmed: 16403496
Marynka-Kalmani K, Treves S, Yafee M, Rachima H, Gafni Y, Cohen MA, Pitaru S (2010) The lamina propria of adult human oral mucosa harbors a novel stem cell population. Stem Cells 28:984–995
pubmed: 20474080
Morsczeck C, Götz W, Schierholz J, Zeilhofer F, Kühn U, Möhl C, Sippel C, Hoffmann K (2005) Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24:155–165
pubmed: 15890265
Sato A, Okumura K, Matsumoto S, Hattori K, Hattori S, Shinohara M, Endo F (2007) Isolation, tissue localization, and cellular characterization of progenitors derived from adult human salivary glands. Cloning Stem Cells 9:191–205
pubmed: 17579552
Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Shi S, Le AD (2009) Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 183:7787. https://doi.org/10.4049/jimmunol.0902318
doi: 10.4049/jimmunol.0902318 pubmed: 19923445
Zhang Q, Nguyen A, Yu W, Le A (2012) Human oral mucosa and gingiva: a unique reservoir for mesenchymal stem cells. J Dent Res 91:1011–1018
pubmed: 22988012 pmcid: 3490281
Huang G-J, Gronthos S, Shi S (2009) Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res 88:792–806
pubmed: 19767575 pmcid: 2830488
Kerkis I, Kerkis A, Dozortsev D, Stukart-Parsons GC, Massironi SMG, Pereira LV, Caplan AI, Cerruti HF (2006) Isolation and characterization of a population of immature dental pulp stem cells expressing OCT-4 and other embryonic stem cell markers. Cells Tissues Organs 184:105–116
pubmed: 17409736
Egusa H, Sonoyama W, Nishimura M, Atsuta I, Akiyama K (2012) Stem cells in dentistry–part I: stem cell sources. J Prosthodont Res 56:151–165
pubmed: 22796367
Jurj A, Zanoaga O, Braicu C, Lazar V, Tomuleasa C, Irimie A, Berindan-Neagoe I (2020) A comprehensive picture of extracellular vesicles and their contents. Mol Transf Cancer Cells Cancers 12:298
Pang B, Zhu Y, Ni J, Thompson J, Malouf D, Bucci J, Graham P, Li Y (2020) Extracellular vesicles: the next generation of biomarkers for liquid biopsy-based prostate cancer diagnosis. Theranostics 10:2309
pubmed: 32089744 pmcid: 7019149
Dickhout A, Koenen RR (2018) Extracellular vesicles as biomarkers in cardiovascular disease; chances and risks. Front Cardiovasc Med 5:113
pubmed: 30186839 pmcid: 6113364
Xu K, Liu Q, Wu K, Liu L, Zhao M, Yang H, Wang X, Wang W (2020) Extracellular vesicles as potential biomarkers and therapeutic approaches in autoimmune diseases. J Transl Med 18:1–8
Gowen A, Shahjin F, Chand S, Odegaard KE, Yelamanchili SV (2020) Mesenchymal stem cell-derived extracellular vesicles: challenges in clinical applications. Front Cell Dev Biol 8:149
pubmed: 32226787 pmcid: 7080981
Rani S, Ryan AE, Griffin MD, Ritter T (2015) Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther 23:812–823
pubmed: 25868399 pmcid: 4427881
30.Giebel B, Kordelas L, Börger V (2017) Clinical potential of mesenchymal stem/stromal cell-derived extracellular vesicles. Stem Cell Investig 4:84. https://doi.org/10.21037/sci.2017.09.06
Jafarinia M, Alsahebfosoul F, Salehi H, Eskandari N, Ganjalikhani-Hakemi M (2020) Mesenchymal stem cell-derived extracellular vesicles: a novel cell-free therapy. Immunol Invest 49:758–780
pubmed: 32009478
Veerman RE, Akpinar GG, Eldh M, Gabrielsson S (2019) Immune cell-derived extracellular vesicles–functions and therapeutic applications. Trends Mol Med 25:382–394
pubmed: 30853173
Merino-González C, Zuñiga FA, Escudero C, Ormazabal V, Reyes C, Nova-Lamperti E, Salomón C, Aguayo C (2016) Mesenchymal stem cell-derived extracellular vesicles promote angiogenesis: potencial clinical application. Front Physiol 7:24
