Advertisement

Mechanisms Regulating Lineage Diversity During Mammalian Cerebral Cortical Neurogenesis and Gliogenesis

  • Mark F. Mehler
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 39)

Summary

During mammalian cerebral cortical development, neural stem cells (NSCs) present within periventricular generative zones give rise to successive waves of neurons and radial glia, followed by oligodendrocytes and astrocytes. The molecular and cellular mechanisms that orchestrate these precisely timed and progressive maturational events are still largely undefined. These developmental processes are likely to involve the dynamic interplay of environmental signals, cell-cell interactions and transcriptional regulatory events. The bone morphogenetic proteins (BMPs), an expanding subclass of the transforming growth factor β cytokine superfamily, may represent an important set of environmental cues for these progressive maturational events because of the broad profiles of developmental expression of the requisite BMP ligands, receptor subunits and intracellular transduction elements, and because of their versatile roles in promoting a spectrum of cellular processes intimately involved in progressive neural fate decisions. The BMPs also interact with complementary regional environmental signals such as the basic fibroblast growth factor (bFGF) and sonic hedgehog (Shh) that promote earlier stages of NSC expansion, self-renewal, lineage restriction and incipient lineage commitment. The ability of these cytokines and trophic signals to act within specific neurodevelopmental contexts may, in turn, depend on the composite actions of cell-cell contact-associated signals, such as Notch-Hes-mediated lateral inhibitory pathways, and additional transcriptional modulatory events, such as those mediated by members of the inhibitor of differentiation (ID) gene family that encode a novel set of negative basic helix-loop-helix (bHLH) transcription factors. In this chapter, we will examine the distinct roles of these different classes of developmental cues in defining the biological properties of an integrated cerebral cortical developmental signaling network. Ongoing studies in this exciting area of mammalian central nervous system (CNS) development will help to identify important molecular and cellular targets for evolving pharmacological, gene and stem cell therapeutic interventions to combat the pathological sequelae of a spectrum of acquired and genetic disorders of the central nervous system.

Keywords

Bone Morphogenetic Protein Radial Glia Bone Morphogenetic Protein Signaling bHLH Protein bHLH Gene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ahmed S, Reynolds BA, Weiss S (1995) BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J Neurosci 15:5765–5778PubMedGoogle Scholar
  2. Andres-Barquin P, Hernandez MC, Israel MA (1998) Injury selectively down-regulates the gene encoding for the Id4 transcription factor in primary cultures of forebrain astrocytes. NeuroReport 9:4075–4080PubMedCrossRefGoogle Scholar
  3. Andres-Barquin PJ, Hernandez MC, Israel MA (1999) Id4 Expression induces apoptosis in astrocytic cultures and is down-regulated by activation of the cAMP-dependent signal transduction pathway. Exp Cell Res 247:347–355PubMedCrossRefGoogle Scholar
  4. Bae S, Bessho Y, Hojo M, Kageyama R (2000) The bHLH gene Hes6, an inhibitor of Hes1, promotes neuronal differentiation. Development 127:2933–2943PubMedGoogle Scholar
  5. Bansal R, Warrington AE, Gard AL, Ranscht B, Pfeiffer SE (1989) Multiple and novel specificities of monoclonal antibodies 01, 04 and R mAb used in the analysis of oligodendrocyte development. J Neurosci Res 24:248–257CrossRefGoogle Scholar
  6. Bongarzone ER, Byravan S, Givogri MI, Schonmann V, Campagnoni AT (2000) Platelet-derived growth factor and basic fibroblast growth factor regulate cell proliferation and the expression of notch-1 receptor in a new oligodendrocyte cell line. J Neurosci Res 62:319–328PubMedCrossRefGoogle Scholar
  7. Bounpheng MA, Dimas JJ, Dodds SG, Christy BA (1999) Degradation of Id proteins by the ubiquitin-proteasome pathway. FASEB J 13:2257–2264PubMedGoogle Scholar
