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Multipotent Stem Cells in the Embryonic Nervous System

  • Chapter
Stem Cells and CNS Development

Part of the book series: Contemporary Neuroscience ((CNEURO))

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Abstract

Neural stem cells are defined by a number of properties, including their ability to proliferate, to maintain themselves (self-renew), to retain multilineage potential over time, and to generate large numbers of progeny, often through transient amplification of intermediate progenitor pools. 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 in many organ systems. Cells that do not self-renew 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 (see Chapters 5 and 6; 1).

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References

  1. Rao, M. S. (1999) Multipotent and restricted precursors in the central nervous system. Anat. Rec. 257, 137–148.

    Article  PubMed  CAS  Google Scholar 

  2. Rakic, P. (1995) Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc. Nat. Acad. Sci. USA 92, 11323–11327.

    Article  PubMed  CAS  Google Scholar 

  3. Rakic, P. (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 8, 383–388.

    Article  Google Scholar 

  4. Caviness, V. S. Jr., and Takahashi, T. (1995) Proliferative events in the cerebral ventricular zone. Brain Dev. 17, 159–163.

    Article  PubMed  Google Scholar 

  5. Chenn, A. and McConnell, S. K. (1995) Cleavage orientation and the asymmetric inheritance of Notch 1 immunoreactivity in mammalian neurogenesis. Cell 82, 631–641.

    Article  PubMed  CAS  Google Scholar 

  6. Qian, X., Goderie, S., Shen, Q., Stern, J., and Temple, S. (1998) Intrinsic programs of patterned cell lineage in isolated vertebrate CNS ventricular zone cells. Development 125, 3143–3152.

    PubMed  CAS  Google Scholar 

  7. Spana, E. P., Kopczynski, C., Goodman, C. S., and Doe, C. Q. (1995) Asymmetric localization of Numb autonomously determines sibling neuron identity in Drosophila CNS Development 121, 3489–3494.

    CAS  Google Scholar 

  8. Jan, Y. N. and Jan, L. Y. (1999) Asymmetry across species Nature Cell Biol. 1, E42–44.

    Article  PubMed  CAS  Google Scholar 

  9. Jan, Y. N. and Jan, L. Y. (1998) Asymmetric cell division. Nature 392, 775–778.

    Article  PubMed  CAS  Google Scholar 

  10. Wakamatsu, Y., Maynard, T. M., Jones, S. U., and Weston, J. A. (1999) NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1 Neuron 23, 71–81.

    Article  PubMed  CAS  Google Scholar 

  11. 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.

    PubMed  CAS  Google Scholar 

  12. Weiss, S., Reynolds, B. A., Vescovi, A., 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.

    Article  PubMed  CAS  Google Scholar 

  13. Johe, K. K., Hazel, T. G., Muller, T., Dugich-Djordjevic, M., and McKay, R. (1996) Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dey. 10, 3129–3140.

    Article  CAS  Google Scholar 

  14. Qian, X., Davis, A. D., 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.

    Article  PubMed  CAS  Google Scholar 

  15. 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.

    PubMed  CAS  Google Scholar 

  16. 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.

    Article  Google Scholar 

  17. Temple, S. (1989) Division and differentiation of isolated CNS blast cells in microculture Nature 340, 471–473.

    Article  PubMed  CAS  Google Scholar 

  18. Sakakibara, S., Imai, T., Hamaguchi, K., Okabe, M., Aruga, J., Nakajima, K., et al. (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dey. Biol. 176, 230–242.

    Article  CAS  Google Scholar 

  19. 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.

    PubMed  CAS  Google Scholar 

  20. 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.

    PubMed  CAS  Google Scholar 

  21. 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.

    Article  PubMed  CAS  Google Scholar 

  22. 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 it ligand, transforming growth factor alpha, in the rat brain J. Comp. Neurol 380, 243–261.

    Article  PubMed  CAS  Google Scholar 

  23. Threadgil, D. W., Flugosz, A. A., Hansen, A. A., Tennenbaum, T., Lichti, U., Yee, D., et al. (1995) Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269, 230–234.

    Article  Google Scholar 

  24. Kornblum, H. I., Hussain, R., Wiesen, J., Miettinen, P., Zurcher, S. D., Chow, K., Derynck, R., and Werb, Z. (1998) Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor J Neurosci Res 53, 697–717.

    Article  PubMed  CAS  Google Scholar 

  25. V, V., and van der Kooy, D. (2000) Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebraion germinal zone. J. Neurosci. 20, 1085–1095.

    Google Scholar 

  26. 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.

    Article  PubMed  CAS  Google Scholar 

  27. Vaccarino, F. M., Schwartz, M. L., Raballo, R., Nilsen, J., Rhee, J., Zhou, M., et al. (1999) Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nature Neurosci. 2, 246–253.

    Article  PubMed  CAS  Google Scholar 

  28. Tao, Y., Black, I. B., and DiCicco-Bloom, E. (1997) In vivo neurogenesis is prevented by neutralizing antibodies to basic fibroblast growth factor. J. Neurobiol. 33, 289–296.

    Article  PubMed  CAS  Google Scholar 

  29. 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.

    Article  Google Scholar 

  30. Emoto, N., Gonzales, A. M., Walicke, P. A., Wada, E., Simmons, D. M., Shimasaki, S., and Baird, A. (1989) Basic fibroblast growth factor in the central nervous system: identification of specific loci of basic FGF expression in the rat brain. Growth Factors 2, 21–29.

    Article  PubMed  CAS  Google Scholar 

  31. Nurcombe, V., Ford, M. D., Wildchut, J. A., and Bartlett, P. F. (1993) Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science 260, 103–106.

    Article  PubMed  CAS  Google Scholar 

  32. Goodrich, L. V. and Scott, M. P. (1998) Hedgehog and patched in neural development and disease. Neuron 21, 1243–1257.

    Article  PubMed  CAS  Google Scholar 

  33. 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.

    PubMed  CAS  Google Scholar 

  34. 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.

    Article  PubMed  CAS  Google Scholar 

  35. Wechsler-Reya, R. J. and Scott, M. P. (1999) Control of neuronal precursor proliferation in the cerebellum by sonic Hedgehog. Neuron 22, 103–114.

    Article  PubMed  CAS  Google Scholar 

  36. 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.

    PubMed  CAS  Google Scholar 

  37. McMahon, A. P. (2000) More surprises in the hedgehog signaling pathway. Cell 100, 185–188.

    Article  PubMed  CAS  Google Scholar 

  38. Gressens, P., Hill, J. M., Paindaveine, B., Gozes, I., Fridkin, M., and Brenneman, D. E. (1994) Severe microcephaly induced by blockade of vaso-active intestinal peptide function in the primitive neuroepithelium of the mouse. J. Clin. Invest. 94, 2020–2027.

    Article  PubMed  CAS  Google Scholar 

  39. Ikeya, M., Lee, S. M., Johnson, S. E., McMahon, A. P., and Takada, S. (1997) Wnt signaling required for expansion of neural crest and CNS progenitors. Nature 389, 966–970.

    Article  PubMed  CAS  Google Scholar 

  40. 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.

    Article  PubMed  CAS  Google Scholar 

  41. Ghosh, A. and Greenberg, M. E. (1995) Distinct role for bFGF and NT3 in the regulation of cortical neurogenesis. Neuron 15, 249–252.

    Article  Google Scholar 

  42. 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.

    Article  PubMed  CAS  Google Scholar 

  43. LoTurco, J. J., Owens, D. F., Heath, M. J. S., Davis, M., and Kriegstein, A. R. (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287–1298.

    Article  PubMed  CAS  Google Scholar 

  44. Lu, N. and DiCicco-Bloom, E. (1997) Pituitary adenylate cyclase-activating polypeptide is an autocrine inhibitor of mitosis in cultured cortical precursor cells. Proc. Natl. Acad. Sci USA 94, 3357–3362.

    Article  PubMed  CAS  Google Scholar 

  45. Blaschke, A. J., Staley, K., and Chun, J. (1996) Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development 122, 1165–1174.

    PubMed  CAS  Google Scholar 

  46. 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. Cerebral Cortex 9, 621–626.

    Article  PubMed  CAS  Google Scholar 

  47. Graham, A. and Lumsden, A. (1996) Patterning the cranial neural crest. Biochem. Soc. Symp. 62, 77–83.

    PubMed  CAS  Google Scholar 

  48. Furuta, Y., Piston, D. W., and Hogan, B. L. (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124, 2203–2212.

    PubMed  CAS  Google Scholar 

  49. 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.

