Wnt2b inhibits differentiation of retinal progenitor cells in the absence of Notch activity by downregulating the expression of proneural genes

Development

Volumn 132, Issue 12, 2005, Pages 2759-2770

  Kubo, Fumi ^a,b,c   Takeichi, Masatoshi ^a,b   Nakagawa, Shinichi ^a,c  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c RIKEN   (Japan)

Author keywords

Cell Cycle; Delta; Differentiation; Notch; Progenitor cells; Proneural gene; Retina; Stem cells; Wnt

Indexed keywords

DELTA1 PROTEIN; HELIX LOOP HELIX PROTEIN; NOTCH RECEPTOR; PROTEIN; PROTEIN CATH5; UNCLASSIFIED DRUG; WNT PROTEIN; WNT2B PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CHICK EMBRYO; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EXPLANT; GENE EXPRESSION REGULATION; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; RETINA DEVELOPMENT; RETINA NEUROEPITHELIAL LAYER; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICK EMBRYO; DOWN-REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NEURONS; RECEPTORS, NOTCH; RETINA; SIGNAL TRANSDUCTION; STEM CELLS; WNT PROTEINS;

ANIMALIA; VERTEBRATA;

EID: 21644436845     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01856     Document Type: Article

References (74)

1. Ahmad, I., Dooley, C. M. and Polk, D. L. (1997). Delta-1 is a regulator of neurogenesis in the vertebrate retina. Dev Biol. 185, 92-103.
2. Ahmad, I., Tang, L. and Pham, H. (2000). Identification of neural progenitors in the adult mammalian eye. Biochem. Biophys. Res. Commun. 270, 517-521.
3. Austin, C. P., Feldman, D. E., Ida, J. A., Jr and Cepko, C. L. (1995). Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121, 3637-3650.
4. Bao, Z. Z. and Cepko, C. L. (1997). The expression and function of Notch pathway genes in the developing rat eye. J. Neurosci. 17, 1425-1434.
5. Bard, J. B. and Ross, A. S. (1982). The morphogenesis of the ciliary body of the avian eye. I. Lateral cell detachment facilitates epithelial folding. Dev. Biol. 92, 73-86.
6. Belecky-Adams, T., Tomarev, S., Li, H. S., Ploder, L., McInnes, R. R., Sundin, O. and Adler, R. (1997). Pax-6, Prox 1, and Chx10 homeobox gene expression correlates with phenotypic fate of retinal precursor cells. Invest. Ophthalmol. Vis. Sci. 38, 1293-1303.
7. Brown, N. L., Kanekar, S., Vetter, M. L., Tucker, P. K., Gemza, D. L. and Glaser, T. (1998). Math5 encodes a murine basic helix-loop-helix transcription factor expressed during early stages of retinal neurogenesis. Development 125, 4821-4833.
8. Brown, N. L., Patel, S., Brzezinski, J. and Glaser, T. (2001). Math5 is required for retinal ganglion cell and optic nerve formation. Development 128, 2497-2508.
9. 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.
10. Cook, B., Portera-Cailliau, C. and Adler, R. (1998). Developmental neuronal death is not a universal phenomenon among cell types in the chick embryo retina. J. Comp. Neurol. 396, 12-19.
11. Cunningham, J. J., Levine, E. M., Zindy, F., Goloubeva, O., Roussel, M. F. and Smeyne, R. J. (2002). The cyclin-dependent kinase inhibitors p19(Ink4d) and p27(Kip1) are coexpressed in select retinal cells and act cooperatively to control cell cycle exit. Mol. Cell. Neurosci. 19, 359-374.
12. Dorsky, R. I., Rapaport, D. H. and Harris, W. A. (1995). Xotch inhibits cell differentiation in the Xenopus retina. Neuron 14, 487-496.
13. Dorsky, R. I., Chang, W. S., Rapaport, D. H. and Harris, W. A. (1997). Regulation of neuronal diversity in the Xenopus retina by Delta signalling. Nature 385, 67-70.