pubmed: 26903875 pmcid: 4746282
Caruso S, Atkin-Smith GK, Baxter AA, Tixeira R, Jiang L, Ozkocak DC, Santavanond JP, Hulett MD et al (2019) Defining the role of cytoskeletal components in the formation of apoptopodia and apoptotic bodies during apoptosis. Apoptosis 24:862–877
pubmed: 31489517
Li B, Zhang H, Zeng M, He W, Li M, Huang X, Deng DY, Wu J (2015) Bone marrow mesenchymal stem cells protect alveolar macrophages from lipopolysaccharide-induced apoptosis partially by inhibiting the Wnt/β-catenin pathway. Cell Biol Int 39:192–200
pubmed: 25229877
Jiang JX, Mikami K, Venugopal S, Li Y, Török NJ (2009) Apoptotic body engulfment by hepatic stellate cells promotes their survival by the JAK/STAT and Akt/NF-κB-dependent pathways. J Hepatol 51:139–148
pubmed: 19457567 pmcid: 2765371
Liu D, Kou X, Chen C, Liu S, Liu Y, Yu W, Yu T, Yang R et al (2018) Circulating apoptotic bodies maintain mesenchymal stem cell homeostasis and ameliorate osteopenia via transferring multiple cellular factors. Cell Res 28:918–933
pubmed: 30030518 pmcid: 6123409
Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Köppel T et al (2009) Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2:ra81
pubmed: 19996457
Liu J, Qiu X, Lv Y, Zheng C, Dong Y, Dou G, Zhu B, Liu A et al (2020) Apoptotic bodies derived from mesenchymal stem cells promote cutaneous wound healing via regulating the functions of macrophages. Stem Cell Res Ther 11:1–15
Lamichhane TN, Sokic S, Schardt JS, Raiker RS, Lin JW, Jay SM (2015) Emerging roles for extracellular vesicles in tissue engineering and regenerative medicine. Tissue Eng B Rev 21:45–54
Ståhl A-l, Johansson K, Mossberg M, Kahn R, Karpman D (2019) Exosomes and microvesicles in normal physiology, pathophysiology, and renal diseases. Pediatr Nephrol 34:11–30
pubmed: 29181712
Lai RC, Tan SS, Yeo RWY, Choo ABH, Reiner AT, Su Y, Shen Y, Fu Z et al (2016) MSC secretes at least 3 EV types each with a unique permutation of membrane lipid, protein and RNA. J Extracell Vesicles 5:29828
pubmed: 26928672
Jimenez JJ, Jy W, Mauro LM, Soderland C, Horstman LL, Ahn YS (2003) Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thromb Res 109:175–180
pubmed: 12757771
Turturici G, Tinnirello R, Sconzo G, Geraci F (2014) Extracellular membrane vesicles as a mechanism of cell-to-cell communication: advantages and disadvantages. Am J Physiol Cell Physiol 306:C621–C633
pubmed: 24452373
Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L (2010) Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 78:838–848
pubmed: 20703216
Johnstone RM, Adam M, Hammond J, Orr L, Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262:9412–9420
pubmed: 3597417
Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, Antoniou A, Arab T et al (2018) Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles 7:1535750
pubmed: 30637094 pmcid: 6322352
Van Niel G, d’Angelo G, Raposo G (2018) Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 19:213
pubmed: 29339798
Konala VBR, Mamidi MK, Bhonde R, Das AK, Pochampally R, Pal R (2016) The current landscape of the mesenchymal stromal cell secretome: a new paradigm for cell-free regeneration. Cytotherapy 18:13–24
pubmed: 26631828
Willms E, Johansson HJ, Mäger I, Lee Y, Blomberg KEM, Sadik M, Alaarg A, Smith CE et al (2016) Cells release subpopulations of exosomes with distinct molecular and biological properties. Sci Rep 6:22519