  8. Bounpheng MA, Melnikova IN, Dimas JJ, Cristy BA (1999) Identification of a novel transcriptional activity of mammalian Id proteins. Nucleic Acids Res 27:1740–1746PubMedCrossRefGoogle Scholar
  9. Briscoe J, Ericson J (1999) The specification of neuronal identity by graded sonic hedgehog signalling. Cell Dev Biol 10:353–362CrossRefGoogle Scholar
  10. Briscoe J, Pierani A, Jessell TM, Ericson J (2000) A homeodomain code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101:435–445PubMedCrossRefGoogle Scholar
  11. Burrows RC, Wancio D, Levitt P, Lillien L (1997) Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19:251–267PubMedCrossRefGoogle Scholar
  12. Cameron RS, Rakic P (1991) Glial cell lineage in the cerebral cortex: a review and synthesis. GLIA 4:124–137PubMedCrossRefGoogle Scholar
  13. Cammer W, Zhang H (1992) Localization of mu class glutathione-S-transferase in the forebrains of neonatal and young rats: implications for astrocyte development. J Comp Neurol 321:33–39PubMedCrossRefGoogle Scholar
  14. Canoll PD, Musacchio JM, Hardy R, Reynolds R, Marchionni MA, Salzer JL (1996) GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17:229–243PubMedCrossRefGoogle Scholar
  15. Canoll PD, Kraemer R, Teng KK, Marchionni MA, Salzer JL (1999) GGF/neuregulin induces a phenotypic reversion of oligodendrocytes. Mol Cell Neurosci 13:79–94PubMedCrossRefGoogle Scholar
  16. Caviness VS Jr, Takahashi T (1995) Proliferative events in the cerebral ventricular zone. Brain Dev 17:159–163PubMedCrossRefGoogle Scholar
  17. Chan SO, Peng D, Chiu FC (1997) Heterogeneous expression of neurofilament proteins in forebrain and cerebellum during development: clinical implications for spinocerebellar ataxia. Brain Res 775:107–118PubMedCrossRefGoogle Scholar
  18. Chanas-Sacre G, Rogister B, Moonen G, Leprince P (2000) Radial glia phenotype: origin, regulation, and transdifferentiation. J Neurosci Res 61:357–363PubMedCrossRefGoogle Scholar
  19. Chiaramello A, Neuman T, Peavy DR, Zuber MX (1996) The GAP-43 gene is a direct downstream target of the basic helix-loop-helix transcription factors. J Biol Chem 271:22035–22043PubMedCrossRefGoogle Scholar
  20. Chiu FC, Feng L, Chan SO, Padin C, Federoff HJ (1995) Expression of neurofilament proteins during retinoic acid-induced differentiation of P19 embryonal carcinoma cells. Mol Brain Res 30:77–86PubMedCrossRefGoogle Scholar
  21. Ciccolini F, Svendsen CN (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 18:7869–7880PubMedGoogle Scholar
  22. Cooper CL, Newburger PE (1998) Differential expression of Id genes in multipotent myeloid progenitor cells: Id-1 is induced by early- and late-acting cytokines while Id-2 is selectively induced by cytokines that drive terminal granulocytic differentiation. J Cell Biochem 71:277–285PubMedCrossRefGoogle Scholar
  23. Culican SM, Baumrind NK, Yamamoto M, Pearlman AL (1990) Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J Neurosci 10:684–692PubMedGoogle Scholar
  24. Deed RW, Jasiok M, Norton JD (1998) Lymphoid-specific expression of the Id3 gene in hematopoietic cells. J Biol Chem 273:8278–8286PubMedCrossRefGoogle Scholar
  25. Ding Q, Fukami SI, Meng X, Nishizaki Y, Zhang X, Sasaki H, Dlugosz A, Nakafuku M, Hui C (1999) Mouse suppressor of fused is a negative regulator of sonic hedgehog signaling and alters the subcellular distribution of Glil. Curr Biol 9:1119–1122PubMedCrossRefGoogle Scholar
  26. 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 97:703–716PubMedCrossRefGoogle Scholar
  27. Drossopoulou G, Lewis KE, Sanz-Ezquerro JJ, Nikbakht N, McMahon AP, Hofmann C, Tickle C (2000) A model for anteroposterior patterning of the vertebrate limb based on sequential long-and short-range Shh signalling and Bmp signalling. Development 127:1337–1348PubMedGoogle Scholar
  28. Ebendal T, Bengtsson H, Soderstrom S (1998) Bone morphogenetic proteins and their receptors: potential functions in the brain. J Neurosci Res 51:139–146PubMedCrossRefGoogle Scholar
  29. Edwards MA, Yamamoto M, Caviness VS (1990) Organization of radial glia and related cells in the developing murine CNS, an analysis based upon a new monoclonal antibody marker. Neuroscience 36:121–144PubMedCrossRefGoogle Scholar
  30. Espinosa A, Zhang M, DeVellis J (1993) O-2A progenitor cells transplanted into the neonatal rat brain develop into oligodendrocytes but not astrocytes. Proc Natl Acad Sci USA 90:50–54CrossRefGoogle Scholar
