Skip to main content

Regulation of Vertebrate Sensory Organ Development: A Scenario for Growth Hormone and Insulin-Like Growth Factors Action

  • Chapter
The Growth Hormone/Insulin-Like Growth Factor Axis During Development

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. S.H. Hendry, S.S. Hsiao and M.C. Brown, in: Fundamental Neuroscience, edited by L.R. Squire, F.E. Bloom, S.K. McConnell, J.L. Roberts, N.C. Spitzer, M.J. Zigmond (Academic Press, San Diego, California, USA, 2003), pp. 577–589.

    Google Scholar 

  2. P. Mombaerts, Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol, 14, 31–36 (2004).

    Article  PubMed  CAS  Google Scholar 

  3. I. Varela-Nieto, E.J. de la Rosa, A.I. Valenciano, and Y. Leon, Cell death in the nervous system: lessons from insulin and insulin-like growth factors. Mol Neurobiol, 28, 23–50 (2003).

    Article  PubMed  CAS  Google Scholar 

  4. P. Moriarty, M. Boulton, A. Dickson and D. McLeod, Production of IGF-I and IGF binding proteins by retinal cells in vitro. Br J Ophthalmol, 78, 638–642 (1994).

    PubMed  CAS  Google Scholar 

  5. G. Calvaruso, R. Vento, M. Giuliano, M. Lauricella, E. Gerbino and G. Tesoriere, Insulin-like growth factors in chick embryo retina during development. Regul Pept, 61, 19–25 (1996).

    Article  PubMed  CAS  Google Scholar 

  6. E. Ayaso, CM. Nolan and L. Byrnes, Zebrafish insulin-like growth factor-I receptor: molecular cloning and developmental expression. Mol Cell Endocrinol, 191, 137–148 (2002).

    Article  PubMed  CAS  Google Scholar 

  7. B. Funkenstein, R. Almuly and S.J. Chan, Localization of IGF-I and IGF-I receptor mRNA in Sparus aurata larvae. Gen Comp Endocrinol, 107, 291–303 (1997).

    Article  PubMed  CAS  Google Scholar 

  8. D.C. Otteson, P.F. Cirenza and P.F. Hitchcock, Persistent neurogenesis in the teleost retina: evidence for regulation by the growth-hormone/insulin-like growth factor-I axis. Mech Dev, 117, 137–149 (2002).

    Article  PubMed  CAS  Google Scholar 

  9. C.P. Burren, J.L. Berka, S.R. Edmondson, G.A. Werther and J.A. Batch, Localization of mRNAs for insulin-like growth factor-I (IGF-I), IGF-I receptor, and IGF binding proteins in rat eye. Invest Ophthalmol Vis Sci, 37, 1459–1468 (1996).

    PubMed  CAS  Google Scholar 

  10. C.P. Burren, J.L. Berka and J.A. Batch, Localization studies of IGFBP-2 and IGFBP-5 in the anterior compartment of the eye. Curr Eye Res, 16, 256–262 (1997).

    Article  PubMed  CAS  Google Scholar 

  11. J. Serna, P.R. Gonzalez-Guerrero, C.G. Scanes, M. Prati, G. Morreale and F. de Pablo, Differential and tissue-specific regulation of (pro)insulin and insulin-like growth factor-I mRNAs and levels of thyroid hormones in growth-retarded embryos. Growth Regul, 6, 73–82 (1996).

    PubMed  CAS  Google Scholar 

  12. L.E. Politi, N.P. Rotstein, G. Salvador, N.M. Giusto and M.F. Insua, Insulin-like growth factor-I is a potential trophic factor for amacrine cells. J Neurochem, 76, 1199–1211 (2001).

    Article  PubMed  CAS  Google Scholar 

  13. W.H. Lee, S. Javedan and C.A. Bondy, Coordinate expression of insulin-like growth factor system components by neurons and neuroglia during retinal and cerebellar development. J Neurosci, 12, 4737–4744 (1992).

    PubMed  CAS  Google Scholar 

  14. Y. Leon, C. Sanz, L.M. Frago, G. Camarero, S. Canon, I. Varela-Nieto and F. Giraldez, Involvement of insulin-like growth factor-I in inner ear organogenesis and regeneration. Horm Metab Res, 31, 126–132 (1999).

    PubMed  CAS  Google Scholar 

  15. T.J. Schoen, C.A. Bondy, J. Zhou, R. Dhawan, K. Mazuruk, D.R. Arnold, I.R. Rodriguez, R.J. Waldbillig, D.C. Beebe and G.J. Chader, Differential temporal and spatial expression of insulin-like growth factor binding protein-2 in developing chick ocular tissues. Invest Ophthalmol Vis Sci, 36, 2652–2662 (1995).

    PubMed  CAS  Google Scholar 

  16. S.K. Pixley, N.S. Dangoria, K.K. Odoms and L. Hastings, Effects of insulin-like growth factor 1 on olfactory neurogenesis in vivo and in vitro. Ann N Y Acad Sci, 855, 244–247 (1998).

    Article  PubMed  CAS  Google Scholar 

  17. M. Holzenberger, F. Lapointe and C. Ayer-LeLievre, Expression of insulin-like growth factor-I (IGF-I) and IGF-II in the avian brain: relationship of in situ hybridization patterns with IGF type 1 receptor expression. Int J Dev Neurosci, 18, 69–82 (2000).

    Article  PubMed  CAS  Google Scholar 

  18. J. Plendl, B. Stierstorfer and F. Sinowatz, Growth factors and their receptors in the olfactory system. Anat Histol Embryol, 28, 73–79 (1999).

    Article  PubMed  CAS  Google Scholar 

  19. F. de Pablo and E.J. de la Rosa, The developing CNS: a scenario for the action of proinsulin, insulin and insulin-like growth factors. Trends Neurosci, 18, 143–150 (1995).

    Article  PubMed  Google Scholar 

  20. K.A. Sullivan and E.L. Feldman, Immunohistochemical localization of insulin-like growth factor-II (IGF-II) and IGF-binding protein-2 during development in the rat brain. Endocrinology, 135, 540–547 (1994).

    Article  PubMed  CAS  Google Scholar 

  21. V.C. Russo, S.R. Edmondson, F.A. Mercuri, C.R. Buchanan and G.A. Werther, Identification, localization, and regulation of insulin-like growth factor binding proteins and their messenger ribonucleic acids in the newborn rat olfactory bulb. Endocrinology, 135, 1437–1446 (1994).

    Article  PubMed  CAS  Google Scholar 

  22. V.C. Russo, L.A. Bach, A.J. Fosang, N.L. Baker and G.A. Werther, Insulin-like growth factor binding protein-2 binds to cell surface proteoglycans in the rat brain olfactory bulb. Endocrinology, 138, 4858–4867 (1997).

    Article  PubMed  CAS  Google Scholar 

  23. MM. Giacobini, R.H. Zetterstrom, D. Young, B. Hoffer, V. Sara and L. Olson, IGF-1 influences olfactory bulb maturation. Evidence from anti-IGF-1 antibody treatment of developing grafts in oculo. Brain Res Dev Brain Res, 84, 67–76 (1995).

    Article  PubMed  CAS  Google Scholar 

  24. C.A. Bondy and W.H. Lee, Patterns of insulin-like growth factor and IGF receptor gene expression in the brain. Functional implications. Ann N Y Acad Sci, 692, 33–43 (1993).

    PubMed  CAS  Google Scholar 

  25. E.J. de la Rosa, C.A. Bondy, C. Hernandez-Sanchez, X. Wu, J. Zhou, A. Lopez-Carranza, L.M. Scavo and F. de Pablo, Insulin and insulin-like growth factor system components gene expression in the chicken retina from early neurogenesis until late development and their effect on neuroepithelial cells. Eur J Neurosci, 6, 1801–1810 (1994).

    Article  PubMed  Google Scholar 

  26. J.L. Marks, D. Porter Jr. and D.G. Baskin, Localization of type I insulin-like growth factor receptor messenger RNA in the adult rat brain by in situ hybridization. Mol Endocrinol, 5, 1158–1168 (1991).

    PubMed  CAS  Google Scholar 

  27. L. Frago and J. Chowen, Physiology of GH-IGF axis. Chapter 1, this book.

    Google Scholar 

  28. J.L. Trejo, E. Cairo and D.J. Burks, Title experimental models for understanding the role of Igf-I and its receptor during development (Chapter 3, this book).

    Google Scholar 

  29. M. Torres and F. Giraldez, The development of the vertebrate inner ear. Mech Dev, 71, 5–21 (1998).

    Article  PubMed  CAS  Google Scholar 

  30. C.V. Baker and M. Bronner-Fraser, Vertebrate cranial placodes I. Embryonic induction. Dev Biol, 232, 1–61 (2001).

    Article  PubMed  CAS  Google Scholar 

  31. M.L. Breitman, D.M. Bryce, E. Giddens, S. Clapoff, D. Goring, L.C. Tsui, G.K. Klintworth and A. Bernstein, Analysis of lens cell fate and eye morphogenesis in transgenic mice ablated for cells of the lens lineage. Development, 106, 457–463 (1989).

    PubMed  CAS  Google Scholar 

  32. L. Harrington, G.K. Klintworth, T.E. Secor and M.L. Breitman, Developmental analysis of ocular morphogenesis in alpha A-crystallin/diphtheria toxin transgenic mice undergoing ablation of the lens. Dev Biol, 148, 508–516 (1991).

    Article  PubMed  CAS  Google Scholar 

  33. D.C. Beebe and J.M. Coats, The lens organizes the anterior segment: specification of neural crest cell differentiation in the avian eye. Dev Biol, 220, 424–431 (2000).

    Article  PubMed  CAS  Google Scholar 

  34. C.J. Thut, R.B. Rountree, M. Hwa and D.M. Kingsley, A large-scale in situ screen provides molecular evidence for the induction of eye anterior segment structures by the developing lens. Dev Biol, 231, 63–76 (2001).

    Article  PubMed  CAS  Google Scholar 

  35. B. Alsina, F. Giráldez and I. Varela-Nieto, in: Growth factors and early development of otic neurons: interactions between intrinsic and extrinsic signals. Edited by R Romand and I. Varela-Nieto (Elsevier Academic Press, San Diego, California, USA, 2003) pp. 177–206.

    Google Scholar 

  36. G. Camarero, C. Avendano, C. Fernandez-Moreno, A. Villar, J. Contreras, F. de Pablo, J.G. Pichel and I. Varela-Nieto, Delayed inner ear maturation and neuronal loss in postnatal Igf-1-deficient mice. J Neurosci, 21, 7630–7641 (2001).

    PubMed  CAS  Google Scholar 

  37. S.E. Boucher and P.F. Hitchcock, Insulin-related growth factors stimulate proliferation of retinal progenitors in the goldfish. J Comp Neurol, 394, 386–394 (1998).

    Article  PubMed  CAS  Google Scholar 

  38. C. Hernandez-Sanchez, A. Lopez-Carranza, C. Alarcon, E.J. de La Rosa and F. de Pablo, Autocrine/paracrine role of insulin-related growth factors in neurogenesis: local expression and effects on cell proliferation and differentiation in retina. Proc Natl Acad Sci USA, 92, 9834–9838 (1995).

    Article  PubMed  CAS  Google Scholar 

  39. A.F. Mack and R.D. Fernald, Regulation of cell division and rod differentiation in the teleost retina. Brain Res Dev Brain Res, 76, 183–187 (1993).

    Article  PubMed  CAS  Google Scholar 

  40. Y. Leon, E. Vazquez, C. Sanz, J.A. Vega, J.M. Mato, F. Giraldez, J. Represa and I. Varela-Nieto, Insulin-like growth factor-I regulates cell proliferation in the developing inner ear, activating glycosyl-phosphatidylinositol hydrolysis and Fos expression. Endocrinology, 136, 3494–3503 (1995).

    Article  PubMed  CAS  Google Scholar 

  41. N. Lu, I.B. Black and E. DiCicco-Bloom, A paradigm for distinguishing the roles of mitogenesis and trophism in neuronal precursor proliferation. Brain Res Dev Brain Res, 94, 31–36 (1996).

    Article  PubMed  CAS  Google Scholar 

  42. M. Mathonnet, P. Cubertafond, A. Gainant and C. Ayer-Le Lievre, The avian peripheral olfactory system: model for study of apoptosis and cellular regeneration. Ann Chir, 126, 888–895 (2001).

    Article  PubMed  CAS  Google Scholar 

  43. Y. Leon, C. Sanz, F. Giraldez and I. Varela-Nieto, Induction of cell growth by insulin and insulin-like growth factor-I is associated with Jun expression in the otic vesicle. J Comp Neurol, 398, 323–332 (1998).

    Article  PubMed  CAS  Google Scholar 

  44. M. Sondell, A. Fex-Svenningsen and M. Kanje, The insulin-like growth factors I and II stimulate proliferation of different types of Schwann cells. Neuroreport, 8, 2871–2876 (1997).

    PubMed  CAS  Google Scholar 

  45. H.J. Stewart, F. Bradke, A. Tabernero, D. Morrell, K.R. Jessen and R. Mirsky, Regulation of rat Schwann cell Po expression and DNA synthesis by insulin-like growth factors in vitro. Eur J Neurosci, 8, 553–564 (1996).

    Article  PubMed  CAS  Google Scholar 

  46. C. Alarcon, J. Serna, B. Perez-Villamil and F. de Pablo, Synthesis and differentially regulated processing of proinsulin in developing chick pancreas, liver and neuroretina. FEBS Lett, 436, 361–366 (1998).

    Article  PubMed  CAS  Google Scholar 

  47. B. Diaz, B. Pimentel, F. de Pablo and E.J. de La Rosa, Apoptotic cell death of proliferating neuroepithelial cells in the embryonic retina is prevented by insulin. Eur J Neurosci, 11, 1624–1632 (1999).

    Article  PubMed  CAS  Google Scholar 

  48. H.B. Rind and C.S. von Bartheld, Target-derived cardiotrophin-1 and insulin-like growth factor-I promote neurite growth and survival of developing oculomotor neurons. Mol Cell Neurosci, 19, 58–71 (2002).

    Article  PubMed  CAS  Google Scholar 

  49. B.R. Ryu, H.W. Ko, I. Jou, J.S. Noh and B.J. Gwag, Phosphatidylinositol 3-kinase-mediated regulation of neuronal apoptosis and necrosis by insulin and IGF-I. J Neurobiol, 39, 536–546 (1999).

    Article  PubMed  CAS  Google Scholar 

  50. P. Kermer, R. Ankerhold, N. Klocker, S. Krajewski, J.C. Reed and M. Bahr, Caspase-9: involvement in secondary death of axotomized rat retinal ganglion cells in vivo. Brain Res Mol Brain Res, 85, 144–150 (2000).

    Article  PubMed  CAS  Google Scholar 

  51. P. Kermer, N. Klocker, M. Labes and M. Bahr, Insulin-like growth factor-I protects axotomized rat retinal ganglion cells from secondary death via PI3-K-dependent Akt phosphorylation and inhibition of caspase-3 In vivo. J Neurosci, 20, 2–8 (2000).

    PubMed  CAS  Google Scholar 

  52. B. Diaz, J. Serna, F. De Pablo and E.J. de la Rosa, In vivo regulation of cell death by embryonic (pro)insulin and the insulin receptor during early retinal neurogenesis. Development, 127, 1641–1649 (2000).

    PubMed  CAS  Google Scholar 

  53. CM. Cheng, G. Joncas, R.R. Reinhardt, R. Farrer, R. Quarles, J. Janssen, M.P. McDonald, J.N. Crawley, L. Powell-Braxton and C.A. Bondy, Biochemical and morphometric analyses show that myelination in the insulin-like growth factor 1 null brain is proportionate to its neuronal composition. J Neurosci, 18, 5673–5681 (1998).

    PubMed  CAS  Google Scholar 

  54. R.W. Oppenheim, Cell death during development of the nervous system. Annu Rev Neurosci, 14, 453–501 (1991).

    Article  PubMed  CAS  Google Scholar 

  55. W.M. Campana, S.J. Darin and J.S. O’Brien, Phosphatidylinositol 3-kinase and Akt protein kinase mediate IGF-I-and prosaptide-induced survival in Schwann cells. J Neurosci Res, 57, 332–341 (1999).

    Article  PubMed  CAS  Google Scholar 

  56. H.L. Cheng, M.L. Steinway, X. Xin and E.L. Feldman, Insulin-like growth factor-I and Bcl-X(L) inhibit c-jun N-terminal kinase activation and rescue Schwann cells from apoptosis. J Neurochem, 76, 935–943 (2001).

    Article  PubMed  CAS  Google Scholar 

  57. C.L. Delaney, J.W. Russell, H.L. Cheng and E.L. Feldman, Insulin-like growth factor-I and over-expression of Bcl-xL prevent glucose-mediated apoptosis in Schwann cells. J Neuropathol Exp Neurol, 60, 147–160 (2001).

    PubMed  CAS  Google Scholar 

  58. C.L. Delaney, H.L. Cheng and E.L. Feldman, Insulin-like growth factor-I prevents caspase-mediated apoptosis in Schwann cells. J Neurobiol, 41, 540–548 (1999).

    Article  PubMed  CAS  Google Scholar 

  59. C. Meier, E. Parmantier, A. Brennan, R. Mirsky and K.R. Jessen, Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor, neurotrophin-3, and platelet-derived growth factor-BB. J Neurosci, 19, 3847–3859 (1999).

    PubMed  CAS  Google Scholar 

  60. J.M. Frade, E. Marti, P. Bovolenta, M.A. Rodriguez-Pena, D. Perez-Garcia, H. Rohrer, D. Edgar and A. Rodriguez-Tebar, Insulin-like growth factor-I stimulates neurogenesis in chick retina by regulating expression of the alpha 6 integrin subunit. Development, 122, 2497–2506 (1996).

    PubMed  CAS  Google Scholar 

  61. R.E. Hausman, G.D. Sagar and B.H. Shah, Initial cholinergic differentiation in embryonic chick retina is responsive to insulin and cell-cell interactions. Brain Res Dev Brain Res, 59, 31–37 (1991).

    Article  PubMed  CAS  Google Scholar 

  62. B.H. Shah and R.E. Hausman, Effects of cell signaling on the development of GABA receptors in chick retina neurons. Neurochem Res, 18, 957–964 (1993).

    Article  PubMed  CAS  Google Scholar 

  63. B. Pettmann and C.E. Henderson, Neuronal cell death. Neuron, 20, 633–647 (1998).

    Article  PubMed  CAS  Google Scholar 

  64. C. Vicario-Abejon, M.J. Yusta-Boyo, C. Fernandez-Moreno and F. de Pablo, Locally born olfactory bulb stem cells proliferate in response to insulin-related factors and require endogenous insulin-like growth factor-I for differentiation into neurons and glia. J Neurosci, 23, 895–906 (2003).

    PubMed  CAS  Google Scholar 

  65. H.L. Cheng and E.L. Feldman, Insulin-like growth factor-I (IGF-I) and IGF binding protein-5 in Schwann cell differentiation. J Cell Physiol, 171, 161–167 (1997).

    Article  PubMed  CAS  Google Scholar 

  66. H.L. Cheng, M. Shy and E.L. Feldman, Regulation of insulin-like growth factor-binding protein-5 expression during Schwann cell differentiation. Endocrinology, 140, 4478–4485 (1999).

    Article  PubMed  CAS  Google Scholar 

  67. T.A. Janiga, H.B. Rind and C.S. von Bartheld, Differential effects of the trophic factors BDNF, NT-4, GDNF, and IGF-I on the isthmo-optic nucleus in chick embryos. J Neurobiol, 43, 289–303 (2000).

    Article  PubMed  CAS  Google Scholar 

  68. K.A. Roth and C. D’Sa, Apoptosis and brain development. Ment Retard Dev Disabil Res Rev, 7, 261–266 (2001).

    Article  PubMed  CAS  Google Scholar 

  69. A.L. Calof, N. Hagiwara, J.D. Holcomb, J.S. Mumm and J. Shou, Neurogenesis and cell death in olfactory epithelium. J Neurobiol, 30, 67–81 (1996).

    Article  PubMed  CAS  Google Scholar 

  70. H.A. Cameron, T.G. Hazel and R.D. McKay, Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol, 36, 287–306 (1998).

    Article  PubMed  CAS  Google Scholar 

  71. G. Camarero, M.A. Villar, J. Contreras, C. Fernandez-Moreno, J.G. Pichel, C. Avendano and I. Varela-Nieto, Cochlear abnormalities in insulin-like growth factor-1 mouse mutants. Hear Res, 170, 2–11 (2002).

    Article  PubMed  CAS  Google Scholar 

  72. L.A. Blair and J. Marshall, IGF-1 modulates N and L calcium channels in a PI 3-kinase-dependent manner. Neuron, 19, 421–429 (1997).

    Article  PubMed  CAS  Google Scholar 

  73. R. Salceda, Insulin-stimulated taurine uptake in rat retina and retinal pigment epithelium. Neurochem Int. 35, 301–306 (1999).

    Article  PubMed  CAS  Google Scholar 

  74. S.L. Stella, E.J. Bryson Jr. and W.B. Thoreson, Insulin inhibits voltage-dependent calcium influx into rod photoreceptors. Neuroreport, 12, 947–951 (2001).

    Article  PubMed  CAS  Google Scholar 

  75. Federico, C. Maremmani, V. Cinquanta, G.I. Baroncelli, G. Fattori and V. Saggese, Mucus of the human olfactory epithelium contains the insulin-like growth factor-I system which is altered in some neurodegenerative diseases. Brain Res, 835, 306–314 (1999).

    Article  PubMed  CAS  Google Scholar 

  76. K.A. Woods, C. Camacho-Hubner, M.O. Savage and A.J. Clark, Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N Engl J Med, 335, 1363–1367 (1996).

    Article  PubMed  CAS  Google Scholar 

  77. K.A. Woods, C. Camacho-Hubner, D. Barter, A.J. Clark and M.O. Savage, Insulin-like growth factor I gene deletion causing intrauterine growth retardation and severe short stature. Ada Paediatr Suppl, 423, 39–45 (1997).

    CAS  Google Scholar 

  78. M. Barrenasa, K. Landin-Wilhelmsenb and C. Hansonc, Ear and hearing in relation to genotype and growth in Turner syndrome. Hear Res, 144, 21–28 (2000).

    Article  Google Scholar 

  79. M. Holzenberger, P. Leneuve, G. Hamard, B. Ducos, L. Perin, M. Binoux and Y. Le Bouc, A targeted partial invalidation of the insulin-like growth factor I receptor gene in mice causes a postnatal growth deficit. Endocrinology, 141, 2557–2566 (2000).

    Article  PubMed  CAS  Google Scholar 

  80. Z. Laron, Growth hormone insensitivity (Laron syndrome). Rev Endocr Metab Disord, 3, 347–355 (2002).

    Article  PubMed  CAS  Google Scholar 

  81. Z. Laron, Laron syndrome (primary growth hormone resistance or insensitivity): the personal experience 1958–2003. J Clin Endocrinol Metab, 89, 1031–1044 (2004).

    Article  PubMed  CAS  Google Scholar 

  82. G. Bonapace, D. Concolino, S. Formicola and P. Strisciuglio, A novel mutation in a patient with insulin-like growth factor 1 (IGF1) deficiency. J Med Genet, 40, 913–917 (2003).

    Article  PubMed  CAS  Google Scholar 

  83. X.M. Ouyang, D. Yam, J.F. Hejtmancik, S.G. Jacobson, A.R. Li, L.L. Du, S. Angeli, M. Kaiser, T. Balkany and X.Z. Liu, Mutational spectrum in Usher syndrome type II. Clin Genet, 65, 288–293 (2004).

    Article  PubMed  CAS  Google Scholar 

  84. M.J. Abuzzahab, A. Schneider, A. Goddard, F. Grigorescu, C. Lautier, E. Keller, W. Kiess, J. Klammt, J. Kratzsch, D. Osgood, R. Pfaffle, K. Raile, B. Seidel, R.J. Smith, and S.D. Chernausek, IGF-I receptor mutations resulting in intrauterine and postnatal growth retardation. N Engl J Med, 349, 2211–2222 (2003).

    Article  PubMed  CAS  Google Scholar 

  85. H. Ehara, C. Nakano, K. Ohno, Y.I. Goto and K. Takeshita, New autosomal-recessive syndrome of Leber congenital amaurosis, short stature, growth hormone insufficiency, mental retardation, hepatic dysfunction, and metabolic acidosis. Am J Med Genet, 71, 258–266 (1997).

    Article  PubMed  CAS  Google Scholar 

  86. C.L. Campbell, Septo-optic dysplasia: a literature review. Optometry, 74, 417–426 (2003).

    PubMed  Google Scholar 

  87. S. Harvey, CD. Johnson and E.J. Sanders, Extra-pituitary growth hormone in peripheral tissues of early chick embryos. J Endocrinol, 166, 489–502 (2000).

    Article  PubMed  CAS  Google Scholar 

  88. S. Harvey, CD. Johnson and E.J. Sanders, Growth hormone in neural tissues of the chick embryo. J Endocrinol, 169, 487–498 (2001).

    Article  PubMed  CAS  Google Scholar 

  89. S. Harvey and K. Hull, Neural growth hormone: an update. J Mol Neurosci, 20, 1–14 (2003).

    Article  PubMed  CAS  Google Scholar 

  90. S. Harvey, M. Kakebeeke, A.E. Murphy and E.J. Sanders, Growth hormone in the nervous system: autocrine or paracrine roles in retinal function? Can J Physiol Pharmacol, 81, 371–384 (2003).

    Article  PubMed  CAS  Google Scholar 

  91. S. Takeuchi, M. Haneda, K. Teshigawara and S. Takahashi, Identification of a novel GH isoform: a possible link between GH and melanocortin systems in the developing chicken eye. Endocrinology, 142, 5158–5166 (2001).

    Article  PubMed  CAS  Google Scholar 

  92. M.L. Baudet, E.J. Sanders and S. Harvey, Retinal growth hormone in the chick embryo. Endocrinology, 144, 5459–5468 (2003).

    Article  PubMed  CAS  Google Scholar 

  93. A. Hellstrom, E. Svensson, B. Carlsson, A. Niklasson and K. Albertsson-Wikland, Reduced retinal vascularization in children with growth hormone deficiency. J Clin Endocrinol Metab, 84, 795–798 (1999).

    Article  PubMed  CAS  Google Scholar 

  94. I. Struman, F. Bentzien, H. Lee, V. Mainfroid, G. D’Angelo, V. Goffin, R.I. Weiner and J.A. Martial, Opposing actions of intact and N-terminal fragments of the human prolactin/growth hormone family members on angiogenesis: an efficient mechanism for the regulation of angiogenesis. Proc Natl Acad Sci USA, 96, 1246–1251 (1999).

    Article  PubMed  CAS  Google Scholar 

  95. F. de Pablo, L.A. Scott and J. Roth, Insulin and insulin-like growth factor I in early development: peptides, receptors and biological events. Endocr Rev, 11, 558–577 (1990).

    Article  PubMed  Google Scholar 

  96. J.J. Kopchick and S. Okada, Growth hormone receptor antagonists: discovery and potential uses. Growth Horm IGF Res, 11Suppl A, S103–109 (2001).

    Article  PubMed  Google Scholar 

  97. S. Okada and J.J. Kopchick, Biological effects of growth hormone and its antagonist. Trends Mol Med, 7, 126–132 (2001).

    Article  PubMed  CAS  Google Scholar 

  98. A. Bereket, C.H. Lang, M.E. Geffner and T.A. Wilson, Normal growth in a patient with septo-optic dysplasia despite both growth hormone and IGF-I deficiency. J Pediatr Endocrinol Metab, 11, 69–75 (1998).

    PubMed  CAS  Google Scholar 

  99. E.H. Hathout, D.J. Baylink and S. Mohan, Normal growth despite GH, IGF-I and IGF-II deficiency. Growth Horm IGF Res, 9, 272–277 (1999).

    Article  PubMed  CAS  Google Scholar 

  100. L. Lazar, S. Dan and M. Phillip, Growth without growth hormone: growth pattern and final height of five patients with idiopathic combined pituitary hormone deficiency, Clin Endocrinol (Oxf), 59, 82–88 (2003).

    Article  CAS  Google Scholar 

  101. M. Ishihara, Optic hypoplasia with pituitary dwarfism (Kaplan-Grumbach-Hoyt syndrome, or DeMorsier syndrome). Endocrinol Jpn, 30, 7–14 (1983).

    PubMed  CAS  Google Scholar 

  102. K. Miyako, M. Takemoto, K. Ihara, R. Kuromaru, H. Kohno and T. Hara, A case of growth hormone and gonadotropin deficiency associated with unilateral anophthalmia, microphallus, cryptorchidism, and mental retardation. Endocr J, 49, 15–20 (2002).

    Article  PubMed  Google Scholar 

  103. A.M. Roth, Retinal vascular development in premature infants. Am J Ophthalmol, 84, 636–640 (1977).

    PubMed  CAS  Google Scholar 

  104. A. Hellstrom, C. Perruzzi, M. Ju, E. Engstrom, A.L. Hard, J.L. Liu, K. Albertsson-Wikland, B. Carlsson, A. Niklasson, L. Sjodell, D. LeRoith, D.R. Senger and L.E. Smith, Low IGF-I suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci USA, 98, 5804–5808 (2001).

    Article  PubMed  CAS  Google Scholar 

  105. A. Hellstrom, B. Carlsson, A. Niklasson, K. Segnestam, M. Boguszewski, L. de Lacerda, M. Savage, E. Svensson, L. Smith, D. Weinberger, K. Albertsson Wikland and Z. Laron, IGF-I is critical for normal vascularization of the human retina. J Clin Endocrinol Metab, 87, 3413–3416 (2002).

    Article  PubMed  CAS  Google Scholar 

  106. L.E. Smith, J.J. Kopchick, W. Chen, J. Knapp, F. Kinose, D. Daley, E. Foley, R.G. Smith and J.M. Schaeffer, Essential role of growth hormone in ischemia-induced retinal neovascularization. Science, 276, 1706–1709 (1997).

    Article  PubMed  CAS  Google Scholar 

  107. P.H. Francis-West, R.K. Ladher and G.C. Schoenwolf, Development of the sensory organs. Sci Prog, 85, 151–173 (2002).

    Article  PubMed  Google Scholar 

  108. M. Schwanzel-Fukuda and D.W. Pfaff, The migration of luteinizing hormone-releasing hormone (LHRH) neurons from the medial olfactory placode into the medial basal forebrain. Experientia, 46, 956–962 (1990).

    Article  PubMed  CAS  Google Scholar 

  109. H.L. Eisthen, R.J Delay, C.R. Wirsig-Wiechmann and V.E. Dionne, Neuromodulatory effects of gonadotropin releasing hormone on olfactory receptor neurons. J Neurosci, 20, 3947–3955 (2000).

    PubMed  CAS  Google Scholar 

  110. A.I. Farbman, Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci, 13, 362–365 (1990).

    Article  PubMed  CAS  Google Scholar 

  111. R. Doucette, Glial cells in the nerve fiber layer of the main olfactory bulb of embryonic and adult mammals. Microsc Res Tech, 24, 113–130 (1993).

    Article  PubMed  CAS  Google Scholar 

  112. I. Arsenejevic, Future perspectives-stem cells (Chapter 17, this book).

    Google Scholar 

  113. M.T. Moreno-Flores, J. Diaz-Nido, F. Wandosell and J. Avila, Olfactory Ensheathing Glia: Drivers of Axonal Regeneration in the Central Nervous System? J Biomed Biotechnol, 2, 37–43 (2002).

    Article  PubMed  CAS  Google Scholar 

  114. A.G. Monti-Graziadei, Cell migration from the olfactory neuroepithelium of neonatal and adult rodents. Brain Res Dev Brain Res, 70, 65–74 (1992).

    Article  PubMed  CAS  Google Scholar 

  115. M. Caggiano, J.S. Kauer and D.D Hunter, Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron, 13, 339–352 (1994).

    Article  PubMed  CAS  Google Scholar 

  116. M. Schwartz Levey, D.M. Chikaraishi and J.S. Kauer, Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J Neurosci, 11, 3556–3564 (1991).

    PubMed  CAS  Google Scholar 

  117. J.L. Willian, Development of the head and neck, in: Human Embryology, third edition, edited by L.S. Sherman, S.S. Potter, W.J. Scott (Churchill Livingstone, New York, Edinburg, London, Philadelphia, 2001), pp. 351–378.

    Google Scholar 

  118. M. Brown, R. Keynes and A. Lumsden, Development of sense organs, in: The Developing Brain, (Oxford University Press, New York, 2001) pp. 194–217.

    Google Scholar 

  119. I.V. Nosrat, S. Lindskog, A. Seiger and C.A. Nosrat, Lingual BDNF and NT-3 mRNA expression patterns and their relation to innervation in the human tongue: similarities and differences compared with rodents. J Comp Neurol, 417, 133–152 (2000).

    Article  PubMed  CAS  Google Scholar 

  120. C.A. Nosrat, D.K. MacCallum and CM. Mistretta, Distinctive spatiotemporal expression patterns for neurotrophins develop in gustatory papillae and lingual tissues in embryonic tongue organ cultures. Cell Tissue Res, 303, 35–45 (2001).

    Article  PubMed  CAS  Google Scholar 

  121. I. Nosrat, A. Seiger, L. Olson and C.A. Nosrat, Expression patterns of neurotrophic factor mRNAs in developing human teeth. Cell Tissue Res, 310, 177–187 (2002).

    Article  PubMed  CAS  Google Scholar 

  122. T. Ringstedt, C.F. Ibanez and C.A. Nosrat, Role of brain-derived neurotrophic factor in target invasion in the gustatory system. J Neurosci, 19, 3507–3518 (1999).

    PubMed  CAS  Google Scholar 

  123. CM. Mistretta, K.A. Goosens, I. Farinas and L.F. Reichardt, Alterations in size, number, and morphology of gustatory papillae and taste buds in BDNF null mutant mice demonstrate neural dependence of developing taste organs. J Comp Neurol, 409, 13–24 (1999).

    Article  PubMed  CAS  Google Scholar 

  124. K.O. Johnson, The roles and functions of cutaneous mechanoreceptors. Curr Opin Neurobiol, 11, 455–461 (2001).

    Article  PubMed  CAS  Google Scholar 

  125. J. Zelena and I. Jirmanova, Reinnervation of rat Pacinian corpuscles after nerve crush during the postcritical period of development. J Neurocytol, 24, 955–964 (1995).

    Article  PubMed  CAS  Google Scholar 

  126. B.T. Fundin, I. Silos-Santiago, P. Ernfors, A.M. Fagan, H. Aldskogius, T.M. DeChiara, U.S. Phillips, M. Barbacid, G.D. Yancopoulos and F.L. Rice, Differential dependency of cutaneous mechanoreceptors on neurotrophins, trk receptors, and P75 LNGFR. Dev Biol, 190, 94–116 (1997).

    Article  PubMed  CAS  Google Scholar 

  127. P. Ernfors, K.F. Lee and R. Jaenisch, Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature, 368, 147–150 (1994).

    Article  PubMed  CAS  Google Scholar 

  128. P. Ernfors, K.F. Lee, J. Kucera and R. Jaenisch, Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell, 77, 503–512 (1994).

    Article  PubMed  CAS  Google Scholar 

  129. R. Cantos, L.K. Cole, D. Acampora, A. Simeone and D.K. Wu, Patterning of the mammalian cochlea. Proc Natl Acad Sci U S A 97, 11707–13 (2000).

    Article  PubMed  CAS  Google Scholar 

  130. D.M. Fekete and D. K. Wu, Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol, 12, 35–42 (2002).

    Article  PubMed  CAS  Google Scholar 

  131. L.D. Saffer, R. Gu and J.T. Corwin, An RT-PCR analysis of mRNA for growth factor receptors in damaged and control sensory epithelia of rat utricles. Hear Res, 94, 14–23 (1996).

    Article  PubMed  CAS  Google Scholar 

  132. K.H. Lee and D.A. Cotanche, Localization of the hair-cell-specific protein fimbrin during regeneration in the chicken cochlea. Audiol Neurootol, 1, 41–53 (1996).

    PubMed  CAS  Google Scholar 

  133. B.L. Resendes, N.G. Robertson, J.D. Szustakowski, R.J. Resendes, Z. Weng and C.C. Morton, Gene discovery in the auditory system: characterization of additional cochlear-expressed sequences. J Assoc Res Otolaryngol, 3, 45–53 (2002).

    Article  PubMed  Google Scholar 

  134. Y. Cho, T.W. Gong, T. Stover, M.I. Lomax and R.A. Altschuler, Gene expression profiles of the rat cochlea, cochlear nucleus, and inferior colliculus. J Assoc Res Otolaryngol, 3, 54–67 (2002).

    Article  PubMed  Google Scholar 

  135. I. Varela-Nieto, J.A. Morales-Garcia, P. Vigil, A. Diaz-Casares, I. Gorospe, S. Sánchez-Galiano, S. Cañon, G. Camarero, J. Contreras, R. Cediel and Y. Leon, Trophic effects of Insulin-like growth factor-I (IGF-I) in the inner ear. Hearing Research (in press) (2004).

    Google Scholar 

  136. L.M. Frago, G. Camarero, S. Canon, C. Paneda, C. Sanz, Y. Leon, F. Giraldez and I. Varela-Nieto, Role of diffusible and transcription factors in inner ear development: implications in regeneration. Histol Histopathol, 15, 657–666 (2000).

    PubMed  CAS  Google Scholar 

  137. C. Sanz, Y. Leon, S. Canon, L. Alvarez, F. Giraldez, and I. Varela-Nieto, Pattern of expression of the jun family of transcription factors during the early development of the inner ear: implications in apoptosis. J Cell Sci, 112 ( Pt 22), 3967–3974 (1999).

    PubMed  CAS  Google Scholar 

  138. C. Sanz, Y. Leon, J. Troppmair, U. R. Rapp and I. Varela-Nieto, Strict regulation of c-Raf kinase levels is required for early organogenesis of the vertebrate inner ear. Oncogene, 18, 429–437 (1999).

    Article  PubMed  CAS  Google Scholar 

  139. L. M. Frago, S. Canon, E. J. de la Rosa, Y. Leon, and I. Varela-Nieto, Programmed cell death in the developing inner ear is balanced by nerve growth factor and insulin-like growth factor I. J Cell Sci, 116, 475–486 (2003).

    Article  PubMed  CAS  Google Scholar 

  140. G. Camarero, Y. Leon, I. Gorospe, F. De Pablo, B. Alsina, F. Giraldez, and I. Varela-Nieto, Insulin-like growth factor 1 is required for survival of transit-amplifying neuroblasts and differentiation of otic neurons. Dev Biol, 262, 242–253 (2003).

    Article  PubMed  CAS  Google Scholar 

  141. E.C. Oesterle, T.T. Tsue and E.W. Rubel, Induction of cell proliferation in avian inner ear sensory epithelia by insulin-like growth factor-I and insulin. J Comp Neurol, 380, 262–274 (1997).

    Article  PubMed  CAS  Google Scholar 

  142. A.L. Kuntz and E.C. Oesterle, Transforming growth factor alpha with insulin stimulates cell proliferation in vivo in adult rat vestibular sensory epithelium. J Comp Neurol, 399, 413–423 (1998).

    Article  PubMed  CAS  Google Scholar 

  143. H. Staecker and T.R. Van De Water, Factors controlling hair-cell regeneration/repair in the inner ear. Curr Opin Neurobiol, 8, 480–487 (1998).

    Article  PubMed  CAS  Google Scholar 

  144. R. Romand and S. Chardin, Effects of growth factors on the hair cells after ototoxic treatment of the neonatal mammalian cochlea in vitro. Brain Res, 825, 46–58 (1999).

    Article  PubMed  CAS  Google Scholar 

  145. M. Duan, K. Agerman, P. Ernfors and B. Canlon, Complementary roles of neurotrophin 3 and a N-methyl-D-aspartate antagonist in the protection of noise and aminoglycoside-induced ototoxicity. Proc Natl Acad Sci USA, 97, 7597–7602 (2000).

    Article  PubMed  CAS  Google Scholar 

  146. D.J. Stacey and W.G. McLean, Cytoskeletal protein mRNA expression in the chick utricle after treatment in vitro with aminoglycoside antibiotics: effects of insulin, iron chelators and cyclic nucleotides. Brain Res, 871, 319–332 (2000).

    Article  PubMed  CAS  Google Scholar 

  147. R.D. Kopke, R.L. Jackson, G. Li, M.D. Rasmussen, M.E. Hoffer, D.A. Frenz, M. Costello, P. Schultheiss and T.R. Van De Water, Growth factor treatment enhances vestibular hair cell renewal and results in improved vestibular function. Proc Natl Acad Sci USA, 98, 5886–5891 (2001).

    Article  PubMed  CAS  Google Scholar 

  148. S. Kanzaki, T. Stover, K. Kawamoto, D.M. Prieskorn, R.A. Altschuler, J.M. Miller and Y. Raphael, Glial cell line-derived neurotrophic factor and chronic electrical stimulation prevent VIII cranial nerve degeneration following denervation. J Comp Neurol, 454, 350–360 (2002).

    Article  PubMed  CAS  Google Scholar 

  149. B. Malgrange, J.M. Rigo, P. Coucke, M. Thiry, G. Hans, L. Nguyen, T.R. van de Water, G. Moonen and P.P. Lefebvre, Identification of factors that maintain mammalian outer hair cells in adult organ of Corti explants. Hear Res, 170, 48–58 (2002).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2005 Springer Science+Business Media, Inc.

About this chapter

Cite this chapter

Diaz-Casares, A., Leon, Y., de la Rosa, E.J., Varela-Nieto, I. (2005). Regulation of Vertebrate Sensory Organ Development: A Scenario for Growth Hormone and Insulin-Like Growth Factors Action. In: Varela-Nieto, I., Chowen, J.A. (eds) The Growth Hormone/Insulin-Like Growth Factor Axis During Development. Advances in Experimental Medicine and Biology, vol 567. Springer, Boston, MA. https://doi.org/10.1007/0-387-26274-1_9

Download citation

  • DOI: https://doi.org/10.1007/0-387-26274-1_9

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-0-387-25119-6

  • Online ISBN: 978-0-387-26274-1

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics