Abstract
Neural stem cells are multipotent stem cells that have an unlimited capacity to proliferate and self-renew but whose progeny are restricted to the neural lineages. Neural stem cells can generate large numbers of mature neuronal and glial progeny, often through transient amplification of intermediate progenitor pools, similar to the pattern observed in other organ systems (1). Although self-renewal can occur through symmetric cell divisions that generate two identical daughter cells, asymmetric cell divisions that generate a renewable stem cell and a more lineage-restricted daughter cell are a hallmark of stem cells. Cells that do not self-renew indefinitely but that nevertheless proliferate and have the capacity to generate multiple phenotypes are often referred to as multipotential progenitor cells, but they will be included in a broad definition of stem cells for the purposes of this review. Other stem cell-derived precursor populations that are able to proliferate but that have more restricted lineage potential (e.g., glial restricted or neuronal restricted cells) are discussed elsewhere in this volume.
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References
Potten, C. S. and Loeffler, M. (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110, 1001–1020.
Lendahl, U., Zimmerman, L. B., and McKay, R. D. (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60, 585–595.
Sakakibara, S., Imai, T., Hamaguchi, K., et al. (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol. 176, 230–242.
Pevny, L. H., Sockanathan, S., Placzek, M., and Lovell-Badge, R. (1998) A role for SOX1 in neural determination. Development 125, 1967–1978.
Graham, V., Khudyakov, J., Ellis, P., and Pevny, L. (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39, 749–765.
Liu, Y., Wu, Y., Lee, J. C., et al. (2002) Oligodendrocyte and astrocyte development in rodents: an in situ and immunohistological analysis during embryonic development. Glia 40, 25–43.
Morrison, S. J., White, P. M., Zock, C., and Anderson, D. J. (1999) Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96, 737–749.
Uchida, N., Buck, D. W., He, D., et al. (2000) Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. USA 97, 14720–14725.
Rietze, R. L., Valcanis, H., Brooker, G. F., Thomas, T., Voss, A. K., and Bartlett, P. F. (2001) Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412, 736–739.
Maric, D., Maric, I., Chang, Y. H., and Barker, J. L. (2003) Prospective cell sorting of embryonic rat neural stem cells and neuronal and glial progenitors reveals selective effects of basic fibroblast growth factor and epidermal growth factor on self-renewal and differentiation. J. Neurosci. 23, 240–251.
Rakic, P. (1995) Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc. Natl. Acad. Sci. USA 92, 11323–11327.
Noctor, S. C., Flint, A. C., Weissman, T. A., Wong, W. S., Clinton, B. K., and Kriegstein, A. R. (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 22, 3161–3173.
Parnavelas, J. G. and Nadarajah, B. (2001) Radial glial cells: Are they really glia? Neuron 31, 881–884.
Rakic, P. (2003) Developmental and evolutionary adaptations of cortical radial glia. Cereb. Cortex 13, 541–549.
Morest, D. K. and Silver, J. (2003) 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 43, 6–18.
Kriegstein, A. R. and Gotz, M. (2003) Radial glia diversity: a matter of cell fate. Glia 43, 37–43.
Hartfuss, E. (2003) Characterization of Subtypes of Precursor Cells in the Developing Central Nervous System. Fakultät für Biologie, Ludwig-Maximilians Universität München. (Ph.D. thesis)
Gotz, M., Hartfuss, E., and 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.
Rakic, P. (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neo-cortical expansion during evolution. Trends Neurosci. 18, 383–388.
Caviness, V. S., Jr. and Takahashi, T. (1995) Proliferative events in the cerebral ventricular zone. Brain Dev. 17, 159–163.
Chenn, A. and McConnell, S. K. (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631–641.
Lu, B., Jan, L., and Jan, Y. N. (2000) Control of cell divisions in the nervous system: symmetry and asymmetry. Annu. Rev. Neurosci. 23, 531–556.
Temple, S. (2001) The development of neural stem cells. Nature 414, 112–117.
Noctor, S. C., Martinez-Cerdeno, V., Ivic, L., and Kriegstein, A. R. (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136–144.
Kilpatrick, T. J. and Bartlett, P. F. (1995) Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J. Neurosci. 15, 3653–3661.
Weiss, S., Reynolds, B. A., Vescovi, A. L., Morshead, C., Craig, C. G., and van der Kooy, D. (1996) Is there a neural stem cell in the mammalian forebrain? Trends Neurosci. 19, 387–393.
Johe, K. K., Hazel, T. G., Muller, T., Dugich-Djordjevic, M. M., and McKay, R. D. (1996) Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10, 3129–3140.
Qian, X., Davis, A. A., Goderie, S. K., and Temple, S. (1997) FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 18, 81–93.
Gage, F. H., Coates, P. W., Palmer, T. D., et al. (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl. Acad. Sci. USA 92, 11879–11883.
Palmer, T. D., Ray, J., and Gage, F. H. (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell Neurosci. 6, 474–486.
