Abstract
The ependyma of the spinal cord is currently proposed as a latent neural stem cell niche. This chapter discusses recent knowledge on the developmental origin and nature of the heterogeneous population of cells that compose this stem cell microenviroment, their diverse physiological properties and regulation. The chapter also reviews relevant data on the ependymal cells as a source of plasticity for spinal cord repair.
References
Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA (2006) International Union of Pharmacology. Update and subclassification of the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58:281–341
Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19–29
Alvarez-Buylla A, Garcı́a-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22:629–634
Alvarez-Buylla A, García-Verdugo JM, Tramontin AD (2001) A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2:287–293
Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N (2007) Brain lipid binding protein is a target of Notch signaling in radial glial cells. Genes Dev 19:1028–1033
Armstrong J, Zhang L, McClelland AD (2003) Axonal regeneration of descending and ascending spinal projection neurons in spinal cord-transected larval lamprey. Exp Neurol 180:156–166
Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, Faden AI, Hsu CY, Noble LJ, Salzman S, Young W (1997) Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148:453–463
Bel-Vialar S, Medevielle F, Pituello F (2007) The on/off of Pax6 controls the tempo of neuronal differentiation in the developing spinal cord. Dev Biol 305:659–673
Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728–739
Ben-Ari Y, Spitzer NC (2010) Phenotypic checkpoints regulate neuronal development. Trends Neurosci 33:485–492
Bittman K, Owens DF, Kriegstein AR, LoTurco JJ (1997) Cell coupling and uncoupling in the ventricular zone of developing neocortex. J Neurosci 17:7037–7044
Bordey A (2007) Enigmatic GABAergic networks in adult neurogenic zones. Brain Res Brain Res Rev 53:124–134
Briscoe J, Pierani A, Jessell TM, Ericson J (2000) A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101:435–445
Butler EG, Ward MB (1965) Reconstitution of the spinal cord following ablation in urodele larvae. J Exp Zool 160:47–65
Cebrián-Silla A, Alfaro-Cervelló C, Herranz-Pérez V, Kaneko N, Hwi Park D, Sawamoto K, Alvarez-Buylla A, Lim DA, García-Verdugo JM (2017) Unique organization of the nuclear envelope in the post-natal quiescent neural stem cells. Stem Cell Rep 9:203–216
Chevallier S, Landry M, Nagy F, Cabelguen JM (2004) Recovery of bimodal locomotion in the spinal-transected salamander, Pleurodeles waltlii. Eur J Neurosci 20:1995–2007
Chittajallu R, Chen Y, Wang H, Yuan X, Ghiani CA, Heckman T, McBain CJ, Gallo V (2002) Regulation of Kv1 subunit expression in oligodendrocyte progenitor cells and their role in G1/S phase progression of the cell cycle. Proc Natl Acad Sci U S A 99:2350–2355
Chittajallu R, Aguirre A, Gallo V (2004) NG2-positive cells in the mouse white and grey matter display distinct physiological properties. J Physiol 561:109–122
Coggeshall RE, Youngblood CS (1983) Recovery from spinal transection in fish: regrowth of axons past the transection. Neurosci Lett 38:227–231
Corns LF, Deuchars J, Deuchars SA (2013) GABAergic responses of mammalian ependymal cells in the central canal neurogenic niche of the postnatal spinal cord. Neurosci Lett 553:57–62
Corns LF, Atkinson L, Daniel J, Edwards IJ, New L, Deuchars J, Deuchars SA (2015) Cholinergic enhancement of cell proliferation in the postnatal neurogenic niche of the mammalian spinal cord. Stem Cells 33:2864–2876
Davies HG, Small JV (1968) Structural units in chromatin and their orientation on membranes. Nature 217:1122–1125
