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The Insulin-Like Growth Factor (IGF) Receptor Type 1 (IGF1R) as an Essential Component of the Signalling Network Regulating Neurogenesis

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Abstract

The insulin-like growth factor receptor type 1 (IGF1R) signalling pathway is activated in the mammalian nervous system from early developmental stages. Its major effect on developing neural cells is to promote their growth and survival. This pathway can integrate its action with signalling pathways of growth and morphogenetic factors that induce cell fate specification and selective expansion of specified neural cell subsets. This suggests that during developmental and adult neurogenesis cellular responses to many signalling factors, including ligands of Notch, sonic hedgehog, fibroblast growth factor family members, ligands of the epidermal growth factor receptor, bone morphogenetic proteins and Wingless and Int-1, may be modified by co-activation of the IGF1R. Modulation of cell migration is another possible role that IGF1R activation may play in neurogenesis. Here, I briefly overview neurogenesis and discuss a role for IGF1R-mediated signalling in the developing and mature nervous system with emphasis on crosstalk between the signalling pathways of the IGF1R and other factors regulating neural cell development and migration. Studies on neural as well as on non-neural cells are highlighted because it may be interesting to test in neurogenic paradigms some of the models based on the information obtained in studies on non-neural cell types.

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References

  1. Baserga R (2007) Is cell size important? Cell Cycle 6:814–816

    CAS  PubMed  Google Scholar 

  2. Sun H, Tu X, Baserga R (2006) A mechanism for cell size regulation by the insulin and insulin-like growth factor-I receptors. Cancer Res 66:11106–11109

    Article  CAS  PubMed  Google Scholar 

  3. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F (1995) Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14:717–730

    Article  CAS  PubMed  Google Scholar 

  4. D’Ercole AJ, Ye P, O’Kusky JR (2002) Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides 36:209–220

    Article  PubMed  CAS  Google Scholar 

  5. LeRoith D, Werner H, Beitner-Johnson D, Roberts C Jr (1995) Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev 16:143–163

    CAS  PubMed  Google Scholar 

  6. Laviola L, Natalicchio A, Giorgino F (2007) The IGF-I signaling pathway. Curr Pharm Des 13:663–669

    Article  CAS  PubMed  Google Scholar 

  7. Li W, Miller WT (2006) Role of the activation loop tyrosines in regulation of the insulin-like growth factor I receptor tyrosine kinase. J Biol Chem 281:23785–23791

    Article  CAS  PubMed  Google Scholar 

  8. Adams TE, Epa VC, Garrett TP, Ward CW (2000) Structure and function of the type 1 insulin-like growth factor receptor. Cell Mol Life Sci 57:1050–1093

    Article  CAS  PubMed  Google Scholar 

  9. Ye P, D’Ercole AJ (2006) Insulin-like growth factor actions during development of neural stem cells and progenitors in the central nervous system. J Neurosci Res 83:1–6

    Article  CAS  PubMed  Google Scholar 

  10. Freude S, Leeser U, Muller M, Hettich MM, Udelhoven M, Schilbach K, Tobe K, Kadowaki T, Kohler C, Schroder H, Krone W, Bruning JC, Schubert M (2008) IRS-2 branch of IGF-1 receptor signaling is essential for appropriate timing of myelination. J Neurochem 107:907–917

    CAS  PubMed  Google Scholar 

  11. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785–789

    Article  CAS  PubMed  Google Scholar 

  12. Whittaker J, Whittaker L (2005) Characterization of the functional insulin binding epitopes of the full-length insulin receptor. J Biol Chem 280:20932–20936

    Article  CAS  PubMed  Google Scholar 

  13. Sun LY, D’Ercole AJ (2006) Insulin-like growth factor-I (IGF-I) stimulates histone H3 and H4 acetylation in the brain in vivo. Endocrinology 147:5480–5490

    Article  CAS  PubMed  Google Scholar 

  14. Broughton SK, Chen H, Riddle A, Kuhn SE, Nagalla S, Roberts CT, Back SA (2007) Large-scale generation of highly enriched neural stem-cell-derived oligodendroglial cultures: maturation-dependent differences in insulin-like growth factor-mediated signal transduction. J Neurochem 100:628–638

    Article  CAS  PubMed  Google Scholar 

  15. Wada A, Yokoo H, Yanagita T, Kobayashi H (2005) New twist on neuronal insulin receptor signaling in health, disease, and therapeutics. J Pharmacol Sci 99:128–143

    Article  CAS  PubMed  Google Scholar 

  16. Johnson-Farley NN, Travkina T, Cowen DS (2006) Cumulative activation of Akt and consequent inhibition of glycogen synthase kinase-3 by brain-derived neurotrophic factor and insulin-like growth factor-1 in cultured hippocampal neurons. J Pharmacol Exp Ther 316:1062–1069

    Article  CAS  PubMed  Google Scholar 

  17. Duarte AI, Santos P, Oliveira CR, Santos MS, Rego AC (2008) Insulin neuroprotection against oxidative stress is mediated by Akt and GSK-3β signaling pathways and changes in protein expression. Biochim Biophys Acta 1783:994–1002

    Article  CAS  PubMed  Google Scholar 

  18. Leinninger GM, Backus C, Uhler MD, Lentz SI, Feldman EL (2004) Phosphatidylinositol 3-kinase and Akt effectors mediate insulin-like growth factor-I neuroprotection in dorsal root ganglia neurons. FASEB J 18:1544–1546

    CAS  PubMed  Google Scholar 

  19. Neufeld TP (2003) Shrinkage control: regulation of insulin-mediated growth by FOXO transcription factors. J Biol 2:18.11–18.15

    Article  Google Scholar 

  20. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–868

    Article  CAS  PubMed  Google Scholar 

  21. Zheng W-H, Kar S, Quirion R (2002) Insulin-like growth factor-1-induced phosphorylation of transcription factor FKHRL1 is mediated by phosphatidylinositol 3-kinase/Akt kinase and role of this pathway in insulin-like growth factor-1-induced survival of cultured hippocampal neurons. Mol Pharmacol 62:225–233

    Article  CAS  PubMed  Google Scholar 

  22. Lixia G, Wenhua Z, Jean-Guy C, Terry GU, Remi Q (2005) Nuclear/cytoplasmic shuttling of the transcription factor FoxO1 is regulated by neurotrophic factors. J Neurochem 93:1209–1219

    Article  CAS  Google Scholar 

  23. Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR (1999) Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 344(Pt 2):427–431

    Article  CAS  PubMed  Google Scholar 

  24. Chenal J, Pierre K, Pellerin L (2008) Insulin and IGF-1 enhance the expression of the neuronal monocarboxylate transporter MCT2 by translational activation via stimulation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin pathway. Eur J Neurosci 27:53–65

    Article  PubMed  Google Scholar 

  25. El-Shewy HM, Johnson KR, Lee MH, Jaffa AA, Obeid LM, Luttrell LM (2006) Insulin-like growth factors mediate heterotrimeric G protein-dependent ERK1/2 activation by transactivating sphingosine-1-phosphate receptors. J Biol Chem 281:31399–31407

    Article  CAS  PubMed  Google Scholar 

  26. Lieskovska J, Ling Y, Badley-Clarke J, Clemmons DR (2006) The role of Src kinase in insulin-like growth factor dependent mitogenic signaling in vascular smooth muscle cells. J Biol Chem 281:25041–25053

    Article  CAS  PubMed  Google Scholar 

  27. Aberg MA, Aberg ND, Palmer TD, Alborn AM, Carlsson-Skwirut C, Bang P, Rosengren LE, Olsson T, Gage FH, Eriksson PS (2003) IGF-I has a direct proliferative effect in adult hippocampal progenitor cells. Mol Cell Neurosci 24:23–40

    Article  CAS  PubMed  Google Scholar 

  28. Johnson-Farley NN, Patel K, Kim D, Cowen DS (2007) Interaction of FGF-2 with IGF-1 and BDNF in stimulating Akt, ERK, and neuronal survival in hippocampal cultures. Brain Res 1154:40–49

    Article  CAS  PubMed  Google Scholar 

  29. Cui QL, Zheng WH, Quirion R, Almazan G (2005) Inhibition of Src-like kinases reveals Akt-dependent and -independent pathways in insulin-like growth factor I-mediated oligodendrocyte progenitor survival. J Biol Chem 280:8918–8928

    Article  CAS  PubMed  Google Scholar 

  30. Subramaniam S, Shahani N, Strelau J, Laliberte C, Brandt R, Kaplan D, Unsicker K (2005) Insulin-like growth factor 1 inhibits extracellular signal-regulated kinase to promote neuronal survival via the phosphatidylinositol 3-kinase/protein kinase A/c-Raf pathway. J Neurosci 25:2838–2852

    Article  CAS  PubMed  Google Scholar 

  31. Roelink H, Porter JA, Chiang C, Tanabe Y, Chang DT, Beachy PA, Jessell TM (1995) Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81:445–455