Palmer, T. D., Takahashi, J., and Gage, F. H. (1997) The adult rat hippocampus contains primordial neural stem cells. Mol. Cell Neurosci. 8, 389–404.
Reynolds, B. A. and 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.
Reynolds, B. A., Tetzlaff, W., and Weiss, S. (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12, 4565–4574.
Vescovi, A. L., Reynolds, B. A., Fraser, D. D., and Weiss, S. (1993) bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11, 951–966.
Temple, S. (1989) Division and differentiation of isolated CNS blast cells in microculture. Nature 340, 471–473.
Mabie, P. C., Mehler, M. F., and Kessler, J. A. (1999) Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J. Neurosci. 19, 7077–7088.
Gaiano, N., Kohtz, J. D., Turnbull, D. H., and Fishell, G. (1999) A method for rapid gain-of-function studies in the mouse embryonic nervous system. Nat. Neurosci. 2, 812–819.
Walsh, C. and Cepko, C. L. (1992) Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science 255, 434–440.
Reid, C. B., Liang, I., and Walsh, C. (1995) Systematic widespread clonal organization in cerebral cortex. Neuron 15, 299–310.
Davis, A. A. and Temple, S. (1994) A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372, 263–266.
Williams, B. P. and Price, J. (1995) Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron 14, 1181–1188.
Burrows, R. C., Wancio, D., Levitt, P., and Lillien, L. (1997) Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19, 251–267.
Viti, J., Feathers, A., Phillips, J., and Lillien, L. (2003) Epidermal growth factor receptors control competence to interpret leukemia inhibitory factor as an astrocyte inducer in developing cortex. J. Neurosci. 23, 3385–3393.
Lillien, L. and Wancio, D. (1998) Changes in epidermal growth factor receptor expression and competence to generate glia regulate timing and choice of differentiation in the retina. Mol. Cell Neurosci. 10, 296–308.
Zhu, G., Mehler, M. F., Mabie, P. C., and Kessler, J. A. (2000) Developmental changes in neural progenitor cell lineage commitment do not depend on epidermal growth factor receptor signaling. J. Neurosci. Res. 59, 312–320.
Zhu, G., Mehler, M. F., Mabie, P. C., and Kessler, J. A. (1999) Developmental changes in progenitor cell responsiveness to cytokines. J. Neurosci. Res. 56, 131–145.
Molne, M., Studer, L., Tabar, V., Ting, Y. T., Eiden, M. V., and McKay, R. D. (2000) Early cortical precursors do not undergo LIF-mediated astrocytic differentiation. J. Neurosci. Res. 59, 301–311.
Monuki, E. S. and Walsh, C. A. (2001) Mechanisms of cerebral cortical patterning in mice and humans. Nat. Neurosci. 4(Suppl), 1199–1206.
O’Leary, D. D. and Nakagawa, Y. (2002) Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex. Curr. Opin. Neurobiol. 12, 14–25.
Campbell, K. (2003) Dorsal-ventral patterning in the mammalian telencephalon. Curr. Opin. Neurobiol. 13, 50–56.
Nadarajah, B., Alifragis, P., Wong, R. O., and Parnavelas, J. G. (2003) Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb. Cortex 13, 607–611.
Jessell, T. M. (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20–29.
Osterfield, M., Kirschner, M. W., and Flanagan, J. G. (2003) Graded positional information: interpretation for both fate and guidance. Cell 113, 425–428.
Parmar, M., Skogh, C., Bjorklund, A., and Campbell, K. (2002) Regional specification of neurosphere cultures derived from subregions of the embryonic telencephalon. Mol. Cell. Neurosci. 21, 645–656.
Hitoshi, S., Tropepe, V., Ekker, M., and van der Kooy, D. (2002) Neural stem cell lineages are regionally specified, but not committed, within distinct compartments of the developing brain. Development 129, 233–244.
Ciccolini, F. and Svendsen, C. N. (1998) Fibroblast growth factor 2 (FGF-2) promotes acquisition of epidermal growth factor (EGF) responsiveness in mouse striatal precursor cells: identification of neural precursors responding to both EGF and FGF-2. J. Neurosci. 18, 7869–7880.
Ortega, S., Ittmann, M., Tsang, S. H., Ehrlich, M., and Basilico, C. (1998) Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc. Natl. Acad. Sci. USA 95, 5672–5677.
Tao, Y., Black, I. B., and DiCicco-Bloom, E. (1997) In vivo neurogenesis is inhibited by neutralizing antibodies to basic fibroblast growth factor. J. Neurobiol. 33, 289–296.
Vaccarino, F. M., Schwartz, M. L., Raballo, R., et al. (1999) Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat. Neurosci. 2, 246–253.
Tao, Y., Black, I. B., and DiCicco-Bloom, E. (1996) Neurogenesis in neonatal rat brain is regulated by peripheral injection of basic fibroblast growth factor (bFGF). J. Comp Neurol. 376, 653–663.
Emoto, N., Gonzalez, A. M., Walicke, P. A., et al. (1989) Basic fibroblast growth factor (FGF) in the central nervous system: identification of specific loci of basic FGF expression in the rat brain. Growth Factors 2, 21–29.
