Abstract
Radial glias have been thought to serve as a scaffold to support and direct neurons in their radial migration during the development of the cerebral cortex. However, a recent series of studies on neocortical development showed that these cells behave as multifunctional cells. These studies have provided strong support for the idea that radial glias function as multipotential progenitor cells that give rise to various cell types, including neurons. Proliferation of the radial glia was thought to result in inheritance of the radial fiber by a postmitotic neuron, and it was considered that one role of the radial fiber was to act as a cable to lift the postmitotic neuron. In this review, we propose another function of the radial fiber in the developing neocortex. This novel function is proposed based on the fact that the characteristics of the radial glias are identical to those of neuroepithelial cells. Before neuron production, the neuroepithelial cells proliferate and increase in number, retaining and reproducing radial fibers attached to the surface of the basement membrane (the pia mater). During neuron production, the radial glias also reproduce radial fibers at the time of each cell division. We believe that the radial fiber functions to receive signals for morphogenesis, proliferation and differentiation from the pia mater and acts as a cable to conduct information transduced from such signals to the cell soma.
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Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD (2001) A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2, 287–93.
Alvarez-Buylla A, Theelen M, Nottebohm F (1990) Proliferation ‘hot spots’ in adult avian ventricular zone reveal radial cell division. Neuron 5, 101–9.
Barres BA (1999) A new role for glia: generation of neurons! Cell 97, 667–70.
Bayer SA, Altman J (1991) Neocortical Development. Raven Press, New York.
Berry M, Rogers AW (1965) The migration of neuroblasts in the developing cerebral cortex. J Anat 99, 691–709.
Chanas-Sacre G, Rogister B, Moonen G, Leprince P (2000) Radial glia phenotype: Origin, regulation, and transdifferentiation. J Neurosci Res 61, 357–63.
Chenn A, McConnell SK (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631–41.
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, 703–16.
Eriksson PS, Perfilieva E, Bjork-Eriksson T et al. (1998) Neurogenesis in the adult human hippocampus. Nat Med 4, 1313–7.
Fujita S (1962) Kinetics of cellular proliferation. Exp Cell Res 28, 52–60.
Gadisseux JF, Evrard PH, Misson JP, Caviness Jr VS (1992) Dynamic changes in the density of radial glial fibers of the developing murine cerebral wall: a quantitative immunohistological analysis. J Comp Neurol 322, 246–54.
Gierdalski M, Jablonska B, Juliano SL (2000) A factor of specific molecular weight rescues radial glia from early differentiation into astrocytes. Soc Neurosci Abst 26, 1609.
Gray GE, Sanes JR (1992) Lineage of radial glia in the chicken optic tectum. Development 114, 271–83.
Halliday AL, Cepko CL (1992) Generation and migration of cells in the developing striatum. Neuron 9, 15–26.
Hamasaki T, Goto S, Nishikawa S, Ushio Y (2001) Earlygenerated preplate neurons in the developing telencephalon: inward migration into the developing striatum. Cereb Cortex 11, 474–84.
Hartfuss E, Galli R, Heins N, Gotz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229, 15–30.
His W (1887) Abh Kgl Sachs Ges Wissensch Math Phys Kl 13, 479–513.
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.
Kamei Y, Inagaki N, Nishizawa M, Tsutsumi O, Taketani Y, Inagaki M (1998) Visualization of mitotic radial glial lineage cells in the developing rat brain by Cdc2 kinasephosphorylated vimentin. Glia 23, 191–9.
Kawaguchi A, Miyata T, Sawamoto K et al. (2001) Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 17, 259–73.
Kitada M, Chakrabortty S, Matsumoto N, Taketomi M, Ide C (2001) Differentiation of choroid plexus ependymal cells into astrocytes after grafting into the pre-lesioned spinal cord in mice. Glia 36, 364–74.
Kornack DR, Rakic P (2001) Cell proliferation without neurogenesis in adult primate neocortex. Science 294, 2127–30.
Lendahl U, Zinnerman LB, McKay RDG (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60, 585–95.
Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253–63.
Miller MW, Nowakowski RS (1988) Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 457, 44–52.
Misson JP, Edwards MA, Yamamoto M, Caviness VS Jr (1988a) Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker. Dev Brain Res 44, 95–108.
Misson JP, Edwards MA, Yamamoto M, Caviness VS Jr (1988b) Mitotic cycling of radial glial cells of the fetal murine cerebral wall: a combined autoradiographic and immunohistochemical study. Brain Res 446, 183–90.
Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727–41.
Morest DK (1970) A study of neurogenesis in the forebrain of opossum pouch young. Zeitscrift für Anat Entwickl-Gesch 130, 265–305.
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, 143–50.
Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714–20.
Parnavelas JG, Nadarajah B (2001) Radial glial cells: Are they really glia? Neuron 31, 881–4.
Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145, 61–84.
Sauer FC (1935) Mitosis in the neural tube. J Comp Neurol 62, 377–405.
Sauer FC (1936) The interkinetic migration of embryonic epithelial nuclei. J Morphol 60, 1–11.
Schmechel DE, Rakic P (1979) Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Nature 277, 303–5.
Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21, 7153–60.
Takahashi T, Nowakowski RS, Caviness Jr VS (1995a) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15, 6046–57.
Takahashi T, Nowakowski RS, Caviness Jr VS (1995b) Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci 15, 6058–68.
Takahashi T, Nowakowski RS, Caviness Jr VS (1996a) Interkinetic and migratory behavior of a cohort of neocortical neurons arising in the early embryonic murine cerebral wall. J Neurosci 16, 5762–76.
Takahashi T, Nowakowski RS, Caviness VS Jr (1996b) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci 16, 6183–96.
Tamamaki N, Nakamura K, Furuta T, Asamoto K, Kaneko T (2000) Neurons in Golgi-stain-like images revealed by GFP-adenovirus infection in vivo. Neurosci Res 38, 231–6.
Tamamaki N, Nakamura K, Okamoto K, Kaneko T (2001) Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res 41, 51–60.
Tomko RP, Johansson CB, Totrov M, Abagyan R, Frisen J, Philipson L (2000) Expression of the adenovirus receptor and its interaction with the fiber knob. Exp Cell Res 255, 47–55.
Van den Pol AN, Mocarski E, Saederup N, Vieira J, Meier TJ (1999) Cytomegalovirus cell tropism, replication, and gene transfer in brain. J Neurosci 19, 10948–65.
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.
Yamaguchi M, Saito H, Suzuki M, Mori K (2000) Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport 11, 1991–6.
Zhong W, Jiang MM, Weinmaster G, Jan LY, Jan YN (1997) Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 124, 1887–97.
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Tamamaki, N. Radial glias and radial fibers: what is the function of radial fibers?. Anato Sci Int 77, 2–11 (2002). https://doi.org/10.1046/j.0022-7722.2002.00013.x
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DOI: https://doi.org/10.1046/j.0022-7722.2002.00013.x