The glial identity of neural stem cells (original) (raw)

• Fields, R.D. & Stevens-Graham, B. New insights into neuron-glia communication. Science 298, 556–562 (2002).
  CAS PubMed PubMed Central Google Scholar
• Haydon, P.G. GLIA: listening and talking to the synapse. Nat. Rev. Neurosci. 2, 185–193 (2001).
  CAS PubMed Google Scholar
• Rakic, P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145, 61–84 (1972).
  CAS PubMed Google Scholar
• Choi, B.H. & Lapham, L.W. Radial glia in the human fetal cerebrum: a combined Golgi, immunofluorescent and electron microscopic study. Brain Res. 148, 295–311 (1978).
  CAS PubMed Google Scholar
• 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. 193, 815–840 (1980).
  CAS PubMed Google Scholar
• Bignami, A. & Dahl, D. Astrocyte-specific protein and radial glia in the cerebral cortex of newborn rat. Nature 252, 55–56 (1974).
  CAS PubMed Google Scholar
• Feng, L., Hatten, M.E. & Heintz, N. Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895–908 (1994).
  CAS PubMed Google Scholar
• Shibata, T. et al. Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J. Neurosci. 17, 9212–9219 (1997).
  CAS PubMed PubMed Central Google Scholar
• Yuasa, S. Development of astrocytes in the mouse embryonic cerebrum tracked by tenascin-C gene expression. Arch. Histol. Cytol. 64, 119–126 (2001).
  CAS PubMed Google Scholar
• Schmechel, D.E. & Rakic, P. A Golgi study of radial glia cells in developing monkey telencephalon: Morphogenesis and transformation into astrocytes. Anat. Embryol. 156, 115–152 (1979).
  CAS Google Scholar
• Voigt, T. 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 (1989).
  CAS PubMed Google Scholar
• Doetsch, F. & Scharff, C. Challenges for brain repair: insights from adult neurogenesis in birds and mammals. Brain Behav. Evol. 58, 306–322 (2001).
  CAS PubMed Google Scholar
• Gould, E., Reeves, A.J., Graziano, M.S. & Gross, C.G. Neurogenesis in the neocortex of adult primates. Science 286, 548–552 (1999).
  CAS PubMed Google Scholar
• Kornack, D.R. & Rakic, P. Cell proliferation without neurogenesis in adult primate neocortex. Science 294, 2127–2130 (2001).
  CAS PubMed Google Scholar
• Koketsu, D., Mikami, A., Miyamoto, Y. & Hisatsune, T. Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J. Neurosci. 23, 937–942 (2003).
  CAS PubMed PubMed Central Google Scholar
• Paton, J.A. & Nottebohm, F. Neurons generated in the adult brain are recruited into functional circuits. Science 225, 1046–1048 (1984).
  CAS PubMed Google Scholar
• van Praag, H. et al. Functional neurogenesis in the adult hippocampus. Nature 415, 1030–1034 (2002).
  Article CAS PubMed Google Scholar
• Carleton, A., Petreanu, L.T., Lansford, R., Alvarez-Buylla, A. & Lledo, P.M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6, 507–518 (2003).
  CAS PubMed Google Scholar
• Temple, S. The development of neural stem cells. Nature 414, 112–117 (2001).
  CAS PubMed Google Scholar
• Gage, F.H. Mammalian neural stem cells. Science 287, 1433–1438 (2000).
  CAS PubMed Google Scholar
• Doetsch, F. & Alvarez-Buylla, A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. USA 93, 14895–14900 (1996).
  CAS PubMed PubMed Central Google Scholar
• Doetsch, F., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046–5061 (1997).
  CAS PubMed PubMed Central Google Scholar
• Lois, C., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Chain migration of neuronal precursors. Science 271, 978–981 (1996).
  CAS PubMed Google Scholar
• Wichterle, H., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18, 779–791 (1997).
  CAS PubMed Google Scholar
• Doetsch, F., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. USA 96, 11619–11624 (1999).
  CAS PubMed PubMed Central Google Scholar
• Cohen, E. & Meininger, V. Ultrastructural analysis of primary cilium in the embryonic nervous tissue of mouse. Int. J. Dev. Neurosci. 5, 43–51 (1987).
