Abstract
During the last decade, the role of radial glia has been radically revisited. Rather than being considered a mere structural component serving to guide newborn neurons towards their final destinations, radial glia is now known to be the main source of neurons in several regions of the central nervous system, notably in the cerebral cortex. Radial glial cells differentiate from neuroepithelial progenitors at the beginning of neurogenesis and share with their ancestors the bipolar shape and the expression of some molecular markers. Radial glia, however, can be distinguished from neuroepithelial progenitors by the expression of astroglial markers. Clonal analyses showed that radial glia is a heterogeneous population, comprising both pluripotent and different lineage-restricted neural progenitors. At late-embryonic and postnatal stages, radial glial cells give rise to the neural stem cells responsible for adult neurogenesis. Embryonic pluripotent radial glia and adult neural stem cells may be clonally linked, thus representing a lineage displaying stem cell features in both the developing and mature central nervous system.
Similar content being viewed by others
References
Aaku-Saraste E, Hellwig A, Huttner WB (1996) Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure–remodeling of the neuroepithelium prior to neurogenesis. Dev Biol 180:664–679
Adolf B, Chapouton P, Lam CS, Topp S, Tannhauser B, Strahle U, Gotz M, Bally-Cuif L (2006) Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev Biol 295:278–293
Akimoto J, Itoh H, Miwa T, Ikeda K (1993) Immunohistochemical study of glutamine synthetase expression in early glial development. Brain Res Dev Brain Res 72:9–14
Alvarez-Buylla A (1990) Mechanism of neurogenesis in adult avian brain. Experientia 46:948–955
Anthony TE, Klein C, Fishell G, Heintz N (2004) Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41:881–890
Appolloni I, Calzolari F, Corte G, Perris R, Malatesta P (2007) Six3 controls the neural progenitor status in the murine CNS. Cereb Cortex DOI 10.1093/cercor/bhm092
Barnabe-Heider F, Wasylnka JA, Fernandes KJ, Porsche C, Sendtner M, Kaplan DR, Miller FD (2005) Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48:253–265
Bartsch S, Bartsch U, Dorries U, Faissner A, Weller A, Ekblom P, Schachner M (1992) Expression of tenascin in the developing and adult cerebellar cortex. J Neurosci 12:736–749
Bibel M, Richter J, Schrenk K, Tucker KL, Staiger V, Korte M, Goetz M, Barde YA (2004) Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat Neurosci 7:1003–1009
Bolteus AJ, Bordey A (2004) GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 24:7623–7631
Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, Stahl N, Yancopoulos GD, Greenberg ME (1997) Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278:477–483
Brenner M, Messing A (1996) GFAP Transgenic Mice. Methods 10:351–364
Britanova O, Akopov S, Lukyanov S, Gruss P, Tarabykin V (2005) Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur J Neurosci 21:658–668
Britz O, Mattar P, Nguyen L, Langevin LM, Zimmer C, Alam S, Guillemot F, Schuurmans C (2006) A role for proneural genes in the maturation of cortical progenitor cells. Cereb Cortex 16(Suppl 1):i138–i151
Cai L, Hayes NL, Nowakowski RS (1997) Local homogeneity of cell cycle length in developing mouse cortex. J Neurosci 17:2079–2087
Calegari F, Huttner WB (2003) An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J Cell Sci 116:4947–4955
Calegari F, Haubensak W, Haffner C, Huttner WB (2005) Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci 25:6533–6538
Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Brauninger M, Eilken HM, Rieger MA, Schroeder TT, Huttner WB, Brakebusch C, Gotz M (2006) The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 9:1099–1107
Chambers CB, Peng Y, Nguyen H, Gaiano N, Fishell G, Nye JS (2001) Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development 128:689–702
Chapouton P, Adolf B, Leucht C, Tannhauser B, Ryu S, Driever W, Bally-Cuif L (2006) her5 expression reveals a pool of neural stem cells in the adult zebrafish midbrain. Development 133:4293–4303
Chenn A, McConnell SK (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82:631–641
Chenn A, Zhang YA, Chang BT, McConnell SK (1998) Intrinsic polarity of mammalian neuroepithelial cells. Mol Cell Neurosci 11:183–193
Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D (1999) Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 19:4462–4471
