Canonical Wnt signaling is required for the maintenance of dorsal retinal identity

Development

Volumn 135, Issue 24, 2008, Pages 4101-4111

  Veien, Eric S ^a   Rosenthal, Judith S ^a   Kruse Bend, Renee C ^a   Chien, Chi Bin ^a,b   Dorsky, Richard I ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Bmp; Dorsal retina; RPE; Wnt; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN; TRANSCRIPTION FACTOR TBX5; WNT PROTEIN; DKK1 PROTEIN, ZEBRAFISH; SIGNAL PEPTIDE; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR 5; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL POLARITY; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; ENZYME ACTIVATION; EYE DEVELOPMENT; FERTILIZATION; GENE EXPRESSION REGULATION; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSGENE; ANIMAL; BIOLOGICAL MODEL; GENETICS; MORPHOGENESIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; RETINA; TRANSGENIC ANIMAL; ZEBRA FISH;

DANIO RERIO;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; RETINA; RETINAL PIGMENT EPITHELIUM; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; WNT PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 60749137698     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.027367     Document Type: Article

References (66)

1. Arce, L., Yokoyama, N. N. and Waterman, M. L. (2006). Diversity of LEF/TCF action in development and disease. Oncogene 25, 7492-7504.
2. Asai-Coakwell, M., French, C. R., Berry, K. M., Ye, M., Koss, R., Somerville, M., Mueller, R., van Heyningen, V., Waskiewicz, A. J. and Lehmann, O. J. (2007). GDF6, a novel locus for a spectrum of ocular developmental anomalies. Am. J. Hum. Genet. 80, 306-315.
3. Barbieri, A. M., Broccoli, V., Bovolenta, P., Alfano, G., Marchitiello, A., Mocchetti, C., Crippa, L., Bulfone, A., Marigo, V., Ballabio, A. et al. (2002). Vax2 inactivation in mouse determines alteration of the eye dorsal-ventral axis, misrouting of the optic fibres and eye coloboma. Development 129, 805-813.
4. Behesti, H., Holt, J. K. and Sowden, J. C. (2006). The level of BMP4 signaling is critical for the regulation of distinct T-box gene expression domains and growth along the dorso-ventral axis of the optic cup. BMC Dev. Biol. 6, 62.
5. Bonner, J., Gribble, S. L., Veien, E. S., Nikolaus, O. B., Weidinger, G. and Dorsky, R. I. (2008). Proliferation and patterning are mediated independently in the dorsal spinal cord downstream of canonical Wnt signaling. Dev. Biol. 313, 398-407.
6. Briscoe, J. and Novitch, B. G. (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.
7. Burns, C., Zhang, J., Brown, E., Van Bibber, A., Van Es, J., Clevers, H., Ishikawa, T., Taketo, M., Vetter, M. and Fuhrmann, S. (2008). Investigation of Firzzled-5 during embryonic neural development in mouse. Dev. Dyn. 237, 1614-1626.
8. Cho, S. H. and Cepko, C. L. (2006). Wnt2b/beta-catenin-mediated canonical Wnt signaling determines the peripheral fates of the chick eye. Development 133, 3167-3177.
9. Chocron, S., Verhoeven, M. C., Rentzsch, F., Hammerschmidt, M. and Bakkers, J. (2007). Zebrafish Bmp4 regulates left-right asymmetry at two distinct developmental time points. Dev. Biol. 305, 577-588.
10. Delot, E., Kataoka, H., Goutel, C., Yan, Y. L., Postlethwait, J., Wittbrodt, J. and Rosa, F. M. (1999). The BMP-related protein radar: a maintenance factor for dorsal neuroectoderm cells? Mech. Dev. 85, 15-25.
11. Dorsky, R. I., Snyder, A., Cretekos, C. J., Grunwald, D. J., Geisler, R., Haffter, P., Moon, R. T. and Raible, D. W. (1999). Maternal and embryonic expression of zebrafish lef1. Mech. Dev. 86, 147-150.
