Spinal cord neural stem cells heterogeneity in postnatal development

  • Jelena Ban Laboratory for Molecular Neurobiology, Department of Biotechnology, University of Rijeka, Croatia
  • Miranda Mladinic Laboratory for Molecular Neurobiology, Department of Biotechnology, University of Rijeka, Croatia https://orcid.org/0000-0002-3985-6629
Keywords: Neural stem cells, Radial glia, Ependymal cells, Development, Spinal cord injury

Abstract

Neural stem cells are capable of generating new neurons during development as well as in the adulthood and represent one of the most promising tools to replace lost or damaged neurons after injury or neurodegenerative disease. Unlike the brain, neurogenesis in the adult spinal cord is poorly explored and the comprehensive characterization of the cells that constitute stem cell neurogenic niche is still missing. Moreover, the terminology used to specify developmental and/or anatomical CNS regions, where neurogenesis in the spinal cord occurs, is not consensual and the analogy with the brain is often unclear. In this review, we will try to describe the heterogeneity of the stem cell types in the spinal cord ependymal zone, based on their origin and stem cell potential. We will also consider specific animal in vitro models that could be useful to identify “the right” stem cell candidate for cell replacement therapies.   

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References

Badhiwala JH, Ahuja CS, Fehlings MG. Time is spine: a review of translational advances in spinal cord injury. J Neurosurg Spine. 2018 20;30(1):1–18.

Courtine G, Sofroniew MV. Spinal cord repair: advances in biology and technology. Nat Med. 2019;25(6):898–908.

Trawczynski M, Liu G, David BT, Fessler RG. Restoring motor neurons in spinal cord injury with induced pluripotent stem cells. Front Cell Neurosci. 2019;13:369.

Ban J, Mladinić Pejatović M. Nanotechnology approaches for autologous stem cell manipulation in personalized regenerative medicine. In: Bodiroga-Vukobrat N, Rukavina D, Pavelić K, Sander GG, editors. Personalized Medicine in Healthcare Systems. Europeanization and Globalization, vol 5. Springer, Cham.

Casarosa S, Bozzi Y, Conti L. Neural stem cells: ready for therapeutic applications? Mol Cell Ther. 2014 Oct 15;2.

Stadtfeld M, Hochedlinger K. Induced pluripotency: history, mechanisms, and applications. Genes Dev. 2010 Oct 15;24(20):2239–63.

Hanna JH, Saha K, Jaenisch R. Somatic cell reprogramming and transitions between pluripotent states: facts, hypotheses, unresolved issues. Cell. 2010 Nov 12;143(4):508–25.

Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006 Aug 25;126(4):663–76.

Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007 Nov 30;131(5):861–72.

Nagoshi N, Tsuji O, Nakamura M, Okano H. Cell therapy for spinal cord injury using induced pluripotent stem cells. Regen Ther. 2019 Dec;11:75–80.

Tsuji O, Sugai K, Yamaguchi R, Tashiro S, Nagoshi N, Kohyama J, et al. Concise Review: laying the groundwork for a first-in-human study of an induced pluripotent stem cell-based intervention for spinal cord injury. Stem Cells. 2019;37(1):6–13.

Yoshihara M, Hayashizaki Y, Murakawa Y. Genomic instability of iPSCs: challenges towards their clinical applications. Stem Cell Rev Rep. 2017 Feb;13(1):7–16.

Hou P, Li Y, Zhang X, Liu C, Guan J, Li H, et al. Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science. 2013 Aug 9;341(6146):651–4.

Zheng J, Choi K-A, Kang PJ, Hyeon S, Kwon S, Moon J-H, et al. A combination of small molecules directly reprograms mouse fibroblasts into neural stem cells. Biochem Biophys Res Commun. 2016 15;476(1):42–8.

Biswas D, Jiang P. Chemically Induced Reprogramming of somatic cells to pluripotent stem cells and neural cells. Int J Mol Sci. 2016 Feb 6;17(2):226.

Qin H, Zhao A, Fu X. Small molecules for reprogramming and transdifferentiation. Cell Mol Life Sci. 2017 Oct 1;74(19):3553–75.

Gaudet AD, Fonken LK. Glial cells shape pathology and repair after spinal cord injury. Neurotherapeutics. 2018;15(3):554–77.

Orr MB, Gensel JC. Spinal cord injury scarring and inflammation: therapies targeting glial and inflammatory responses. Neurotherapeutics. 2018;15(3):541–53.

Liddelow SA, Barres BA. Reactive astrocytes: production, function, and therapeutic potential. Immunity. 2017 Jun 20; 46(6):957–67.

Ban J, Sámano C, Mladinic M, Munitic I. Glia in amyotrophic lateral sclerosis and spinal cord injury: common therapeutic targets. Croat Med J. 2019 Apr;60(2):109–20.

Hugnot JP, Franzen R. The spinal cord ependymal region: a stem cell niche in the caudal central nervous system. Front Biosci (Landmark Ed). 2011 Jan 1;16:1044–59.

Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci. 2009;32(1):149–84.

Schwartz JH, Siegelbaum SA, Hudspeth AJ. Principles of neural science, Fifth Edition. McGraw Hill Professional; 2013. 1761 p.

Morest DK, Silver J. Precursors of neurons, neuroglia, and ependymal cells in the CNS: What are they? Where are they from? How do they get where they are going? Glia. 2003;43(1):6–18.

Malatesta P, Appolloni I, Calzolari F. Radial glia and neural stem cells. Cell Tissue Res. 2008 Jan;331(1):165–78.

McDonough A, Martínez-Cerdeño V. Endogenous proliferation after spinal cord injury in animal models. Stem Cells Int. 2012;2012:387513.

Mladinic M, Bianchetti E, Dekanic A, Mazzone GL, Nistri A. ATF3 is a novel nuclear marker for migrating ependymal stem cells in the rat spinal cord. Stem Cell Res. 2014 May;12(3):815–27.

Sabourin J-C, Ackema KB, Ohayon D, Guichet P-O, Perrin FE,Garces A, et al. A mesenchymal-like ZEB1(+) nicheharbors dorsal radial glial fibrillary acidic protein-positive stem cells in the spinal cord. Stem Cells. 2009 Nov;27(11):2722–33.

Xia B, Yanai I. A periodic table of cell types. Development. 2019 Jun 27;146(12).

Paridaen JTML, Huttner WB. Neurogenesis during development of the vertebrate central nervous system. EMBO Rep. 2014 Apr;15(4):351–64.

Englund C, Fink A, Lau C, Pham D, Daza RAM, Bulfone A, et al. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci. 2005 Jan 5;25(1):247–51.

Rushing G, Ihrie RA. Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone. Front Biol. 2016 Aug 1;11(4):261–84.

Martínez-Cerdeño V, Noctor SC. Neural progenitor cell terminology. Front Neuroanat. 2018 Dec 6;12.

Malatesta P, Götz M. Radial glia - from boring cables to stem cell stars. Development. 2013 Feb 1;140(3):483–6.

Merkle FT, Tramontin AD, García-Verdugo JM, Alvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA. 2004 Dec 14;101(50):17528–32.

Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. Neurons derived from radial glial cells establish radial units in neocortex. Nature. 2001 Feb 8;409(6821):714–20.

Verkhratsky A, Parpura V. Introduction to neuroglia. Colloquium Series on Neuroglia in Biology and Medicine: From Physiology to Disease. 2014 Feb 24;1(1):1–74.

Gubert F, Zaverucha-do-Valle C, Pimentel-Coelho PM, Mendez-Otero R, Santiago MF. Radial glia-like cells persist in the adult rat brain. Brain Res. 2009 Mar 3;1258:43–52.

Levitt P, Rakic P. Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol. 1980 Oct 1;193(3):815–40.

Marichal N, Reali C, Trujillo-Cenóz O, Russo RE. Spinal cord stem cells in their microenvironment: the ependyma as a stem cell niche. Adv Exp Med Biol. 2017;1041:55–79.

Verkhratsky A, Butt A. Introduction to glia. In: Glial Neurobiology. John Wiley & Sons, Ltd; 2007. p. 1–12.

Spassky N, Merkle FT, Flames N, Tramontin AD, García-Verdugo JM, Alvarez-Buylla A. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci. 2005 Jan 5;25(1):10–8.

Sevc J, Daxnerová Z, Haňová V, Koval’ J. Novel observations on the origin of ependymal cells in the ventricular zone of the rat spinal cord. Acta Histochem. 2011 Feb;113(2):156–62.

Meletis K, Barnabé-Heider F, Carlén M, Evergren E, Tomilin N, Shupliakov O, et al. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol. 2008 Jul 22;6(7):e182.

Goodman T, Hajihosseini MK. Hypothalamic tanycytes-masters and servants of metabolic, neuroendocrine, and neurogenic functions. Front Neurosci. 2015;9:387.

Laywell ED, Rakic P, Kukekov VG, Holland EC, Steindler DA. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA. 2000 Dec 5;97(25):13883–8.

Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisén J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell. 1999 Jan 8; 96(1):25–34.

Fiorelli R, Cebrian-Silla A, Garcia-Verdugo J-M, Raineteau O. The adult spinal cord harbors a population of GFAP-positive progenitors with limited self-renewal potential. Glia. 2013;61(12):2100–13.

Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992 Mar 27;255(5052):1707–10.

Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell. 2011 May 6;8(5):486–98.

Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, et al. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci. 1996 Dec 1;16(23):7599–609.

Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999 Jun 11; 97(6):703–16.

Shihabuddin LS, Horner PJ, Ray J, Gage FH. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci. 2000 Dec 1;20(23):8727–35.

Mladinic M, Muller KJ, Nicholls JG. Central nervous system regeneration: from leech to opossum. J Physiol (Lond). 2009 Jun 15;587(Pt 12):2775–82.

Nicholls J, Saunders N. Regeneration of immature mammalian spinal cord after injury. Trends Neurosci. 1996 Jun;19(6):229–34.

Published
2020-01-02
How to Cite
BanJ., & MladinicM. (2020). Spinal cord neural stem cells heterogeneity in postnatal development. STEMedicine, 1(1), e19. https://doi.org/10.37175/stemedicine.v1i1.19
Section
Review articles