    Google Scholar 

  50. 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.

    Article  PubMed  CAS  Google Scholar 

  51. Zhu, G., Mehler, M. F., Mabie, P. C., and Kessler, J. A. (1999) Developmental changes in progenitor cells responsiveness to cytokines J. Neurosci. Res. 56, 131–145.

    Article  PubMed  CAS  Google Scholar 

  52. Molne, M., Studer, L., Tabar, L., Ting, Y., Eiden, M., and McKay, R. (2000) Early cortical precursors do not undergo LIF-mediated astrocytic differentiation. J. Neurosci. Res. 59, 301–311.

    Article  PubMed  CAS  Google Scholar 

  53. Austin, C. P., Feldman, D. E., Ida, J. A., and Cepko, C. L. (1995) Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121, 3637–3650.

    PubMed  CAS  Google Scholar 

  54. 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.

    Article  PubMed  CAS  Google Scholar 

  55. 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.

    Article  PubMed  CAS  Google Scholar 

  56. Wang, S., Sdrulla, A. D., diSibio, G., Bush, G., Nofziger, D., Hicks, C., Weinmaster, G., and Barres, B. A. (1998) Notch receptor activation inhibits oligodendroglial differentiation. Neuron 21, 63–75.

    Article  PubMed  Google Scholar 

  57. Galano, N., Nye, J. S., and Fishell, G. (2000) Radial glial identity is promoted by Notch] signaling in the murine forebrain. Neuron 26, 395–404.

    Article  Google Scholar 

  58. Akazawa, C., Sasai, Y., Nakanishi, S., and Kageyama, R. (1992) Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominately expressed in the developing system. J. Biol. Chem. 267, 21879–21885.

    Google Scholar 

  59. Sasai, Y., Kageyama, R., Tagawa, Y., Shigemoto, R., and Nakanishi, S. (1992) Two mammolian helix-loop-helix factors structurally related to Drosophilia hairy and enhancor of split. Gene Dey. 6, 2620–2634.

    Article  CAS  Google Scholar 

  60. Nakamura, Y., Sakakibara, S., Miyata, T., Ogawa, M., Shimazaki, T., Weiss, S., Kageyama, R., and Okana, H. (2000) The bHLH gene hesl as a repressor of the neuronal commitment of CNS stem cells. J. Neurosci. 20, 283–293.

    PubMed  CAS  Google Scholar 

  61. 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.

    PubMed  CAS  Google Scholar 

  62. Ishibashi, M., Siew-Lan, A., Shiota, K., Nakanishi, S., Kagyeyama, R., and Guillemot, F. (1995) Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to upregulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects Genes Dey. 9, 3136–3148.

    Article  CAS  Google Scholar 

  63. Norton, J. D., Deed, R. W., Craggs, G., and Sablitzky, F. (1998) ID helixloop-helix proteins in cell growth and differentiation. Trends Cell Biol. 8, 58–65.

    PubMed  CAS  Google Scholar 

  64. 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. Dey. Dyn. 208, 92–106.

    Article  CAS  Google Scholar 

  65. 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.

    PubMed  CAS  Google Scholar 

  66. Lyden, D., Young, A. Z., Zagzag, D., Yan, W., Gerald, W., O’Reilly, R., Bader, B. L., Hynes, R. O., Zhuang, Y., Manova, K., and Benezra, R. (1999) ID1 and ID3 are required for neurogenesis, angiogenesis and vascularization of tumor xenografts. Nature 401, 670–677.

    Article  PubMed  CAS  Google Scholar 

  67. Sasai, Y. (1998) Identifying the missing links: genes that connect neural induction and primary neurogenesis in vertebrate embryos. Neuron 21, 455–458.

    Article  PubMed  CAS  Google Scholar 

  68. Weinstein, D. C. and Hemmati-Brivanlou, A. (1999) Neural induction. Annu. Rev. Cell Dey. Biol. 15, 411–433.

    Article  CAS  Google Scholar 

  69. Lee, J. E. (1997) Basic helix-loop-helix genes in neural development. Curr. Opin. Neurobiol. 7, 13–20.

    Article  PubMed  Google Scholar 

  70. Kageyama, R. and Nakanishi, S. (1997) Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr. Opin. Genes Dey. 7, 659–665.

    Article  CAS  Google Scholar 

  71. Bellefroid, E. J., Bourguignon, C., Hollemann, T., Ma, Q., Anderson, D. J., Kinter, C., and Pieler, T. (1996) X-MyT1, a Xenopus C2HC-type zinc finger protein with a regulatory function in neuronal differentiation. Cell 87, 1191–1202.

    Article  PubMed  CAS  Google Scholar 

  72. Morin, X., Cremer, H., Hirsch, M. R., Kapur, R. P., Goridis, C., and Brunet, J. F. (1997) Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a Neuron 18, 411–423.

    Article  PubMed  CAS  Google Scholar 

  73. Hirsch, M. R., Tiveron, M. C., Guillemot, F., Brunet, J. F., and Goridis, C. (1998) Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 125, 599–608.

    PubMed  CAS  Google Scholar 

  74. 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.

    Article  PubMed  CAS  Google Scholar 

  75. 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.

    PubMed  CAS  Google Scholar 

  76. Bartlett, P. F., Brooker, G. J., Faux, C. H., Dutton, R., Murphy, M., Turnley, A., and Kilpatrick, T. J. (1998) Regulation of neural stem cell differentiation in the forebrain Immunol. Cell. Biol. 76, 414–418.

    Article  PubMed  CAS  Google Scholar 

  77. 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.

    Article  PubMed  CAS  Google Scholar 

  78. Orentas, D. M. and Miller, R. H. (1996) The origin of spinal cord oligodendrocytes is dependent on local influences from the notocord. Dev. Biol. 177, 45–53.

    Article  Google Scholar 

  79. Pringle, N. P., Yu, W. P., Guthrie, S., Roelink, H., Lumsden, A., Peterson, A. C., and Richardson, W. D. (1996) Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and sonic hedgehog. Dev. Biol. 177, 30–42.

    Article  PubMed  CAS  Google Scholar 

  80. Hynes, M., Ye, W., Wang, K., Stone, D., Murone, M., Sauvage, F. D., and Rosenthal, A. (2000) The seven-transmembrane receptor smoothened cell-autonomously induces multiple ventral cell types. Nature Neurosci. 3, 41–46.

    Article  PubMed  CAS  Google Scholar 

  81. Briscoe, J., Sussel, L., Serup, P., Hartigan-O’Conner D., Jessell, T. M., Rubenstein, J. L., and Ericson, J. (1999) Homeobox gene Nkx2.2 and specification of neuronal identity by graded sonic hedgehog signaling. Nature 398, 622–627.

    Article  PubMed  CAS  Google Scholar 

  82. 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.

    Article  PubMed  CAS  Google Scholar 

  83. Hirsinger, E., Duprez, D., JOuve, C., Malapert, P., Cooke, J., and Pourquie, O. (1997) Noggin acts downstream of Wnt and sonic hedgehog to antagonize BMPU in avian somite patterning. Development 124, 4605–4614.

    PubMed  CAS  Google Scholar 

  84. Verdi, J. M., Bashirullah, A., Goldhawk, D. E., Kubu, C. J., Jamali, M., Meakin, S. O., and Lipshitz, H. D. (1999) Distinct human NUMB isoforms regulate differentiation vs. proliferation in the neuronal lineage. Proc. Natl. Acad. Sci. USA 96, 10472–10476.

    Article  PubMed  CAS  Google Scholar 

  85. Guo, S., Brush, J., Teraoka, H., Goddard, A., Wilson, S. W., Mullins, M. C., and Rosenthal, A. (1999) Development of noradrenergic neurons in the zebrafish hindbrain requires BMP, FGF8, and the homeodomain protein soulless/Phox2a. Neuron 24, 555–566.

    Article  PubMed  CAS  Google Scholar 

  86. Alder, J., Lee, K. J., Jessell, T. M., and Hatten, M. E. (1999) Generation of cerebellar granule neurons in vivo by transplantation of BMP-treated neural progenitor cells. Nature Neurosci. 2, 535–540.

    Article  PubMed  CAS  Google Scholar 

  87. Lumsden, A. and Krumlauf, R. (1996) Patterning the vertebrate neuraxis. Science 274, 1109–1115.

    Article  PubMed  CAS  Google Scholar 

  88. Toresson, H., Mata de Urqiza, 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.

    PubMed  CAS  Google Scholar 

  89. 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.