Choi BH (1981) Radial glia of developing human fetal spinal cord: Golgi, immunohistochemical and electron microscopic study. Brain Res 227:249–267
Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A (2005) Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3:e283
Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249
Doetsch F (2003a) The glial identity of neural stem cells. Nat Neurosci 6:1127–1134
Doetsch F (2003b) A niche for adult neural stem cells. Curr Opin Genet Dev 13:543–550
Doetsch F, Scharff C (2001) Challenges for brain repair: insights from adult neurogenesis in birds and mammals. Brain Behav Evol 58:306–322
Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046–5061
Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716
Echeverri K, Tanaka EM (2002) Ectoderm to mesoderm lineage switching during axolotl tail regeneration. Science 298:1993–1996
Edwards MA, Yamamoto M, Caviness VS Jr (1990) Organization of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience 36:121–144
Englund U, Bjorklund A, Wictorin K (2002) Migration patterns and phenotypic differentiation of long-term expanded human neural progenitor cells after transplantation into the adult rat brain. Brain Res Dev Brain Res 134:123–141
Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247–251
Feng L, Hatten ME, Heintz N (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12:895–908
Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14:67–80
Frederiksen K, McKay RD (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144–1151
Gaiano N, Fishell G (2002) The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 25:471–490
Gaiano N, Nye JS, Fishell G (2000) Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26:395–404
Galli R, Fiocco R, De Filippis L, Muzio L, Gritti A, Mercurio S, Broccoli V, Pellegrini M, Mallamaci A, Vescovi AL (2002) Emx2 regulates the proliferation of stem cells of the adult mammalian central nervous system. Development 129:1633–1644
Gangemi RM, Daga A, Marubbi D, Rosatto N, Capra MC, Corte G (2001) Emx2 in adult neural precursor cells. Mech Dev 109:323–329
Gangemi RM, Daga A, Muzio L, Marubbi D, Cocozza S, Perera M, Verardo S, Bordo D, Griffero F, Capra MC, Mallamaci A, Corte G (2006) Effects of Emx2 inactivation on the gene expression profile of neural precursors. Eur J Neurosci 23:325–334
Garcia-Verdugo JM, Ferron S, Flames N, Collado L, Desfilis E, Font E (2002) The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res Bull 57:765–775
Glaser T, Pollard SM, Smith A, Brustle O (2007) Tripotential differentiation of adherently expandable neural stem (NS) cells. PLoS ONE 2:e298
Gotz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777–788
Gotz M, Bolz J, Joester A, Faissner A (1997) Tenascin-C synthesis and influence on axonal growth during rat cortical development. Eur J Neurosci 9:496–506
Gotz M, Stoykova A, Gruss P (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21:1031–1044
Gotz M, Hartfuss E, Malatesta P (2002) Radial glial cells as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res Bull 57:777–788
Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M (2006) Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295:263–277
Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo PM, Gotz M (2005) Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8:865–872
Hartfuss E, Galli R, Heins N, Gotz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15–30
Hartfuss E, Forster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, Frotscher M, Gotz M (2003) Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130:4597–4609
Hatakeyama J, Bessho Y, Katoh K, Ookawara S, Fujioka M, Guillemot F, Kageyama R (2004) Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131:5539–5550
Haubensak W, Attardo A, Denk W, Huttner WB (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 101:3196–3201
Haubst N, Georges-Labouesse E, De Arcangelis A, Mayer U, Gotz M (2006) Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 133:3245–3254
Haydar TF, Ang E Jr, Rakic P (2003) Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc Natl Acad Sci USA 100:2890–2895
He F, Ge W, Martinowich K, Becker-Catania S, Coskun V, Zhu W, Wu H, Castro D, Guillemot F, Fan G, de Vellis J, Sun YE (2005) A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci 8:616–625
Heins N, Cremisi F, Malatesta P, Gangemi RM, Corte G, Price J, Goudreau G, Gruss P, Gotz M (2001) Emx2 promotes symmetric cell divisions and a multipotential fate in precursors from the cerebral cortex. Mol Cell Neurosci 18:485–502
Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, Barde YA, Gotz M (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 5:308–315
Hermanson O, Jepsen K, Rosenfeld MG (2002) N-CoR controls differentiation of neural stem cells into astrocytes. Nature 419:934–939
Iacopetti P, Michelini M, Stuckmann I, Oback B, Aaku-Saraste E, Huttner WB (1999) Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc Natl Acad Sci USA 96:4639–4644
Jankovski A, Sotelo C (1996) Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J Comp Neurol 371:376–396
Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25–34
Kosodo Y, Roper K, Haubensak W, Marzesco AM, Corbeil D, Huttner WB (2004) Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. Embo J 23:2314–2324
Landrieu P, Goffinet A (1979) Mitotic spindle fiber orientation in relation to cell migration in the neo-cortex of normal and reeler mouse. Neurosci Lett 13:69–72
Levitt P, Rakic P (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol 193:815–840
Liour SS, Yu RK (2003) Differentiation of radial glia-like cells from embryonic stem cells. Glia 42:109–117
Lobe CG, Koop KE, Kreppner W, Lomeli H, Gertsenstein M, Nagy A (1999) Z/AP, a double reporter for cre-mediated recombination. Dev Biol 208:281–292
Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:5253–5263
Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, Gotz M (2003) Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37:751–764
McCarthy M, Turnbull DH, Walsh CA, Fishell G (2001) Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J Neurosci 21:6772–6781
Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A (2004) Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 101:17528–17532
Messier PE, Auclair C (1974) Effect of cytochalasin B on interkinetic nuclear migration in the chick embryo. Dev Biol 36:218–223
Miller FD, Gauthier AS (2007) Timing is everything: making neurons versus glia in the developing cortex. Neuron 54:357–369
Misson JP, Edwards MA, Yamamoto M, Caviness VS Jr (1988) Mitotic cycling of radial glial cells of the fetal murine cerebral wall: a combined autoradiographic and immunohistochemical study. Brain Res 466:183–190
Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727–741
Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131:3133–3145
Mizutani K, Saito T (2005) Progenitors resume generating neurons after temporary inhibition of neurogenesis by Notch activation in the mammalian cerebral cortex. Development 132:1295–1304
Mo Z, Moore AR, Filipovic R, Ogawa Y, Kazuhiro I, Antic SD, Zecevic N (2007) Human cortical neurons originate from radial glia and neuron-restricted progenitors. J Neurosci 27:4132–4145
Mollgoard K, Saunders NR (1975) Complex tight junctions of epithelial and of endothelial cells in early foetal brain. J Neurocytol 4:453–468
Murciano A, Zamora J, Lopez-Sanchez J, Frade JM (2002) Interkinetic nuclear movement may provide spatial clues to the regulation of neurogenesis. Mol Cell Neurosci 21:285–300
Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143–150
Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T (1999) Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284:479–482
Namihira M, Nakashima K, Taga T (2004) Developmental stage dependent regulation of DNA methylation and chromatin modification in a immature astrocyte specific gene promoter. FEBS Lett 572:184–188
Nieto M, Schuurmans C, Britz O, Guillemot F (2001) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29:401–413
Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714–720
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
Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136–144
Novak A, Guo C, Yang W, Nagy A, Lobe CG (2000) Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28:147–155
Patten BA, Sardi SP, Koirala S, Nakafuku M, Corfas G (2006) Notch1 signaling regulates radial glia differentiation through multiple transcriptional mechanisms. J Neurosci 26:3102–3108
Peretto P, Merighi A, Fasolo A, Bonfanti L (1997) Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull 42:9–21
Perez-Canellas MM, Font E, Garcia-Verdugo JM (1997) Postnatal neurogenesis in the telencephalon of turtles: evidence for nonradial migration of new neurons from distant proliferative ventricular zones to the olfactory bulbs. Brain Res Dev Brain Res 101:125–137
Plachta N, Bibel M, Tucker KL, Barde YA (2004) Developmental potential of defined neural progenitors derived from mouse embryonic stem cells. Development 131:5449–5456