Davis BM, Ayers JL, Koran L, Carlson J, Anderson MC, Simpson SB Jr (1990) Time course of salamander spinal cord regeneration and recovery of swimming: HRP retrograde pathway tracing and kinematic analysis. Exp Neurol 108:198–213
Dervan AG, Roberts BL (2003) Reaction of spinal cord central canal cells to cord transaction and their contribution to cord regeneration. J Comp Neurol 458:293–306
Dessaud E, McMahon AP, Briscoe J (2008) Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135:2489–2503
Diaz Queiroz JP, Echeverri K (2013) Spinal cord regeneration: where fish, frogs and salamanders lead the way, can we follow? Biochem J 451:353–364
Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subgerminal zone in the adult mammalian brain. J Neurosci 17:5046–5061
Egar M, Simpson SB, Singer M (1970) The growth and differentiation of the regenerating spinal cord of the lizard Anolis carolinensis. J Morphol 131:131–152
Eisch AJ, Mandyam CD (2007) Adult neurogenesis: can analysis of cell cycle proteins move us "Beyond BrdU"? Curr Pharm Biotechnol 8:147–165
Fernández A, Radmilovich M, Trujillo-Cenóz O (2002) Neurogenesis and gliogenesis in the spinal cord of turtles. J Comp Neurol 453:131–144
Filippov V, Kronenberg G, Pivneva T et al (2003) Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 23:373–382
Fiorelli R, Cebrian-Silla A, Garcia-Verdugo JM, Raineteau O (2013) The adult spinal cord harbors a population of GFAP-positive progenitors with limited self-renewal potential. Glia 61:2100–2113
Frischknecht F, Randall AD (1998) Voltage- and ligand-gated ion channels in floor plate neuroepithelia of the rat. Neuroscience 85:1135–1149
Fu H, Qi Y, Tan MIN, Cai J, Hu X, Liu Z, Qiu M (2003) Molecular mapping of the origin of postnatal spinal cord ependymal cells: evidence that adult ependymal cells are derived from Nkx6.1 + ventral neural progenitor cells. J Comp Neurol 456:237–244
Gandelman M, Levy M, Cassina P, Barbeito L, Beckman JS (2013) P2X7 receptor-induced death of motor neurons by a peroxynitrite/FAS-dependent pathway. J Neurochem 126:382–388
Ganguly K, Schinder AF, Wong ST, Poo M (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105:521–532
Gao Z, Nissen JC, Legakis L, Tsirka SE (2015) Nicotine modulates neurogenesis in the central canal during experimental autoimmune encephalomyelitis. Neuroscience 297:11–21
Ghiani CA, Yuan X, Eisen AM, Knutson PL, DePinho RA, McBain CJ, Gallo V (1999) Voltage-activated K+ channels and membrane depolarization regulate accumulation of the cyclin-dependent kinase inhibitors p27(Kip1) and p21(CIP1) in glial progenitor cells. J Neurosci 19:5380–5392
Gibbs KM, Szaro BG (2006) Regeneration of descending projections in Xenopus laevis tadpole spinal cord demonstrated by retrograde double labeling. Brain Res 1088:68–72
Glaser T, Resende RR, Ulrich H (2013) Implications of purinergic receptor-mediated intracellular calcium transients in neural differentiation. Cell Commun Signal 11:12. https://doi.org/10.1186/1478-811X-11-12
Goodman T, Hajihosseini MK (2015) Hypothalamic tanycytes—masters and servants of metabolic, neuroendocrine, and neurogenic functions. Front Neurosci 9:387. https://doi.org/10.3389/fnins.2015.00387
Götz M, Stoykova A, Gruss P (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21:1031–1044
Guillemot F (2007) Spatial and temporal specification of neural fates by transcription factor codes. Development 134:3771–3780
Hamilton LK, Truong MK, Bednarczyk MR, Aumont A, Fernandes KJ (2009) Cellular organization of the central canal ependymal zone, a niche of latent neural stem cells in the adult mammalian spinal cord. Neuroscience 164:1044–1056