  31. Feng L, Hatten ME, Heintz N (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12:895–908PubMedCrossRefGoogle Scholar
  32. Feng L, Heintz N (1995) Differentiating neurons activate transcription of the brain lipid-binding protein gene in radial glia through a novel regulatory element. Development 121:1719–1730PubMedGoogle Scholar
  33. Ferrer I, Alcantara S, Ballabriga J, Olive M, Blanco M, Carulla R, Rivera R, Carmona M, Berruezo M, Pitrach S, Planas A (1996) Transforming growth factor α and epidermal growth factor-receptor immunoreactivity in normal and pathological brain. Prog Neurobiol 49:99–123PubMedCrossRefGoogle Scholar
  34. Florio M, Hernandez MC, Yang H, Shu HK, Cleveland JL, Israel MA (1998) Id2 promotes apoptosis by a novel mechanism independent of dimerization to basic helix-loop-helix factors. Mol Cell Biol 18:5435–5444PubMedGoogle Scholar
  35. Franklin RGM, Blakemore WF (1995) Glial-cell transplantation and plasticity in the O-2A lineage — implication for CNS repair. Trends Neurosci 18:151–156PubMedCrossRefGoogle Scholar
  36. Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203–2212PubMedGoogle Scholar
  37. Gage FH, Ray J, Fisher LJ (1995) Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 18:159–192PubMedCrossRefGoogle Scholar
  38. Gaiano N, Nye JS, Fishell G (2000) Radial glial identity is promoted by notch 1 signaling in the murine forebrain. Neuron 26:395–404PubMedCrossRefGoogle Scholar
  39. Ghosh A, Greenberg ME (1995) Distinct role for bFGF and NT3 in the regulation of cortical neurogenesis. Neuron 15:249–252CrossRefGoogle Scholar
  40. Gokhan S, Yung SY, Kessler JA, Mehler MF (2000) Cerebral cortical neurogenesis and gliogenesis require transcriptional activation of inhibitor of differentiation (ID) 2 and 4 in neural stem cells by bone morphogenetic proteins. Ann Neurol 48:415–416Google Scholar
  41. Goldman JE, Zerlin M, Newman S, Zhang L, Gensert J (1997) Fate determination and migration of progenitors in the postnatal mammalian CNS. Dev Neurosci 19:42–48PubMedCrossRefGoogle Scholar
  42. Graham A, Koentges G, Lumsden A (1996) Neural crest apoptosis and the establishment of craniofacial pattern: an honorable death. Mol Cell Neurosci 8:76–83CrossRefGoogle Scholar
  43. Gray GE, Sanes JR (1992) Lineage of radial glia in the chicken optic tectum. Development 114:271–283PubMedGoogle Scholar
  44. Grinspan JB, Reeves MF, Coulaloglou MJ, Nathanson D, Pleasure D (1996) Re-entry into the cell cycle is required for bFGF-induced oligodendroglial dedifferentiation and survival. J Neurosci Res 46:456–464PubMedCrossRefGoogle Scholar
  45. Gross RE, Mehler MF, Mabie PC, Zang Z, Santschi L, Kessler JA (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17:595–606PubMedCrossRefGoogle Scholar
  46. Hammang JP, Archer DR, Duncan ID (1997) Myelination following transplantation of EGF-responsive neural stem cells into a myelin-deficient environment. Exp Neurol 147:84–95PubMedCrossRefGoogle Scholar
  47. Hardy RJ, Friedrich VL Jr (1996) Oligodendrocyte progenitors are generated throughout the embryonic mouse brain, but differentiate in restricted foci. Development 122:2059–2069PubMedGoogle Scholar
  48. Henrique D, Adam J, Myat A, Chitnis A, Lewis J, Ish-Horowicz D (1995) Expression of a delta homologue in prospective neurons in the chick. Nature 375:787–790PubMedCrossRefGoogle Scholar
  49. Hirsinger E, Duprez D, Jouve C, Malapert P, Cooke J, Pourquie O (1997) Noggin acts downstream of Wnt and sonic hedgehog to antagonize BMP4 in avian somite patterning. Development 124:4605–4614PubMedGoogle Scholar
  50. Hogan BL (1996) Bone morphogenetic proteins in development. Curr Opin Genet Develop 6:432–438CrossRefGoogle Scholar
  51. Hu M, Krause D, Greaves M, Sharkis S, Dexter M, Heyworth C, Enver T (1997) Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev 11:774–785PubMedCrossRefGoogle Scholar
  52. Iantosca MR, McPherson CE, Ho S-Y, Maxwell GD (1999) Bone morphogenetic proteins 2 and 4 attenuate apoptosis in a cerebellar primitive neuroectodermal tumor cell line. J Neurosci Res 56:248–258PubMedCrossRefGoogle Scholar
  53. Inoue T, Shoji W, Obinata M (1999) MIDA1, an Id-associating protein, has two distinct DNA binding activities that are converted by the association with Id1: a novel function of Id protein. Biochem Biophys Res Commun 266:147–151PubMedCrossRefGoogle Scholar
  54. Ishibashi M, Moriyoshi K, Sasai Y, Shiota K, Nakanishi S, Kageyama R (1994) Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 13:1799–1805PubMedGoogle Scholar
  55. Ishibashi M, Siew-Lan A, Shiota K, Nakanishi S, Kagyeyama R, 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 Dev 9:3136–3148PubMedCrossRefGoogle Scholar
  56. Jen Y, Manova K, Benezra R (1997) Each member of the ID gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev Dyn 208:92–106PubMedCrossRefGoogle Scholar
  57. Johe KK, Hazel TG, Muller T, Dugich-Djordjevic M, McKay R (1996) Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev 10:3129–3140PubMedCrossRefGoogle Scholar
  58. Kalyani A, Hobson K, Rao MS (1997) Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev Biol 186:202–223PubMedCrossRefGoogle Scholar
  59. 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 kinase-phosphorylated vimentin. GLIA 23:191–199PubMedCrossRefGoogle Scholar
  60. Kawabata M, Miyazono K (1999) Signal transduction of the TGFβ superfamily by Smad proteins. J Biochem 125:9–16PubMedCrossRefGoogle Scholar
  61. Kenney AM, Rowitch DH (2000) Sonic hedgehog promotes G(l) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 20:9055–9067PubMedCrossRefGoogle Scholar
  62. Kilpatrick TJ, Bartlett PF (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 15:3653–3661PubMedGoogle Scholar
  63. Kilpatrick TJ, Richards LJ, Bartlett P (1995) The regulation of neural precursor cells within the mammalian brain. Mol Cell Neurosci 6:2–15PubMedCrossRefGoogle Scholar
  64. Kim Dale J, Vesque C, Lints TJ, Kuber Sampath T, Furley A, Dodd J, Placzek M (1997) Cooperation of BMP7 and SHH in the induction of forebrain ventral midline cells by prechordal mesoderm. Cell 90:257–269CrossRefGoogle Scholar
  65. Koblar SA, Turnley AM, Classon BJ, Reid KL, Ware CB, Cheema SS, Murphy M, Bartlett PF (1998) Neural precursor differentiation into astrocytes requires signaling through leukemia inhibitory factor receptor. Proc Natl Acad Sci USA 95:3178–3181PubMedCrossRefGoogle Scholar
  66. Kondo T, Raff M (2000a) Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289:1754–1757PubMedCrossRefGoogle Scholar
  67. Kondo T, Raff M (2000b) The Id4HLH protein and the timing of oligodendrocyte differentiation. EMBO J 19:1998–2007PubMedCrossRefGoogle Scholar
  68. Kornblum HI, Hussain RJ, Bronstein JM, Gall CM, Lee DC, Seroogy KB (1997) Prenatal ontogeny of the epidermal growth factor receptor and its ligand, transforming growth factor alpha, in the rat brain. J Comp Neurol 380:243–261PubMedCrossRefGoogle Scholar
  69. Kornblum HI, Hussain R, Wiesen HJ, Miettinen P, Zurcher SD, Chow K, Derynck R, Werb Z (1998) Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor. J Neurosci Res 53:697–717PubMedCrossRefGoogle Scholar
  70. Koyano-Nakagawa N, Kim J, Anderson D, Kintner C (2000) Hes6 acts in a positive feedback loop with the neurogenins to promote neuronal differentiation. Development 127:4203–4216PubMedGoogle Scholar
  71. Labbe E, Letamendia A, Attisano L (2000) Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and wnt pathways. Proc Natl Acad Sci USA 97:8358–8363PubMedCrossRefGoogle Scholar
  72. Lasorella A, Iavarone A, Israel MA (1996) Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins. Mol Cell Biol 16:2570–2578PubMedGoogle Scholar
  73. Lasorella A, Noseda M, Beyna M, Iavarone A (2000) Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 407:592–598PubMedCrossRefGoogle Scholar
  74. Lazar LM, Blum M (1992) Regional distribution and developmental expression of epidermal growth factor and transforming growth factor a mRNA in mouse brain by a quantitative nuclease protection assay. J Neurosci 12:1688–1697PubMedGoogle Scholar
  75. Leavitt BR, Hernit-Grant CS, Macklis JD (1999) Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp Neurol 157:43–57PubMedCrossRefGoogle Scholar
  76. Levine JM, Card JP (1987) Light and electron microscopic localization of a cell surface antigen (NG2) in the rat cerebellum: association with smooth and protoplasmic astrocytes. J Neurosci 7:2711–2720PubMedGoogle Scholar