Pollard SM, Conti L, Sun Y, Goffredo D, Smith A (2006) Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb Cortex 16(Suppl 1):i112–i120
Price J, Thurlow L (1988) Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development 104:473–482
Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, Temple S (2000) Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28:69–80
Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–83
Rakic P (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18:383–388
Rakic P (2003) Developmental and evolutionary adaptations of cortical radial glia. Cereb Cortex 13:541–549
Reynolds BA, Weiss S (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175:1–13
Sancho-Tello M, Valles S, Montoliu C, Renau-Piqueras J, Guerri C (1995) Developmental pattern of GFAP and vimentin gene expression in rat brain and in radial glial cultures. Glia 15:157–166
Sauer FC (1935) Mitosis in the neural tube. J Comp Neurol 62:377–405
Schmid RS, McGrath B, Berechid BE, Boyles B, Marchionni M, Sestan N, Anton ES (2003) Neuregulin 1-erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc Natl Acad Sci USA 100:4251–4256
Schnitzer J, Franke WW, Schachner M (1981) Immunocytochemical demonstration of vimentin in astrocytes and ependymal cells of developing and adult mouse nervous system. J Cell Biol 90:435–447
Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182:311–322
Schuurmans C, Armant O, Nieto M, Stenman JM, Britz O, Klenin N, Brown C, Langevin LM, Seibt J, Tang H, Cunningham JM, Dyck R, Walsh C, Campbell K, Polleux F, Guillemot F (2004) Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. Embo J 23:2892–2902
Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S (2006) The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9:743–751
Shibata T, Yamada K, Watanabe M, Ikenaka K, Wada K, Tanaka K, Inoue Y (1997) Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J Neurosci 17:9212–9219
Smart IH (1973) Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures. J Anat 116:67–91
Smart IH (1976) A pilot study of cell production by the ganglionic eminences of the developing mouse brain. J Anat 121:71–84
Smith AG (2001) Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol 17:435–462
Sommer L, Ma Q, Anderson DJ (1996) Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol Cell Neurosci 8:221–241
Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70–71
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
Stricker SH, Meiri K, Gotz M (2006) P-GAP-43 is enriched in horizontal cell divisions throughout rat cortical development. Cereb Cortex 16(Suppl 1):i121–i131
Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, Fan G, Greenberg ME (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104:365–376
Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1:749–758
Tarabykin V, Stoykova A, Usman N, Gruss P (2001) Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128:1983–1993
Ventura RE, Goldman JE (2007) Dorsal radial glia generate olfactory bulb interneurons in the postnatal murine brain. J Neurosci 27:4297–4302
Vives V, Alonso G, Solal AC, Joubert D, Legraverend C (2003) Visualization of S100B-positive neurons and glia in the central nervous system of EGFP transgenic mice. J Comp Neurol 457:404–419
Voigt T (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 289:74–88
Williams BP, Price J (1995) Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron 14:1181–1188
Winkler C, Fricker RA, Gates MA, Olsson M, Hammang JP, Carpenter MK, Bjorklund A (1998) Incorporation and glial differentiation of mouse EGF-responsive neural progenitor cells after transplantation into the embryonic rat brain. Mol Cell Neurosci 11:99–116
Zhong W, Feder JN, Jiang MM, Jan LY, Jan YN (1996) Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17:43–53
Acknowledgment
We would like to acknowledge Prof. M. Götz for helpful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by AIRC (Associazione Italiana per la Ricerca sul Cancro) NUSUG grant (In vivo screening for genes implicated in glioma formation and development of new animal models of glial tumors) and by Fondazione CARIGE grant (Basi molecolari e cellulari dei gliomi: individuazione di marcatori diagnostici e di nuovi bersagli terapeutici).
Rights and permissions
About this article
Cite this article
Malatesta, P., Appolloni, I. & Calzolari, F. Radial glia and neural stem cells. Cell Tissue Res 331, 165–178 (2008). https://doi.org/10.1007/s00441-007-0481-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-007-0481-8