    Article  CAS  PubMed  Google Scholar 

  32. Hebert JM, Mishina Y, McConnell SK (2002) BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron 35:1029–1041

    Article  CAS  PubMed  Google Scholar 

  33. Ragsdale CW, Grove EA (2001) Patterning the mammalian cerebral cortex. Curr Opin Neurobiol 11:50–58

    Article  CAS  PubMed  Google Scholar 

  34. Takahashi H, Liu FC (2006) Genetic patterning of the mammalian telencephalon by morphogenetic molecules and transcription factors. Birth Defects Res C Embryo Today 78:256–266

    Article  CAS  PubMed  Google Scholar 

  35. Bertrand N, Dahmane N (2006) Sonic hedgehog signaling in forebrain development and its interactions with pathways that modify its effects. Trends Cell Biol 16:597–605

    Article  CAS  PubMed  Google Scholar 

  36. Riquelme PA, Drapeau E, Doetsch F (2007) Brain micro-ecologies: neural stem cell niches in the adult mammalian brain. Philos Trans R Soc Lond B Biol Sci 363:123–137

    Google Scholar 

  37. Ponti G, Aimar P, Bonfanti L (2006) Cellular composition and cytoarchitecture of the rabbit subventricular zone and its extensions in the forebrain. J Comp Neurol 498:491–507

    Article  CAS  PubMed  Google Scholar 

  38. Ayuso-Sacido A, Roy NS, Schwartz TH, Greenfield JP, Boockvar JA (2008) Long-term expansion of adult human brain subventricular zone precursors. Neurosurgery 62:223–229 discussion 229–231

    Article  PubMed  Google Scholar 

  39. Moe MC, Westerlund U, Varghese M, Berg-Johnsen J, Svensson M, Langmoen IA (2005) Development of neuronal networks from single stem cells harvested from the adult human brain. Neurosurgery 56:1182–1188 discussion 1188–1190

    Article  PubMed  Google Scholar 

  40. Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41:683–686

    Article  CAS  PubMed  Google Scholar 

  41. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046–5061

    CAS  PubMed  Google Scholar 

  42. Barkho BZ, Munoz AE, Li X, Li L, Cunningham LA, Zhao X (2008) Endogenous matrix metalloproteinase (MMP)-3 and MMP-9 promote the differentiation and migration of adult neural progenitor cells in response to chemokines. Stem Cells 26:3139–3149

    Article  CAS  PubMed  Google Scholar 

  43. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, Vandenberg S, Alvarez-Buylla A (2006) PDGFRα-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51:187–199

    Article  CAS  PubMed  Google Scholar 

  44. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A (2006) Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26:7907–7918

    Article  CAS  PubMed  Google Scholar 

  45. Zhao C, Zawadzka M, Roulois AJ, Bruce CC, Franklin RJ (2008) Promoting remyelination in multiple sclerosis by endogenous adult neural stem/precursor cells: defining cellular targets. J Neurol Sci 265:12–16

    Article  CAS  PubMed  Google Scholar 

  46. Baer K, Eriksson PS, Faull RL, Rees MI, Curtis MA (2007) Sox-2 is expressed by glial and progenitor cells and Pax-6 is expressed by neuroblasts in the human subventricular zone. Exp Neurol 204:828–831

    Article  CAS  PubMed  Google Scholar 

  47. Navarro-Quiroga I, Hernandez-Valdes M, Lin SL, Naegele JR (2006) Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex. J Comp Neurol 497:833–845

    Article  PubMed  Google Scholar 

  48. Sottile V, Li M, Scotting PJ (2006) Stem cell marker expression in the Bergmann glia population of the adult mouse brain. Brain Res 1099:8–17

    Article  CAS  PubMed  Google Scholar 

  49. Alcock J, Lowe J, England T, Bath P, Sottile V (2008) Expression of Sox1, Sox2 and Sox9 is maintained in adult human cerebellar cortex. Neurosci Lett 450:114–116

    Article  PubMed  CAS  Google Scholar 

  50. Ponti G, Peretto P, Bonfanti L (2006) A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 294:168–180

    Article  CAS  PubMed  Google Scholar 

  51. Pekcec A, Loscher W, Potschka H (2006) Neurogenesis in the adult rat piriform cortex. Neuroreport 17:571–574

    Article  PubMed  Google Scholar 

  52. Franklin RJ, Kotter MR (2008) The biology of CNS remyelination: the key to therapeutic advances. J Neurol 255(Suppl 1):19–25

    Article  CAS  PubMed  Google Scholar 

  53. Bauer S, Patterson PH (2006) Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain. J Neurosci 26:12089–12099

    Article  CAS  PubMed  Google Scholar 

  54. Kuo CT, Mirzadeh Z, Soriano-Navarro M, Rasin M, Wang D, Shen J, Sestan N, Garcia-Verdugo J, Alvarez-Buylla A, Jan LY, Jan YN (2006) Postnatal deletion of numb/numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 127:1253–1264

    Article  CAS  PubMed  Google Scholar 

  55. Covey MV, Levison SW (2007) Leukemia inhibitory factor participates in the expansion of neural stem/progenitors after perinatal hypoxia/ischemia. Neuroscience 148:501–509

    Article  CAS  PubMed  Google Scholar 

  56. Bohannon NJ, Corp ES, Wilcox BJ, Figlewicz DP, Dorsa DM, Baskin DG (1988) Localization of binding sites for insulin-like growth factor-I (IGF-I) in the rat brain by quantitative autoradiography. Brain Res 444:205–213

    Article  CAS  PubMed  Google Scholar 

  57. Sherrard RM, Richardson NA, Sara VR (1997) Localisation of insulin-like growth factor-I (IGF-I) immunoreactivity in the olivocerebellar system of developing and adult rats. Brain Res Dev Brain Res 98:102–113

    Article  CAS  PubMed  Google Scholar 

  58. Garcia-Segura LM, Rodriguez JR, Torres-Aleman I (1997) Localization of the insulin-like growth factor I receptor in the cerebellum and hypothalamus of adult rats: an electron microscopic study. J Neurocytol 26:479–490

    Article  CAS  PubMed  Google Scholar 

  59. Dore S, Kar S, Rowe W, Quirion R (1997) Distribution and levels of [125I]IGF-I, [125I]IGF-II and [125I]insulin receptor binding sites in the hippocampus of aged memory-unimpaired and -impaired rats. Neuroscience 80:1033–1040

    Article  CAS  PubMed  Google Scholar 

  60. Schechter R, Whitmire J, Beju D, Jackson KW, Harlow R, Gavin JR 3rd (1995) An immunohistochemical and in situ hybridization study of insulin-like growth factor I within fetal neuron cell cultures. Brain Res 670:1–13

    Article  CAS  PubMed  Google Scholar 

  61. Torres-Aleman I, Pons S, Arevalo MA (1994) The insulin-like growth factor I system in the rat cerebellum: developmental regulation and role in neuronal survival and differentiation. J Neurosci Res 39:117–126

    Article  CAS  PubMed  Google Scholar 

  62. Folli F, Bonfanti L, Renard E, Kahn CR, Merighi A (1994) Insulin receptor substrate-1 (IRS-1) distribution in the rat central nervous system. J Neurosci 14:6412–6422

    CAS  PubMed  Google Scholar 

  63. Kar S, Chabot JG, Quirion R (1993) Quantitative autoradiographic localization of [125I]insulin-like growth factor I, [125I]insulin-like growth factor II, and [125I]insulin receptor binding sites in developing and adult rat brain. J Comp Neurol 333:375–397

    Article  CAS  PubMed  Google Scholar 

  64. Shinar Y, McMorris FA (1995) Developing oligodendroglia express mRNA for insulin-like growth factor-I, a regulator of oligodendrocyte development. J Neurosci Res 42:516–527

    Article  CAS  PubMed  Google Scholar 

  65. Wilkins A, Chandran S, Compston A (2001) A role for oligodendrocyte-derived IGF-1 in trophic support of cortical neurons. Glia 36:48–57

    Article  CAS  PubMed  Google Scholar 

  66. Salehi Z, Mashayekhi F, Naji M, Pandamooz S (2009) Insulin-like growth factor-1 and insulin-like growth factor binding proteins in cerebrospinal fluid during the development of mouse embryos. J Clin Neurosci 16:950–953

    Article  CAS  PubMed  Google Scholar 

  67. Davila D, Piriz J, Trejo JL, Nunez A, Torres-Aleman I (2007) Insulin and insulin-like growth factor I signalling in neurons. Front Biosci 12:3194–3202

    Article  CAS  PubMed  Google Scholar 

  68. Llorens-Martin M, Torres-Aleman I, Trejo JL (2009) Mechanisms mediating brain plasticity: IGF1 and adult hippocampal neurogenesis. Neuroscientist 15:134–148

    Article  CAS  PubMed  Google Scholar 

  69. Fushimi S, Shirabe T (2004) Expression of insulin-like growth factors in remyelination following ethidium bromide-induced demyelination in the mouse spinal cord. Neuropathology 24:208–218