  77. Levine JM, Stallcup WB (1987) Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. J Neurosci 7:2721–2731PubMedGoogle Scholar
  78. Levison SW, Goldman JE (1997) Multipotential and lineage restricted precursors coexist in the mammalian perinatal subventricular zone. J Neurosci Res 48:83–94PubMedCrossRefGoogle Scholar
  79. Li CM, Yan RT, Wang SZ (1999) Misexpression of a bHLH gene, cNSCL1, results in abnormal brain development. Dev Dyn 215:238–247PubMedCrossRefGoogle Scholar
  80. Litingtung Y, Chiang C (2000) Control of Shh activity and signaling in the neural tube. Dev Dyn 219:143–154PubMedCrossRefGoogle Scholar
  81. Liu F, Massague J, Ruiz I, Altaba A (1998) Carboxy-terminally truncated Gli3 proteins associate with Smads. Nat Genet 20:325–326PubMedCrossRefGoogle Scholar
  82. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH (2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25:317–329PubMedCrossRefGoogle Scholar
  83. Lyden D, Young AZ, Zagzag D, Yan W, Gerald WO, Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401:670–677PubMedCrossRefGoogle Scholar
  84. Mabie PC, Mehler MF, Papavasiliou A, Song Q, Kessler JA (1997) Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J Neurosci 17: 4112–4120PubMedGoogle Scholar
  85. Mabie PC, Mehler MF, Kessler JA (1999) Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J Neurosci 19:7077–7088PubMedGoogle Scholar
  86. Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:5253–5263PubMedGoogle Scholar
  87. Mantani A, Hernandez MC, Kuo WL, Israel MA (1998) The mouse Id2 and Id4 genes: structural organization and chromosomal localization. Gene 222:229–235PubMedCrossRefGoogle Scholar
  88. Marcelle C, Stark MR, Bronner-Fraser M (1997) Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124:3955–3963PubMedGoogle Scholar
  89. Marmur R, Kessler JA, Zu G, Gokhan S, Mehler MF (1998a) Differentiation of oligodendroglial progenitors from cortical multipotent cells requires extrinsic signals including activation of gp130/LIFβ receptors. J Neurosci 18:9800–9811PubMedGoogle Scholar
  90. Marmur R, Mabie PC, Gokhan S, Song Q, Kessler JA, Mehler MF (1998b) Isolation and developmental characterization of cerebral cortical multipotent progenitors. Dev Biol 204:577–591PubMedCrossRefGoogle Scholar
  91. Martens DJ, Tropepe V, van der Kooy D (2000) Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebrain germinal zone. J Neurosci 20:1085–1095PubMedGoogle Scholar
  92. Martinsen BJ, Bronner-Fraser M (1998) Neural crest specification regulated by the helix-loop-helix repressor Id2. Science 281:988–991PubMedCrossRefGoogle Scholar
  93. Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753–791PubMedCrossRefGoogle Scholar
  94. Massague J, Blain SW, Lo RS (2000) TGFβ signaling in growth control, cancer, and heritable disorders. Cell 103:295–309PubMedCrossRefGoogle Scholar
  95. Mayer-Proschel M, Kalyani AJ, Mujtaba T, Rao MS (1997) Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 19:773–785PubMedCrossRefGoogle Scholar
  96. McKay R (1997) Stem cells in the central nervous system. Science 276:66–71PubMedCrossRefGoogle Scholar
  97. Mehler MF, Gokhan S (1999) Postnatal cerebral cortical multipotent progenitors: regulatory mechanisms and potential role in the development of novel neural regenerative strategies. Brain Pathol 9:515–526PubMedCrossRefGoogle Scholar
  98. Mehler MF, Kessler JA (1996) Cytokine regulation of neuronal development. Crit Rev Neurobiol 9:419–446Google Scholar
  99. Mehler MF, Kessler JA (1997) Hematolymphopoietic and inflammatory cytokines in neural development. Trends Neurosci 20:357–365PubMedCrossRefGoogle Scholar
  100. Mehler MF, Marmur R, Gross R, Mabie PC, Zang Z, Papavasiliou A, Kessler JA (1995) Cytokines regulate the cellular phenotype of developing neural lineage species. Int J Dev Neurosci 13: 213–240PubMedCrossRefGoogle Scholar
  101. Mehler MF, Mabie PC, Zhang D, Kessler JA (1997) Bone morphogenetic proteins in the nervous system. Trends Neurosci 20:309–317PubMedCrossRefGoogle Scholar
  102. Mehler MF, Mabie PC, Zhu G, Gokhan S, Kessler JA (2000) Developmental changes in progenitor cell responsiveness to bone morphogenetic proteins differentially modulate progressive CNS lineage fate. Dev Neurosci 22:74–85PubMedCrossRefGoogle Scholar