  CAS PubMed Google Scholar
• Doetsch, F., Caille, I., Lim, D.A., García-Verdugo, J.M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703–716 (1999).
  CAS PubMed Google Scholar
• Holland, E.C. & Varmus, H.E. Basic fibroblast growth factor induces cell migration and proliferation after glia-specific gene transfer in mice. Proc. Natl. Acad. Sci. USA 95, 1218–1223 (1998).
  CAS PubMed PubMed Central Google Scholar
• Levison, S.W. & Goldman, J.E. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10, 201–212 (1993).
  CAS PubMed Google Scholar
• Marshall, C.A. & Goldman, J.E. Subpallial dlx2-expressing cells give rise to astrocytes and oligodendrocytes in the cerebral cortex and white matter. J. Neurosci. 22, 9821–9830 (2002).
  CAS PubMed PubMed Central Google Scholar
• Nait-Oumesmar, B. et al. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur. J. Neurosci. 11, 4357–4366 (1999).
  CAS PubMed Google Scholar
• Seri, B., Garcia-Verdugo, J.M., McEwen, B.S. & Alvarez-Buylla, A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21, 7153–7160 (2001).
  CAS PubMed PubMed Central Google Scholar
• Peters, A., Palay, S.L. & de Webster, H.F. The Fine Structure of the Nervous System: Neurons and their Supporting Cells (Oxford Univ. Press, New York, 1991).
  Google Scholar
• Morshead, C.M. et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13, 1071–1082 (1994).
  CAS PubMed Google Scholar
• Gritti, A. et al. Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J. Neurosci. 19, 3287–3297 (1999).
  CAS PubMed PubMed Central Google Scholar
• Doetsch, F., Petreanu, L., Caille, I., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36, 1021–1034 (2002).
  CAS PubMed Google Scholar
• Doetsch, F. et al. Lack of the cell-cycle inhibitor p27Kip1 results in selective increase of transit-amplifying cells for adult neurogenesis. J. Neurosci. 22, 2255–2264 (2002).
  CAS PubMed PubMed Central Google Scholar
• Imura, T., Kornblum, H.I. & Sofroniew, M.V. The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J. Neurosci. 23, 2824–2832 (2003).
  CAS PubMed PubMed Central Google Scholar
• Morshead, C.M., Garcia, A.D., Sofroniew, M.V. & van Der Kooy, D. The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur. J. Neurosci. 18, 76–84 (2003).
  PubMed Google Scholar
• Rietze, R.L. et al. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412, 736–739 (2001).
  CAS PubMed Google Scholar
• Capela, A. & Temple, S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as non-ependymal. Neuron 35, 865–875 (2002).
  PubMed Google Scholar
• Johansson, C.B. et al. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96, 25–34 (1999).
  CAS PubMed Google Scholar
• Chiasson, B.J., Tropepe, V., Morshead, C.M. & van der Kooy, D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J. Neurosci. 19, 4462–4471 (1999).
  CAS PubMed PubMed Central Google Scholar
• Laywell, E.D., Rakic, P., Kukekov, V.G., Holland, E.C. & Steindler, D.A. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc. Natl. Acad. Sci. USA 97, 13883–13888 (2000).
  CAS PubMed PubMed Central Google Scholar
• Lim, D.A. et al. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713–726 (2000).
  CAS PubMed Google Scholar
• Doetsch, F. A niche for adult neural stem cells. Curr. Opin. Gen. Dev. 13, 543–550 (2003).
  CAS Google Scholar
• Geschwind, D.H. et al. A genetic analysis of neural progenitor differentiation. Neuron 29, 325–339 (2001).
  CAS PubMed Google Scholar
• Terskikh, A.V. et al. From hematopoiesis to neuropoiesis: evidence of overlapping genetic programs. Proc. Natl. Acad. Sci. USA 98, 7934–7939 (2001).
  CAS PubMed PubMed Central Google Scholar
• Ivanova, N.B. et al. A stem cell molecular signature. Science 298, 601–604 (2002).
  CAS PubMed Google Scholar
• Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R.C. & Melton, D.A. “Stemness”: transcriptional profiling of embryonic and adult stem cells. Science 298, 597–600 (2002).
  CAS PubMed Google Scholar
• Garcia-Verdugo, J.M. et al. The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res. Bull. 57, 765–775 (2002).
  PubMed Google Scholar
• Alvarez-Buylla, A., García-Verdugo, J.M., Mateo, A. & Merchant-Larios, H. Primary neural precursors and intermitotic nuclear migration in the ventricular zone of adult canaries. J. Neurosci. 18, 1020–1037 (1998).
  CAS PubMed PubMed Central Google Scholar
• Alvarez-Buylla, A. & Nottebohm, F. Migration of young neurons in adult avian brain. Nature 335, 353–354 (1988).
  CAS PubMed Google Scholar
• Font, E., Desfilis, E., Perez-Canellas, M.M., Alcantara, S. & García-Verdugo, J.M. 3-Acetylpyridine-induced degeneration and regeneration in the adult lizard brain: a qualitative and quantitative analysis. Brain Res. 754, 245–259 (1997).
  CAS PubMed Google Scholar
• Echeverri, K. & Tanaka, E.M. Ectoderm to mesoderm lineage switching during axolotl tail regeneration. Science 298, 1993–1996 (2002).
  CAS PubMed Google Scholar
• Frederiksen, K. & McKay, R.D.G. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci. 8, 1144–1151 (1988).
  CAS PubMed PubMed Central Google Scholar
• Noctor, S.C. et al. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 22, 3161–3173 (2002).
  CAS PubMed PubMed Central Google Scholar
• Hartfuss, E., Galli, R., Heins, N. & Gotz, M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229, 15–30 (2001).
  CAS PubMed Google Scholar
• Gray, G.E. & Sanes, J.R. Lineage of radial glia in the chicken optic tectum. Development 114, 271–283 (1992).
  CAS PubMed Google Scholar
• Noctor, S.C., Flint, A.C., Weissman, T.A., Dammerman, R.S. & Kriegstein, A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714–720 (2001).
  CAS PubMed Google Scholar
• Tamamaki, N., Nakamura, K., Okamoto, K. & Kaneko, T. Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci. Res. 41, 51–60 (2001).
  CAS PubMed Google Scholar
• Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727–741 (2001).
  CAS PubMed Google Scholar
• Malatesta, P., Hartfuss, E. & Gotz, M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253–5263 (2000).
  CAS PubMed Google Scholar
• Skogh, C. et al. Generation of regionally specified neurons in expanded glial cultures derived from the mouse and human lateral ganglionic eminence. Mol. Cell. Neurosci. 17, 811–820 (2001).
  CAS PubMed Google Scholar
• Delaney, C.L., Brenner, M. & Messing, A. Conditional ablation of cerebellar astrocytes in postnatal transgenic mice. J. Neurosci. 16, 6908–6918 (1996).
  CAS PubMed PubMed Central Google Scholar
• Marino, S., Vooijs, M., van Der Gulden, H., Jonkers, J. & Berns, A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 14, 994–1004 (2000).
  CAS PubMed PubMed Central Google Scholar
• Zhuo, L. et al. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31, 85–94 (2001).
  CAS PubMed Google Scholar
• Malatesta, P. et al. Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37, 751–764 (2003).
  CAS PubMed Google Scholar
• Kwon, C.H. et al. Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat. Genet. 29, 404–411 (2001).
  CAS PubMed Google Scholar
• He, W., Ingraham, C., Rising, L., Goderie, S. & Temple, S. Multipotent stem cells from the mouse basal forebrain contribute GABAergic neurons and oligodendrocytes to the cerebral cortex during embryogenesis. J. Neurosci. 21, 8854–8862 (2001).
  CAS PubMed PubMed Central Google Scholar
• Matthias, K. et al. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J. Neurosci. 23, 1750–1758 (2003).
  CAS PubMed PubMed Central Google Scholar
• Alvarez-Buylla, A., Garcia-Verdugo, J.M. & Tramontin, A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2, 287–293 (2001).
  CAS PubMed Google Scholar
• Eckenhoff, M.F. & Rakic, P. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the Rhesus monkey. J. Neurosci. 8, 2729–2747 (1988).
  CAS PubMed PubMed Central Google Scholar
• Alves, J.A., Barone, P., Engelender, S., Froes, M.M. & Menezes, J.R. Initial stages of radial glia astrocytic transformation in the early postnatal anterior subventricular zone. J. Neurobiol. 52, 251–265 (2002).
  PubMed Google Scholar
• Gaiano, N., Nye, J.S. & Fishell, G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26, 395–404 (2000).
  CAS PubMed Google Scholar
• Zhou, M. & Kimelberg, H.K. Freshly isolated hippocampal CA1 astrocytes comprise two populations differing in glutamate transporter and AMPA receptor expression. J. Neurosci. 21, 7901–7908 (2001).
  CAS PubMed PubMed Central Google Scholar
• D'Ambrosio, R., Wenzel, J., Schwartzkroin, P.A., McKhann, G.M. & Janigro, D. Functional specialization and topographic segregation of hippocampal astrocytes. J. Neurosci. 18, 4425–4438 (1998).
  CAS PubMed PubMed Central Google Scholar
• Song, H., Stevens, C.F. & Gage, F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39–44 (2002).
  CAS PubMed Google Scholar
• Palmer, T.D., Markakis, E.A., Willhoite, A.R., Safar, F. & Gage, F.H. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci. 19, 8487–8497 (1999).
  CAS PubMed PubMed Central Google Scholar
• Weiss, S. et al. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16, 7599–7609 (1996).
  CAS PubMed PubMed Central Google Scholar
• Shihabuddin, L.S., Horner, P.J., Ray, J. & Gage, F.H. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J. Neurosci. 20, 8727–8735 (2000).
  CAS PubMed PubMed Central Google Scholar
• Lie, D.C. et al. The adult substantia nigra contains progenitor cells with neurogenic potential. J. Neurosci. 22, 6639–6649 (2002).
  CAS PubMed PubMed Central Google Scholar
• Gomez-Pinilla, F., Vu, L. & Cotman, C.W. Regulation of astrocyte proliferation by FGF-2 and heparan sulfate in vivo. J. Neurosci. 15, 2021–2029 (1995).
  CAS PubMed PubMed Central Google Scholar
• Yazaki, N. et al. Differential expression patterns of mRNAs for members of the fibroblast growth factor receptor family, FGFR-1 – FGFR-4, in rat brain. J. Neurosci. Res. 37, 445–452 (1994).
  CAS PubMed Google Scholar
• Fischer, A.J. & Reh, T.A. Muller glia are a potential source of neural regeneration in the postnatal chicken retina. PG. Nat. Neurosci. 4, 247–252 (2001).
  CAS PubMed Google Scholar
• Raff, M.C. Glial cell diversification in the rat optic nerve. Science 243, 1450–1455 (1989).
  CAS PubMed Google Scholar
• Kondo, T. & Raff, M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289, 1754–1757 (2000).
  CAS PubMed Google Scholar
• Belachew, S. et al. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J. Cell Biol. 161, 169–86 (2003).
  CAS PubMed PubMed Central Google Scholar
• Lu, Q.R. et al. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75–86 (2002).
  CAS PubMed Google Scholar
• Zhou, Q. & Anderson, D.J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61–73 (2002).
  CAS PubMed Google Scholar
• Kruger, G.M. et al. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35, 657–669 (2002).
  CAS PubMed PubMed Central Google Scholar
• Nakatomi, H. et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429–441 (2002).
  CAS PubMed Google Scholar
• Schuurmans, C. & Guillemot, F. Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol. 12, 26–34 (2002).
  CAS PubMed Google Scholar
• Heins, N. et al. Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5, 308–315 (2002).
  CAS PubMed Google Scholar
• Takizawa, T. et al. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell 1, 749–758 (2001).
  CAS PubMed Google Scholar
• Nieto, M., Schuurmans, C., Britz, O. & Guillemot, F. Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29, 401–413 (2001).
  CAS PubMed Google Scholar
• Sun, Y. et al. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104, 365–376 (2001).
  CAS PubMed Google Scholar
• Sakakibara, S. & Okano, H. Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J. Neurosci. 17, 8300–8312 (1997).
  CAS PubMed PubMed Central Google Scholar
• Kaneko, Y. et al. Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev. Neurosci. 22, 139–153 (2000).
  CAS PubMed Google Scholar
• Ramón y Cajal, S. Histology of the Nervous System of Man and Vertebrates Vol. 1 (Oxford Univ. Press, Oxford, 1995).
  Google Scholar