12. Dorsky, R. I., Sheldahl, L. C. and Moon, R. T. (2002). A transgenic Lef1/betacatenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev. Biol. 241, 229-237.
13. Dorsky, R. I., Itoh, M., Moon, R. T. and Chitnis, A. (2003). Two tcf3 genes cooperate to pattern the zebrafish brain. Development 130, 1937-1947.
14. Durbin, L., Brennan, C., Shiomi, K., Cooke, J., Barrios, A., Shanmugalingam, S., Guthrie, B., Lindberg, R. and Holder, N. (1998). Eph signaling is required for segmentation and differentiation of the somites. Genes Dev. 12, 3096-3109.
15. Ekker, S. C., Ungar, A. R., Greenstein, P., von Kessler, D. P., Porter, J. A., Moon, R. T. and Beachy, P. A. (1995). Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr. Biol. 5, 944-955.
16. Fokina, V. M. and Frolova, E. I. (2006). Expression patterns of Wnt genes during development of an anterior part of the chicken eye. Dev. Dyn. 235, 496-505.
17. French, C. R., Erickson, T., Callander, D., Berry, K. M., Koss, R., Hagey, D. W., Stout, J., Wuennenberg-Stapleton, K., Ngai, J., Moens, C. B. et al. (2007). Pbx homeodomain proteins pattern both the zebrafish retina and tectum. BMC Dev. Biol. 7, 85.
18. Fuentealba, L. C., Eivers, E., Ikeda, A., Hurtado, C., Kuroda, H., Pera, E. M. and De Robertis, E. M. (2007). Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131, 980-993.
19. Hanel, M. L. and Hensey, C. (2006). Eye and neural defects associated with loss of GDF6. BMC Dev. Biol. 6, 43.
20. Hedgepeth, C. M., Conrad, L. J., Zhang, J., Huang, H. C., Lee, V. M. and Klein, P. S. (1997). Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev. Biol. 185, 82-91.
21. Hocking, J. C. and McFarlane, S. (2007). Expression of Bmp ligands and receptors in the developing Xenopus retina. Int. J. Dev. Biol. 51, 161-165.
22. Ille, F., Atanasoski, S., Falk, S., Ittner, L. M., Marki, D., Buchmann-Moller, S., Wurdak, H., Suter, U., Taketo, M. M. and Sommer, L. (2007). Wnt/BMP signal integration regulates the balance between proliferation and differentiation of neuroepithelial cells in the dorsal spinal cord. Dev. Biol. 304, 394-408.
23. Jowett, T. and Lettice, L. (1994). Whole-mount in situ hybridizations on zebrafish embryos using a mixture of digoxigenin- and fluorescein-labelled probes. Trends Genet. 10, 73-74.
24. Kapsimali, M., Caneparo, L., Houart, C. and Wilson, S. W. (2004). Inhibition of Wnt/Axin/beta-catenin pathway activity promotes ventral CNS midline tissue to adopt hypothalamic rather than floorplate identity. Development 131, 5923-5933.
25. Kelly, G. M., Greenstein, P., Erezyilmaz, D. F. and Moon, R. T. (1995). Zebrafish wnt8 and wnt8b share a common activity but are involved in distinct developmental pathways. Development 121, 1787-1799.
26. 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.
27. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
28. Klaus, A., Saga, Y., Taketo, M. M., Tzahor, E. and Birchmeier, W. (2007). Distinct roles of Wnt/beta-catenin and Bmp signaling during early cardiogenesis. Proc. Natl. Acad. Sci. USA 104, 18531-18536.