  103. Melnikova IN, Bounpheng M, Schatteman GC, Gilliam D, Christy BA (1999) Differential biological activities of mammalian Id proteins in muscle cells. Exp Cell Res 247:94–104PubMedCrossRefGoogle Scholar
  104. Memberg SP, Hall AK (1995) Dividing neuron precursors express neuron-specific tubulin. J Neurobiol 27:26–43PubMedCrossRefGoogle Scholar
  105. Miller RH (1996) Oligodendrocyte origins. Trends Neurosci 19:92–96PubMedCrossRefGoogle Scholar
  106. Molne M, Studer L, Tabar L, Ting Y, Eiden M, McKay R (2000) Early cortical precursors do not undergo LIF-mediated astrocytic differentiation. J Neurosci Res 59:301–311PubMedCrossRefGoogle Scholar
  107. Morrison SJ, Shah NM, Anderson DJ (1997) Regulatory mechanisms in stem cell biology. Cell 88:287–298PubMedCrossRefGoogle Scholar
  108. Morrison SJ, Perez SE, Qiao Z, Verdi JM, Hicks C, Weinmaster G, Anderson DJ (2000) Transient notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101:499–510PubMedCrossRefGoogle Scholar
  109. Morrow MA, Mayer EW, Perez CA, Adlam M, Siu G (1999) Overexpression of the helix-loop-helix protein Id2 blocks T cell development at multiple stages. Mol Immunol 36:491–503PubMedCrossRefGoogle Scholar
  110. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morasutti D, Weiss S, van der Kooy D (1994) Neuronal stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071–1082PubMedCrossRefGoogle Scholar
  111. Murtagh LC, Chyung JH, Lassar AB (1999) Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev 13:225–237CrossRefGoogle Scholar
  112. Nakamura Y, Sakakibara S, Miyata T, Ogawa M, Shimazaki T, Weiss S, Kageyama R, Okana H (2000) The bHLH gene Hes 1 as a repressor of the neuronal commitment of CNS stem cells. J Neurosci 20:283–293PubMedGoogle Scholar
  113. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T (1999a) Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284:479–482PubMedCrossRefGoogle Scholar
  114. Nakashima K, Wiese S, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Yoshida K, Kishimoto T, Sendtner M, Taga T (1999b) Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. J Neurosci 19:5429–5434PubMedGoogle Scholar
  115. Neuman K, Nornes HO, Neuman T (1995) Helix-loop-helix transcription factors regulate Id2 gene promoter activity. FEBS Lett 374:279–283PubMedCrossRefGoogle Scholar
  116. Neuman T, Keen A, Zuber MX, Kristjansson GI, Gruss P, Nornes HO (1993) Neuronal expression of regulatory helix-loop-helix factor Id2 gene in mouse. Dev Biol 160:186–195PubMedCrossRefGoogle Scholar
  117. Nguyen VH, Trout J, Connors SA, Andermann P, Weinberg E, Mullins MC (2000) Dorsal and intermediate neuronal cell types of the spinal cord are established by a BMP signaling pathway. Development 127:1209–1220PubMedGoogle Scholar
  118. Nishiyama A, Lin X-H, Giese N, Heldin C-H, Stallcup WB (1996) Co-localization of NG2 proteoglycan and PDGF a-receptor on 02A progenitor cells in the developing rat brain. J Neurosci Res 43:299–314PubMedCrossRefGoogle Scholar
  119. Norton JD, Atherton GT (1998) Coupling of cell growth control and apoptosis functions of Id proteins. Mol Cell Biol 18:2371–2381PubMedGoogle Scholar
  120. Norton JD, Deed RW, Craggs G, Sablitzky F (1998) ID helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol 8:58–65PubMedGoogle Scholar
  121. Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R (1999) Hesl and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO J 18:2196–2207PubMedCrossRefGoogle Scholar
  122. Patapoutian A, Reichardt LF (2000) Roles of Wnt proteins in neural development and maintenance. Curr Opin Neurobiol 10:392–399PubMedCrossRefGoogle Scholar
  123. Pfeiffer SE, Warrington AE, Bansal R (1993) Oligodendrocyte and its many cellular processes. Trends Cell Biol 3:191–198PubMedCrossRefGoogle Scholar
  124. Qian X, Goderie S, Shen Q, Stern J, Temple S (1998) Intrinsic programs of patterned cell lineage in isolated vertebrate CNS ventricular zone cells. Development 125:3143–3152PubMedGoogle Scholar
  125. Qian X, Davis AD, Goderie SK, Temple S (1997) FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 18:81–93PubMedCrossRefGoogle Scholar
  126. Rajan P, McKay RDG (1998) Multiple routes to astrocytic differentiation in the CNS. J Neurosci 18:3620–3629PubMedGoogle Scholar