Goodrich, L. V. and Scott, M. P. (1998) Hedgehog and patched in neural development and disease. Neuron 21, 1243–1257.
Kornblum, H. I., Hussain, R., Wiesen, J., et al. (1998) Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor. J. Neurosci. Res. 53, 697–717.
Kornblum, H. I., Hussain, R. J., Bronstein, J. M., Gall, C. M., Lee, D. C., and Seroogy, K. B. (1997) Prenatal ontogeny of the epidermal growth factor receptor and its ligand, transforming growth factor alpha, in the rat brain. J. Comp. Neurol. 380, 243–261.
Marti, E. and Bovolenta, P. (2002) Sonic hedgehog in CNS development: one signal, multiple outputs. Trends Neurosci. 25, 89–96.
Rowitch, D. H., S-Jacques, B., Lee, S. M., Flax, J. D., Snyder, E. Y., and McMahon, A. P. (1999) Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J. Neurosci. 19, 8954–8965.
Gabay, L., Lowell, S., Rubin, L. L., and Anderson, D. J. (2003) Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40, 485–499.
Zhu, G., Mehler, M. F., Zhao, J., Yu Yung, S., and Kessler, J. A. (1999) Sonic hedgehog and BMP2 exert opposing actions on proliferation and differentiation of embryonic neural progenitor cells. Dev. Biol. 215, 118–129.
Wechsler-Reya, R. J. and Scott, M. P. (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103–114.
Kalyani, A. J., Piper, D., Mujtaba, T., Lucero, M. T., and Rao, M. S. (1998) Spinal cord neuronal precursors generate multiple neuronal phenotypes in culture. J. Neurosci. 18, 7856–7868.
Lee, S. M., Tole, S., Grove, E., and McMahon, A. P. (2000) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127, 457–467.
Megason, S. G. and McMahon, A. P. (2002) A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087–2098.
Viti, J., Gulacsi, A., and Lillien, L. (2003) Wnt regulation of progenitor maturation in the cortex depends on Shh or fibroblast growth factor 2. J. Neurosci. 23, 5919–5927.
Ikeya, M., Lee, S. M., Johnson, J. E., McMahon, A. P., and Takada, S. (1997) Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389, 966–970.
Chenn, A. and Walsh, C. A. (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365–369.
Gressens, P., Hill, J. M., Paindaveine, B., Gozes, I., Fridkin, M., and Brenneman, D. E. (1994) Severe microcephaly induced by blockade of vasoactive intestinal peptide function in the primitive neuroepithelium of the mouse. J. Clin. Invest 94, 2020–2027.
Arsenijevic, Y., Weiss, S., Schneider, B., and Aebischer, P. (2001) Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J. Neurosci. 21, 7194–7202.
Lin, X. and Bulleit, R. F. (1997) Insulin-like growth factor I (IGF-I) is a critical trophic factor for developing cerebellar granule cells. Brain Res. Dev. Brain Res. 99, 234–242.
Frade, J. M., Marti, E., Bovolenta, P., et al. (1996) Insulin-like growth factor-I stimulates neurogenesis in chick retina by regulating expression of the alpha 6 integrin subunit. Development 122, 2497–2506.
Drago, J., Murphy, M., Carroll, S. M., Harvey, R. P., and Bartlett, P. F. (1991) Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc. Natl. Acad. Sci. USA 88, 2199–2203.
Raballo, R., Rhee, J., Lyn-Cook, R., Leckman, J. F., Schwartz, M. L., and Vaccarino, F. M. (2000) Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J. Neurosci. 20, 5012–5023.
Ghosh, A. and Greenberg, M. E. (1995) Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15, 89–103.
Lukaszewicz, A., Savatier, P., Cortay, V., Kennedy, H., and Dehay, C. (2002) Contrasting effects of basic fibroblast growth factor and neurotrophin 3 on cell cycle kinetics of mouse cortical stem cells. J. Neurosci. 22, 6610–6622.
Hajihosseini, M. K. and Dickson, C. (1999) A subset of fibroblast growth factors (Fgfs) promote survival, but Fgf-8b specifically promotes astroglial differentiation of rat cortical precursor cells. Mol. Cell. Neurosci. 14, 468–485.
Riese, D. J., Kim, E. D., Elenius, K., et al. (1996) The epidermal growth factor receptor couples transforming growth factor-alpha, heparin-binding epidermal growth factor-like factor, and amphiregulin to Neu, ErbB-3, and ErbB-4. J. Biol. Chem. 271, 20047–20052.
Dumstrei, K., Nassif, C., Abboud, G., Aryai, A., and Hartenstein, V. (1998) EGFR signaling is required for the differentiation and maintenance of neural progenitors along the dorsal midline of the Drosophila embryonic head. Development 125, 3417–3426.
Calaora, V., Rogister, B., Bismuth, K., et al. (2001) Neuregulin signaling regulates neural precursor growth and the generation of oligodendrocytes in vitro. J. Neurosci. 21, 4740–4751.
Barnabe-Heider, F. and Miller, F. D. (2003) Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J. Neurosci. 23, 5149–5160.
Yu, X., Shacka, J. J., Eells, J. B., et al. (2002) Erythropoietin receptor signalling is required for normal brain development. Development 129, 505–516.
Sommer, L. and Rao, M. (2002) Neural stem cells and regulation of cell number. Prog. Neurobiol. 66, 1–18.
Haydar, T. F., Kuan, C. Y., Flavell, R. A., and Rakic, P. (1999) The role of cell death in regulating the size and shape of the mammalian forebrain. Cereb. Cortex 9, 621–626.
D’Sa-Eipper, C. and Roth, K. A. (2000) Caspase regulation of neuronal progenitor cell apoptosis. Dev. Neurosci. 22, 116–124.
Motoyama, N., Wang, F., Roth, K. A., et al. (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267, 1506–1510.
Roth, K. A., Kuan, C., Haydar, T. F., et al. (2000) Epistatic and independent functions of caspase-3 and Bcl-X(L) in developmental programmed cell death. Proc. Natl. Acad. Sci. USA 97, 466–471.
Cheema, Z. F., Wade, S. B., Sata, M., Walsh, K., Sohrabji, F., and Miranda, R. C. (1999) Fas/Apo [apoptosis]-1 and associated proteins in the differentiating cerebral cortex: induction of caspase-dependent cell death and activation of NF-kappaB. J. Neurosci. 19, 1754–1770.
Thibert, C., Teillet, M. A., Lapointe, F., Mazelin, L., Le Douarin, N. M., and Mehlen, P. (2003) Inhibition of neuroepithelial patched-induced apoptosis by sonic hedgehog. Science 301, 843–846.
Austin, C. P., Feldman, D. E., Ida, J. A., Jr., and Cepko, C. L. (1995) Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121, 3637–3650.
Henrique, D., Adam, J., Myat, A., Chitnis, A., Lewis, J., and Ish-Horowicz, D. (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature 375, 787–790.
Myat, A., Henrique, D., Ish-Horowicz, D., and Lewis, J. (1996) A chick homologue of Serrate and its relationship with Notch and Delta homologues during central neurogenesis. Dev. Biol. 174, 233–247.
Artavanis-Tsakonas, S., Rand, M. D., and Lake, R. J. (1999) Notch signaling: cell fate control and signal integration in development. Science 284, 770–776.
Wang, S., Sdrulla, A. D., diSibio, G., et al. (1998) Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21, 63–75.
Gaiano, N., Nye, J. S., and Fishell, G. (2000) Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26, 395–404.
Wang, S. and Barres, B. A. (2000) Up a notch: instructing gliogenesis. Neuron 27, 197–200.
Malatesta, P., Hartfuss, E., and Gotz, M. (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253–5263.
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., and Kriegstein, A. R. (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714–720.
Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703–716.
Shimazaki, T., Shingo, T., and Weiss, S. (2001) The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian fore-brain neural stem cells. J. Neurosci. 21, 7642–7653.
Chojnacki, A., Shimazaki, T., Gregg, C., Weinmaster, G., and Weiss, S. (2003) Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J. Neurosci. 23, 1730–1741.
Israsena, N., Hu, M., Fu, W., Kan, L., and Kessler, J. A. (2004) The presence of FGF2 signaling determines whether β-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev. Biol. 268, 220–231.
Zindy, F., Soares, H., Herzog, K. H., Morgan, J., Sherr, C. J., and Roussel, M. F. (1997) Expression of INK4 inhibitors of cyclin D-dependent kinases during mouse brain development. Cell Growth Differ. 8, 1139–1150.
van Lookeren Campagne, M. and Gill, R. (1998) Tumor-suppressor p53 is expressed in proliferating and newly formed neurons of the embryonic and postnatal rat brain: comparison with expression of the cell cycle regulators p21Waf1/Cip1, p27Kip1, p57Kip2, p16Ink4a, cyclin G1, and the proto-oncogene Bax. J. Comp. Neurol. 397, 181–198.
Watanabe, G., Pena, P., Shambaugh, G. E., 3rd, Haines, G. K., 3rd, and Pestell, R. G. (1998) Regulation of cyclin dependent kinase inhibitor proteins during neonatal cerebella development. Brain Res. Dev. Brain Res. 108, 77–87.
Coskun, V., Venkatraman, G., Yang, H., Rao, M. S., and Luskin, M. B. (2001) Retroviral manipulation of the expression of bone morphogenetic protein receptor Ia by SVZa progenitor cells leads to changes in their p19(INK4d) expression but not in their neuronal commitment. Int. J. Dev. Neurosci. 19, 219–227.
Gross, R. E., Mehler, M. F., Mabie, P. C., Zang, Z., Santschi, L., and Kessler, J. A. (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17, 595–606.
Suh, J., Lu, N., Nicot, A., Tatsuno, I., and DiCicco-Bloom, E. (2001) PACAP is an anti-mitogenic signal in developing cerebral cortex. Nat. Neurosci. 4, 123–124.