Hartfuss E, Galli R, Heins N, Götz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15–30
Hasegawa K, Chang Y-W, Li H, Berlin Y, Ikeda O, Kane-Goldsmith N, Grumet M (2004) Embryonic radial glia bridge spinal cord lesions and promote functional recovery following spinal cord injury. Exp Neurol 193:394–410
Hattiangady B, Shetty AK (2008) Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol Aging 29:129–147
Haydar TF, Wang F, Schwartz ML, Rakic P (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 20:5764–5774
Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, Barde A, Götz M (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 5:308–315
Hooker D (1932) Spinal cord regeneration in the young rainbow fish, Lebistes reticulatus. J Comp Neurol 56:277–297
Horner PJ, Palmer TD (2003) New roles for astrocytes: the nightlife of an ‘astrocyte’. La vida loca! Trends Neurosci 26:597–603
Horner PH, Power AE, Kempermann G, Kuhn GH, Palmer TD, Winkler J, Thal LJ, Gage FH (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20:2218–2228
Horstmann E (1954) Die Faserglia des Selachiergehirns. Zellforsch 39:588–617
Hugnot JP, Franzen R (2011) The spinal cord ependymal region: a stem cell niche in the caudal central nervous system. Front Biosci 16:1044–1059
Jacquet BV, Salinas-Mondragon R, Liang H, Therit B, Buie JD, Dykstra M, Campbell K, Ostrowski LE, Brody SL, Ghashghaei HT (2009) FoxJ1-dependent gene expression is required for differentiation of radial glia into ependymal cells and a subset of astrocytes in the postnatal brain. Development 136:4021–4031
Jang MH, Song H, Ming GL (2008) Regulation of adult neurogenesis by neurotransmitters. In: Gage FH, Kempermann G, Song H (eds) Adult neurogenesis. Cold Spring Harbor Laboratory Press, New York, pp 397–421
Jessell TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1:20–29
Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisén J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25–34
Kempermann G (2008) Activity dependency and aging in the regulation of adult neurogenesis. In: Gage FH, Kempermann G, Song H (eds) Adult neurogenesis. Cold Spring Harbor Laboratory Press, New York, pp 341–362
Kempermann G, Song H, Gage F (2008) Neurogenesis in the adult hippocampus. In: Gage FH, Kempermann G, Song H (eds) Adult neurogenesis. Cold Spring Harbor Laboratory Press, New York, pp 159–174
Khakh BS, North RA (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442:527–532
Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A (2005) Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25:6997–7003
Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184
Kutna V, Sevc J, Gombalov Z, Matiasova A, Daxnerova Z (2014) Enigmatic cerebrospinal fluid-contacting neurons arise even after the termination of neurogenesis in the rat spinal cord during embryonic development and retain their immature-like characteristics until adulthood. Acta Histochem 116:278–285
Lee SK, Pfaff SL (2001) Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat Neurosci 4:1183–1191
Lee-Liu D, Edwards-Faret G, Tapia VS, Larraín J (2013) Spinal cord regeneration: Lessons for mammals from non-mammalian vertebrates. Genesis 51:529–544
Levine JM, Reynolds R, Fawcett JW (2001) The oligodendrocyte precursor cell in health and disease. Trends Neurosci 24:39–47
Li X, Floriddia EM, Toskas K, Fernandes KJL, Guérout N, Barnabé-Heider F (2016) Regenerative potential of ependymal cells for spinal cord injuries over time. EBioMedicine 13:55–65
Lim DA, Huang Y-C, Alvarez-Buylla A (2008) Adult subventricular zone and olfactory bulb neurogenesis. In: Gage FH, Kempermann G, Song H (eds) Adult neurogenesis. Cold Spring Harbor, New York
Lin JH, Takano T, Arcuino G, Wang X, Hu F, Darzynkiewicz Z, Nunes M, Goldman SA, Nedergaard M (2007) Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev Biol 302:356–366
Liu X, Wang Q, Haydar TF, Bordey A (2005) Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci 8:1179–1187
Liu X, Bolteus AJ, Balkin DM, Henschel O, Bordey A (2006) GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia 54:394–410
Liu X, Hashimoto-Torii K, Torii M, Haydar TF, Rakic P (2008) The role of ATP signalling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone. Proc Natl Acad Sci U S A 105:11802–11807
Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179–193
Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981
LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287–1298
Lucassen PJ, Oomen CA, van Dam AM, Czéh B (2008) Regulation of hippocampal neurogenesis by systemic factors including stress, glucocorticoids, sleep and inflammation. In: Gage FH, Kempermann G, Song H (eds) Adult neurogenesis. Cold Spring Harbor Laboratory Press, New York, pp 363–396
Ma DK, Ming G-l, Gage FH, Song H (2008) Neurogenic niches in the adult mammalian brain. In: Gage FH, Kempermann G, Song H (eds) Adult neurogenesis. Cold Spring Harbor, New York, pp 207–226
MacFarlane SN, Sontheimer H (2000a) Modulation of Kv1.5 currents by Src tyrosine phosphorylation: potential role in the differentiation of astrocytes. J Neurosci 20:5245–5253
MacFarlane SN, Sontheimer H (2000b) Changes in ion channel expression accompany cell cycle progression of spinal cord astrocytes. Glia 30:39–48
Maekawa M, Takashima N, Arai Y, Nomura T, Inokuchi K, Yuasa S, Osumi N (2005) Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis. Genes Cells 10:1001–1014
Marichal N, García G, Radmilovich M, Trujillo-Cenóz O, Russo RE (2009) Enigmatic central canal contacting cells: immature neurons in “standby mode”? J Neurosci 29:10010–10024
Marichal N, García G, Radmilovich M, Trujillo-Cenóz O, Russo RE (2012) Spatial domains of progenitor-like cells and functional complexity of a stem cell niche in the neonatal rat spinal cord. Stem Cells 30:2020–2031
Marichal N, Fabbiani G, Trujillo-Cenóz O, Russo RE (2016) Purinergic signalling in a latent stem cell niche of the rat spinal cord. Purinergic Signal 12:331–341
Marzesco AM, Janich P, Wilsch-Bräuninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner WB (2005) Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 118:2849–2858
Masahira N, Takebayashi H, Ono K, Watanabe K, Ding L, Furusho M, Ogawa Y, Nabeshima Y, Alvarez-Buylla A, Shimizu K, Ikenaka K (2006) Olig2-positive progenitors in the embryonic spinal cord give rise not only to motoneurons and oligodendrocytes, but also to a subset of astrocytes and ependymal cells. Dev Biol 293:358–369
Massé K, Bhamra S, Eason R, Dale N, Jones EA (2007) Purine-mediated signalling triggers eye development. Nature 449:1058–1062
McHedlishvili L, Epperlein HH, Telzerow A, Tanaka EM (2007) A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors. Development 134:2083–2093
Meletis K, Barnabé-Heider F, Carlén M, Evergren E, Tomilin N, Shupliakov O, Frisén J (2008) Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6:1494–1507
Mestres P, Garfia A (1980) Effects of cytochalasin B on the ependyma. Scan Electron Microsc 3:465–474
Michel ME, Reier PJ (1979) Axonal-ependymal associations during early regeneration of the transected spinal cord in Xenopus laevis tadpoles. J Neurocytol 8:529–548
Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250
Miras-Portugal MT, Gomez-Villafuertes R, Gualix J, Diaz-Hernandez JI, Artalejo AR, Ortega F, Delicado EG, Perez-Sen R (2015) Nucleotides in neuroregeneration and neuroprotection. Neuropharmacology 104:243–254
Mokalled MH, Patra C, Dickson AL, Endo T, Stainier DYR, Poss KD (2016) Injury-induced ctgf directs glial bridging and spinal cord regeneration in Zebrafish. Science 354:630–634
Molina B, Rodríguez EM, Peruzzo B, Caprile T, Nualart F (2001) Spatial distribution of Reissner’s fiber glycoproteins in the filum terminale of the rat and rabbit. Microsc Res Tech 52:552–563
Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE, Morrison SJ (2006) Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443:448–452
Mothe AJ, Tator CH (2005) Proliferation, migration, and diferentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord inury in the adult rat. Neuroscience 131:177–187
Nacher J, Varea E, Blasco-Ibanez JM, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ, McEwen BS (2005) Expression of the transcription factor Pax 6 in the adult rat dentate gyrus. J Neurosci Res 81:753–761
Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22:3161–3173
Nornes HO, Das GD (1972) Temporal pattern of neurogenesis in spinal cord: cytoarchitecture and directed growth of axons. Proc Natl Acad Sci U S A 69:1962–1966
Nornes HO, Das GD (1974) Temporal pattern of neurogenesis in spinal cord of rat. I. An autoradiographic study—time and sites of origin and migration and settling patterns of neuroblasts. Brain Res 73:121–138
Peng W, Cotrina ML, Han X, Yu H, Bekar L, Blum L, Takano T, Tian GF, Goldman SA, Nedergaard M (2009) Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc Natl Acad Sci U S A 106:12489–12493
Peters A, Palay SL, Webster H dF (1991) The ependyma. In: The fine structure of the nervous system. Neurons and their supporting cells. Oxford University Press, Oxford, pp 312–327
Petracca YL, Sartoretti MM, Di Bella DJ, Marin-Burgin A, Carcagno AL, Schinder AF, Lanuza GM (2016) The late and dual origin of cerebrospinal fluid-contacting neurons in the mouse spinal cord. Development 143:880–891
Piatt J, Piatt M (1958) Transection of the spinal cord in the adult frog. Anat Rec 131:81–95
Pinto L, Götz M (2007) Radial glial cell heterogeneity-the source of diverse progeny in the CNS. Prog Neurobiol 83:2–23
Ramón y Cajal S (1909) Histologie du Systeme Nerveux de l’homme et des vertébres, vol I. (Edited by Consejo superior de Investigaciones Científicas, 1952). Maloine, Paris
Ramón y Cajal SR (1913) Estudios sobre la degeneración y regeneración del sistema nervioso. T I-II. Degeneración y regeneración de los centros nerviosos. Nicolás Moya, Madrid
Reali C, Fernández A, Radmilovich M, Trujillo-Cenóz O, Russo RE (2011) GABAergic signalling in a neurogenic niche of the turtle spinal cord. J Physiol 589:5633–5647
Rehermann MI, Marichal N, Russo R, Trujillo-Cenoz O (2009) Neural Reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi. J Comp Neurol 515:197–214
Rehermann MI, Santiñaqui FF, López-Carro B, Russo R, Trujillo-Cenoz O (2011) Cell proliferation and cytoarchitectural remodelling in the fresh-water turtle Trachemys dorbignyi. Cell Tissue Res 344:415–433
Reimer MM, Sörensen I, Kuscha V, Frank RE, Liu C, Becker CG, Becker T (2008) Motor neuron regeneration in adult zebrafish. J Neurosci 28:8510–8516
Ren Y, Ao Y, O’Shea TM, Burda JE, Bernstein AM, Brumm AJ, Muthusamy N, Ghashghaei HT, Carmichael ST, Cheng L, Sofroniew MV (2017) Ependymal cell contribution to scar formation after spinal cord injury is minimal, local and dependent on direct ependymal injury. Sci Rep 7:41122. https://doi.org/10.1038/srep41122
Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251–255
Roberts BL, Maslam S, Scholten G, Smit W (1995) Dopaminergic and GABAergic cerebrospinal fluid-contacting neurons along the central canal of the spinal cord of the eel and trout. J Comp Neurol 354:423–437
Rovainen CM (1976) Regeneration of Müller and Mauthner axons after spinal cord transection in larval lampreys. J Comp Neurol 168:545–554
Rowitch DH (2004) Glial specification in the vertebrate neural tube. Nat Rev Neurosci 5:409–419
Russo RE, Hounsgaard J (1999) Dynamics of intrinsic electrophysiological properties in spinal cord neurones. Prog Biophys Mol Biol 72:329–365
Russo RE, Fernández A, Reali C, Radmilovich M, Trujillo-Cenóz O (2004) Functional and molecular clues reveal precursor-like cells and immature neurones in the turtle spinal cord. J Physiol 3:831–838
Russo RE, Reali C, Radmilovich M, Fernández A, Trujillo-Cenóz O (2008) Connexin 43 delimits functional domains of neurogenic precursors in the spinal cord. J Neurosci 28:3298–3309
Sabelström H, Stenudd M, Réu P, Dias DO, Elfineh M, Zdunek S, Damberg P, Göritz C, Frisén J (2013) Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science 342:637–640
Sabourin JC, Ackema KB, Ohayon D, Guichet PO, Perrin FE, Garces A, Ripoll C, Charite J, Simonneu L, Ketenmann H, Zine A, Pivat A, Valmier J, Pattyn A, Hugnot JP (2009) A mesenchymal-like ZEB1+ niche harbors dorsal radial glial fibrillary acidic protein-positive stem cells in the spinal cord. Stem Cells 27:2722–2733
Schaarschmidt G, Wegner F, Schwarz SC, Schmidt H, Schwarz J (2009) Characterization of voltage-gated potassium channels in human neural progenitor cells. PLoS One 4:e6168. https://doi.org/10.1371/journal.pone.0006168
Schnapp E, Kragl M, Rubin L, Tanaka EM (2005) Hedgehog signaling controls dorsoventral patterning, blastema cell proliferation and cartilage induction during axolotl tail regeneration. Development 132:3243–3253
Seri B, García-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160
Sevc J, Daxnerova Z, Hanova V, Koval J (2011) Novel observations on the origin of ependymal cells in the ventricular zone of the rat spinal cord. Acta Histochem 113:156–162
Shifman MI, Jin LQ, Selzer M (2007) Regeneration in the lamprey spinal cord. In: Becker CG, Becker T (eds) Model organisms in spinal cord regeneration. Wiley-VCH Verlag, Weinheim, pp 229–262
Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5:146–156
Sims RT (1962) Transection of the spinal cord in developing Xenopus laevis. Embryol Exp Morphol 10:115–126
Singer M, Nordlander RTH, Egar M (1979) Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt: the blue print hypothesis of neural pathway patterning. J Comp Neurol 185:1–22
Smith DO, Rosenheimer JL, Kalil RE (2008) Delayed rectifier and A-type potassium channels associated with Kv 2.1 and Kv 4.3 expression in embryonic rat neural progenitor cells. PLoS One 3:e1604
Sontheimer H, Trotter J, Schachner M, Kettenmann H (1989) Channel expression correlates with differentiation stage during the development of oligodendrocytes from their precursor cells in culture. Neuron 2:1135–1145
Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A (2005) Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 25:10–18
Spitzer NC, Root CM, Borodinsky LN (2004) Orchestrating neuronal differentiation: patterns of Ca2+ spikes specify transmitter choice. Trends Neurosci 27:415–421
Stewart RR, Zigova T, Luskin MB (1999) Potassium currents in precursor cells isolated from the anterior subventricular zone of the neonatal rat forebrain. J Neurophysiol 81:95–102
Stoeckel ME, Uhl-Bronner S, Hugel S, Veinante P, Klein MJ, Mutterer J, Freund-Mercier MJ, Schlichter R (2003) Cerebrospinal fluid-contacting neurons in the rat spinal cord, a gamma-aminobutyric acidergic system expressing the P2X2 subunit of purinergic receptors, PSA-NCAM, and GAP-43 immunoreactivities: light and electron microscopic study. J Comp Neurol 457:159–174
Sugimori M, Nagao M, Bertrand N, Parras CM, Guillemot F, Nakafuku M (2007) Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development 134:1617–1629
Surprenant A, North RA (2009) Signaling at purinergic P2X receptors. Annu Rev Physiol 71:333–359
Surprenant A, Rassendren F, Kawashima E, North RA, Buell G (1996) The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272:735–738
Takeda A, Goris RC, Funakoshi K (2007) Regeneration of descending projections to the spinal cord neurons after spinal hemisection in the goldfish. Brain Res 1155:17–23
Tanaka EM, Ferretti P (2009) Considering the evolution of regeneration in the central nervous system. Nat Rev Neurosci 10:713–723
Thuret S, Moon LD, Gage FH (2006) Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7:628–643
Trujillo-Cenóz O, Fernández A, Radmilovich M, Realli C, Russo R (2007) Cytological organization of the central gelatinosa in the turtle spinal cord. J Comp Neurol 502:291–308
Valentin-Kahan A, García-Tejedor GB, Robello C, Trujillo-Cenóz O, Russo RE, Alvarez-Valin F (2017) Gene expression profiling in the injured spinal cord of Trachemys scripta elegans: an amniote with self-repair capabilities. Front Mol Neurosci 10:17. https://doi.org/10.3389/fnmol.2017.00017
Vigh B, Vigh-Teichmann I (1998) Actual problems of the cerebrospinal fluid-contacting neurons. Microsc Res Tech 41:57–83
Vigh B, Vigh-Teichmann I, Aros B (1977) Special dendritic and axonal endings formed by the cerebrospinal fluid contacting neurons of the spinal cord. Cell Tissue Res 183:541–552
Vigh B, Vigh-Teichmann I, Manzano e Silva MJ, van den Pol AN (1983) Cerebrospinal fluid-contacting neurons of the central canal and terminal ventricle in various vertebrates. Cell Tissue Res 231:615–621
Vigh-Teichmann I, Vigh B (1983) The system of cerebrospinal. Arch Histol Jap 46:427–468
Wang DD, Kriegstein AR (2009) Defining the role of GABA in cortical development. J Physiol 587:1873–1879
Wang X, Arcuino G, Takano T, Lin J, Peng WG, Wan P, Li P, Xu Q, Liu QS, Goldman SA, Nedergaard M (2004) P2X7 receptor inhibition improves recovery after spinal cord injury. Nat Med 10:821–827
Webb SE, Moreau M, Leclerc C, Miller AL (2005) Calcium transients and neural induction in vertebrates. Cell Calcium 37:375–385
Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16:7599–7609
Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43:647–661
Wood MR, Cohen MJ (1979) Synaptic regeneration in identified neurons of the lamprey spinal cord. Science 206:344–347
Yamanaka S (2012) Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10:678–684
Yu K, McGlynn S, Matise MP (2013) Floor plate-derived sonic hedgehog regulates glial and ependymal cell fates in the developing spinal cord. Development 140:1594–1604
Zhang F, Clarke JDW, Ferretti P (2000) FGF-2 up-regulation and proliferation of neural progenitors in the regenerating amphibian spinal cord in vivo. Dev Biol 225:381–391
Zimmermann H (2006) Nucleotide signaling in nervous system development. Pflügers Arch 452:573–588
Acknowledgments
This work was partly supported by grant FCE 103356 from ANII and grant #167 from Wings for Life Spinal Cord Research Foundation to RER. The authors would like to thank the kind donation of GATA3-GFP transgenic mice by Dr. Stavros Malas, The Cyprus Institute of Neurology and Genetics, Cyprus.
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Marichal, N., Reali, C., Trujillo-Cenóz, O., Russo, R.E. (2017). Spinal Cord Stem Cells In Their Microenvironment: The Ependyma as a Stem Cell Niche. In: Birbrair, A. (eds) Stem Cell Microenvironments and Beyond. Advances in Experimental Medicine and Biology, vol 1041. Springer, Cham. https://doi.org/10.1007/978-3-319-69194-7_5
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