14. Dovey, H. F., John, V., Anderson, J. P., Chen, L. Z., de Saint Andrieu, P., Fang, L. Y., Freedman, S. B., Folmer, B., Goldbach, E., Holsztynska, E. J. et al. (2001). Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J. Neurochem. 76, 173-181.
15. Dyer, M. A. and Cepko, C. L. (2001). Regulating proliferation during retinal development. Nat. Rev. Neurosci. 2, 333-342.
16. Fischer, A. J. and Reh, T. A. (2000). Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev. Biol. 220, 197-210.
17. Fischer, A. J., Dierks, B. D. and Reh, T. A. (2002). Exogenous growth factors induce the production of ganglion cells at the retinal margin. Development 129, 2283-2291.
18. Fuhrmann, S., Levine, E. M. and Reh, T. A. (2000). Extraocular mesenchyme patterns the optic vesicle during early eye development in the embryonic chick. Development 127, 4599-4609.
19. Furukawa, T., Mukherjee, S., Bao, Z. Z., Morrow, E. M. and Cepko, C. L. (2000). rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26, 383-394.
20. Geling, A., Steiner, H., Willem, M., Bally-Cuif, L. and Haass, C. (2002). A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep. 3, 688-694.
21. Givol, I., Tsarfaty, I., Resau, J., Rulong, S., da Silva, P, P., Nasioulas, G., DuHadaway, J., Hughes, S. H. and Ewert, D. L. (1994). Bcl-2 expressed using a retroviral vector is localized primarily in the nuclear membrane and the endoplasmic reticulum of chicken embryo fibroblasts. Cell Growth Differ. 5, 419-429.
22. Haruta, M., Kosaka, M., Kanegae, Y., Saito, I., Inoue, T., Kageyama, R., Nishida, A., Honda, Y. and Takahashi, M. (2001). Induction of photoreceptor-specific phenotypes in adult mammalian iris tissue. Nat. Neurosci. 4, 1163-1164.
23. Hatakenaka, S., Kiyama, H., Tohyama, M. and Miki, N. (1985). Immunohistochemical localization of chick retinal 24 kdalton protein (visinin) in various vertebrate retinae. Brain Res. 331, 209-215.
24. Henrique, D., Hirsinger, E., Adam, J., le Roux, I., Pourquie, O., Ish-Horowicz, D. and Lewis, J. (1997). Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr. Biol. 7, 661-670.
25. Hirabayashi, Y., Itoh, Y., Tabata, H., Nakajima, K., Akiyama, T., Masuyama, N. and Gotoh, Y. (2004). The Wnt /[beta]-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131, 2791-2801.
26. Hollyfield, J. G. (1968). Differential addition of cells to the retina in Rana pipiens tadpoles. Dev. Biol. 18, 163-179.
27. Hsieh, J. C., Rattner, A., Smallwood, P. M. and Nathans, J. (1999). Biochemical characterization of Wnt-frizzled interactions using a soluble, biologically active vertebrate Wnt protein. Proc. Natl. Acad. Sci. USA 96, 3546-3551.
28. Hutcheson, D. A. and Vetter, M. L. (2001). The bHLH factors Xath5 and XNeuroD can upregulate the expression of XBrn3d, a POU-homeodomain transcription factor. Dev. Biol. 232, 327-338.
29. Inoue, T., Hojo, M., Bessho, Y., Tano, Y., Lee, J. E. and Kageyama, R. (2002). Math3 and NeuroD regulate amacrine cell fate specification in the retina. Development 129, 831-842.
30. Jacobson, M. (1968). Cessation of DNA synthesis in retinal ganglion cells correlated with the time of specification of their central conections. Dev. Biol. 17, 219-232.
31. Jasoni, C., Hendrickson, A. and Roelink, H. (1999). Analysis of chicken Wnt-13 expression demonstrates coincidence with cell division in the developing eye and is consistent with a role in induction. Dev. Dyn. 215, 215-224.