    Article  PubMed  Google Scholar 

  70. Trejo JL, Llorens-Martin MV, Torres-Aleman I (2008) The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol Cell Neurosci 37:402–411

    Article  CAS  PubMed  Google Scholar 

  71. Pera EM, Ikeda A, Eivers E, De Robertis EM (2003) Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev 17:3023–3028

    Article  CAS  PubMed  Google Scholar 

  72. Pera EM, Wessely O, Li SY, De Robertis EM (2001) Neural and head induction by insulin-like growth factor signals. Dev Cell 1:655–665

    Article  CAS  PubMed  Google Scholar 

  73. Richard-Parpaillon L, Heligon C, Chesnel F, Boujard D, Philpott A (2002) The IGF pathway regulates head formation by inhibiting Wnt signaling in Xenopus. Dev Biol 244:407–417

    Article  CAS  PubMed  Google Scholar 

  74. Mason JL, Goldman JE (2002) A2B5+ and O4+ cycling progenitors in the adult forebrain white matter respond differentially to PDGF-AA, FGF-2, and IGF-1. Mol Cell Neurosci 20:30–42

    Article  CAS  PubMed  Google Scholar 

  75. Hsieh J, Aimone JB, Kaspar BK, Kuwabara T, Nakashima K, Gage FH (2004) IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J Cell Biol 164:111–122

    Article  CAS  PubMed  Google Scholar 

  76. Palacios N, Sanchez-Franco F, Fernandez M, Sanchez I, Cacicedo L (2005) Intracellular events mediating insulin-like growth factor I-induced oligodendrocyte development: modulation by cyclic AMP. J Neurochem 95:1091–1107

    Article  CAS  PubMed  Google Scholar 

  77. Espinosa-Jeffrey A, Kumar S, Zhao PM, Awosika O, Agbo C, Huang A, Chang R, De Vellis J (2002) Transferrin regulates transcription of the MBP gene and its action synergizes with IGF-1 to enhance myelinogenesis in the md rat. Dev Neurosci 24:227–241

    Article  CAS  PubMed  Google Scholar 

  78. Chang MY, Sun W, Ochiai W, Nakashima K, Kim SY, Park CH, Kang JS, Shim JW, Jo AY, Kang CS, Lee YS, Kim JS, Lee SH (2007) Bcl-XL/Bax proteins direct the fate of embryonic cortical precursor cells. Mol Cell Biol 27:4293–4305

    Article  CAS  PubMed  Google Scholar 

  79. Fernando P, Megeney LA (2007) Is caspase-dependent apoptosis only cell differentiation taken to the extreme? FASEB J 21:8–17

    Article  CAS  PubMed  Google Scholar 

  80. Aranha MM, Sola S, Low WC, Steer CJ, Rodrigues CM (2009) Caspases and p53 modulate FOXO3A/Id1 signaling during mouse neural stem cell differentiation. J Cell Biochem 107:748–758

    Article  CAS  PubMed  Google Scholar 

  81. Flores AI, Narayanan SP, Morse EN, Shick HE, Yin X, Kidd G, Avila RL, Kirschner DA, Macklin WB (2008) Constitutively active Akt induces enhanced myelination in the CNS. J Neurosci 28:7174–7183

    Article  CAS  PubMed  Google Scholar 

  82. Tyler WA, Gangoli N, Gokina P, Kim HA, Covey M, Levison SW, Wood TL (2009) Activation of the mammalian target of rapamycin (mTOR) is essential for oligodendrocyte differentiation. J Neurosci 29:6367–6378

    Article  CAS  PubMed  Google Scholar 

  83. Ulloa F, Briscoe J (2007) Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 6:2640–2649

    CAS  PubMed  Google Scholar 

  84. Kessaris N, Pringle N, Richardson WD (2008) Specification of CNS glia from neural stem cells in the embryonic neuroepithelium. Philos Trans R Soc Lond B Biol Sci 363:71–85

    Article  CAS  PubMed  Google Scholar 

  85. Briscoe J, Novitch BG (2008) Regulatory pathways linking progenitor patterning, cell fates and neurogenesis in the ventral neural tube. Philos Trans R Soc Lond B Biol Sci 363:57–70

    Article  CAS  PubMed  Google Scholar 

  86. Rallu M, Corbin JG, Fishell G (2002) Parsing the prosencephalon. Nat Rev Neurosci 3:943–951

    Article  CAS  PubMed  Google Scholar 

  87. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA (1996) Cyclopia and defective axial patterning in mice lacking sonic hedgehog gene function. Nature 383:407–413

    Article  CAS  PubMed  Google Scholar 

  88. Wilson SW, Rubenstein JL (2000) Induction and dorsoventral patterning of the telencephalon. Neuron 28:641–651

    Article  CAS  PubMed  Google Scholar 

  89. Britto J, Tannahill D, Keynes R (2002) A critical role for sonic hedgehog signaling in the early expansion of the developing brain. Nat Neurosci 5:103–110

    Article  CAS  PubMed  Google Scholar 

  90. Knoepfler PS, Kenney AM (2006) Neural precursor cycling at sonic speed: N-Myc pedals, GSK-3 brakes. Cell Cycle 5:47–52

    CAS  PubMed  Google Scholar 

  91. Lai K, Kaspar BK, Gage FH, Schaffer DV (2003) Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 6:21–27

    Article  CAS  PubMed  Google Scholar 

  92. Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, Alvarez-Buylla A (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11:277–284

    Article  CAS  PubMed  Google Scholar 

  93. Angot E, Loulier K, Nguyen-Ba-Charvet KT, Gadeau AP, Ruat M, Traiffort E (2008) Chemoattractive activity of sonic hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb. Stem Cells 26:2311–2320

    Article  CAS  PubMed  Google Scholar 

  94. Balordi F, Fishell G (2007) Mosaic removal of hedgehog signaling in the adult SVZ reveals that the residual wild-type stem cells have a limited capacity for self-renewal. J Neurosci 27:14248–14259

    Article  CAS  PubMed  Google Scholar 

  95. Cayuso J, Ulloa F, Cox B, Briscoe J, Marti E (2006) The Sonic hedgehog pathway independently controls the patterning, proliferation and survival of neuroepithelial cells by regulating Gli activity. Development 133:517–528

    Article  CAS  PubMed  Google Scholar 

  96. Peltier J, O’Neill A, Schaffer DV (2007) PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev Neurobiol 67:1348–1361

    Article  CAS  PubMed  Google Scholar 

  97. Oliver TG, Grasfeder LL, Carroll AL, Kaiser C, Gillingham CL, Lin SM, Wickramasinghe R, Scott MP, Wechsler-Reya RJ (2003) Transcriptional profiling of the Sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors. Proc Natl Acad Sci U S A 100:7331–7336

    Article  CAS  PubMed  Google Scholar 

  98. Kenney AM, Widlund HR, Rowitch DH (2004) Hedgehog and PI-3 kinase signaling converge on N-myc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131:217–228

    Article  CAS  PubMed  Google Scholar 

  99. Parathath SR, Mainwaring LA, Fernandez LA, Campbell DO, Kenney AM (2008) Insulin receptor substrate 1 is an effector of sonic hedgehog mitogenic signaling in cerebellar neural precursors. Development 135:3291–3300

    Article  CAS  PubMed  Google Scholar 

  100. Campbell K (2003) Dorsal–ventral patterning in the mammalian telencephalon. Curr Opin Neurobiol 13:50–56

    Article  CAS  PubMed  Google Scholar 

  101. Lee SM, Tole S, Grove E, McMahon AP (2000) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127:457–467

    CAS  PubMed  Google Scholar 

  102. Maurer MH, Bromme JO, Feldmann RE Jr, Jarve A, Sabouri F, Burgers HF, Schelshorn DW, Kruger C, Schneider A, Kuschinsky W (2007) Glycogen synthase kinase 3β (GSK3β) regulates differentiation and proliferation in neural stem cells from the rat subventricular zone. J Proteome Res 6:1198–1208

    Article  CAS  PubMed  Google Scholar 

  103. Mao Y, Ge X, Frank CL, Madison JM, Koehler AN, Doud MK, Tassa C, Berry EM, Soda T, Singh KK, Biechele T, Petryshen TL, Moon RT, Haggarty SJ, Tsai LH (2009) Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 136:1017–1031

    Article  CAS  PubMed  Google Scholar 

  104. Kunke D, Bryja V, Mygland L, Arenas E, Krauss S (2009) Inhibition of canonical Wnt signaling promotes gliogenesis in P0-NSCs. Biochem Biophys Res Commun 386:628–633

    Article  CAS  PubMed  Google Scholar 

  105. Fuentealba LC, Eivers E, Ikeda A, Hurtado C, Kuroda H, Pera EM, De Robertis EM (2007) Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131:980–993

    Article  CAS  PubMed  Google Scholar 

  106. Desbois-Mouthon C, Cadoret A, Blivet-Van Eggelpoel MJ, Bertrand F, Cherqui G, Perret C, Capeau J (2001) Insulin and IGF-1 stimulate the β-catenin pathway through two signalling cascades involving GSK-3β inhibition and Ras activation. Oncogene 20:252–259