    Article  PubMed  CAS  Google Scholar 

  90. Cameron, H. A., Hazel, T. G., and McKay, R. (1998) Regulation of neuro-genesis by growth factors and neurotransmitters. J. Neurobiol. 36, 287–306.

    Article  PubMed  CAS  Google Scholar 

  91. Temple, S. and Qian, X. (1996) Vertebrate neural progenitor cells: subtypes and regulation. Curr. Opin. Neurobiol. 6, 11–17.

    Article  PubMed  CAS  Google Scholar 

  92. Mabie, P. C., Mehler, M. F., 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.

    CAS  Google Scholar 

  93. McKay, R. (1997) Stem cells in the central nervous system. Science 276, 66–71.

    Article  PubMed  CAS  Google Scholar 

  94. Koblar, S. A., Turnley, A. M., Classon, B. J., Reid, K. L., Ware, C. B., Cheema, S. S., Murphy, M., and Bartlett, P. F. (1998) Neural precursor differentiation into astrocytes requires signaling through leukemia inhibitory factor receptor. Proc. Natl. Acad. Sci. USA 95, 3178–3181.

    Article  PubMed  CAS  Google Scholar 

  95. Nakashima, K., Yanagisawa, M., Arakawa, H., Kimura, N., Hisatsune, T., Kawabata, M., Miyazono, K., and Taga, T. (1999) Synergistic signaling in fetal brain by STAT3-Smadl complex bridged by p300. Science 16, 479–482.

    Article  Google Scholar 

  96. Rogister, B., Ben-Hur, T., and Dubois-Dalcq, M. (1999) From neural stem cells to myelinating oligodendrocytes. Mol. Cell. Neurosci. 14, 287–300.

    Article  PubMed  CAS  Google Scholar 

  97. Vartanian, T., Fischbach, G., and Miller, R. H. (1999) Failure of spinal cord oligodendrocyte development in mice lacking neuregulin. Proc. Natl. Acad. Sci. USA 96, 731–735.

    Article  PubMed  CAS  Google Scholar 

  98. Luskin, M. B., Pearlman, A. L., and Sanes, J. R. (1988) Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1, 635–647.

    Article  PubMed  CAS  Google Scholar 

  99. Price, J. and Thurlow, L. (1988) Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development 104, 473–482.

    PubMed  CAS  Google Scholar 

  100. Walsh, C. and Cepko, C. L. (1988) Clonally related cortical cells show several migration patterns. Science 241, 1342–1345.

    Article  PubMed  CAS  Google Scholar 

  101. Parnavelas, J. G., Barfield, J. A., Franke, E., and Luskin, M. B. (1991) Separate progenitor cells give rise to pyramidal and nonpyramidal neurons in the rat telencephalon. Cerebral Cortex 1, 463–468.

    Article  PubMed  CAS  Google Scholar 

  102. Walsh, C. and Cepko, C. (1992) Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science 255, 434–440.

    Article  PubMed  CAS  Google Scholar 

  103. Reid, C. B., Liang, I., and Walsh, C. (1995) Systematic widespread clonal organization in cerebral cortex. Neuron 15, 299–310.

    Article  PubMed  CAS  Google Scholar 

  104. Davis, A. A. and Temple, S. (1994) A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372, 263–266.

    Article  PubMed  CAS  Google Scholar 

  105. Williams, B. P. and Price, J. (1995) Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron 14, 1181–1188.

    Article  PubMed  CAS  Google Scholar 

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Authors
  1. John A. Kessler
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  2. Mark F. Mehler
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  3. Peter C. Mabie
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Editor information

Editors and Affiliations

  1. Department of Neurobiology and Anatomy, University of Utah Medical School, Salt Lake City, UT, USA

    Mahendra S. Rao

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© 2001 Springer Science+Business Media New York

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Kessler, J.A., Mehler, M.F., Mabie, P.C. (2001). Multipotent Stem Cells in the Embryonic Nervous System. In: Rao, M.S. (eds) Stem Cells and CNS Development. Contemporary Neuroscience. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-59259-107-7_2

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  • DOI: https://doi.org/10.1007/978-1-59259-107-7_2

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-61737-237-7

  • Online ISBN: 978-1-59259-107-7

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