  127. Rao MS (1999) Multipotent and restricted precursors in the central nervous system. Anat Rec 257:137–148PubMedCrossRefGoogle Scholar
  128. Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565–4574PubMedGoogle Scholar
  129. Reynolds BA, Weiss S (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175:1–13PubMedCrossRefGoogle Scholar
  130. Richards LJ, Kilpatrick TJ, Dutton R, Tan S-S, Gearing DP, Bartlett PF, Murphy M (1996) Leukemia inhibitory factor or related factors promote the differentiation of neuronal and astrocytic precursors within the developing murine spinal cord. Eur J Neurosci 2:291–299CrossRefGoogle Scholar
  131. Riechmann V, 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 6:837–843PubMedGoogle Scholar
  132. Riechmann V, van Cruchten I, Sablitzky F (1994) The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3. Nucleic Acids Res 22: 749–755PubMedCrossRefGoogle Scholar
  133. Rubenstein JLR, Anderson S, Shi L, Miyashita-Lin E, Bulfone A, Hevner R (1999) Genetic control of cortical regionalization and connectivity. Cereb Cortex 9:524–532PubMedCrossRefGoogle Scholar
  134. Sablitzky F, Moore A, Bromley M, Deed RW, Newton JS, Norton JD (1998) Stage- and subcellular-specific expression of Id proteins in male germ and Sertoli cells implicates distinctive regulatory roles for Id proteins during meiosis, spermatogenesis, and Sertoli cell function. Cell Growth Differ 9:1015–1024PubMedGoogle Scholar
  135. Sasai Y (1998) Identifying the missing links: genes that connect neural induction and primary neurogenesis in vertebrate embryos. Neuron 21:455–458PubMedCrossRefGoogle Scholar
  136. Sdrulla A, Wang S, Barres BA (1999) Overexpression of the Id2 protein inhibits oligodendrocyte differentiation in vitro. Soc Neurosci Abstr 25:2039Google Scholar
  137. Shah NM, Marchionni MA, Isaacs I, Stroobant P, Anderson DJ (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77:349–360PubMedCrossRefGoogle Scholar
  138. Shah NM, Groves AK, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGFβ superfamily members. Cell 85:331–343PubMedCrossRefGoogle Scholar
  139. Shen Q, Qian X, Capela A, Temple S (1998) Stem cells in the embryonic cerebral cortex: their role in histogenesis and patterning. J Neurobiol 36:162–174PubMedCrossRefGoogle Scholar
  140. Shou J, Rim PC, Calof AL (1999) BMPs inhibit neurogenesis by a mechanism involving degradation of a transcription factor. Nat Neurosci 2:339–345PubMedCrossRefGoogle Scholar
  141. Soderstrom S, Bengtsson H, Ebendal T (1996) Expression of serine/threonine kinase receptors including the bone morphogenetic factor type II receptor in the developing and adult rat brain. Cell Tissue Res 286:269–279PubMedCrossRefGoogle Scholar
  142. Song Q, Mehler MF, Kessler JA (1998) Bone morphogenetic proteins induce apoptosis and growth factor dependence of cultured sympathoadrenal progenitor cells. Dev Biol 196:119–127PubMedCrossRefGoogle Scholar
  143. Stewart HJ, Zoidl G, Rossner M, Brennan A, Zoidl C, Nave KA, Mirsky R, Jessen KR (1997) Helix-loop-helix proteins in Schwann cells: a study of regulation and subcellular localization of Ids, REB, and E12/47 during embryonic and postnatal development. J Neurosci Res 50:684–701PubMedCrossRefGoogle Scholar
  144. Takahashi T, Misson JP, Caviness VS (1990) Glial process elongation and branching in the developing murine neocortex: a qualitative and quantitative immunohistochemical analysis. J Comp Neurol 302:15–28PubMedCrossRefGoogle Scholar
  145. Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M, Nabeshima Y (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 99:143–148PubMedCrossRefGoogle Scholar
  146. Thatikunta P, Qin W, Christy BA, Tennekoon GI, Rutkowski JL (1999) Reciprocal Id expression and myelin gene regulation in Schwann cells. Mol Cell Neurosci 14:519–528PubMedCrossRefGoogle Scholar
  147. Thomas J-L, Spassky N, Perez-Villegas EM, Olivier C, Cobos I, Goujet-Zalc C, Martinez S, Zalc B (2000) Spatiotemporal development of oligodendrocytes in the embryonic brain. J Neurosci Res 59:471–476PubMedCrossRefGoogle Scholar
  148. Threadgil DW, Flugosz AA, Hansen AA, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris RC (1995) Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269:230–234CrossRefGoogle Scholar