    Article  CAS  PubMed  Google Scholar 

  107. Satyamoorthy K, Li G, Vaidya B, Patel D, Herlyn M (2001) Insulin-like growth factor-1 induces survival and growth of biologically early melanoma cells through both the mitogen-activated protein kinase and β-catenin pathways. Cancer Res 61:7318–7324

    CAS  PubMed  Google Scholar 

  108. Verras M, Sun Z (2005) β-catenin is involved in insulin-like growth factor 1-mediated transactivation of the androgen receptor. Mol Endocrinol 19:391–398

    Article  CAS  PubMed  Google Scholar 

  109. Kalani MY, Cheshier SH, Cord BJ, Bababeygy SR, Vogel H, Weissman IL, Palmer TD, Nusse R (2008) Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci U S A 105:16970–16975

    Article  CAS  PubMed  Google Scholar 

  110. Nusse R (2008) Wnt signaling and stem cell control. Cell Res 18:523–527

    Article  CAS  PubMed  Google Scholar 

  111. Woodhead GJ, Mutch CA, Olson EC, Chenn A (2006) Cell-autonomous β-catenin signaling regulates cortical precursor proliferation. J Neurosci 26:12620–12630

    Article  CAS  PubMed  Google Scholar 

  112. Adachi K, Mirzadeh Z, Sakaguchi M, Yamashita T, Nikolcheva T, Gotoh Y, Peltz G, Gong L, Kawase T, Alvarez-Buylla A, Okano H, Sawamoto K (2007) β-Catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25:2827–2836

    Article  CAS  PubMed  Google Scholar 

  113. Hirsch C, Campano LM, Wohrle S, Hecht A (2007) Canonical Wnt signaling transiently stimulates proliferation and enhances neurogenesis in neonatal neural progenitor cultures. Exp Cell Res 313:572–587

    Article  CAS  PubMed  Google Scholar 

  114. Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, Masuyama N, Gotoh Y (2004) The Wnt/β-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131:2791–2801

    Article  CAS  PubMed  Google Scholar 

  115. Israsena N, Hu M, Fu W, Kan L, Kessler JA (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

    Article  CAS  PubMed  Google Scholar 

  116. Jin T, George Fantus I, Sun J (2008) Wnt and beyond Wnt: multiple mechanisms control the transcriptional property of β-catenin. Cell Signal 20:1697–1704

    Article  CAS  PubMed  Google Scholar 

  117. Chen J, Wu A, Sun H, Drakas R, Garofalo C, Cascio S, Surmacz E, Baserga R (2005) Functional significance of type 1 insulin-like growth factor-mediated nuclear translocation of the insulin receptor substrate-1 and β-catenin. J Biol Chem 280:29912–29920

    Article  CAS  PubMed  Google Scholar 

  118. Hoogeboom D, Essers MA, Polderman PE, Voets E, Smits LM, Burgering BM (2008) Interaction of FOXO with β-catenin inhibits β-catenin/T cell factor activity. J Biol Chem 283:9224–9230

    Article  CAS  PubMed  Google Scholar 

  119. Manolagas SC, Almeida M (2007) Gone with the Wnts: β-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol 21:2605–2614

    Article  CAS  PubMed  Google Scholar 

  120. Fukunaga K, Ishigami T, Kawano T (2005) Transcriptional regulation of neuronal genes and its effect on neural functions: expression and function of forkhead transcription factors in neurons. J Pharmacol Sci 98:205–211

    Article  CAS  PubMed  Google Scholar 

  121. Chambers C, Peng Y, Nguyen H, Gaiano N, Fishell G, Nye J (2001) Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development 128:689–702

    CAS  PubMed  Google Scholar 

  122. Gaiano N, Nye JS, Fishell G (2000) Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26:395–404

    Article  CAS  PubMed  Google Scholar 

  123. Louvi A, Artavanis-Tsakonas S (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7:93–102

    Article  CAS  PubMed  Google Scholar 

  124. Alexson TO, Hitoshi S, Coles BL, Bernstein A, van der Kooy D (2006) Notch signaling is required to maintain all neural stem cell populations—irrespective of spatial or temporal niche. Dev Neurosci 28:34–48

    Article  CAS  PubMed  Google Scholar 

  125. Yang X, Klein R, Tian X, Cheng HT, Kopan R, Shen J (2004) Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway. Dev Biol 269:81–94

    Article  CAS  PubMed  Google Scholar 

  126. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442:823–826

    Article  CAS  PubMed  Google Scholar 

  127. Mason HA, Rakowiecki SM, Gridley T, Fishell G (2006) Loss of notch activity in the developing central nervous system leads to increased cell death. Dev Neurosci 28:49–57

    Article  CAS  PubMed  Google Scholar 

  128. Mandinova A, Lefort K, Tommasi di Vignano A, Stonely W, Ostano P, Chiorino G, Iwaki H, Nakanishi J, Dotto GP (2008) The FoxO3a gene is a key negative target of canonical Notch signalling in the keratinocyte UVB response. EMBO J 27:1243–1254

    Article  CAS  PubMed  Google Scholar 

  129. Jin YH, Kim H, Oh M, Ki H, Kim K (2009) Regulation of Notch1/NICD and Hes1 expressions by GSK-3alpha/beta. Mol Cells 27:15–19

    Article  CAS  PubMed  Google Scholar 

  130. Espinosa L, Ingles-Esteve J, Aguilera C, Bigas A (2003) Phosphorylation by glycogen synthase kinase-3 beta down-regulates Notch activity, a link for Notch and Wnt pathways. J Biol Chem 278:32227–32235

    Article  CAS  PubMed  Google Scholar 

  131. Xiong L, Kou F, Yang Y, Wu J (2007) A novel role for IGF-1R in p53-mediated apoptosis through translational modulation of the p53-Mdm2 feedback loop. J Cell Biol 178:995–1007

    Article  CAS  PubMed  Google Scholar 

  132. Yamaguchi A, Tamatani M, Matsuzaki H, Namikawa K, Kiyama H, Vitek MP, Mitsuda N, Tohyama M (2001) Akt activation protects hippocampal neurons from apoptosis by inhibiting transcriptional activity of p53. J Biol Chem 276:5256–5264

    Article  CAS  PubMed  Google Scholar 

  133. Givogri MI, de Planell M, Galbiati F, Superchi D, Gritti A, Vescovi A, de Vellis J, Bongarzone ER (2006) Notch signaling in astrocytes and neuroblasts of the adult subventricular zone in health and after cortical injury. Dev Neurosci 28:81–91

    Article  CAS  PubMed  Google Scholar 

  134. Nyfeler Y, Kirch RD, Mantei N, Leone DP, Radtke F, Suter U, Taylor V (2005) Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self-renewal. EMBO J 24:3504–3515

    Article  CAS  PubMed  Google Scholar 

  135. 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 22:74–85

    Article  CAS  PubMed  Google Scholar 

  136. Chen HL, Panchision DM (2007) BMP pleiotropism in neural stem cells and their derivatives—alternative pathways, convergent signals. Stem Cells 25:63–68

    Article  CAS  PubMed  Google Scholar 

  137. Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203–2212

    CAS  PubMed  Google Scholar 

  138. Cheng X, Hsu CM, Currle DS, Hu JS, Barkovich AJ, Monuki ES (2006) Central roles of the roof plate in telencephalic development and holoprosencephaly. J Neurosci 26:7640–7649

    Article  CAS  PubMed  Google Scholar 

  139. Arkell R, Beddington RS (1997) BMP-7 influences pattern and growth of the developing hindbrain of mouse embryos. Development 124:1–12

    CAS  PubMed  Google Scholar 

  140. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28:713–726

    Article  CAS  PubMed  Google Scholar 

  141. Bonaguidi MA, Peng CY, McGuire T, Falciglia G, Gobeske KT, Czeisler C, Kessler JA (2008) Noggin expands neural stem cells in the adult hippocampus. J Neurosci 28:9194–9204

    Article  CAS  PubMed  Google Scholar 

  142. Mathieu C, Sii-Felice K, Fouchet P, Etienne O, Haton C, Mabondzo A, Boussin FD, Mouthon MA (2008) Endothelial cell-derived bone morphogenetic proteins control proliferation of neural stem/progenitor cells. Mol Cell Neurosci 38:569–577

    Article  CAS  PubMed  Google Scholar 

  143. Panchision DM, Pickel JM, Studer L, Lee SH, Turner PA, Hazel TG, McKay RD (2001) Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev 15:2094–2110

    Article  CAS  PubMed  Google Scholar 

  144. Weinstein DC, Hemmati-Brivanlou A (1999) Neural induction. Annu Rev Cell Dev Biol 15:411–433

    Article  CAS  PubMed  Google Scholar 

  145. Sailer MH, Hazel TG, Panchision DM, Hoeppner DJ, Schwab ME, McKay RD (2005) BMP2 and FGF2 cooperate to induce neural-crest-like fates from fetal and adult CNS stem cells. J Cell Sci 118:5849–5860

    Article  CAS  PubMed  Google Scholar 

  146. Itoh S, Itoh F, Goumans MJ, Ten Dijke P (2000) Signaling of transforming growth factor-β family members through Smad proteins. Eur J Biochem 267:6954–6967

    Article  CAS  PubMed  Google Scholar 

  147. Rajan P, Panchision DM, Newell LF, McKay RD (2003) BMPs signal alternately through a SMAD or FRAP-STAT pathway to regulate fate choice in CNS stem cells. J Cell Biol 161:911–921

    Article  CAS  PubMed  Google Scholar 

  148. Kendall SE, Battelli C, Irwin S, Mitchell JG, Glackin CA, Verdi JM (2005) NRAGE mediates p38 activation and neural progenitor apoptosis via the bone morphogenetic protein signaling cascade. Mol Cell Biol 25:7711–7724

    Article  CAS  PubMed  Google Scholar 

  149. Langenfeld EM, Kong Y, Langenfeld J (2005) Bone morphogenetic protein-2-induced transformation involves the activation of mammalian target of rapamycin. Mol Cancer Res 3:679–684

    Article  CAS  PubMed  Google Scholar 

  150. Kretzschmar M, Doody J, Massague J (1997) Opposing BMP and EGF signalling pathways converge on the TGF-β family mediator Smad1. Nature 389:618–622

    Article  CAS  PubMed  Google Scholar 

  151. Eivers E, Fuentealba LC, De Robertis EM (2008) Integrating positional information at the level of Smad1/5/8. Curr Opin Genet Dev 18:304–310

    Article  CAS  PubMed  Google Scholar 

  152. Bilican B, Fiore-Heriche C, Compston A, Allen ND, Chandran S (2008) Induction of Olig2 precursors by FGF involves BMP signalling blockade at the Smad level. PLoS ONE 3:e2863

    Article  PubMed  CAS  Google Scholar 

  153. Takahashi T, Morris EA, Trippel SB (2007) Bone morphogenetic protein-2 and -9 regulate the interaction of insulin-like growth factor-I with growth plate chondrocytes. Int J Mol Med 20:53–57

    CAS  PubMed  Google Scholar 

  154. Celil AB, Campbell PG (2005) BMP-2 and insulin-like growth factor-I mediate Osterix (Osx) expression in human mesenchymal stem cells via the MAPK and protein kinase D signaling pathways. J Biol Chem 280:31353–31359

    Article  CAS  PubMed  Google Scholar 

  155. Celil AB, Hollinger JO, Campbell PG (2005) Osx transcriptional regulation is mediated by additional pathways to BMP2/Smad signaling. J Cell Biochem 95:518–528

    Article  CAS  PubMed  Google Scholar 

  156. Osyczka AM, Leboy PS (2005) Bone morphogenetic protein regulation of early osteoblast genes in human marrow stromal cells is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase signaling. Endocrinology 146:3428–3437

    Article  CAS  PubMed  Google Scholar 

  157. Nishida K, Hirano T (2003) The role of Gab family scaffolding adapter proteins in the signal transduction of cytokine and growth factor receptors. Cancer Sci 94:1029–1033

    Article  CAS  PubMed  Google Scholar 

  158. Mao Y, Lee AW (2005) A novel role for Gab2 in bFGF-mediated cell survival during retinoic acid-induced neuronal differentiation. J Cell Biol 170:305–316

    Article  CAS  PubMed  Google Scholar 

  159. Hayakawa-Yano Y, Nishida K, Fukami S, Gotoh Y, Hirano T, Nakagawa T, Shimazaki T, Okano H (2007) Epidermal growth factor signaling mediated by grb2 associated binder1 is required for the spatiotemporally regulated proliferation of olig2-expressing progenitors in the embryonic spinal cord. Stem Cells 25:1410–1422

    Article  CAS  PubMed  Google Scholar 

  160. Jones N, Dumont DJ (1999) Recruitment of Dok-R to the EGF receptor through its PTB domain is required for attenuation of Erk MAP kinase activation. Curr Biol 9:1057–1060

    Article  CAS  PubMed  Google Scholar 

  161. Belsches AP, Haskell MD, Parsons SJ (1997) Role of c-Src tyrosine kinase in EGF-induced mitogenesis. Front Biosci 2:d501–518

    CAS  PubMed  Google Scholar 

  162. Zhao M, Schmitz AA, Qin Y, Di Cristofano A, Pandolfi PP, Van Aelst L (2001) Phosphoinositide 3-kinase-dependent membrane recruitment of p62(dok) is essential for its negative effect on mitogen-activated protein (MAP) kinase activation. J Exp Med 194:265–274

    Article  CAS  PubMed  Google Scholar 

  163. Yoshida K, Yamashita Y, Miyazato A, Ohya K, Kitanaka A, Ikeda U, Shimada K, Yamanaka T, Ozawa K, Mano H (2000) Mediation by the protein-tyrosine kinase Tec of signaling between the B cell antigen receptor and Dok-1. J Biol Chem 275:24945–24952

    Article  CAS  PubMed  Google Scholar 

  164. Songyang Z, Yamanashi Y, Liu D, Baltimore D (2001) Domain-dependent function of the rasGAP-binding protein p62Dok in cell signaling. J Biol Chem 276:2459–2465

    Article  CAS  PubMed  Google Scholar 

  165. Di Cristofano A, Carpino N, Dunant N, Friedland G, Kobayashi R, Strife A, Wisniewski D, Clarkson B, Pandolfi PP, Resh MD (1998) Molecular cloning and characterization of p56dok-2 defines a new family of RasGAP-binding proteins. J Biol Chem 273:4827–4830

    Article  PubMed  Google Scholar 

  166. Van Slyke P, Coll ML, Master Z, Kim H, Filmus J, Dumont DJ (2005) Dok-R mediates attenuation of epidermal growth factor-dependent mitogen-activated protein kinase and Akt activation through processive recruitment of c-Src and Csk. Mol Cell Biol 25:3831–3841

    Article  PubMed  CAS  Google Scholar 

  167. Pamonsinlapatham P, Hadj-Slimane R, Lepelletier Y, Allain B, Toccafondi M, Garbay C, Raynaud F (2009) P120-Ras GTPase activating protein (RasGAP): a multi-interacting protein in downstream signaling. Biochimie 91:320–328

    Article  CAS  PubMed  Google Scholar 

  168. Smith A, Wang J, Cheng CM, Zhou J, Weickert CS, Bondy CA (2004) High-level expression of Dok-1 in neurons of the primate prefrontal cortex and hippocampus. J Neurosci Res 75:218–224

    Article  CAS  PubMed  Google Scholar 

  169. Ford-Perriss M, Abud H, Murphy M (2001) Fibroblast growth factors in the developing central nervous system. Clin Exp Pharmacol Physiol 28:493–503

    Article  CAS  PubMed  Google Scholar 

  170. Thisse B, Thisse C (2005) Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 287:390–402

    Article  CAS  PubMed  Google Scholar 

  171. Itoh N, Ornitz DM (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet 20:563–569

    Article  CAS  PubMed  Google Scholar 

  172. Zhang Y, McKeehan K, Lin Y, Zhang J, Wang F (2008) Fibroblast growth factor receptor 1 (FGFR1) tyrosine phosphorylation regulates binding of FGFR substrate 2alpha (FRS2alpha) but not FRS2 to the receptor. Mol Endocrinol 22:167–175

    Article  CAS  PubMed  Google Scholar 

  173. Maric D, Fiorio Pla A, Chang YH, Barker JL (2007) Self-renewing and differentiating properties of cortical neural stem cells are selectively regulated by basic fibroblast growth factor (FGF) signaling via specific FGF receptors. J Neurosci 27:1836–1852

    Article  CAS  PubMed  Google Scholar 

  174. Bansal R, Lakhina V, Remedios R, Tole S (2003) Expression of FGF receptors 1, 2, 3 in the embryonic and postnatal mouse brain compared with PDGFRα, Olig2 and Plp/dm20: implications for oligodendrocyte development. Dev Neurosci 25:83–95

    Article  CAS  PubMed  Google Scholar 

  175. Fortin D, Rom E, Sun H, Yayon A, Bansal R (2005) Distinct fibroblast growth factor (FGF)/FGF receptor signaling pairs initiate diverse cellular responses in the oligodendrocyte lineage. J Neurosci 25:7470–7479

    Article  CAS  PubMed  Google Scholar 

  176. Oh LYS, Denninger A, Colvin JS, Vyas A, Tole S, Ornitz DM, Bansal R (2003) Fibroblast growth factor receptor 3 signaling regulates the onset of oligodendrocyte terminal differentiation. J Neurosci 23:883–894

    CAS  PubMed  Google Scholar 

  177. Hecht D, Zimmerman N, Bedford M, Avivi A, Yayon A (1995) Identification of fibroblast growth factor 9 (FGF9) as a high affinity, heparin dependent ligand for FGF receptors 3 and 2 but not for FGF receptors 1 and 4. Growth Factors 12:223–233

    Article  CAS  PubMed  Google Scholar 

  178. Nakamura H, Katahira T, Matsunaga E, Sato T (2005) Isthmus organizer for midbrain and hindbrain development. Brain Res Brain Res Rev 49:120–126

    Article  PubMed  Google Scholar 

  179. Fukuchi-Shimogori T, Grove EA (2001) Neocortex patterning by the secreted signaling molecule FGF8. Science 294:1071–1074

    Article  CAS  PubMed  Google Scholar 

  180. Garel S, Huffman KJ, Rubenstein JLR (2003) Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants. Development 130:1903–1914

    Article  CAS  PubMed  Google Scholar 

  181. Assimacopoulos S, Grove EA, Ragsdale CW (2003) Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex. J Neurosci 23:6399–6403

    CAS  PubMed  Google Scholar 

  182. Xu J, Liu Z, Ornitz D (2000) Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 127:1833–1843

    CAS  PubMed  Google Scholar 

  183. Hasegawa H, Ashigaki S, Takamatsu M, Suzuki-Migishima R, Ohbayashi N, Itoh N, Takada S, Tanabe Y (2004) Laminar patterning in the developing neocortex by temporally coordinated fibroblast growth factor signaling. J Neurosci 24:8711–8719

    Article  CAS  PubMed  Google Scholar 

  184. Gutin G, Fernandes M, Palazzolo L, Paek H, Yu K, Ornitz DM, McConnell SK, Hebert JM (2006) FGF signalling generates ventral telencephalic cells independently of SHH. Development 133:2937–2946

    Article  CAS  PubMed  Google Scholar 

  185. Ligon KL, Fancy SP, Franklin RJ, Rowitch DH (2006) Olig gene function in CNS development and disease. Glia 54:1–10

    Article  PubMed  Google Scholar 

  186. Gómez-Pinilla F, Lee JW-K, Cotman CW (1994) Distribution of basic fibroblast growth factor in the developing rat brain. Neuroscience 61:911–923

    Article  PubMed  Google Scholar 

  187. Gomez-Pinilla F, Lee J, Cotman C (1992) Basic FGF in adult rat brain: cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J Neurosci 12:345–355

    CAS  PubMed  Google Scholar 

  188. Zheng W, Nowakowski RS, Vaccarino FM (2004) Fibroblast growth factor 2 is required for maintaining the neural stem cell pool in the mouse brain subventricular zone. Dev Neurosci 26:181–196

    Article  CAS  PubMed  Google Scholar 

  189. Korada S, Zheng W, Basilico C, Schwartz ML, Vaccarino FM (2002) Fibroblast growth factor 2 is necessary for the growth of glutamate projection neurons in the anterior neocortex. J Neurosci 22:863–875

    CAS  PubMed  Google Scholar 

  190. Chen K, Ohkubo Y, Shin D, Doetschman T, Sanford LP, Li H, Vaccarino FM (2008) Decrease in excitatory neurons, astrocytes and proliferating progenitors in the cerebral cortex of mice lacking exon 3 from the Fgf2 gene. BMC Neurosci 9:94–102

    Article  PubMed  CAS  Google Scholar 

  191. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci U S A 98:5874–5879

    Article  CAS  PubMed  Google Scholar 

  192. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17:5820–5829

    CAS  PubMed  Google Scholar 

  193. Erickson RI, Paucar AA, Jackson RL, Visnyei K, Kornblum H (2008) Roles of insulin and transferrin in neural progenitor survival and proliferation. J Neurosci Res 86:1884–1894

    Article  CAS  PubMed  Google Scholar 

  194. Arsenijevic Y, Weiss S, Schneider B, 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

    CAS  PubMed  Google Scholar 

  195. Hodge RD, D’Ercole AJ, O’Kusky JR (2004) Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J Neurosci 24:10201–10210

    Article  CAS  PubMed  Google Scholar 

  196. Kalluri HS, Vemuganti R, Dempsey RJ (2007) Mechanism of insulin-like growth factor I-mediated proliferation of adult neural progenitor cells: role of Akt. Eur J Neurosci 25:1041–1048

    Article  PubMed  Google Scholar 

  197. Sherr CJ, Roberts JM (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9:1149–1163

    Article  CAS  PubMed  Google Scholar 

  198. Elledge SJ (1996) Cell cycle checkpoints: preventing an identity crisis. Science 274:1664–1672

    Article  CAS  PubMed  Google Scholar 

  199. Frederick TJ, Wood TL (2004) IGF-I and FGF-2 coordinately enhance cyclin D1 and cyclin E-cdk2 association and activity to promote G1 progression in oligodendrocyte progenitor cells. Mol Cell Neurosci 25:480–492

    Article  CAS  PubMed  Google Scholar 

  200. Bonthius DJ, Karacay B, Dai D, Pantazis NJ (2003) FGF-2, NGF and IGF-1, but not BDNF, utilize a nitric oxide pathway to signal neurotrophic and neuroprotective effects against alcohol toxicity in cerebellar granule cell cultures. Brain Res Dev Brain Res 140:15–28

    Article  CAS  PubMed  Google Scholar 

  201. Zheng WH, Quirion R (2004) Comparative signaling pathways of insulin-like growth factor-1 and brain-derived neurotrophic factor in hippocampal neurons and the role of the PI3 kinase pathway in cell survival. J Neurochem 89:844–852

    Article  CAS  PubMed  Google Scholar 

  202. Zheng WH, Kar S, Dore S, Quirion R (2000) Insulin-like growth factor-1 (IGF-1): a neuroprotective trophic factor acting via the Akt kinase pathway. J Neural Transm Suppl 261–272

  203. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D (1999) Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208:166–188

    Article  CAS  PubMed  Google Scholar 

  204. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021–1034

    Article  CAS  PubMed  Google Scholar 

  205. Grinspan JB, Franceschini B (1995) Platelet-derived growth factor is a survival factor for PSA-NCAM+ oligodendrocyte pre-progenitor cells. J Neurosci Res 41:540–551

    Article  CAS  PubMed  Google Scholar 

  206. Gago N, Avellana-Adalid V, Evercooren AB, Schumacher M (2003) Control of cell survival and proliferation of postnatal PSA-NCAM+ progenitors. Mol Cell Neurosci 22:162–178

    Article  CAS  PubMed  Google Scholar 

  207. Fleming JM, Desury G, Polanco TA, Cohick WS (2006) Insulin growth factor-I and epidermal growth factor receptors recruit distinct upstream signaling molecules to enhance AKT activation in mammary epithelial cells. Endocrinology 147:6027–6035

    Article  CAS  PubMed  Google Scholar 

  208. Liu R, Cai J, Hu X, Tan M, Qi Y, German M, Rubenstein J, Sander M, Qiu M (2003) Region-specific and stage-dependent regulation of Olig gene expression and oligodendrogenesis by Nkx6.1 homeodomain transcription factor. Development 130:6221–6231

    Article  CAS  PubMed  Google Scholar 

  209. Marmur R, Mabie PC, Gokhan S, Song Q, Kessler JA, Mehler MF (1998) Isolation and developmental characterization of cerebral cortical multipotent progenitors. Dev Biol 204:577–591

    Article  CAS  PubMed  Google Scholar 

  210. Marin O, Rubenstein JLR (2001) A long remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780–790

    Article  CAS  PubMed  Google Scholar 

  211. Schmechel DE, Rakic P (1979) Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Nature 277:303–305

    Article  CAS  PubMed  Google Scholar 

  212. Cayre M, Bancila M, Virard I, Borges A, Durbec P (2006) Migrating and myelinating potential of subventricular zone neural progenitor cells in white matter tracts of the adult rodent brain. Mol Cell Neurosci 31:748–758

    Article  CAS  PubMed  Google Scholar 

  213. Jain M, Armstrong RJ, Elneil S, Barker RA (2006) Transplanted human neural precursor cells migrate widely but show no lesion-specific tropism in the 6-hydroxydopamine rat model of Parkinson’s disease. Cell Transplant 15:579–593

    Article  CAS  PubMed  Google Scholar 

  214. Pokutta S, Drees F, Yamada S, Nelson WJ, Weis WI (2008) Biochemical and structural analysis of α-catenin in cell–cell contacts. Biochem Soc Trans 36:141–147

    Article  CAS  PubMed  Google Scholar 

  215. Niessen CM, Gottardi CJ (2008) Molecular components of the adherens junction. Biochim Biophys Acta 1778:562–571

    Article  CAS  PubMed  Google Scholar 

  216. Lobo MV, Alonso FJ, Redondo C, Lopez-Toledano MA, Caso E, Herranz AS, Paino CL, Reimers D, Bazan E (2003) Cellular characterization of epidermal growth factor-expanded free-floating neurospheres. J Histochem Cytochem 51:89–103

    PubMed  Google Scholar 

  217. Seki T, Namba T, Mochizuki H, Onodera M (2007) Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 502:275–290

    Article  CAS  PubMed  Google Scholar 

  218. Hughson E, Dowler S, Geall K, Johnson G, Rumsby M (1998) Rat oligodendrocyte O-2A precursor cells and the CG-4 oligodendrocyte precursor cell line express cadherins, β-catenin and the neural cell adhesion molecule, NCAM. Neurosci Lett 251:157–160

    Article  CAS  PubMed  Google Scholar 

  219. Payne HR, Hemperly JJ, Lemmon V (1996) N-cadherin expression and function in cultured oligodendrocytes. Brain Res Dev Brain Res 97:9–15

    Article  CAS  PubMed  Google Scholar 

  220. Angst B, Marcozzi C, Magee A (2001) The cadherin superfamily: diversity in form and function. J Cell Sci 114:629–641

    CAS  PubMed  Google Scholar 

  221. Rubenstein JL, Anderson S, Shi L, Miyashita-Lin E, Bulfone A, Hevner R (1999) Genetic control of cortical regionalization and connectivity. Cereb Cortex 9:524–532

    Article  CAS  PubMed  Google Scholar 

  222. Nakagawa S, Takeichi M (1998) Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125:2963–2971

    CAS  PubMed  Google Scholar 

  223. Takahashi M, Osumi N (2008) Expression study of cadherin7 and cadherin20 in the embryonic and adult rat central nervous system. BMC Dev Biol 8:87–105

    Article  PubMed  CAS  Google Scholar 

  224. Paez PM, Marta CB, Moreno MB, Soto EF, Pasquini JM (2002) Apotransferrin decreases migration and enhances differentiation of oligodendroglial progenitor cells in an in vitro system. Dev Neurosci 24:47–58

    Article  CAS  PubMed  Google Scholar 

  225. Huber AH, Stewart DB, Laurents DV, Nelson WJ, Weis WI (2001) The cadherin cytoplasmic domain is unstructured in the absence of β-catenin. A possible mechanism for regulating cadherin turnover. J Biol Chem 276:12301–12309

    Article  CAS  PubMed  Google Scholar 

  226. Gumbiner BM (2000) Regulation of cadherin adhesive activity. J Cell Biol 148:399–404

    Article  CAS  PubMed  Google Scholar 

  227. Nagato M, Heike T, Kato T, Yamanaka Y, Yoshimoto M, Shimazaki T, Okano H, Nakahata T (2005) Prospective characterization of neural stem cells by flow cytometry analysis using a combination of surface markers. J Neurosci Res 80:456–466

    Article  CAS  PubMed  Google Scholar 

  228. Campos LS, Leone DP, Relvas JB, Brakebusch C, Fassler R, Suter U, Ffrench-Constant C (2004) β1 Integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 131:3433–3444

    Article  CAS  PubMed  Google Scholar 

  229. Flanagan LA, Rebaza LM, Derzic S, Schwartz PH, Monuki ES (2006) Regulation of human neural precursor cells by laminin and integrins. J Neurosci Res 83:845–856

    Article  CAS  PubMed  Google Scholar 

  230. Milner R, Edwards G, Streuli C, Ffrench-Constant C (1996) A role in migration for the αvβ1 integrin expressed on oligodendrocyte precursors. J Neurosci 16:7240–7252

    CAS  PubMed  Google Scholar 

  231. Guvakova MA, Adams JC, Boettiger D (2002) Functional role of α-actinin, PI 3-kinase and MEK1/2 in insulin-like growth factor I receptor kinase regulated motility of human breast carcinoma cells. J Cell Sci 115:4149–4165

    Article  CAS  PubMed  Google Scholar 

  232. Schlenska-Lange A, Knupfer H, Lange TJ, Kiess W, Knupfer M (2008) Cell proliferation and migration in glioblastoma multiforme cell lines are influenced by insulin-like growth factor I in vitro. Anticancer Res 28:1055–1060

    CAS  PubMed  Google Scholar 

  233. Kanekar S, Borg TK, Terracio L, Carver W (2000) Modulation of heart fibroblast migration and collagen gel contraction by IGF-I. Cell Adhes Commun 7:513–523

    Article  CAS  PubMed  Google Scholar 

  234. Osterhout DJ, Ebner S, Xu J, Ornitz DM, Zazanis GA, McKinnon RD (1997) Transplanted oligodendrocyte progenitor cells expressing a dominant-negative FGF receptor transgene fail to migrate in vivo. J Neurosci 17:9122–9132

    CAS  PubMed  Google Scholar 

  235. Frost EE, Zhou Z, Krasnesky K, Armstrong RC (2008) Initiation of oligodendrocyte progenitor cell migration by a PDGF-A activated extracellular regulated kinase (ERK) signaling pathway. Neurochem Res 34:69–81

    Google Scholar 

  236. Milner R, Anderson HJ, Rippon RF, McKay JS, Franklin RJM, Marchionni MA, Reynolds R, Ffrench-Constant C (1997) Contrasting effects of mitogenic growth factors on oligodendrocyte precursor cell migration. Glia 19:85–90

    Article  CAS  PubMed  Google Scholar 

  237. Espinosa-Jeffrey A, Zhao P, Awosika W, Wu N, Macias F, Cepeda C, Levine M, de Vellis J (2006) Activation, proliferation and commitment of endogenous stem/progenitor cells to the oligodendrocyte lineage by TS1 in a rat model of dysmyelination. Dev Neurosci 28:488–498

    Article  CAS  PubMed  Google Scholar 

  238. Kumar S, Biancotti JC, Yamaguchi M, de Vellis J (2007) Combination of growth factors enhances remyelination in a cuprizone-induced demyelination mouse model. Neurochem Res 32:783–797

    Article  CAS  PubMed  Google Scholar 

  239. Guvakova MA (2007) Insulin-like growth factors control cell migration in health and disease. Int J Biochem Cell Biol 39:890–909

    Article  CAS  PubMed  Google Scholar 

  240. Playford MP, Bicknell D, Bodmer WF, Macaulay VM (2000) Insulin-like growth factor 1 regulates the location, stability, and transcriptional activity of β-catenin. Proc Natl Acad Sci U S A 97:12103–12108

    Article  CAS  PubMed  Google Scholar 

  241. Mauro L, Salerno M, Morelli C, Boterberg T, Bracke ME, Surmacz E (2003) Role of the IGF-I receptor in the regulation of cell–cell adhesion: implications in cancer development and progression. J Cell Physiol 194:108–116

    Article  CAS  PubMed  Google Scholar 

  242. Morali OG, Delmas V, Moore R, Jeanney C, Thiery JP, Larue L (2001) IGF-II induces rapid beta-catenin relocation to the nucleus during epithelium to mesenchyme transition. Oncogene 20:4942–4950

    Article  CAS  PubMed  Google Scholar 

  243. Yue Q, Groszer M, Gil JS, Berk AJ, Messing A, Wu H, Liu X (2005) PTEN deletion in Bergmann glia leads to premature differentiation and affects laminar organization. Development 132:3281–3291

    Article  CAS  PubMed  Google Scholar 

  244. Marino S, Krimpenfort P, Leung C, van der Korput HA, Trapman J, Camenisch I, Berns A, Brandner S (2002) PTEN is essential for cell migration but not for fate determination and tumourigenesis in the cerebellum. Development 129:3513–3522

    CAS  PubMed  Google Scholar 

  245. Tamura M, Gu J, Matsumoto K, Aota S, Parsons R, Yamada KM (1998) Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 280:1614–1617

    Article  CAS  PubMed  Google Scholar 

  246. Tamura M, Gu J, Danen EH, Takino T, Miyamoto S, Yamada KM (1999) PTEN interactions with focal adhesion kinase and suppression of the extracellular matrix-dependent phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 274:20693–20703

    Article  CAS  PubMed  Google Scholar 

  247. Tamura M, Gu J, Takino T, Yamada KM (1999) Tumor suppressor PTEN inhibition of cell invasion, migration, and growth: differential involvement of focal adhesion kinase and p130Cas. Cancer Res 59:442–449

    CAS  PubMed  Google Scholar 

  248. Jones JI, Prevette T, Gockerman A, Clemmons DR (1996) Ligand occupancy of the αVβ3 integrin is necessary for smooth muscle cells to migrate in response to insulin-like growth factor. Proc Natl Acad Sci U S A 93:2482–2487

    Article  CAS  PubMed  Google Scholar 

  249. Hollier BG, Kricker JA, Van Lonkhuyzen DR, Leavesley DI, Upton Z (2008) Substrate-bound insulin-like growth factor (IGF)-I-IGF binding protein-vitronectin-stimulated breast cell migration is enhanced by coactivation of the phosphatidylinositide 3-Kinase/AKT pathway by αv-integrins and the IGF-I receptor. Endocrinology 149:1075–1090

    Article  CAS  PubMed  Google Scholar 

  250. Manes S, Mira E, Gomez-Mouton C, Zhao ZJ, Lacalle RA, Martinez AC (1999) Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol Cell Biol 19:3125–3135

    CAS  PubMed  Google Scholar 

  251. Canonici A, Steelant W, Rigot V, Khomitch-Baud A, Boutaghou-Cherid H, Bruyneel E, Van Roy F, Garrouste F, Pommier G, Andre F (2008) Insulin-like growth factor-I receptor, E-cadherin and αv integrin form a dynamic complex under the control of α-catenin. Int J Cancer 122:572–582

    Article  CAS  PubMed  Google Scholar 

  252. Casamassima A, Rozengurt E (1998) Insulin-like growth factor I stimulates tyrosine phosphorylation of p130(Cas), focal adhesion kinase, and paxillin. Role of phosphatidylinositol 3′-kinase and formation of a p130(Cas). Crk complex. J Biol Chem 273:26149–26156

    Article  CAS  PubMed  Google Scholar 

  253. Leventhal PS, Shelden EA, Kim B, Feldman EL (1997) Tyrosine phosphorylation of paxillin and focal adhesion kinase during insulin-like growth factor-I-stimulated lamellipodial advance. J Biol Chem 272:5214–5218

    Article  CAS  PubMed  Google Scholar 

  254. Ron D, Chen CH, Caldwell J, Jamieson L, Orr E, Mochly-Rosen D (1994) Cloning of an intracellular receptor for protein kinase C: a homolog of the β subunit of G proteins. Proc Natl Acad Sci U S A 91:839–843

    Article  CAS  PubMed  Google Scholar 

  255. Liliental J, Chang DD (1998) Rack1, a receptor for activated protein kinase C, interacts with integrin β subunit. J Biol Chem 273:2379–2383

    Article  CAS  PubMed  Google Scholar 

  256. McCahill A, Warwicker J, Bolger GB, Houslay MD, Yarwood SJ (2002) The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol Pharmacol 62:1261–1273

    Article  CAS  PubMed  Google Scholar 

  257. Buensuceso CS, Woodside D, Huff JL, Plopper GE, O’Toole TE (2001) The WD protein Rack1 mediates protein kinase C and integrin-dependent cell migration. J Cell Sci 114:1691–1698

    CAS  PubMed  Google Scholar 

  258. Doan AT, Huttenlocher A (2007) RACK1 regulates Src activity and modulates paxillin dynamics during cell migration. Exp Cell Res 313:2667–2679

    Article  CAS  PubMed  Google Scholar 

  259. Vomastek T, Iwanicki MP, Schaeffer HJ, Tarcsafalvi A, Parsons JT, Weber MJ (2007) RACK1 targets the extracellular signal-regulated kinase/mitogen-activated protein kinase pathway to link integrin engagement with focal adhesion disassembly and cell motility. Mol Cell Biol 27:8296–8305

    Article  CAS  PubMed  Google Scholar 

  260. Hermanto U, Zong CS, Li W, Wang LH (2002) RACK1, an insulin-like growth factor I (IGF-I) receptor-interacting protein, modulates IGF-I-dependent integrin signaling and promotes cell spreading and contact with extracellular matrix. Mol Cell Biol 22:2345–2365

    Article  CAS  PubMed  Google Scholar 

  261. Kiely PA, Sant A, O’Connor R (2002) RACK1 is an insulin-like growth factor 1 (IGF-1) receptor-interacting protein that can regulate IGF-1-mediated Akt activation and protection from cell death. J Biol Chem 277:22581–22589

    Article  CAS  PubMed  Google Scholar 

  262. Kiely PA, O’Gorman D, Luong K, Ron D, O’Connor R (2006) Insulin-like growth factor I controls a mutually exclusive association of RACK1 with protein phosphatase 2A and β1 integrin to promote cell migration. Mol Cell Biol 26:4041–4051

    Article  CAS  PubMed  Google Scholar 

  263. O’Donovan HC, Kiely PA, O’Connor R (2007) Effects of RACK1 on cell migration and IGF-I signalling in cardiomyocytes are not dependent on an association with the IGF-IR. Cell Signal 19:2588–2595

    Article  PubMed  CAS  Google Scholar 

  264. Kiely PA, Baillie GS, Lynch MJ, Houslay MD, O’Connor R (2008) Tyrosine 302 in RACK1 is essential for insulin-like growth factor-I-mediated competitive binding of PP2A and β1 integrin and for tumor cell proliferation and migration. J Biol Chem 283:22952–22961

    Article  CAS  PubMed  Google Scholar 

  265. Angenstein F, Evans AM, Settlage RE, Moran ST, Ling SC, Klintsova AY, Shabanowitz J, Hunt DF, Greenough WT (2002) A receptor for activated C kinase is part of messenger ribonucleoprotein complexes associated with polyA-mRNAs in neurons. J Neurosci 22:8827–8837

    CAS  PubMed  Google Scholar 

  266. Brandon NJ, Jovanovic JN, Smart TG, Moss SJ (2002) Receptor for activated C kinase-1 facilitates protein kinase C-dependent phosphorylation and functional modulation of GABA(A) receptors with the activation of G-protein-coupled receptors. J Neurosci 22:6353–6361

    CAS  PubMed  Google Scholar 

  267. Ashique AM, Kharazia V, Yaka R, Phamluong K, Peterson AS, Ron D (2006) Localization of the scaffolding protein RACK1 in the developing and adult mouse brain. Brain Res 1069:31–38

    Article  CAS  PubMed  Google Scholar 

  268. Onishi I, Lin PJ, Diering GH, Williams WP, Numata M (2007) RACK1 associates with NHE5 in focal adhesions and positively regulates the transporter activity. Cell Signal 19:194–203

    Article  CAS  PubMed  Google Scholar 

  269. Pulai JI, Del Carlo M Jr, Loeser RF (2002) The α5β1 integrin provides matrix survival signals for normal and osteoarthritic human articular chondrocytes in vitro. Arthritis Rheum 46:1528–1535

    Article  CAS  PubMed  Google Scholar 

  270. Van Lonkhuyzen DR, Hollier BG, Shooter GK, Leavesley DI, Upton Z (2007) Chimeric vitronectin: insulin-like growth factor proteins enhance cell growth and migration through co-activation of receptors. Growth Factors 25:295–308

    Article  PubMed  CAS  Google Scholar 

  271. Maile LA, Aday AW, Busby WH, Sanghani R, Veluvolu U, Clemmons DR (2008) Modulation of integrin antagonist signaling by ligand binding of the heparin-binding domain of vitronectin to the αVβ3 integrin. J Cell Biochem 105:437–446

    Article  CAS  PubMed  Google Scholar 

  272. Maile LA, Clemmons DR (2002) The αVβ3 integrin regulates insulin-like growth factor I (IGF-I) receptor phosphorylation by altering the rate of recruitment of the Src-homology 2-containing phosphotyrosine phosphatase-2 to the activated IGF-I receptor. Endocrinology 143:4259–4264

    Article  CAS  PubMed  Google Scholar 

  273. Garcion E, Faissner A, Ffrench-Constant C (2001) Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development 128:2485–2496

    CAS  PubMed  Google Scholar 

  274. Scolnick JA, Cui K, Duggan CD, Xuan S, Yuan XB, Efstratiadis A, Ngai J (2008) Role of IGF signaling in olfactory sensory map formation and axon guidance. Neuron 57:847–857

    Article  CAS  PubMed  Google Scholar 

  275. Glasper ER, Llorens-Martin MV, Leuner B, Gould E, Trejo JL (2009) Blockade of insulin-like growth factor-I has complex effects on structural plasticity in the hippocampus. Hippocampus (in press)

  276. Ozdinler PH, Macklis JD (2006) IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat Neurosci 9:1371–1381

    Article  PubMed  CAS  Google Scholar 

  277. Laurino L, Wang XX, de la Houssaye BA, Sosa L, Dupraz S, Caceres A, Pfenninger KH, Quiroga S (2005) PI3K activation by IGF-1 is essential for the regulation of membrane expansion at the nerve growth cone. J Cell Sci 118:3653–3662

    Article  CAS  PubMed  Google Scholar 

  278. Shiraishi M, Tanabe A, Saito N, Sasaki Y (2006) Unphosphorylated MARCKS is involved in neurite initiation induced by insulin-like growth factor-I in SH-SY5Y cells. J Cell Physiol 209:1029–1038

    Article  CAS  PubMed  Google Scholar 

  279. Sosa L, Dupraz S, Laurino L, Bollati F, Bisbal M, Caceres A, Pfenninger KH, Quiroga S (2006) IGF-1 receptor is essential for the establishment of hippocampal neuronal polarity. Nat Neurosci 9:993–995

    Article  CAS  PubMed  Google Scholar 

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The author thanks the National Multiple Sclerosis Society for financial support and Yuti Chernajovsky for critically reading the manuscript.

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Annenkov, A. The Insulin-Like Growth Factor (IGF) Receptor Type 1 (IGF1R) as an Essential Component of the Signalling Network Regulating Neurogenesis. Mol Neurobiol 40, 195–215 (2009). https://doi.org/10.1007/s12035-009-8081-0

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