Lu, N., Zhou, R., and DiCicco-Bloom, E. (1998) Opposing mitogenic regulation by PACAP in sympathetic and cerebral cortical precursors correlates with differential expression of PACAP receptor (PAC1-R) isoforms. J. Neurosci. Res. 53, 651–662.
Carey, R. G., Li, B., and DiCicco-Bloom, E. (2002) Pituitary adenylate cyclase activating polypeptide anti-mitogenic signaling in cerebral cortical progenitors is regulated by p57Kip2-dependent CDK2 activity. J. Neurosci. 22, 1583–1591.
Lee, M., Lelievre, V., Zhao, P., et al. (2001) Pituitary adenylyl cyclase-activating polypeptide stimulates DNA synthesis but delays maturation of oligodendrocyte progenitors. J. Neurosci. 21, 3849–3859.
Nguyen, L., Rigo, J. M., Rocher, V., et al. (2001) Neurotransmitters as early signals for central nervous system development. Cell Tissue Res. 305, 187–202.
Fiszman, M. L., Borodinsky, L. N., and Neale, J. H. (1999) GABA induces proliferation of immature cerebellar granule cells grown in vitro. Brain Res. Dev. Brain Res. 115, 1–8.
Haydar, T. F., Wang, F., Schwartz, M. L., and Rakic, P. (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J. Neurosci. 20, 5764–5774.
LoTurco, J. J., Owens, D. F., Heath, M. J., Davis, M. B., and Kriegstein, A. R. (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287–1298.
Antonopoulos, J., Pappas, I. S., and Parnavelas, J. G. (1997) Activation of the GABAA receptor inhibits the proliferative effects of bFGF in cortical progenitor cells. Eur. J. Neurosci. 9, 291–298.
Ohtani, N., Goto, T., Waeber, C., and Bhide, P. G. (2003) Dopamine modulates cell cycle in the lateral ganglionic eminence. J. Neurosci. 23, 2840–2850.
Luk, K. C., Kennedy, T. E., and Sadikot, A. F. (2003) Glutamate promotes proliferation of striatal neuronal progenitors by an NMDA receptor-mediated mechanism. J. Neurosci. 23, 2239–2250.
Sadikot, A. F., Burhan, A. M., Belanger, M. C., and Sasseville, R. (1998) NMDA receptor antagonists influence early development of GABAergic interneurons in the mammalian striatum. Brain Res. Dev. Brain Res. 105, 35–42.
Cameron, H. A., Hazel, T. G., and McKay, R. D. (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol. 36, 287–306.
Contestabile, A. (2000) Roles of NMDA receptor activity and nitric oxide production in brain development. Brain Res. Brain Res. Rev. 32, 476–509.
Ferguson, K. L. and Slack, R. S. (2003) Growth factors: Can they promote neurogenesis? Trends Neurosci. 26, 283–285.
Santa-Olalla, J. and Covarrubias, L. (1999) Basic fibroblast growth factor promotes epidermal growth factor responsiveness and survival of mesencephalic neural precursor cells. J. Neurobiol. 40, 14–27.
Daadi, M. M. and Weiss, S. (1999) Generation of tyrosine hydroxylase-producing neurons from precursors of the embryonic and adult forebrain. J. Neurosci. 19, 4484–4497.
Bartlett, P. F., Brooker, G. J., Faux, C. H., et al. (1998) Regulation of neural stem cell differentiation in the forebrain. Immunol. Cell Biol. 76, 414–418.
Ye, W., Shimamura, K., Rubenstein, J. L., Hynes, M. A., and Rosenthal, A. (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93, 755–766.
Hynes, M., Ye, W., Wang, K., et al. (2000) The seven-transmembrane receptor smoothened cell-autonomously induces multiple ventral cell types. Nat. Neurosci. 3, 41–46.
Ruiz, I. A. A., Palma, V., and Dahmane, N. (2002) Hedgehog-Gli signalling and the growth of the brain. Nat. Rev. Neurosci. 3, 24–33.
Roelink, H. (1996) Tripartite signaling of pattern: interactions between Hedgehogs, BMPs and Wnts in the control of vertebrate development. Curr. Opin. Neurobiol. 6, 33–40.
Hirsinger, E., Duprez, D., Jouve, C., Malapert, P., Cooke, J., and Pourquie, O. (1997) Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. Development 124, 4605–4614.
Lumsden, A. and Krumlauf, R. (1996) Patterning the vertebrate neuraxis. Science 274, 1109–1115.
Toresson, H., Mata de Urquiza, A., Fagerstrom, C., Perlmann, T., and Campbell, K. (1999) Retinoids are produced by glia in the lateral ganglionic eminence and regulate striatal neuron differentiation. Development 126, 1317–1326.
Pierani, A., Brenner-Morton, S., Chiang, C., and Jessell, T. M. (1999) A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97, 903–915.
Williams, B. P., Park, J. K., Alberta, J. A., et al. (1997) A PDGF-regulated immediate early gene response initiates neuronal differentiation in ventricular zone progenitor cells. Neuron 18, 553–562.
Park, J. K., Williams, B. P., Alberta, J. A., and Stiles, C. D. (1999) Bipotent cortical progenitor cells process conflicting cues for neurons and glia in a hierarchical manner. J. Neurosci. 19, 10383–10389.
Dihne, M., Bernreuther, C., Sibbe, M., Paulus, W., and Schachner, M. (2003) A new role for the cell adhesion molecule L1 in neural precursor cell proliferation, differentiation, and transmitter-specific subtype generation. J. Neurosci. 23, 6638–6650.
Cheng, A., Wang, S., Cai, J., Rao, M. S., and Mattson, M. P. (2003) Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev. Biol. 258, 319–333.
Sun, Y. E., Martinowich, K., and Ge, W. (2003) Making and repairing the mammalian brain—signaling toward neurogenesis and gliogenesis. Semin. Cell Dev. Biol. 14, 161–168.
Temple, S. and Qian, X. (1996) Vertebrate neural progenitor cells: subtypes and regulation. Curr. Opin. Neurobiol. 6, 11–17.
Mabie, P. C., Mehler, M. F., Marmur, R., Papavasiliou, A., Song, Q., and Kessler, J. A. (1997) Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J. Neurosci. 17, 4112–4120.
Gomes, W. A., Mehler, M. F., and Kessler, J. A. (2003) Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev. Biol. 255, 164–177.
McKay, R. (1997) Stem cells in the central nervous system. Science 276, 66–71.
Koblar, S. A., Turnley, A. M., Classon, B. J., et al. (1998) Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor. Proc. Natl. Acad. Sci. USA 95, 3178–3181.
Nakashima, K., Yanagisawa, M., Arakawa, H., et al. (1999) Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284, 479–482.
Hojo, M., Ohtsuka, T., Hashimoto, N., Gradwohl, G., Guillemot, F., and Kageyama, R. (2000) Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development 127, 2515–2522.
Tanigaki, K., Nogaki, F., Takahashi, J., Tashiro, K., Kurooka, H., and Honjo, T. (2001) Notch 1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate. Neuron 29, 45–55.
Vallejo, I. and Vallejo, M. (2002) Pituitary adenylate cyclase-activating polypeptide induces astrocyte differentiation of precursor cells from developing cerebral cortex. Mol. Cell Neurosci. 21, 671–683.
Canoll, P. D., Musacchio, J. M., Hardy, R., Reynolds, R., Marchionni, M. A., and Salzer, J. L. (1996) GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17, 229–243.
Qi, Y., Stapp, D., and Qiu, M. (2002) Origin and molecular specification of oligodendrocytes in the telencephalon. Trends Neurosci. 25, 223–225.
Rogister, B., Ben-Hur, T., and Dubois-Dalcq, M. (1999) From neural stem cells to myelinating oligodendrocytes. Mol. Cell Neurosci. 14, 287–300.
Nery, S., Wichterle, H., and Fishell, G. (2001) Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128, 527–540.
Murray, K., Calaora, V., Rottkamp, C., Guicherit, O., and Dubois-Dalcq, M. (2002) Sonic hedgehog is a potent inducer of rat oligodendrocyte development from cortical precursors in vitro. Mol. Cell. Neurosci. 19, 320–332.
Orentas, D. M. and Miller, R. H. (1996) The origin of spinal cord oligodendrocytes is dependent on local influences from the notochord. Dev. Biol. 177, 43–53.
Pringle, N. P., Yu, W. P., Guthrie, S., et al. (1996) Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and sonic hedgehog. Dev. Biol. 177, 30–42.
Chandran, S., Kato, H., Gerreli, D., Compston, A., Svendsen, C. N., and Allen, N. D. (2003) FGF-dependent generation of oligodendrocytes by a hedgehog-independent pathway. Development 130, 6599–6609.
Mekki-Dauriac, S., Agius, E., Kan, P., and Cochard, P. (2002) Bone morphogenetic proteins negatively control oligodendrocyte precursor specification in the chick spinal cord. Development 129, 5117–5130.
Akazawa, C., Sasai, Y., Nakanishi, S., and Kageyama, R. (1992) Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. J. Biol. Chem. 267, 21879–21885.
Sasai, Y., Kageyama, R., Tagawa, Y., Shigemoto, R., and Nakanishi, S. (1992) Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 6, 2620–2634.
Blokzijl, A., Dahlqvist, C., Reissmann, E., et al. (2003) Cross-talk between the Notch and TGF-β signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J. Cell. Biol. 163, 723–728.
Ross, D. A. and Kadesch, T. (2001) The notch intracellular domain can function as a coactivator for LEF-1. Mol. Cell Biol. 21, 7537–7544.
Wu, Y., Liu, Y., Levine, E. M., and Rao, M. S. (2003) Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors. Dev. Dyn. 226, 675–689.
Ishibashi, M., Moriyoshi, K., Sasai, Y., Shiota, K., Nakanishi, S., and Kageyama, R. (1994) Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J. 13, 1799–1805.