  149. Toma JG, El-Bizri H, Barnabe-Heider F, Aloyz R, Miller FD (2000) Evidence that helix-loop-helix proteins collaborate with retinoblastoma tumor suppressor protein to regulate cortical neurogenesis. J Neurosci 20:7648–7656PubMedGoogle Scholar
  150. Torii M, Matsuzaki F, Osumi N, Kaibuchi K, Nakamura S, Casarosa S, Guillemot F, Nakafuku M (1999) Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development 126:443–456PubMedGoogle Scholar
  151. Tzeng SF, de Vellis J (1998) Id1, Id2, and Id3 gene expression in neural cells during development. GLIA 24:372–381PubMedCrossRefGoogle Scholar
  152. Vescovi AL, Reynolds BA, Fraser DD, Weiss S (1993) bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11:951–966Google Scholar
  153. Wang S, Barres BA (2000) Up a notch: instructing gliogenesis. Neuron 27:197–200PubMedCrossRefGoogle Scholar
  154. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, Weinmaster G, Barres BA (1998) Notch receptor activation inhibits oligodendrocytes differentiation. Neuron 21:63–75PubMedCrossRefGoogle Scholar
  155. Wang S, Hicks C, Weinmaster G, Barres BA (1999) Does the notch pathway control the timing and location of myelination? Soc Neurosci Abstr 25:2040Google Scholar
  156. Warburton D, Schwarz M, Tefft D, Flores-Delgado G, Anderson KD, Cardoso WV (2000) The molecular basis of lung morphogenesis. Mech Dev 92:55–81PubMedCrossRefGoogle Scholar
  157. Ware CB, Horowitz MC, Renshaw BR, Hunt JS, Liggit D, Koblar SA, Gliniak BC, McKenna HJ, Papayannopoulou T, Thoma B, Cheng L, Donovan PJ, Peschon JJ, Bartlett PF, Willis CR, Wright BD, Carpenter MK, Davison BL, Gearing DP (1995) Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 121:1283–1299PubMedGoogle Scholar
  158. Weiss S, Reynolds BA, Vescovi AL, Morshead C, Craig CG, van der Kooy D (1996a) Is there a neural stem cell in the mammalian forebrain? Trends Neurosci 9:387–393CrossRefGoogle Scholar
  159. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA (1996b) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16:7599–7609PubMedGoogle Scholar
  160. Weiwei L, Cogswell CA, LoTurco J J (1998) Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J Neurosci 18:8853–8862Google Scholar
  161. Whitman M (1998) Smads and early developmental signaling by the TGFf superfamily. Genes Dev 12:2445–2462PubMedCrossRefGoogle Scholar
  162. Wrana JL (2000) Regulation of smad activity. Cell 100:189–192PubMedCrossRefGoogle Scholar
  163. Yamaguchi A, Katagiri T, Ikeda T, Wozney JM, Rosen V, Wang EA, Kohn AJ, Suda T, Yoshida S (1991) Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 113:681–687PubMedCrossRefGoogle Scholar
  164. Ye W, Shimamura K, Rubenstein JL, Hynes MA, Rosenthal A (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93:755–766PubMedCrossRefGoogle Scholar
  165. Zhang D, Mehler MF, Song Q, Kessler JA (1998) Development of bone morphogenetic protein receptors in the nervous system and possible roles in regulating TrkC expression. J Neurosci 18:3314–3326PubMedGoogle Scholar
  166. Zhong W, Jiang M-M, Schonemann MD, Meneses JJ, Pedersen RA, Jan LY, Jan YN (2000) Mouse numb is an essential gene involved in cortical neurogenesis. Proc Natl Acad Sci USA 97: 6844–6849PubMedCrossRefGoogle Scholar
  167. Zhou Q, Wang S, Anderson DJ (2000) Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25:331–343PubMedCrossRefGoogle Scholar
  168. Zhu G, Mehler MF, Mabie PC, Kessler JA (1999a) Developmental changes in progenitor cells responsiveness to cytokines. J Neurosci Res 56:131–145PubMedCrossRefGoogle Scholar
  169. Zhu G, Mehler MF, Zhao J, Yung SY, Kessler JA (1999b) Sonic hedgehog and BMP2 exert opposing actions on proliferation and differentiation of embryonic neural progenitor cells. Dev Biol 215:118–129PubMedCrossRefGoogle Scholar
  170. Zuniga A, Haramis AP, McMahon AP, Zeller R (1999) Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature 401:598–602PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • Mark F. Mehler
    • 1
  1. 1.F.M. Kirby Program in Neural Protection and Repair, Departments of Neurology, Neuroscience and Psychiatry, Rose F. Kennedy Center for Research in Mental Retardation and Developmental Disabilities, Einstein Comprehensive Cancer CenterAlbert Einstein College of MedicineBronxUSA

Personalised recommendations