29. Koshiba-Takeuchi, K., Takeuchi, J. K., Matsumoto, K., Momose, T., Uno, K., Hoepker, V., Ogura, K., Takahashi, N., Nakamura, H., Yasuda, K. et al. (2000). Tbx5 and the retinotectum projection. Science 287, 134-137
30. Krauss, S., Johansen, T., Korzh, V., Moens, U., Ericson, J. U. and Fjose, A. (1991). Zebrafish pax[zf-a]: a paired box-containing gene expressed in the neural tube. EMBO J. 10, 3609-3619.
31. Kudoh, T., Wilson, S. W. and Dawid, I. B. (2002). Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development 129, 4335-4346.
32. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C. B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
33. Lewis, J. L., Bonner, J., Modrell, M., Ragland, J. W., Moon, R. T., Dorsky, R. I. and Raible, D. W. (2004). Reiterated Wnt signaling during zebrafish neural crest development. Development 131, 1299-1308.
34. Liu, H., Thurig, S., Mohamed, O., Dufort, D. and Wallace, V. A. (2006). Mapping canonical Wnt signaling in the developing and adult retina. Invest. Ophthalmol. Vis. Sci. 47, 5088-5097.
35. Liu, J., Wilson, S. and Reh, T. (2003). BMP receptor 1b is required for axon guidance and cell survival in the developing retina. Dev. Biol. 256, 34-48.
36. Lupo, G., Liu, Y., Qiu, R., Chandraratna, R. A., Barsacchi, G., He, R. Q. and Harris, W. A. (2005). Dorsoventral patterning of the Xenopus eye: a collaboration of Retinoid, Hedgehog and FGF receptor signaling. Development 132, 1737-1748.
37. 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.
38. Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M. and Piccolo, S. (2003). Mapping Wnt/betacatenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 100, 3299-3304.
39. McLaughlin, T., Hindges, R. and O'Leary, D. D. (2003). Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr. Opin. Neurobiol. 13, 57-69.
40. McLaughlin, T. and O'Leary, D. D. (2005). Molecular gradients and development of retinotopic maps. Annu. Rev. Neurosci. 28, 327-355.
41. Mui, S. H., Hindges, R., O'Leary, D. D., Lemke, G. and Bertuzzi, S. (2002). The homeodomain protein Vax2 patterns the dorsoventral and nasotemporal axes of the eye. Development 129, 797-804.
42. Muncan, V., Faro, A., Haramis, A. P., Hurlstone, A. F., Wienholds, E., van Es, J., Korving, J., Begthel, H., Zivkovic, D. and Clevers, H. (2007). T-cell factor 4 (Tcf7l2) maintains proliferative compartments in zebrafish intestine. EMBO Rep. 8, 966-973.
43. Murali, D., Yoshikawa, S., Corrigan, R. R., Plas, D. J., Crair, M. C., Oliver, G., Lyons, K. M., Mishina, Y. and Furuta, Y. (2005). Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development 132, 913-923.
44. Muroyama, Y., Fujihara, M., Ikeya, M., Kondoh, H. and Takada, S. (2002). Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev. 16, 548-553.
45. Nikaido, M., Tada, M., Saji, T. and Ueno, N. (1997). Conservation of BMP signaling in zebrafish mesoderm patterning. Mech. Dev. 61, 75-88.
46. Plas, D. T., Dhande, O. S., Lopez, J. E., Murali, D., Thaller, C., Henkemeyer, M., Furuta, Y., Overbeek, P. and Crair, M. C. (2008). Bone morphogenetic proteins, eye patterning, and retinocollicular map formation in the mouse. J. Neurosci. 28, 7057-7067.
47. Puschel, A. W., Gruss, P. and Westerfield, M. (1992). Sequence and expression pattern of pax-6 are highly conserved between zebrafish and mice. Development 114, 643-651.
48. Ramel, M. C., Buckles, G. R., Baker, K. D. and Lekven, A. C. (2005). WNT8 and BMP2B co-regulate non-axial mesoderm patterning during zebrafish gastrulation. Dev. Biol. 287, 237-248.
49. Rissi, M., Wittbrodt, J., Delot, E., Naegeli, M. and Rosa, F. M. (1995). Zebrafish Radar: a new member of the TGF-beta superfamily defines dorsal regions of the neural plate and the embryonic retina. Mech. Dev. 49, 223-234.
50. Rossi, E., Siwiec, F. and Yan, C. Y. (2007). Pattern of Wnt ligand expression during chick eye development. Braz. J. Med. Biol. Res. 40, 1333-1338.
51. Ruvinsky, I., Oates, A. C., Silver, L. M. and Ho, R. K. (2000). The evolution of paired appendages in vertebrates: T-box genes in the zebrafish. Dev. Genes Evol. 210, 82-91.
52. Sakuta, H., Takahashi, H., Shintani, T., Etani, K., Aoshima, A. and Noda, M. (2006). Role of bone morphogenic protein 2 in retinal patterning and retinotectal projection. J. Neurosci. 26, 10868-10878.
53. Sasagawa, S., Takabatake, T., Takabatake, Y., Muramatsu, T. and Takeshima, K. (2002). Axes establishment during eye morphogenesis in Xenopus by coordinate and antagonistic actions of BMP4, Shh, and RA. Genesis 33, 86-96.
54. Schmitt, A. M., Shi, J., Wolf, A. M., Lu, C. C., King, L. A. and Zou, Y. (2006). Wnt-Ryk signalling mediates medial-lateral retinotectal topographic mapping. Nature 439, 31-37.
55. Schulte, D., Furukawa, T., Peters, M. A., Kozak, C. A. and Cepko, C. L. (1999). Misexpression of the Emx-related homeobox genes cVax and mVax2 ventralizes the retina and perturbs the retinotectal map. Neuron 24, 541-553.
56. Stoick-Cooper, C. L., Weidinger, G., Riehle, K. J., Hubbert, C., Major, M. B., Fausto, N. and Moon, R. T. (2007). Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134, 479-489.
57. Szeto, D. P. and Kimelman, D. (2004). Combinatorial gene regulation by Bmp and Wnt in zebrafish posterior mesoderm formation. Development 131, 3751-3760.
58. Take-uchi, M., Clarke, J. D. and Wilson, S. W. (2003). Hedgehog signalling maintains the optic stalk-retinal interface through the regulation of Vax gene activity. Development 130, 955-968.
59. Tendeng, C. and Houart, C. (2006). Cloning and embryonic expression of five distinct sfrp genes in the zebrafish Danio rerio. Gene Expr. Patterns 6, 761-771.
60. Thisse, C. and Thisse, B. (2005). High throughput expression analysis of ZF-models consortium clones. ZFIN direct data submission (http://zfin.org).
61. Ulloa, F. and Briscoe, J. (2007). Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 6, 2640-2649.
62. Van Raay, T. J. and Vetter, M. L. (2004). Wnt/frizzled signaling during vertebrate retinal development. Dev. Neurosci. 26, 352-358.
63. Veien, E. S., Grierson, M. J., Saund, R. S. and Dorsky, R. I. (2005). Expression pattern of zebrafish tcf7 suggests unexplored domains of Wnt/beta-catenin activity. Dev. Dyn. 233, 233-239.
64. Zechner, D., Muller, T., Wende, H., Walther, I., Taketo, M. M., Crenshaw, E. B., 3rd, Treier, M., Birchmeier, W. and Birchmeier, C. (2007). Bmp and Wnt/beta-catenin signals control expression of the transcription factor Olig3 and the specification of spinal cord neurons. Dev. Biol. 303, 181-190.
65. Zhang, X. M. and Yang, X. J. (2001). Temporal and spatial effects of Sonic hedgehog signaling in chick eye morphogenesis. Dev. Biol. 233, 271-290.
66. Zhuang, B. and Sockanathan, S. (2006). Dorsal-ventral patterning: a view from the top. Curr. Opin. Neurobiol. 16, 20-24.