Ishibashi, M., Ang, S. L., Shiota, K., Nakanishi, S., Kageyama, R., and Guillemot, F. (1995) Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 9, 3136–3148.
Ohtsuka, T., Sakamoto, M., Guillemot, F., and Kageyama, R. (2001) Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain. J. Biol. Chem. 276, 30467–30474.
Nakamura, Y., Sakakibara, S., Miyata, T., et al. (2000) The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. J. Neurosci. 20, 283–293.
Gratton, M. O., Torban, E., Jasmin, S. B., Theriault, F. M., German, M. S., and Stifani, S. (2003) Hes6 promotes cortical neurogenesis and inhibits Hes1 transcription repression activity by multiple mechanisms. Mol. Cell Biol. 23, 6922–6935.
Norton, J. D., Deed, R. W., Craggs, G., and Sablitzky, F. (1998) Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 8, 58–65.
Norton, J. D. (2000) ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J. Cell Sci. 113(Pt 22), 3897–3905.
Toma, J. G., El-Bizri, H., Barnabe-Heider, F., Aloyz, R., and Miller, F. D. (2000) Evidence that helix-loop-helix proteins collaborate with retinoblastoma tumor suppressor protein to regulate cortical neurogenesis. J. Neurosci. 20, 7648–7656.
Jen, Y., Manova, K., and Benezra, R. (1997) Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev. Dyn. 208, 92–106.
Riechmann, V. and Sablitzky, F. (1995) Mutually exclusive expression of two dominant-negative helix-loop-helix (dnHLH) genes, Id4 and Id3, in the developing brain of the mouse suggests distinct regulatory roles of these dnHLH proteins during cellular proliferation and differentiation of the nervous system. Cell Growth Differ. 6, 837–843.
Lyden, D., Young, A. Z., Zagzag, D., et al. (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401, 670–677.
Hinck, L., Nathke, I. S., Papkoff, J., and Nelson, W. J. (1994) Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly. J. CellBiol. 125, 1327–1340.
Nathke, I. S., Hinck, L., Swedlow, J. R., Papkoff, J., and Nelson, W. J. (1994) Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells. J. Cell Biol. 125, 1341–1352.
Kikuchi, A. (2000) Regulation of beta-catenin signaling in the Wnt pathway. Biochem. Biophys. Res. Commun. 268, 243–248.
Chenn, A. and Walsh, C. A. (2003) Increased neuronal production, enlarged forebrains and cytoarchitectural distortions in beta-catenin overexpressing transgenic mice. Cereb. Cortex 13, 599–606.
Sommer, L., Ma, Q., and Anderson, D. J. (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.
Lo, L. C., Johnson, J. E., Wuenschell, C. W., Saito, T., and Anderson, D. J. (1991) Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev. 5, 1524–1537.
Guillemot, F., Lo, L. C., Johnson, J. E., Auerbach, A., Anderson, D. J., and Joyner, A. L. (1993) Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463–476.
Nieto, M., Schuurmans, C., Britz, O., and Guillemot, F. (2001) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29, 401–413.
Ross, S. E., Greenberg, M. E., and Stiles, C. D. (2003) Basic helix-loop-helix factors in cortical development. Neuron 39, 13–25.
Lee, J. K., Cho, J. H., Hwang, W. S., Lee, Y. D., Reu, D. S., and Suh-Kim, H. (2000) Expression of neuroD/BETA2 in mitotic and postmitotic neuronal cells during the development of nervous system. Dev. Dyn. 217, 361–367.
Farah, M. H., Olson, J. M., Sucic, H. B., Hume, R. I., Tapscott, S. J., and Turner, D. L. (2000) Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127, 693–702.
Casarosa, S., Fode, C., and Guillemot, F. (1999) Mash1 regulates neurogenesis in the ventral telencephalon. Development 126, 525–534.
Fode, C., Ma, Q., Casarosa, S., Ang, S. L., Anderson, D. J., and Guillemot, F. (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 14, 67–80.
Chapouton, P., Schuurmans, C., Guillemot, F., and Gotz, M. (2001) The transcription factor neurogenin 2 restricts cell migration from the cortex to the striatum. Development 128, 5149–5159.
Parras, C. M., Schuurmans, C., Scardigli, R., Kim, J., Anderson, D. J., and Guillemot, F. (2002) Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev. 16, 324–338.
Sun, Y., Nadal-Vicens, M., Misono, S., et al. (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104, 365–376.
Lu, Q. R., Yuk, D., Alberta, J. A., et al. (2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317–329.
Takebayashi, H., Yoshida, S., Sugimori, M., et al. (2000) Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech. Dev. 99, 143–148.
Zhou, Q., Wang, S., and Anderson, D. J. (2000) Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25, 331–343.
Zhou, Q. and Anderson, D. J. (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61–73.
Mizuguchi, R., Sugimori, M., Takebayashi, H., et al. (2001) Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31, 757–771.
Novitch, B. G., Chen, A. I., and Jessell, T. M. (2001) Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31, 773–789.