pubmed: 26931825 pmcid: 4773763
Keller S, Sanderson MP, Stoeck A, Altevogt P (2006) Exosomes: from biogenesis and secretion to biological function. Immunol Lett 107:102–108
pubmed: 17067686
Spaull R, McPherson B, Gialeli A, Clayton A, Uney J, Heep A, Cordero-Llana Ó (2019) Exosomes populate the cerebrospinal fluid of preterm infants with post-haemorrhagic hydrocephalus. Int J Dev Neurosci 73:59–65. https://doi.org/10.1016/j.ijdevneu.2019.01.004
doi: 10.1016/j.ijdevneu.2019.01.004 pubmed: 30639393
Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Möbius W, Hoernschemeyer J, Slot J-W, Geuze HJ et al (2003) Proteomic and biochemical analyses of human B cell-derived exosomes Potential implications for their function and multivesicular body formation. J Biol Chem 278:10963–10972
pubmed: 12519789
Hurley JH, Odorizzi G (2012) Get on the exosome bus with ALIX. Nat Cell Biol 14:654–655
pubmed: 22743708
Gangoda L, Boukouris S, Liem M, Kalra H, Mathivanan S (2015) Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics 15:260–271
pubmed: 25307053
Greening DW, Gopal SK, Xu R, Simpson RJ, Chen W (2015) Exosomes and their roles in immune regulation and cancer. Semin Cell Dev Biol 40:72–81
Dorayappan KDP, Wallbillich JJ, Cohn DE, Selvendiran K (2016) The biological significance and clinical applications of exosomes in ovarian cancer. Gynecol Oncol 142:199–205
pubmed: 27058839 pmcid: 4917458
Escudero CA, Herlitz K, Troncoso F, Acurio J, Aguayo C, Roberts JM, Truong G, Duncombe G et al (2016) Role of extracellular vesicles and microRNAs on dysfunctional angiogenesis during preeclamptic pregnancies. Front Physiol 7:98
pubmed: 27047385 pmcid: 4796029
Théry C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9:581–593
pubmed: 19498381
Simpson RJ, Lim JW, Moritz RL, Mathivanan S (2009) Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics 6:267–283
pubmed: 19489699
Colombo M, Raposo G, Théry C (2014) Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 30:255–289
pubmed: 25288114
Burger D, Schock S, Thompson CS, Montezano AC, Hakim AM, Touyz RM (2013) Microparticles: biomarkers and beyond. Clin Sci 124:423–441
Borges FT, Reis L, Schor N (2013) Extracellular vesicles: structure, function, and potential clinical uses in renal diseases. Braz J Med Biol Res 46:824–830
pubmed: 24141609 pmcid: 3854311
Doyle LM, Wang MZ (2019) Overview of extracellular vesicles, their origin, composition, purpose, and methods for exosome isolation and analysis. Cells 8:727
pmcid: 6678302
Zolezzi, JM, Bastías-Candia S, Inestrosa NC (2018) Molecular basis of neurodegeneration: Lessons from Alzheimer’s and Parkinson’s diseases. In Recent advances in neurodegeneration. IntechOpen. https://doi.org/10.5772/intechopen.81270
Jellinger KA (2011) Interaction between α-Synuclein and other proteins in neurodegenerative disorders. Sci World J 11:1893–1907
Wang J, Gu BJ, Masters CL, Wang Y-J (2017) A systemic view of Alzheimer disease—insights from amyloid-β metabolism beyond the brain. Nat Rev Neurol 13:612–623
pubmed: 28960209
Mangialasche F, Solomon A, Winblad B, Mecocci P, Kivipelto M (2010) Alzheimer’s disease: clinical trials and drug development. Lancet Neurol 9:702–716
pubmed: 20610346
Berk C, Paul G, Sabbagh M (2014) Investigational drugs in Alzheimer’s disease: current progress. Expert Opin Investig Drugs 23:837–846
pubmed: 24702504
Plassman BL, Langa KM, Fisher GG, Heeringa SG, Weir DR, Ofstedal MB, Burke JR, Hurd MD et al (2007) Prevalence of dementia in the United States: the aging, demographics, and memory study. Neuroepidemiology 29:125–132
