The hedgehog-PKA pathway regulates two distinct steps of the differentiation of retinal ganglion cells: The cell-cycle exit of retinoblasts and their neuronal maturation

Development

Volumn 132, Issue 7, 2005, Pages 1539-1553

  Masai, Ichiro ^a   Yamaguchi, Masahiro ^a   Tonou Fujimori, Noriko ^a   Komori, Atsuko ^a   Okamoto, Hitoshi ^b  

^a INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

cAMP dependent protein kinase; Cyclin D; Danio rerio; p27; Wnt; Zebrafish

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; FORSKOLIN; PROTEIN KINASE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; WNT PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; GENE EXPRESSION; IN SITU HYBRIDIZATION; MITOSIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RETINA DEVELOPMENT; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; STEM CELL; ZEBRA FISH;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; FORSKOLIN; GENE EXPRESSION; GROWTH SUBSTANCES; HEDGEHOG PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOSIS; NEURONS; ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; RETINA; RETINAL GANGLION CELLS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; WNT PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 17744384947     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01714     Document Type: Article

References (67)

1. Barresi, M. J. F., Stickney, H. L. and Devoto, S. H. (2000). The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development 127, 2189-2199.
2. Britto, J., Tannahill, D. and Keynes, R. (2002). A critical role for sonic hedgehog signaling in the early expansion of the developing brain. Nat. Neurosci. 5, 103-110.
3. Chen, J. K., Taipale, J., Cooper, M. K. and Beachy, P. A. (2002). Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16, 2743-2748.
4. Chenn, A. and Walsh, C. A. (2002). Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365-369.
5. Chuang, J. C., Mathers, P. H. and Raymond, P. A. (1999). Expression of three Rx homeobox genes in embryonic and adult zebrafish. Mech. Dev. 84, 195-198.
6. Cohen, M. M., Jr (2003). The hedgehog signaling network. Am. J. Med. Genet. 123A, 5-28.
7. Concordet, J.-P., Lewis, K. E., Moore, J. W., Goodrich, L. V., Johnson, R. L., Scott, M. P. and Ingham, P. W. (1996). Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122, 2835-2846.
8. Cooper, M. K., Porter, J. A., Young, K. E. and Beachy, P. A. (1998). Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 280, 1603-1607.
9. Dorsky, R. I., Sheldahl, L. C. and Moon, R. T. (2002). A transgenic Lef1/β-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev. Biol. 241, 229-237.
10. Dowling, J. (1987). The Retina. Cambridge, MA: Harvard University Press.
11. Duman-Scheel, M., Weng, L., Xin, S. and Du, W. (2002). Hedgehog regulates cell growth and proliferation by inducing Cyclin D and Cyclin E. Nature 417, 299-304.
12. Dyer, M. A. and Cepko, C. L. (2001). Regulating proliferation during retinal development. Nat. Rev. Neurosci. 2 333-342.
13. Fantl, V., Stamp, G., Andrews, A., Rosewell, I. and Dickson, C. (1995). Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev. 9, 2364-2372.
14. Galderisi, U., Jori, F. P. and Giordano, A. (2003). Cell cycle regulation and neuronal differentiation. Oncogene 22 5208-5219.
15. Kip1 gene restores normal development in cyclin D1-deficient mice. Proc. Natl. Acad. Sci. USA 98, 194-199.
16. Glasgow, E., Karavanov, A. A. and Dawid, I. B. (1997). Neuronal and neuroendcrine expression of lim3, a LIM class homeobox gene, is altered in mutant zebrafish with axial signaling defects. Dev. Biol. 192, 405-419.
17. Halloran, M. C., Sato-Maeda, M., Warren, J. T., Su, F., Lele, Z., Krone, P. H., Kuwada, J. Y. and Shoji, W. (2000). Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127, 1953-1960.
18. Hammerschmidt, M., Bitgood, M. J. and McMahon, A. P. (1996). Protein kinase A is a common negative regulator of Hedgehog signaling in the vertebrate embryo. Genes Dev. 10, 647-658.
19. Hu, M. and Easter, S. S., Jr (1999). Retinal neurogenesis: the formation of the initial central patch of postmitotic cells. Dev Biol. 207, 309-321.
20. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
21. Inoue, A., Takahashi, M., Hatta, K., Hotta, Y. and Okamoto, H. (1994). Developmental regulation of Islet-1 mRNA expression during neuronal differentiation in embryonic zebrafish. Dev. Dyn. 199, 1-11.
22. Ishibashi, M. and McMahon, A. P. (2002). A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo. Development 129, 4807-4819.
23. Karlstrom, R. O., Tyurina, O. V., Kawakami, A., Nishioka, N., Talbot, W. S., Sasaki, H. and Schier, A. F. (2003). Genetic analysis of zebrafish gli1 and gli2 reveals divergent requirements for gli genes in vertebrate development. Development 130, 1549-1564.
24. Kay, J. N., Finger-Baier, K. C., Roeser, T., Staub, W. and Baier, H. (2001). Retinal ganglion cells genesis requires lakritz a zebrafish atonal homolog. Neuron 30, 725-736.
25. Kim, C.-H., Oda, T., Itoh, M., Jiang, D., Artinger, K. B., Chandrasekharappa, S. C., Driever, W. and Chitnis, A. B. (2000). Repressor activity of Headless/Tcf3 is essential for vertebrate head formation. Nature 407, 913-916.
26. Kubo, F., Takeichi, M. and Nakagawa, S. (2003). Wnt2b controls retinal cell differentiation at the ciliary marginal zone. Development 130, 587-598.
27. Kumar, J. P. (2001). Signalling pathways in Drosophila and vertebrate retinal development. Nat. Rev. Genet. 2, 846-857.
28. Laessing, U. and Stuermer, C. A. O. (1996). Spatiotemporal pattern of retinal ganglion cell differentiation revealed by the expression of neurolin in embryonic zebrafish. J. Neurobiol. 29, 65-74.
29. Levine, E. M. and Green, E. S. (2004). Cell-intrinsic regulators of proliferation in vertebrate retinal progenitors. Semi. Cell Dev. Biol. 15, 63-74.
30. Livesey, F. J. and Cepko, C. L. (2001). Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2, 109-118.
31. Lonze, B. E. and Ginty, D. D. (2002). Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623.
32. Macdonald, R., Barth, K. A., Xu, Q., Holder, N., Mikkola, I. and Wilson, S. W. (1995). Midline signalling is required for Pax gene regulation and patterning of the eyes. Development 121, 3267-3278.
33. Marquardt, T. and Gruss, P. (2002). Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci. 25 32-38.
34. Masai, I., Stemple, D. L., Okamoto, H. and Wilson, S. W. (2000). Midline signals regulate retinal neurogenesis in zebrafish. Neuron 27, 251-263.
35. Masai, I., Lele, Z., Yamaguchi, M., Komori, A., Nakata, A., Nishiwaki, Y., Wada, H., Tanaka, H., Nojima, Y., Hammerschmidt et al. (2003). N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neuritis. Development 130, 2479-2494.
36. Murray, A. W. (2004). Recycling the cell cycle: cyclins revisited. Cell 116, 221-234.
37. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
38. Neumann, C. J. and Nuesslein-Volhard, C. (2000). Patterning of the zebrafish retina by a wave of Sonic Hedgehog activity. Science 289, 2137-2139.
39. Ohnuma, S. and Harris, W. A. (2003). Neurogenesis and the cell cycle. Neuron 40, 199-208.
40. Ohnuma, S., Hopper, S., Wang, K. C., Philpott, A. and Harris, W. A. (2002). Co-ordinating retinal histogenesis: early cell cycle exit enhances early cell fate determination in the Xenopus retina. Development 129, 2435-2446.
41. Perron, M., Boy, S., Amato, M. A., Viczian, A., Koebernick, K., Pieler, T. and Harris, W. A. (2003). A novel function for Hedgehog signalling in retinal pigment epithelium differentiation. Development 130, 1565-1577.
42. Pons, S., Trejo, J. L., Martínez-Morales, J. R. and Martí, E. (2001). Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128, 1481-1492.
43. Pujic, Z. and Malicki, J. (2004). Retinal pattern and the genetic basis of its formation in zebrafish. Semi. Cell Dev. Biol. 15, 105-114.
44. Radtke, F. and Raj, K. (2003). The role of Notch in tumorigenesis: oncogene or tumor suppressor? Nat. Rev. Cancer 3 756-767.
45. -/- mice. Cancer Cell 6, 229-240.
46. Roy, S. and Ingham, P. W. (2002). Hedgehogs tryst with the cell cycle. J. Cell Sci. 115, 4393-4397.
47. Ruiz i Altaba, A., Palma, V. and Dahmane, N. (2002). Hedgehog-Gli signalling and the growth of the brain. Nat. Rev. Neurosci. 3, 24-33.
48. Rupp, R. A. W., Snider, L. and Weintraub, H. (1994). Xenopus embryos regulate the nuclear localization of XmyoD. Genes Dev. 8, 1311-1323.
49. Russell, C. (2003). The roles of Hedgehogs and Fibroblast Growth Factors in eye development and retinal cell rescue. Vision Res. 43, 899-912.
50. Schmitt, E. A. and Dowling, J. E. (1996). Comparison of topographical patterns of ganglion and photoreceptor cell differentiation in the retina of the zebrafish, Danio rerio. J. Comp. Neurol. 371, 222-234.
51. Shkumatava, A., Fisher, S., Müller, F., Strahle, U. and Neumann, C. J. (2004). Sonic hedgehog, secreted by amacrine cells, acts as a short-range signal to direct differentiation and lamination in the zebrafish retina. Development 131, 3849-3858.
52. Shtutman, M., Zhurinsky, J., Simcha, I., Albanese, C., D'Amico, M., Pestell, R. and Ben-Zéev, A. (1999). The cyclin D1 gene is a target of the β-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA 96, 5522-5527.
53. Sicinski, P., Donaher, J. L., Parker, S. B., Li, T., Fazeli, A., Gardner, H., Haslam, S. Z., Bronson, R. T., Elledge, S. J. and Weinberg, R. A. (1995). Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82 621-630.
54. Stenkamp, D. L., Frey, R. A., Prabhudesai, S. N. and Raymond, P. A. (2000). Function for Hedgehog genes in zebrafish retinal development. Dev. Biol. 220, 238-252.
55. Stenkamp, D. L. and Frey, R. A. (2003). Extraretinal and retinal hedgehog signaling sequentially regulate retinal differentiation in zebrafish. Dev. Biol. 258, 349-363.
56. XIC1. Proc. Natl. Acad. Sci. USA 92, 10187-10191.
57. Tetsu, O. and McCormick, F. (1999). β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426.
58. Ungar, A. R. and Moon, R. T. (1996). Inhibition of protein kinase A phenocopies ectopic expression of hedgehog in the CNS of wild-type and cyclops mutant embryos. Dev. Biol. 178, 186-191.
59. van den Brink, G. R., Bleuming, S. A., Hardwick, J. C. H., Schepman, B. L., Offerhaus, G. J., Keller, J. J., Nielsen, C., Gaffield, W., van Deventer, S. J. H., Roberts, D. J. et al. (2004). Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat. Genet. 36, 277-282.
60. van Es, J. H., Barker, N. and Clevers, H. (2003). You Wnt some, you lose some: oncogenes in the Wnt signaling pathway. Curr. Opin. Genet. Dev. 13, 28-33.
61. Varga, Z. M., Amores, A., Lewis, K. E., Yan, Y.-L., Postlethwait, J. H., Eisen, J. S. and Westerfield, M. (2001). Zebrafish smoothened functions in ventral neural tube specification and axon tract formation. Development 128, 3497-3509.
62. Wang, Y. P., Dakubo, G., Howley, P., Campsall, K. D., Mazarolle, C. J., Shiga, S. A., Lewis, P. M., McMahon, A. P. and Wallace, V. A. (2002). Development of normal retinal organization depends on Sonic hedgehog signaling from ganglion cells. Nat. Neurosci. 5 831-832.
63. Wechsler-Reya, R. J. and Scott, M. P. (1999). Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114.
64. Wei, Y. and Allis, C. D. (1998). Pictures in cell biology. Trends Cell Biol. 8, 226.
65. Williams, J. A., Guicherit, O. M., Zaharian, B. I., Xu, Y., Chai, L., Wichterle, H., Kon, C., Gatchalian, C., Porter, J. A., Rubin, L. L. and Wang, F. Y. (2003). Identification of a small molecule inhibitor of the hedgehog signaling pathway: Effects on basal call carcinoma-like lesions. Proc. Natl. Acad. Sci. USA 100, 4616-4621.
66. Yang, X.-J. (2004). Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin. Cell Dev. Biol. 15, 91-103.
67. Yarden, A., Salomon, D. and Geiger, B. (1995). Zebrafish cyclin D1 is differentially expressed during early embryogenesis. Biochim. Biophys. Acta. 1264, 257-260.