Sakamoto, M., Hirata, H., Ohtsuka, T., Bessho, Y., and Kageyama, R. (2003) The basic helix-loop-helix genes Hesr1/Hey1 and Hesr2/Hey2 regulate maintenance of neural precursor cells in the brain. J. Biol. Chem. 278, 44808–44815.
Tomita, K., Ishibashi, M., Nakahara, K., et al. (1996) Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. Neuron 16, 723–734.
Castella, P., Wagner, J. A., and Caudy, M. (1999) Regulation of hippocampal neuronal differentiation by the basic helix-loop-helix transcription factors HES-1 and MASH-1. J. Neurosci. Res. 56, 229–240.
Furukawa, T., Mukherjee, S., Bao, Z. Z., Morrow, E. M., and Cepko, C. L. (2000) rax, Hes1, and notch 1 promote the formation of Müller glia by postnatal retinal progenitor cells. Neuron 26, 383–394.
Walther, C. and Gruss, P. (1991) Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435–1449.
Gotz, M., Stoykova, A., and Gruss, P. (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031–1044.
Stoykova, A., Gotz, M., Gruss, P., and Price, J. (1997) Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing fore-brain. Development 124, 3765–3777.
Heins, N., Malatesta, P., Cecconi, F., et al. (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5, 308–315.
Scardigli, R., Schuurmans, C., Gradwohl, G., and Guillemot, F. (2001) Crossregulation between Neurogenin2 and pathways specifying neuronal identity in the spinal cord. Neuron 31, 203–217.
Anderson, S. A., Eisenstat, D. D., Shi, L., and Rubenstein, J. L. (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474–476.
Anderson, S. A., Qiu, M., Bulfone, A., et al. (1997) Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19, 27–37.
Stuhmer, T., Anderson, S. A., Ekker, M., and Rubenstein, J. L. (2002) Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression. Development 129, 245–252.
Stuhmer, T., Puelles, L., Ekker, M., and Rubenstein, J. L. (2002) Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb. Cortex 12, 75–85.
Panganiban, G. and Rubenstein, J. L. (2002) Developmental functions of the Distal-less/Dlx homeobox genes. Development 129, 4371–4386.
Allan, D. W. and Thor, S. (2003) Together at last: bHLH and LIM-HD regulators cooperate to specify motor neurons. Neuron 38, 675–677.
Lee, S. K. and Pfaff, S. L. (2003) Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 38, 731–745.
Sun, T., Dong, H., Wu, L., Kane, M., Rowitch, D. H., and Stiles, C. D. (2003) Cross-repressive interaction of the Olig2 and Nkx2.2 transcription factors in developing neural tube associated with formation of a specific physical complex. J. Neurosci. 23, 9547–9556.
Hardcastle, Z. and Papalopulu, N. (2000) Distinct effects of XBF-1 in regulating the cell cycle inhibitor p27(XIC1) and imparting a neural fate. Development 127, 1303–1314.
Dou, C. L., Li, S., and Lai, E. (1999) Dual role of brain factor-1 in regulating growth and patterning of the cerebral hemispheres. Cereb. Cortex 9, 543–550.
Heins, N., Cremisi, F., Malatesta, P., et al. (2001) Emx2 promotes symmetric cell divisions and a multipotential fate in precursors from the cerebral cortex. Mol. Cell Neurosci. 18, 485–502.
Estivill-Torrus, G., Pearson, H., van Heyningen, V., Price, D. J., and Rashbass, P. (2002) Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development 129, 455–466.
Loosli, F., Winkler, S., Burgtorf, C., et al. (2001) Medaka eyeless is the key factor linking retinal determination and eye growth. Development 128, 4035–4044.
Andreazzoli, M., Gestri, G., Angeloni, D., Menna, E., and Barsacchi, G. (1999) Role of Xrx1 in Xenopus eye and anterior brain development. Development 126, 2451–2460.
Carl, M., Loosli, F., and Wittbrodt, J. (2002) Six3 inactivation reveals its essential role for the formation and patterning of the vertebrate eye. Development 129, 4057–4063.
Zuber, M. E., Perron, M., Philpott, A., Bang, A., and Harris, W. A. (1999) Giant eyes in Xenopus laevis by overexpression of XOptx2. Cell 98, 341–352.
Zezula, J., Casaccia-Bonnefil, P., Ezhevsky, S. A., et al. (2001) p21cip1 is required for the differentiation of oligodendrocytes independently of cell cycle withdrawal. EMBO Rep. 2, 27–34.
Murciano, A., Zamora, J., Lopez-Sanchez, J., and Frade, J. M. (2002) Interkinetic nuclear movement may provide spatial clues to the regulation of neurogenesis. Mol. Cell Neurosci. 21, 285–300.
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Jalali, A., Bonaguidi, M., Hamill, C., Kessler, J.A. (2006). Multipotent Stem Cells in the Embryonic Nervous System. In: Rao, M.S. (eds) Neural Development and Stem Cells. Contemporary Neuroscience. Humana Press. https://doi.org/10.1385/1-59259-914-1:067
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