pubmed: 17975326 pmcid: 2705925
As A (2019) 2019 Alzheimer’s disease facts and figures. Alzheimers Dement 15:321–387
Latta CH, Brothers HM, Wilcock DM (2015) Neuroinflammation in Alzheimer’s disease; a source of heterogeneity and target for personalized therapy. Neuroscience 302:103–111
pubmed: 25286385
Jaber VR, Zhao Y, Sharfman NM, Li W, Lukiw WJ (2019) Addressing Alzheimer’s disease (AD) neuropathology using anti-microRNA (AM) strategies. Mol Neurobiol 56:8101–8108
pubmed: 31183807 pmcid: 6842093
Selkoe DJ, Hardy J (2016) The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol Med 8:595–608
pubmed: 27025652 pmcid: 4888851
Hyman BT, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Carrillo MC, Dickson DW, Duyckaerts C et al (2012) National Institute on aging–Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer’s disease. Alzheimers Dement 8:1–13
pubmed: 22265587 pmcid: 3266529
Mhatre SD, Tsai CA, Rubin AJ, James ML, Andreasson KI (2015) Microglial malfunction: the third rail in the development of Alzheimer’s disease. Trends Neurosci 38:621–636
pubmed: 26442696 pmcid: 4670239
Religa P, Cao R, Religa D, Xue Y, Bogdanovic N, Westaway D, Marti HH, Winblad B, Cao Y (2013) VEGF significantly restores impaired memory behavior in Alzheimer’s mice by improvement of vascular survival. Sci Rep 3:2053
pubmed: 23792494 pmcid: 3690383
Cho S-H, Sun B, Zhou Y, Kauppinen TM, Halabisky B, Wes P, Ransohoff RM, Gan L (2011) CX3CR1 protein signaling modulates microglial activation and protects against plaque-independent cognitive deficits in a mouse model of Alzheimer disease. J Biol Chem 286:32713–32722
pubmed: 21771791 pmcid: 3173153
Ahmed NE-MB, Murakami M, Hirose Y, Nakashima M (2016) Therapeutic potential of dental pulp stem cell secretome for Alzheimer’s disease treatment: an in vitro study. Stem Cells Int 2016:8102478. https://doi.org/10.1155/2016/8102478
doi: 10.1155/2016/8102478 pmcid: 4923581
Zhang X-M, Ouyang Y-J, Yu B-Q, Li W, Yu M-Y, Li J-Y, Jiao Z-M, Yang D et al (2021) Therapeutic potential of dental pulp stem cell transplantation in a rat model of Alzheimer’s disease. Neural Regen Res 16:893
pubmed: 33229725
Mita T, Furukawa-Hibi Y, Takeuchi H, Hattori H, Yamada K, Hibi H, Ueda M, Yamamoto A (2015) Conditioned medium from the stem cells of human dental pulp improves cognitive function in a mouse model of Alzheimer’s disease. Behav Brain Res 293:189–197
pubmed: 26210934
McDonald C, Gordon G, Hand A, Walker RW, Fisher JM (2018) 200 Years of Parkinson’s disease: what have we learnt from James Parkinson? Age Ageing 47:209–214
pubmed: 29315364
Migliore L, Coppedè F (2009) Genetics, environmental factors and the emerging role of epigenetics in neurodegenerative diseases. Mutat Res Fundam Mol Mech Mutagen 667:82–97
Sveinbjornsdottir S (2016) The clinical symptoms of Parkinson’s disease. J Neurochem 139:318–324
pubmed: 27401947
Pringsheim T, Jette N, Frolkis A, Steeves TD (2014) The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 29:1583–1590
pubmed: 24976103
Braak H, Del Tredici K, Rüb U, De Vos RA, Steur ENJ, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211
pubmed: 12498954
Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318:121–134
pubmed: 15338272
Jankovic J, Stacy M (2007) Medical management of levodopa-associated motor complications in patients with Parkinson’s disease. CNS Drugs 21:677–692
pubmed: 17630819
Leggio L, Paternò G, Vivarelli S, L’episcopo F, Tirolo C, Raciti G, Pappalardo F, Giachino C et al (2020) Extracellular vesicles as nanotherapeutics for Parkinson’s disease. Biomolecules 10:1327
pmcid: 7563168
Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, Patel T, Piroyan A et al (2015) Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release 207:18–30
pubmed: 25836593 pmcid: 4430381
Fujii H, Matsubara K, Sakai K, Ito M, Ohno K, Ueda M, Yamamoto A (2015) Dopaminergic differentiation of stem cells from human deciduous teeth and their therapeutic benefits for Parkinsonian rats. Brain Res 1613:59–72
pubmed: 25863132
Narbute K, Piļipenko V, Pupure J, Dzirkale Z, Jonavičė U, Tunaitis V, Kriaučiūnaitė K, Jarmalavičiūtė A et al (2019) Intranasal administration of extracellular vesicles derived from human teeth stem cells improves motor symptoms and normalizes tyrosine hydroxylase expression in the substantia nigra and striatum of the 6-hydroxydopamine-treated rats. Stem Cells Transl Med 8:490–499
pubmed: 30706999 pmcid: 6477008
Schober A (2004) Classic toxin-induced animal models of Parkinson’s disease: 6-OHDA and MPTP. Cell Tissue Res 318:215–224
pubmed: 15503155
Zhang N, Lu X, Wu S, Li X, Duan J, Chen C, Wang W, Song H et al (2018) Intrastriatal transplantation of stem cells from human exfoliated deciduous teeth reduces motor defects in Parkinsonian rats. Cytotherapy 20:670–686
pubmed: 29576501
Cova L, Bossolasco P, Armentero M-T, Diana V, Zennaro E, Mellone M, Calzarossa C, Cerri S et al (2012) Neuroprotective effects of human mesenchymal stem cells on neural cultures exposed to 6-hydroxydopamine: implications for reparative therapy in Parkinson’s disease. Apoptosis 17:289–304
pubmed: 22160861
Apel C, Forlenza O, De Paula V, Talib L, Denecke B, Eduardo C, Gattaz W (2009) The neuroprotective effect of dental pulp cells in models of Alzheimer’s and Parkinson’s disease. J Neural Transm 116:71
pubmed: 18972063
Nosrat IV, Smith CA, Mullally P, Olson L, Nosrat CA (2004) 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 19:2388–2398
pubmed: 15128393
Gnanasegaran N, Govindasamy V, Mani V, Abu Kasim NH (2017) Neuroimmunomodulatory properties of DPSCs in an in vitro model of Parkinson’s disease. IUBMB Life 69:689–699
pubmed: 28685937
Upadhya R, Shetty AK (2021) Extracellular vesicles for the diagnosis and treatment of Parkinson’s disease. Aging Dis 12:1438
pubmed: 34527420 pmcid: 8407884
Long Q, Upadhya D, Hattiangady B, Kim D-K, An SY, Shuai B, Prockop DJ, Shetty AK (2017) Intranasal MSC-derived A1-exosomes ease inflammation, and prevent abnormal neurogenesis and memory dysfunction after status epilepticus. Proc Natl Acad Sci 114:E3536–E3545
pubmed: 28396435 pmcid: 5410779
Pinheiro A, Silva AM, Teixeira JH, Gonçalves RM, Almeida MI, Barbosa MA, Santos SG (2018) Extracellular vesicles: intelligent delivery strategies for therapeutic applications. J Control Release 289:56–69
pubmed: 30261205
Simon C, Gan QF, Kathivaloo P, Mohamad NA, Dhamodharan J, Krishnan A, Sengodan B, Palanimuthu VR et al (2019) Deciduous DPSCs ameliorate MPTP-mediated neurotoxicity, sensorimotor coordination and olfactory function in Parkinsonian mice. Int J Mol Sci 20:568
pmcid: 6387212
Al Mamun A, Wu Y, Monalisa I, Jia C, Zhou K, Munir F, Xiao J (2021) Role of pyroptosis in spinal cord injury and its therapeutic implications. J Adv Res 28:97–109
pubmed: 33364048
Nicola F, Marques MR, Odorcyk F, Petenuzzo L, Aristimunha D, Vizuete A, Sanches EF, Pereira DP et al (2019) Stem cells from human exfoliated deciduous teeth modulate early astrocyte response after spinal cord contusion. Mol Neurobiol 56:748–760
