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Stem Cells from Human Exfoliated Deciduous Teeth Modulate Early Astrocyte Response after Spinal Cord Contusion

Molecular Neurobiology volume 56, pages 748–760 (2019)Cite this article

A Correction to this article was published on 16 June 2018

This article has been updated

Abstract

The transplantation of stem cells from human exfoliated deciduous teeth (SHED) has been studied as a possible treatment strategy for spinal cord injuries (SCIs) due to its potential for promoting tissue protection and functional recovery. The aim of the present study was to investigate the effects of the early transplantation of SHED on glial scar formation and astrocytic reaction after an experimental model of SCI. Wistar rats were spinalized using the NYU Impactor. Animals were randomly distributed into three groups: control (naive) (animal with no manipulation); SCI (receiving laminectomy followed by SCI and treated with vehicle), and SHED (SCI rat treated with intraspinal SHED transplantation, 1 h after SCI). In vitro investigation demonstrated that SHED were able to express mesenchymal stem cells, vimentin and S100B markers, related with neural progenitor and glial cells, respectively. The acute SHED transplantation promoted functional recovery, measured as from the first week after spinal cord contusion by Basso, Beattie, and Bresnahan scale. Twenty-four and 48 h after lesion, flow cytometry revealed a spinal cord vimentin+ cells increment in the SHED group. The increase of vimentin+ cells was confirmed by immunofluorescence. Moreover, the bioavailability of astrocytic proteins such as S100B and Kir4.1 shown to be increased in the spinal cord of SHED group, whereas there was a glial scar reduction, as indicated by ELISA and Western blot techniques. The presented results support that SHED act as a neuroprotector agent after transplantation, probably through paracrine signaling to reduce glial scar formation, inducing tissue plasticity and functional recovery.

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  • 16 June 2018

    The authors hereby declare that the Figure 4 in page eight of the paper “Stem cells from human exfoliated deciduous teeth modulate early astrocyte response after spinal cord contusion” authored by Fabrício Nicola and colleagues (DOI: 10.1007/s12035-018-1127-4) was mistakenly included.

Abbreviations

APC:

Allophycocyanin

AQP4:

Aquaporin 4

BBB:

Basso, Beattie, and Bresnahan scale

FITC:

Fluorescein isothiocyanate

GFAP:

Glial fibrillary acidic protein

Kir:

Inward rectifying potassium channel

MASCIS:

Multicenter Animal Spinal Cord Injury Study

MSCs:

Mesenchymal stem cells

PE:

Phycoerythrin

PMSF:

Phenylmethyl-sulphonyl fluoride

SCI:

Spinal cord injury

SHED:

Stem cells from human exfoliated deciduous teeth

S100B:

Calcium-binding protein

TBS:

Tris-buffered saline

Tx:

Triton X-100

Vimentin:

Progenitor neural cells

βIII-tubulin:

Neuronal microtubule protein

References

  1. Lee BB, Cripps R a, Fitzharris M, Wing PC (2014) The global map for traumatic spinal cord injury epidemiology: update 2011, global incidence rate. Spinal Cord 52:110–116. https://doi.org/10.1038/sc.2012.158

    Article  CAS  PubMed  Google Scholar 

  2. Oyinbo CA (2011) Secondary injury mechanisms in traumatic spinal cord injury: a nugget of this multiply cascade. Acta Neurobiol Exp (Wars) 71:281–299

    Google Scholar 

  3. Cerqueira SR, Oliveira JM, Silva N a et al (2013) Microglia response and in vivo therapeutic potential of methylprednisolone-loaded dendrimer nanoparticles in spinal cord injury. Small 9:738–749. https://doi.org/10.1002/smll.201201888

    Article  CAS  PubMed  Google Scholar 

  4. Casella GTB, Bunge MB, Wood PM (2006) Endothelial cell loss is not a major cause of neuronal and glial cell death following contusion injury of the spinal cord. Exp Neurol 202:8–20. https://doi.org/10.1016/j.expneurol.2006.05.028

    Article  PubMed  Google Scholar 

  5. Nicola F do C, Marques MR, Odorcyk F et al (2017) Neuroprotector effect of stem cells from human exfoliated deciduous teeth transplanted after traumatic spinal cord injury involves inhibition of early neuronal apoptosis. Brain Res 1663:95–105. https://doi.org/10.1016/j.brainres.2017.03.015

    Article  CAS  Google Scholar 

  6. Seki T, Namba T, Mochizuki H, Onodera M (2007) Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 502:275–290. https://doi.org/10.1002/cne

    Article  CAS  PubMed  Google Scholar 

  7. Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ (2010) Quantitative analysis of cellular inflammation after traumatic spinal cord injury: Evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 133:433–447. https://doi.org/10.1093/brain/awp322

    Article  PubMed  PubMed Central  Google Scholar 

  8. Burda JE, Sofroniew MV (2014) Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 81:229–248. https://doi.org/10.1016/j.neuron.2013.12.034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ridet JL, Malhotra SK, Privat A, Gage FH (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20:570–577. https://doi.org/10.1016/S0166-2236(97)01139-9

    Article  CAS  PubMed  Google Scholar 

  10. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638–647. https://doi.org/10.1016/j.tins.2009.08.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Saadoun S, Papadopoulos MC (2010) Aquaporin-4 in brain and spinal cord oedema. Neuroscience 168:1036–1046. https://doi.org/10.1016/j.neuroscience.2009.08.019

    Article  CAS  PubMed  Google Scholar 

  12. Tait MJ, Saadoun S, Bell BA, Papadopoulos MC (2008) Water movements in the brain: Role of aquaporins. Trends Neurosci 31:37–43. https://doi.org/10.1016/j.tins.2007.11.003

    Article  CAS  PubMed  Google Scholar 

  13. Nesic O, Guest JD, Zivadinovic D, Narayana PA, Herrera JJ, Grill RJ, Mokkapati VUL, Gelman BB et al (2010) Aquaporins in spinal cord injury: the janus face of aquaporin 4. Neuroscience 168:1019–1035. https://doi.org/10.1016/j.neuroscience.2010.01.037

    Article  CAS  PubMed  Google Scholar 

  14. Butt AM, Kalsi A (2006) Inwardly rectifying potassium channels (Kir) in central nervous system glia: A special role for Kir4.1 in glial functions. J Cell Mol Med 10:33–44. https://doi.org/10.1111/j.1582-4934.2006.tb00289.x

    Article  CAS  PubMed  Google Scholar 

  15. Nichols CG, Lopatin a N (1997) Inward rectifier potassium channels. Annu Rev Physiol 59:171–191. https://doi.org/10.1146/annurev.physiol.59.1.171

    Article  CAS  PubMed  Google Scholar 

  16. Sibille J, Pannasch U, Rouach N (2014) Astroglial potassium clearance contributes to short-term plasticity of synaptically evoked currents at the tripartite synapse. J Physiol 592:87–102. https://doi.org/10.1113/jphysiol.2013.261735

    Article  CAS  PubMed  Google Scholar 

  17. Allaman I, Bélanger M, Magistretti PJ (2011) Astrocyte-neuron metabolic relationships: For better and for worse. Trends Neurosci 34:76–87

    Article  CAS  PubMed  Google Scholar 

  18. Donato R, R. Cannon B, Sorci G, et al (2013) Functions of S100 proteins. Curr Mol Med 13:24–57 . doi: https://doi.org/10.2174/156652413804486214

  19. Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, Deloulme JC (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55:165–177. https://doi.org/10.1002/glia.20445

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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 U S A 97:13625–13630. https://doi.org/10.1073/pnas.240309797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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 U S A 100:5807–5812. https://doi.org/10.1073/pnas.0937635100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. De Berdt P, Bottemanne P, Bianco J, et al (123AD) Stem cells from human apical papilla decrease neuro-inflammation and stimulate oligodendrocyte progenitor differentiation via activin-A secretion. Cell Mol Life Sci 1: . doi: https://doi.org/10.1007/s00018-018-2764-5

  23. Nicola FC, Rodrigues LP, Crestani T, Quintiliano K, Sanches EF, Willborn S, Aristimunha D, Boisserand L et al (2016) Human dental pulp stem cells transplantation combined with treadmill training in rats after traumatic spinal cord injury. Brazilian J Med Biol Res = Rev Bras Pesqui medicas e Biol 49:e5319. https://doi.org/10.1590/1414-431X20165319

    Article  CAS  Google Scholar 

  24. 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 Invest 122:80–90. https://doi.org/10.1172/JCI59251

    Article  CAS  PubMed  Google Scholar 

  25. Taghipour Z, Karbalaie K, Kiani A, Niapour A, Bahramian H, Nasr-Esfahani MH, Baharvand H (2012) Transplantation of undifferentiated and induced human exfoliated deciduous teeth-derived stem cells promote functional recovery of rat spinal cord contusion injury model. Stem Cells Dev 21:1794–1802. https://doi.org/10.1089/scd.2011.0408

    Article  CAS  PubMed  Google Scholar 

  26. Matsubara K, Matsushita Y, Sakai K, Kano F, Kondo M, Noda M, Hashimoto N, Imagama S et al (2015) Secreted ectodomain of sialic acid-binding Ig-like lectin-9 and monocyte chemoattractant protein-1 promote recovery after rat spinal cord injury by altering macrophage polarity. J Neurosci 35:2452–2464. https://doi.org/10.1523/JNEUROSCI.4088-14.2015

    Article  PubMed  PubMed Central  Google Scholar 

  27. Bernardi L, Luisi SB, Fernandes R, Dalberto TP, Valentim L, Bogo Chies JA, Medeiros Fossati AC, Pranke P (2011) The isolation of stem cells from human deciduous teeth pulp is related to the physiological process of resorption. J Endod 37:973–979. https://doi.org/10.1016/j.joen.2011.04.010

    Article  PubMed  Google Scholar 

  28. Luisi S, Barbachan J, Chies J, Filho M (2007) Behavior of human dental pulp cells exposed to transforming growth factor-beta1 and acidic fibroblast growth factor in culture. J Endod 33:833–835. https://doi.org/10.1016/j.joen.2007.04.002

    Article  PubMed  Google Scholar 

  29. Maurmann N, Pereira DP, Burguez D, de S Pereira FDA, Inforçatti Neto P, Rezende RA, Gamba D, da Silva JVL et al (2017) Mesenchymal stem cells cultivated on scaffolds formed by 3D printed PCL matrices, coated with PLGA electrospun nanofibers for use in tissue engineering. Biomed Phys Eng Express 3. https://doi.org/10.1088/2057-1976/aa6308

  30. Weeks J, Hart RP (2004) SCI-base: An open-source spinal cord injury animal experimentation database. Lab Anim (NY) 33:35–41

    Article  Google Scholar 

  31. Park DY, Mayle RE, Smith RL, Corcoran-Schwartz I, Kharazi AI, Cheng I (2013) Combined transplantation of human neuronal and mesenchymal stem cells following spinal cord injury. Glob Spine J 3:1–6. https://doi.org/10.1055/s-0033-1337118

    Article  CAS  Google Scholar 

  32. Xavier Acasigua G, Bernardi L, Braghirolli D, Filho M, Pranke P, Medeiros Fossati A (2014) Nanofiber scaffolds support bone regeneration associated with pulp stem cells. Curr Stem Cell Res Ther 9:330–337. https://doi.org/10.2174/1574888X09666140228123911

    Article  PubMed  Google Scholar 

  33. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1–21

    Article  CAS  PubMed  Google Scholar 

  34. Tramontina F, Leite MC, Cereser K, de Souza DF, Tramontina AC, Nardin P, Andreazza AC, Gottfried C et al (2007) Immunoassay for glial fibrillary acidic protein: Antigen recognition is affected by its phosphorylation state. J Neurosci Methods 162:282–286. https://doi.org/10.1016/j.jneumeth.2007.01.001

    Article  CAS  PubMed  Google Scholar 

  35. Leite MC, Galland F, Brolese G, Guerra MC, Bortolotto JW, Freitas R, Almeida LMV, Gottfried C et al (2008) A simple, sensitive and widely applicable ELISA for S100B: methodological features of the measurement of this glial protein. J Neurosci Methods 169:93–99. https://doi.org/10.1016/j.jneumeth.2007.11.021

    Article  CAS  PubMed  Google Scholar 

  36. Heimfarth L, Loureiro SO, Dutra MF, Petenuzzo L, de Lima BO, Fernandes CG, da Rocha JBT, Pessoa-Pureur R (2013) Disrupted cytoskeletal homeostasis, astrogliosis and apoptotic cell death in the cerebellum of preweaning rats injected with diphenyl ditelluride. Neurotoxicology 34:175–188. https://doi.org/10.1016/j.neuro.2012.10.015

    Article  CAS  PubMed  Google Scholar 

  37. Weis SN, Pettenuzzo LF, Krolow R, Valentim LM, Mota CS, Dalmaz C, Wyse ATS, Netto CA (2012) Neonatal hypoxia-ischemia induces sex-related changes in rat brain mitochondria. Mitochondrion 12:271–279. https://doi.org/10.1016/j.mito.2011.10.002

    Article  CAS  PubMed  Google Scholar 

  38. Encinas JM, Vaahtokari A, Enikolopov G (2006) Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A 103:8233–8238. https://doi.org/10.1073/pnas.0601992103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Donato R, Sorci G, Riuzzi F, Arcuri C, Bianchi R, Brozzi F, Tubaro C, Giambanco I (2009) S100B’s double life: Intracellular regulator and extracellular signal. Biochim Biophys Acta - Mol Cell Res 1793:1008–1022. https://doi.org/10.1016/j.bbamcr.2008.11.009

    Article  CAS  Google Scholar 

  40. Ellis KM, Carroll DCO, Lewis MD et al (2014) Neurogenic potential of dental pulp stem cells isolated from murine incisors. Stem Cell Res Ther 5:1–13. https://doi.org/10.1186/scrt419

    Article  CAS  Google Scholar 

  41. Yamamoto S, Yamamoto N, Kitamura T, Nakamura K, Nakafuku M (2001) Proliferation of parenchymal neural progenitors in response to injury in the adult rat. Spinal Cord 127:115–127. https://doi.org/10.1006/exnr.2001.7798

    Article  Google Scholar 

  42. Blades DA, Baldwin SA, Broderick R, Scheff SW (1998) Alterations in temporal/spatial distribution of GFAP- and vimentin-positive astrocytes after spinal cord injury contusion with the New York University spinal cord injury device. J Neurotrauma 15:1015–1026

    Article  PubMed  Google Scholar 

  43. Obermair F, Schröter A, Thallmair M (2008) Endogenous neural progenitor cells as therapeutic target after spinal cord injury. Physiology (Bethesda) 23:296–304. https://doi.org/10.1152/physiol.00017.2008

    Article  Google Scholar 

  44. Frisén J, Johansson CB, Török C, Risling M, Lendahl U (1995) Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131:453–464. https://doi.org/10.1083/jcb.131.2.453

    Article  PubMed  Google Scholar 

  45. McKeon RJ, Schreiber RC, Rudge JS, Silver J (1991) Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398–3411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ahuja CS, Wilson JR, Nori S, Kotter MRN, Druschel C, Curt A, Fehlings MG (2017) Traumatic spinal cord injury. Nat Rev Dis Prim 3:17018. https://doi.org/10.1038/nrdp.2017.18

    Article  PubMed  Google Scholar 

  47. Wu D, Klaw MC, Connors T, Kholodilov N, Burke RE, Côté MP, Tom VJ (2017) Combining constitutively active Rheb expression and chondroitinase promotes functional axonal regeneration after cervical spinal cord injury. Mol Ther 25:2715–2726. https://doi.org/10.1016/j.ymthe.2017.08.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Xu C, Klaw MC, Lemay M a et al (2015) Pharmacologically inhibiting kinesin-5 activity with monastrol promotes axonal regeneration following spinal cord injury. Exp Neurol 263:172–176. https://doi.org/10.1016/j.expneurol.2014.10.013

    Article  CAS  PubMed  Google Scholar 

  49. Faulkner JR (2004) Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24:2143–2155. https://doi.org/10.1523/JNEUROSCI.3547-03.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lee SJ, Kim CW, Lee KJ, Choe JW, Kim SE, Oh JH, Park YS (2010) Elevated serum S100B levels in acute spinal fracture without head injury. Emerg Med J 27:209–212. https://doi.org/10.1136/emj.2008.063743

    Article  PubMed  Google Scholar 

  51. Vos PE, Jacobs B, Andriessen TMJC, Lamers KJB, Borm GF, Beems T, Edwards M, Rosmalen CF et al (2010) GFAP and S100B are biomarkers of traumatic brain injury: an observational cohort study. Neurology 75:1786–1793. https://doi.org/10.1212/WNL.0b013e3181fd62d2

    Article  CAS  PubMed  Google Scholar 

  52. Do Carmo Cunha J, De Freitas Azevedo Levy B, De Luca BA et al (2007) Responses of reactive astrocytes containing S100?? protein and fibroblast growth factor-2 in the border and in the adjacent preserved tissue after a contusion injury of the spinal cord in rats: Implications for wound repair and neuroregeneration. Wound Repair Regen 15:134–146. https://doi.org/10.1111/j.1524-475X.2006.00194.x

    Article  PubMed  Google Scholar 

  53. Chen J-Q, Zhang C-C, Jiang S-N, Lu H, Wang W (2016) Effects of aquaporin 4 knockdown on brain edema of the uninjured side after traumatic brain injury in rats. Med Sci Monit 22:4809–4819. https://doi.org/10.12659/MSM.898190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 90:291–366. https://doi.org/10.1152/physrev.00021.2009

    Article  CAS  PubMed  Google Scholar 

  55. Becker D, Sadowsky CL, McDonald JW (2003) Restoring function after spinal cord injury. Neurologist 9:1–15

    Article  PubMed  Google Scholar 

  56. Nesic O, Lee J, Ye Z, Unabia GC, Rafati D, Hulsebosch CE, Perez-Polo JR (2006) Acute and chronic changes in aquaporin 4 expression after spinal cord injury. Neuroscience 143:779–792. https://doi.org/10.1016/j.neuroscience.2006.08.079

    Article  CAS  PubMed  Google Scholar 

  57. Nagelhus E a, Mathiisen TM, Ottersen OP (2004) Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 129:905–913. https://doi.org/10.1016/j.neuroscience.2004.08.053

    Article  CAS  PubMed  Google Scholar 

  58. Olsen ML, Campbell SC, McFerrin MB et al (2010) Spinal cord injury causes a wide-spread, persistent loss of Kir4.1 and glutamate transporter 1: Benefit of 17??-oestradiol treatment. Brain 133:1013–1025. https://doi.org/10.1093/brain/awq049

    Article  PubMed  PubMed Central  Google Scholar 

  59. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1–21. https://doi.org/10.1089/neu.1995.12.1

    Article  CAS  PubMed  Google Scholar 

  60. Rodrigues LP, Iglesias D, Nicola FC, Steffens D, Valentim L, Witczak A, Zanatta G, Achaval M et al (2012) Transplantation of mononuclear cells from human umbilical cord blood promotes functional recovery after traumatic spinal cord injury in Wistar rats. Brazilian J Med Biol Res 45:49–57. https://doi.org/10.1590/S0100-879X2011007500162

    Article  CAS  Google Scholar 

  61. de Almeida FM, Marques SA, Ramalho BDS, et al (2011) Human dental pulp cells: a new source of cell therapy in a mouse model of compressive spinal cord injury. J Neurotrauma 28:1939–1949 . doi: https://doi.org/10.1089/neu.2010.1317

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Acknowledgements

This work was supported by funds from the Conselho Nacional de Desenvolvimento Cientifico e Tecnológico do Brasil (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Stem Cell Research Institute.

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Authors and Affiliations

  1. Post Graduate Program in Neuroscience, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

    Fabrício Nicola, Marília Rossato Marques & Felipe Odorcyk

  2. Department of Biochemistry, Institute of Basic Health Sciences, Universidade Federal do Rio Grande do Sul, R. Ramiro Barcelos, 2600 anexo, Porto Alegre, Rio Grande do Sul, 90035-003, Brazil

    Fabrício Nicola, Marília Rossato Marques, Felipe Odorcyk, Letícia Petenuzzo, Dirceu Aristimunha, Adriana Vizuete, Eduardo Farias Sanches, Carlos-Alberto Gonçalves & Carlos Alexandre Netto

  3. Hematology and Stem Cell Laboratory, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

    Daniela Pavulack Pereira, Natasha Maurmann & Patricia Pranke

  4. Post Graduate Program in Physiology, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

    Natasha Maurmann & Patricia Pranke

  5. Stem Cell Research Institute, Porto Alegre, Brazil

    Patricia Pranke

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Correspondence to Fabrício Nicola.

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All procedures were in accordance with the Guide for the Care and Use of Laboratory Animals adopted by the National Institute of Health (USA) and with the Federation of Brazilian Societies for Experimental Biology and with the Brazilian Law for Laboratory Animals care no 11.794. The experimental study was approved by the Research Ethics Committee of the University (#26116). The procedures for obtaining and isolate the SHED were approved by the Ethics Committee of the Universidade Federal do Rio Grande do Sul (#296/08).

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Nicola, F., Marques, M.R., Odorcyk, F. et al. Stem Cells from Human Exfoliated Deciduous Teeth Modulate Early Astrocyte Response after Spinal Cord Contusion. Mol Neurobiol 56, 748–760 (2019). https://doi.org/10.1007/s12035-018-1127-4

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