32. Johns, P. R. (1977). Growth of the adult goldfish eye. III. Source of the new retinal cells. J. Comp. Neurol. 176, 343-357.
33. Kageyama, R., Ishibashi, M., Takebayashi, K. and Tomita, K. (1997). bHLH transcription factors and mammalian neuronal differentiation. Int. J. Biochem. Cell Biol. 29, 1389-1399.
34. Kageyama, R., Ohtsuka, T. and Tomita, K. (2000). The bHLH gene Hes1 regulates differentiation of multiple cell types. Mol. Cells 10, 1-7.
35. Kahn, A. J. (1974). An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. Dev. Biol. 38, 30-40.
36. Kanekar, S., Perron, M., Dorsky, R., Harris, W. A., Jan, L. Y., Jan, Y. N. and Vetter, M. L. (1997). Xath5 participates in a network of bHLH genes in the developing Xenopus retina. Neuron 19, 981-994.
37. Kay, J. N., Finger-Baier, K. C., Roeser, T., Staub, W. and Baier, H. (2001). Retinal ganglion cell genesis requires lakritz, a Zebrafish atonal Homolog. Neuron 30, 725-736.
38. Kelley, M. W., Turner, J. K. and Reh, T. A. (1995). Regulation of proliferation and photoreceptor differentiation in fetal human retinal cell cultures. Invest. Ophthalmol. Vis. Sci. 36, 1280-1289.
39. Kubo, F., Takeichi, M. and Nakagawa, S. (2003). Wnt2b controls retinal cell differentiation at the ciliary marginal zone. Development 130, 587-598.
40. Liu, H., Mohamed, O., Dufort, D. and Wallace, V. A. (2003). Characterization of Wnt signaling components and activation of the Wnt canonical pathway in the murine retina. Dev. Dyn. 227, 323-334.
41. Liu, W., Mo, Z. and Xiang, M. (2001). The Ath5 proneural genes function upstream of Brn3 POU domain transcription factor genes to promote retinal ganglion cell development. Proc. Natl. Acad. Sci. USA 98, 1649-1654.
42. Livesey, F. J. and Cepko, C. L. (2001). Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2, 109-118.
43. Marquardt, T., Ashery-Padan, R., Andrejewski, N., Scardigli, R., Guillemot, F. and Gruss, P. (2001). Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105, 43-55.
44. Matter-Sadzinski, L., Matter, J. M., Ong, M. T., Hernandez, J. and Ballivet, M. (2001). Specification of neurotransmitter receptor identity in developing retina: the chick ATH5 promoter integrates the positive and negative effects of several bHLH proteins. Development 128, 217-231.
45. Megason, S. G. and McMahon, A. P. (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087-2098.
46. Morrow, E. M., Furukawa, T., Lee, J. E. and Cepko, C. L. (1999). NeuroD regulates multiple functions in the developing neural retina in rodent. Development 126, 23-36.
47. Moshiri, A. and Reh, T. A. (2004). Persistent progenitors at the retinal margin of ptc+/- mice. J. Neurosci. 24, 229-237.
48. Mu, X. and Klein, W. H. (2004). A gene regulatory hierarchy for retinal ganglion cell specification and differentiation. Semin. Cell Dev. Biol. 15, 115-123.
49. Muroyama, Y., Kondoh, H. and Takada, S. (2004). Wnt proteins promote neuronal differentiation in neural stem cell culture. Biochem. Biophys. Res. Commun. 313, 915-921.
50. Nakagawa, S., Takada, S., Takada, R. and Takeichi, M. (2003). Identification of the laminar-inducing factor: Wnt-signal from the anterior rim induces correct laminar formation of the neural retina in vitro. Dev. Biol. 260, 414-425.
51. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
52. Norenberg, M. D., Dutt, K. and Reif-Lehrer, L. (1980). Glutamine synthetase localization in cortisol-induced chick embryo retinas. J. Cell Biol. 84, 803-807.
53. Ohnuma, S. and Harris, W. A. (2003). Neurogenesis and the cell cycle. Neuron 40, 199-208.
54. 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.
55. Perron, M. and Harris, W. A. (2000a). Determination of vertebrate retinal progenitor cell fate by the Notch pathway and basic helix-loop-helix transcription factors. Cell Mol. Life Sci. 57, 215-223.
56. Perron, M. and Harris, W. A. (2000b). Retinal stem cells in vertebrates. BioEssays 22, 685-688.
57. Perron, M., Kanekar, S., Vetter, M. L. and Harris, W. A. (1998). The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. Dev. Biol. 199, 185-200.
58. Perron, M., Opdecamp, K., Butler, K., Harris, W. A. and Bellefroid, E. J. (1999). X-ngnr-1 and Xath3 promote ectopic expression of sensory neuron markers in the neurula ectoderm and have distinct inducing properties in the retina. Proc. Natl. Acad. Sci. USA 96, 14996-15001.
59. Reh, T. A. and Levine, E. M. (1998). Multipotential stem cells and progenitors in the vertebrate retina. J. Neurobiol. 36, 206-220.
60. Roztocil, T., Matter-Sadzinski, L., Alliod, C., Ballivet, M. and Matter, J. M. (1997). NeuroM, a neural helix-loop-helix transcription factor, defines a new transition stage in neurogenesis. Development 124, 3263-3272.
61. Satow, T., Bae, S. K., Inoue, T., Inoue, C., Miyoshi, G., Tomita, K., Bessho, Y., Hashimoto, N. and Kageyama, R. (2001). The basic helix-loop-helix gene hesr2 promotes gliogenesis in mouse retina. J. Neurosci. 21, 1265-1273.
62. Scheer, N., Groth, A., Hans, S. and Campos-Ortega, J. A. (2001). An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development 128, 1099-1107.
63. Schmidt, M., Tanaka, M. and Munsterberg, A. (2000). Expression of (beta)-catenin in the developing chick myotome is regulated by myogenic signals. Development 127, 4105-4113.
64. Sidman, R. (1961). Histogenesis of Mouse Retina Studied with Thymidine-H3. New York: Academic Press.
65. Tetsu, O. and McCormick, F. (1999). Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426.
66. Thut, C. J., Rountree, R. B., Hwa, M. and Kingsley, D. M. (2001). 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.
67. Tomita, K., Nakanishi, S., Guillemot, F. and Kageyama, R. (1996). Mash1 promotes neuronal differentiation in the retina. Genes Cells 1, 765-774.
68. Tomita, K., Moriyoshi, K., Nakanishi, S., Guillemot, F. and Kageyama, R. (2000). Mammalian achaete-scute and atonal homologs regulate neuronal versus glial fate determination in the central nervous system. EMBO J. 19, 5460-5472.
69. Tropepe, V., Coles, B. L., Chiasson, B. J., Horsford, D. J., Elia, A. J., McInnes, R. R. and van der Kooy, D. (2000). Retinal stem cells in the adult mammalian eye. Science 287, 2032-2036.
70. Vetter, M. L. and Brown, N. L. (2001). The role of basic helix-loop-helix genes in vertebrate retinogenesis. Semin. Cell Dev. Biol. 12, 491-498.
71. Wang, S. W., Kim, B. S., Ding, K., Wang, H., Sun, D., Johnson, R. L., Klein, W. H. and Gan, L. (2001). Requirement for math5 in the development of retinal ganglion cells. Genes Dev. 15, 24-29.
72. Wodarz, A. and Nusse, R. (1998). Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14, 59-88.
73. Yan, R. T. and Wang, S. Z. (1998). neuroD induces photoreceptor cell overproduction in vivo and de novo generation in vitro. J. Neurobiol. 36, 485-496.
74. Zakin, L. D., Mazan, S., Maury, M., Martin, N., Guenet, J. L. and Brulet, P. (1998). Structure and expression of Wnt13, a novel mouse Wnt2 related gene. Mech. Dev. 73, 107-116.