pubmed: 29796991
Goldshmit Y, Lythgo N, Galea MP, Turnley AM (2008) Treadmill training after spinal cord hemisection in mice promotes axonal sprouting and synapse formation and improves motor recovery. J Neurotrauma 25:449–465
pubmed: 18352823
Nicola FC, Rodrigues LP, Crestani T, Quintiliano K, Sanches EF, Willborn S, Aristimunha D, Boisserand L, Pranke P, Netto CA (2016) Human dental pulp stem cells transplantation combined with treadmill training in rats after traumatic spinal cord injury. Braz J Med Biol Res 49(9):e5319
Sakai K, Yamamoto A, Matsubara K, Nakamura S, Naruse M, Yamagata M, Sakamoto K, Tauchi R et al (2012) Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. J Clin Investig 122:80–90
pubmed: 22133879
Zhang J, Lu X, Feng G, Gu Z, Sun Y, Bao G, Xu G, Lu Y et al (2016) Chitosan scaffolds induce human dental pulp stem cells to neural differentiation: potential roles for spinal cord injury therapy. Cell Tissue Res 366:129–142
pubmed: 27147262
Prado C, Fratini P, Matias GdSS, Bocabello RZ, Monteiro J, do Santos CJ Jr, Joaquim JG, Giglio RF et al (2019) Combination of stem cells from deciduous teeth and electroacupuncture for therapy in dogs with chronic spinal cord injury: A pilot study. Res Vet Sci 123:247–251
pubmed: 30703615
Feitosa MLT, Sarmento CAP, Bocabello RZ, Beltrão-Braga PCB, Pignatari GC, Giglio RF, Miglino MA, Orlandin JR et al (2017) Transplantation of human immature dental pulp stem cell in dogs with chronic spinal cord injury 1. Acta Cir Bras 32:540–549
pubmed: 28793038
Rajan TS, Giacoppo S, Diomede F, Ballerini P, Paolantonio M, Marchisio M, Piattelli A, Bramanti P et al (2016) The secretome of periodontal ligament stem cells from MS patients protects against EAE. Sci Rep 6:38743
pubmed: 27924938 pmcid: 5141419
Mammana S, Gugliandolo A, Cavalli E, Diomede F, Iori R, Zappacosta R, Bramanti P, Conti P et al (2019) Human gingival mesenchymal stem cells pretreated with vesicular moringin nanostructures as a new therapeutic approach in a mouse model of spinal cord injury. J Tissue Eng Regen Med 13:1109–1121
pubmed: 30942960 pmcid: 6771565
Rajan TS, Diomede F, Bramanti P, Trubiani O, Mazzon E (2017) Conditioned medium from human gingival mesenchymal stem cells protects motor-neuron-like NSC-34 cells against scratch-injury-induced cell death. Int J Immunopathol Pharmacol 30:383–394
pubmed: 29140156 pmcid: 5806806
Fletcher JM, Lalor S, Sweeney C, Tubridy N, Mills K (2010) T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin Exp Immunol 162:1–11
pubmed: 20682002 pmcid: 2990924
Rodriguez M (2007) Effectors of demyelination and remyelination in the CNS: implications for multiple sclerosis. Brain Pathol 17:219–229
pubmed: 17388953 pmcid: 8095636
Rostami A, Ciric B (2013) Role of Th17 cells in the pathogenesis of CNS inflammatory demyelination. J Neurol Sci 333:76–87
pubmed: 23578791 pmcid: 3726569
Loos J, Schmaul S, Noll TM, Paterka M, Schillner M, Löffel JT, Zipp F, Bittner S (2020) Functional characteristics of Th1, Th17, and ex-Th17 cells in EAE revealed by intravital two-photon microscopy. J Neuroinflamm 17:1–12
Jadidi-Niaragh F, Mirshafiey A (2011) Th17 cell, the new player of neuroinflammatory process in multiple sclerosis. Scand J Immunol 74:1–13
pubmed: 21338381
Renno T, Krakowski M, Piccirillo C, Lin J, Owens T (1995) TNF-alpha expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. Regulation by Th1 cytokines. J Immunol 154:944–953
pubmed: 7814894
Juedes AE, Hjelmström P, Bergman CM, Neild AL, Ruddle NH (2000) Kinetics and cellular origin of cytokines in the central nervous system: insight into mechanisms of myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis. J Immunol 164:419–426
pubmed: 10605038
Goverman J (2009) Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 9:393–407
pubmed: 19444307 pmcid: 2813731
Mei F-J, Osoegawa M, Ochi H, Minohara M, Nan S, Murai H, Ishizu T, Taniwaki T et al (2006) Long-term favorable response to interferon beta-1b is linked to cytokine deviation toward the Th2 and Tc2 sides in Japanese patients with multiple sclerosis. J Neurol Sci 246:71–77
pubmed: 16581087
Payne NL, Sun G, McDonald C, Moussa L, Emerson-Webber A, Loisel-Meyer S, Medin JA, Siatskas C et al (2013) Human adipose-derived mesenchymal stem cells engineered to secrete IL-10 inhibit APC function and limit CNS autoimmunity. Brain Behav Immun 30:103–114
pubmed: 23369732
Rossato C, Brandao WN, Castro SB, de Almeida DC, Maranduba CM, Camara NO, Peron JP, Silva FS (2017) Stem cells from human-exfoliated deciduous teeth reduce tissue-infiltrating inflammatory cells improving clinical signs in experimental autoimmune encephalomyelitis. Biologicals 49:62–68
pubmed: 28666719
Vespa P, Bergsneider M, Hattori N, Wu H-M, Huang S-C, Martin NA, Glenn TC, McArthur DL et al (2005) Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J Cereb Blood Flow Metab 25:763–774
pubmed: 15716852
Song M, Lee J-H, Bae J, Bu Y, Kim E-C (2017) Human dental pulp stem cells are more effective than human bone marrow-derived mesenchymal stem cells in cerebral ischemic injury. Cell Transplant 26:1001–1016
pubmed: 28105979 pmcid: 5657745
Nito C, Sowa K, Nakajima M, Sakamoto Y, Suda S, Nishiyama Y, Nakamura-Takahashi A, Nitahara-Kasahara Y et al (2018) Transplantation of human dental pulp stem cells ameliorates brain damage following acute cerebral ischemia. Biomed Pharmacother 108:1005–1014
pubmed: 30372800
Inoue T, Sugiyama M, Hattori H, Wakita H, Wakabayashi T, Ueda M (2013) Stem cells from human exfoliated deciduous tooth-derived conditioned medium enhance recovery of focal cerebral ischemia in rats. Tissue Eng Part A 19:24–29
pubmed: 22839964
Bunggulawa EJ, Wang W, Yin T, Wang N, Durkan C, Wang Y, Wang G (2018) Recent advancements in the use of exosomes as drug delivery systems. J Nanobiotechnol 16:81. https://doi.org/10.1186/s12951-018-0403-9
doi: 10.1186/s12951-018-0403-9
Chen TS, Arslan F, Yin Y, Tan SS, Lai RC, Choo ABH, Padmanabhan J, Lee CN et al (2011) Enabling a robust scalable manufacturing process for therapeutic exosomes through oncogenic immortalization of human ESC-derived MSCs. J Transl Med 9:1–10
Wang J, Bonacquisti EE, Brown AD and Nguyen J (2020) Boosting the biogenesis and secretion of mesenchymal stem cell-derived exosomes. Cells 9.  https://doi.org/10.3390/cells9030660

Auteurs

Masoumeh Pourhadi (M)

Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

Hakimeh Zali (H)

Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran. h.zali@sbmu.ac.ir.

Rasoul Ghasemi (R)

Department of Physiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

Saeed Vafaei-Nezhad (S)

Cellular & Molecular Research Center, Birjand University of Medical Sciences, Birjand, Iran.
Department of Anatomical Sciences, Faculty of Medicine, Birjand University of Medical Sciences, Birjand, Iran.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH