Abstract
The vertebrate eye is a laterally extended structure of the forebrain. It develops through a series of events, including specification and regionalization of the anterior neural plate, evagination of the optic vesicle (OV), and development of three distinct optic structures: the neural retina (NR), optic stalk (OS), and retinal pigment epithelium (RPE). Various external signals that act on the optic neuroepithelium in a spatial- and temporal-specific manner control the fates of OV subdomains by inducing localized expression of key transcription factors. Investigating the mechanisms underlying compartmentalization of these distinct optic neuroepithelium-derived tissues is therefore not only important from the standpoint of accounting for vertebrate eye morphogenesis, it is also helpful for understanding the fundamental basis of fate determination of other neuroectoderm- derived tissues. This review focuses on the molecular signatures of OV subdomains and the external factors that direct the development of tissues originating from the OV.
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Ando, H., Kobayashi, M., Tsubokawa, T., Uyemura, K., Furuta, T., and Okamoto, H. (2005). Lhx2 mediates the activity of Six3 in zebrafish forebrain growth. Dev. Biol. 287, 456–468.
Andreazzoli, M., Gestri, G., Angeloni, D., Menna, E., and Barsacchi, G. (1999). Role of Xrx1 in Xenopus eye and anterior brain development. Development 126, 2451–2460.
Amato, M.A., Boy, S., and Perron, M. (2004). Hedgehog signaling in vertebrate eye development: a growing puzzle. Cell Mol. Life Sci. 61, 899–910.
Ashery-Padan, R., and Gruss, P. (2001). Pax6 lights-up the way for eye development. Curr. Opin. Cell Biol. 13, 706–714.
Barabino, S.M., Spada, F., Cotelli, F., and Boncinelli, E. (1997). Inactivation of the zebrafish homologue of Chx10 by antisense oligonucleotides causes eye malformations similar to the ocular retardation phenotype. Mech. Dev. 63, 133–143.
Barbieri, A.M., Lupo, G., Bulfone, A., Andreazzoli, M., Mariani, M., Fougerousse, F., Consalez, G.G., Borsani, G., Beckmann, J.S., Barsacchi, G., et al. (1999). A homeobox gene, vax2, controls the patterning of the eye dorsoventral axis. Proc. Natl. Acad. Sci. USA 96, 10729–10734.
Baumer, N., Marquardt, T., Stoykova, A., Spieler, D., Treichel, D., Ashery-Padan, R., and Gruss, P. (2003). Retinal pigmented epithelium determination requires the redundant activities of Pax2 and Pax6. Development 130, 2903–2915.
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.
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
Bellipanni, G., Murakami, T., Doerre, O.G., Andermann, P., and Weinberg, E.S. (2000). Expression of Otx homeodomain proteins induces cell aggregation in developing zebrafish embryos. Dev. Biol. 223, 339–353.
Bertuzzi, S., Hindges, R., Mui, S.H., O’Leary, D.D., and Lemke, G. (1999). The homeodomain protein vax1 is required for axon guidance and major tract formation in the developing forebrain. Genes Dev. 13, 3092–3105.
Bovolenta, P., Mallamaci, A., Briata, P., Corte, G., and Boncinelli, E. (1997). Implication of OTX2 in pigment epithelium determination and neural retina differentiation. J. Neurosci. 17, 4243–4252.
Bovolenta, P., Mallamaci, A., Briata, P., Corte, G., and Boncinelli, E. (1997). Implication of OTX2 in pigment epithelium determination and neural retina differentiation. J. Neurosci. 17, 4243–4252.
Bumsted, K.M., and Barnstable, C.J. (2000). Dorsal retinal pigment epithelium differentiates as neural retina in the microphthalmia (mi/mi) mouse. Invest. Ophthalmol. Vis. Sci. 41, 903–908.
Cavodeassi, F., Carreira-Barbosa, F., Young, R.M., Concha, M.L., Allende, M.L., Houart, C., Tada, M., and Wilson, S.W. (2005). Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/beta-catenin pathway. Neuron 47, 43–56.
Cepko, C.L., Austin, C.P., Yang, X., Alexiades, M., and Ezzeddine, D. (1996). Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. USA 93, 589–595.
Chen, A.E., Ginty, D.D., and Fan, C.M. (2005). Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433, 317–322.
Chiang, C., Litingtung, Y., Lee, E., Young, K.E., Corden, J.L., Westphal, H., and Beachy, P.A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407–413.
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.
Chow, R.L., and Lang, R.A. (2001). Early eye development in vertebrates. Annu. Rev. Cell Dev. Biol. 17, 255–296.
Crossley, P.H., Martinez, S., Ohkubo, Y., and Rubenstein, J.L. (2001). Coordinate expression of Fgf8, Otx2, Bmp4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles. Neuroscience 108, 183–206.
de Iongh, R.U., Chen, Y., Kokkinos, M.I., and McAvoy, J.W. (2004). BMP and activin receptor expression in lens development. Mol. Vis. 10, 566–576.
de Iongh, R.U., Abud, H.E., and Hime, G.R. (2006). WNT/Frizzled signaling in eye development and disease. Front Biosci. 11, 2442–2464.
Decembrini, S., Andreazzoli, M., Vignali, R., Barsacchi, G., and Cremisi, F. (2006). Timing the generation of distinct retinal cells by homeobox proteins. PLoS Biol. 4, e272.
Dorsky, R.I., Raible, D.W., and Moon, R.T. (2000). Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev. 14, 158–162
Dressler, G.R., Deutsch, U., Chowdhury, K., Nornes, H.O., and Gruss, P. (1990). Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system. Development 109, 787–795.
Dudley, A.T., and Robertson, E.J. (1997). Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev. Dyn. 208, 349–362.
Edlund, T., and Jessell, T.M. (1999). Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 96, 211–224.
Esteve, P., Sandonis, A., Ibanez, C., Shimono, A., Guerrero, I., and Bovolenta, P. (2011). Secreted frizzled-related proteins are required for Wnt/beta-catenin signalling activation in the vertebrate optic cup. Development 138, 4179–4184.
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.
Fuhrmann, S. (2010). Eye morphogenesis and patterning of the optic vesicle. Curr. Top Dev. Biol. 93, 61–84
Fuhrmann, S., Chow, L., and Reh, T.A. (2000). Molecular control of cell diversification in the vertebrate retina. Results Probl. Cell Differ. 31, 69–91.
Fujimura, N., Taketo, M.M., Mori, M., Korinek, V., and Kozmik, Z. (2009). Spatial and temporal regulation of Wnt/beta-catenin signaling is essential for development of the retinal pigment epithelium. Dev. Biol. 334, 31–45.
Furukawa, T., Kozak, C.A., and Cepko, C.L. (1997). rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. Proc. Natl. Acad. Sci. USA 94, 3088–3093.
Furuta, Y., and Hogan, B.L. (1998). BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12, 3764–3775.
Furimsky, M., and Wallace, V.A. (2006). Complementary Gli activity mediates early patterning of the mouse visual system. Dev. Dyn. 235, 594–606.
Galy, A., Neron, B., Planque, N., Saule, S., and Eychene, A. (2002). Activated MAPK/ERK kinase (MEK-1). induces transdifferentiation of pigmented epithelium into neural retina. Dev. Biol. 248, 251–264.
Graw, J. (2010). Eye development. Curr. Top Dev. Biol. 90, 343–386.
Hallonet, M., Hollemann, T., Wehr, R., Jenkins, N.A., Copeland, N.G., Pieler, T., and Gruss, P. (1998). Vax1 is a novel homeobox-containing gene expressed in the developing anterior ventral forebrain. Development 125, 2599–2610.
Hallonet, M., Hollemann, T., Pieler, T., and Gruss, P. (1999). Vax1, a novel homeobox-containing gene, directs development of the basal forebrain and visual system. Genes Dev. 13, 3106–3114.
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.
Harris, W.A. (1997). Cellular diversification in the vertebrate retina. Curr. Opin. Genet. Dev. 7, 651–658.
He, J., Sheng, T., Stelter, A.A., Li, C., Zhang, X., Sinha, M., Luxon, B.A., and Xie, J. (2006). Suppressing Wnt signaling by the hedgehog pathway through sFRP-1. J. Biol. Chem. 281, 35598–35602.
Heller, N., and Brandli, A.W. (1997). Xenopus Pax-2 displays multiple splice forms during embryogenesis and pronephric kidney development. Mech. Dev. 69, 83–104.
Herbrand, H., Guthrie, S., Hadrys, T., Hoffmann, S., Arnold, H.H., Rinkwitz-Brandt, S., and Bober, E. (1998). Two regulatory genes, cNkx5-1 and cPax2, show different responses to local signals during otic placode and vesicle formation in the chick embryo. Development 125, 645–654.
Hill, R.E., Favor, J., Hogan, B.L., Ton, C.C., Saunders, G.F., Hanson, I.M., Prosser, J., Jordan, T., Hastie, N.D., and van Heyningen, V. (1991). Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354, 522–525.
Hirsch, N., and Harris, W.A. (1997). Xenopus Pax-6 and retinal development. J. Neurobiol. 32, 45–61.
Hodgkinson, C.A., Moore, K.J., Nakayama, A., Steingrimsson, E., Copeland, N.G., Jenkins, N.A., and Arnheiter, H. (1993). Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix-zipper protein. Cell 74, 395–404.
Horsford, D.J., Nguyen, M.T., Sellar, G.C., Kothary, R., Arnheiter, H., and McInnes, R.R. (2005). Chx10 repression of Mitf is required for the maintenance of mammalian neuroretinal identity. Development 132, 177–187.
Hyer, J., Mima, T., and Mikawa, T. (1998). FGF1 patterns the optic vesicle by directing the placement of the neural retina domain. Development 125, 869–877.
Iwakiri, R., Kobayashi, K., Okinami, S., and Kobayashi, H. (2005). Suppression of Mitf by small interfering RNA induces dedifferentiation of chick embryonic retinal pigment epithelium. Exp. Eye Res. 81, 15–21.
Jessell, T.M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20–29.
Katanaev, V.L., Ponzielli, R., Semeriva, M., and Tomlinson, A. (2005). Trimeric G protein-dependent frizzled signaling in Drosophila. Cell 120, 111–122.
Kennedy, B.N., Stearns, G.W., Smyth, V.A., Ramamurthy, V., van Eeden, F., Ankoudinova, I., Raible, D., Hurley, J.B., and Brockerhoff, S.E. (2004). Zebrafish rx3 and mab21l2 are required during eye morphogenesis. Dev. Biol. 270, 336–349.
Kiecker, C., and Lumsden, A. (2005). Compartments and their boundaries in vertebrate brain development. Nat. Rev. Neurosci. 6, 553–564.
Kim, J.W., and Lemke, G. (2006). Hedgehog-regulated localization of Vax2 controls eye development. Genes Dev. 20, 2833–2847.
Kim, H.S., Shin, J., Kim, S.H., Chun, H.S., Kim, J.D., Kim, Y.S., Kim, M.J., Rhee, M., Yeo, S.Y., and Huh, T.L. (2007). Eye field requires the function of Sfrp1 as a Wnt antagonist. Neurosci. Lett. 414, 26–29.
Koike, C., Nishida, A., Ueno, S., Saito, H., Sanuki, R., Sato, S., Furukawa, A., Aizawa, S., Matsuo, I., Suzuki, N., et al. (2007). Functional roles of Otx2 transcription factor in postnatal mouse retinal development. Mol. Cell. Biol. 27, 8318–8329.
Kondoh, H., Uchikawa, M., Yoda, H., Takeda, H., Furutani-Seiki, M., and Karlstrom, R.O. (2000). Zebrafish mutations in Gli-mediated hedgehog signaling lead to lens transdifferentiation from the adenohypophysis anlage. Mech. Dev. 96, 165–174.
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.
Kumasaka, M., Sato, H., Sato, S., Yajima, I., and Yamamoto, H. (2004). Isolation and developmental expression of Mitf in Xenopus laevis. Dev. Dyn. 230, 107–113.
Lad, E.M., Cheshier, S.H., and Kalani, M.Y. (2009). Wnt-signaling in retinal development and disease. Stem Cells Dev. 18, 7–16.
Leconte, L., Lecoin, L., Martin, P., and Saule, S. (2004). Pax6 interacts with cVax and Tbx5 to establish the dorsoventral boundary of the developing eye. J. Biol. Chem. 279, 47272–47277.
Liu, I.S., Chen, J.D., Ploder, L., Vidgen, D., van der Kooy, D., Kalnins, V.I., and McInnes, R.R. (1994). Developmental expression of a novel murine homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron 13, 377–393.
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.
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.
Liu, H., Xu, S., Wang, Y., Mazerolle, C., Thurig, S., Coles, B.L., Ren, J.C., Taketo, M.M., van der Kooy, D., and Wallace, V.A. (2007). Ciliary margin transdifferentiation from neural retina is controlled by canonical Wnt signaling. Dev. Biol. 308, 54–67.
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.
Martinez-Morales, J.R., Signore, M., Acampora, D., Simeone, A., and Bovolenta, P. (2001). Otx genes are required for tissue specification in the developing eye. Development 128, 2019–2030.
Martinez-Morales, J.R., Dolez, V., Rodrigo, I., Zaccarini, R., Leconte, L., Bovolenta, P., and Saule, S. (2003). OTX2 activates the molecular network underlying retina pigment epithelium differentiation. J. Biol. Chem. 278, 21721–21731.
Martinez-Morales, J.R., Rodrigo, I., and Bovolenta, P. (2004). Eye development: a view from the retina pigmented epithelium. Bioessays 26, 766–777.
Masai, I., Yamaguchi, M., Tonou-Fujimori, N., Komori, A., and Okamoto, H. (2005). 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 132, 1539–1553.
Mathers, P.H., Grinberg, A., Mahon, K.A., and Jamrich, M. (1997). The Rx homeobox gene is essential for vertebrate eye development. Nature 387, 603–607.
Matsuo, T., Osumi-Yamashita, N., Noji, S., Ohuchi, H., Koyama, E., Myokai, F., Matsuo, N., Taniguchi, S., Doi, H., Iseki, S., et al. (1993). A mutation in the Pax-6 gene in rat small eye is associated with impaired migration of midbrain crest cells. Nat. Genet. 3, 299–304.
Miller, D.T., Read, R., Rusconi, J., and Cagan, R.L. (2000). The Drosophila primo locus encodes two low-molecular-weight tyrosine phosphatases. Gene 243, 1–9.
Mochii, M., Mazaki, Y., Mizuno, N., Hayashi, H., and Eguchi, G. (1998). Role of Mitf in differentiation and transdifferentiation of chicken pigmented epithelial cell. Dev. Biol. 193, 47–62.
Morcillo, J., Martinez-Morales, J.R., Trousse, F., Fermin, Y., Sowden, J.C., and Bovolenta, P. (2006). Proper patterning of the optic fissure requires the sequential activity of BMP7 and SHH. Development 133, 3179–3190.
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.
Mui, S.H., Kim, J.W., Lemke, G., and Bertuzzi, S. (2005). Vax genes ventralize the embryonic eye. Genes Dev. 19, 1249–1259.
Muller, F., Rohrer, H., and Vogel-Hopker, A. (2007). Bone morphogenetic proteins specify the retinal pigment epithelium in the chick embryo. Development 134, 3483–3493.
Nguyen, M., and Arnheiter, H. (2000). Signaling and transcriptional regulation in early mammalian eye development: a link between FGF and MITF. Development 127, 3581–3591.
Nornes, H.O., Dressler, G.R., Knapik, E.W., Deutsch, U., and Gruss, P. (1990). Spatially and temporally restricted expression of Pax2 during murine neurogenesis. Development 109, 797–809.
Ogden, S.K., Fei, D.L., Schilling, N.S., Ahmed, Y.F., Hwa, J., and Robbins, D.J. (2008). G protein Galphai functions immediately downstream of Smoothened in Hedgehog signalling. Nature 456, 967–970.
Ohkubo, Y., Chiang, C., and Rubenstein, J.L. (2002). Coordinate regulation and synergistic actions of BMP4, SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111, 1–17.
Oliver, G., Mailhos, A., Wehr, R., Copeland, N.G., Jenkins, N.A., and Gruss, P. (1995). Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121, 4045–4055.
Pan, D., and Rubin, G.M. (1995). cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80, 543–552.
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.
Pittack, C., Grunwald, G.B., and Reh, T.A. (1997). Fibroblast growth factors are necessary for neural retina but not pigmented epithelium differentiation in chick embryos. Development 124, 805–816.
Planque, N., Turque, N., Opdecamp, K., Bailly, M., Martin, P., and Saule, S. (1999). Expression of the microphthalmia-associated basic helix-loop-helix leucine zipper transcription factor Mi in avian neuroretina cells induces a pigmented phenotype. Cell Growth Differ. 10, 525–536.
Porter, F.D., Drago, J., Xu, Y., Cheema, S.S., Wassif, C., Huang, S.P., Lee, E., Grinberg, A., Massalas, J.S., Bodine, D., Alt, F., and Westphal, H. (1997). Lhx2, a LIM homeobox gene, is required for eye, forebrain, and definitive erythrocyte development. Development 124, 2935–2944.
Rowan, S., Chen, C.M., Young, T.L., Fisher, D.E., and Cepko, C.L. (2004). Transdifferentiation of the retina into pigmented cells in ocular retardation mice defines a new function of the homeodomain gene Chx10. Development 131, 5139–5152.
Sakuta, H., Suzuki, R., Takahashi, H., Kato, A., Shintani, T., Iemura, S., Yamamoto, T.S., Ueno, N., and Noda, M. (2001). Ventroptin: a BMP-4 antagonist expressed in a double-gradient pattern in the retina. Science 293, 111–115.
Schwarz, M., Cecconi, F., Bernier, G., Andrejewski, N., Kammandel, B., Wagner, M., and Gruss, P. (2000).. Spatial specification of mammalian eye territories by reciprocal transcriptional repression of Pax2 and Pax6. Development 127, 4325–4334.
Sehgal, R., Karcavich, R., Carlson, S., and Belecky-Adams, T.L. (2008). Ectopic Pax2 expression in chick ventral optic cup phenocopies loss of Pax2 expression. Dev. Biol. 319, 23–33.
Simeone, A., Acampora, D., Mallamaci, A., Stornaiuolo, A., D’Apice, M.R., Nigro, V., and Boncinelli, E. (1993). A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 12, 2735–2747.
Stoykova, A., and Gruss, P. (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci. 14, 1395–1412.
Suzuki, A., Ozono, K., Kubota, T., Kondou, H., Tachikawa, K., and Michigami, T. (2008). PTH/cAMP/PKA signaling facilitates canonical Wnt signaling via inactivation of glycogen synthase kinase- 3beta in osteoblastic Saos-2 cells. J. Cell Biochem. 104, 304–317
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.
Takeda, K., Yokoyama, S., Yasumoto, K., Saito, H., Udono, T., Takahashi, K., and Shibahara, S. (2003). OTX2 regulates expression of DOP Achrome tautomerase in human retinal pigment epithelium. Biochem. Biophys. Res. Commun. 300, 908–914.
Tang, K., Xie, X., Park, J.I., Jamrich, M., Tsai, S., and Tsai, M.J. (2010). COUP-TFs regulate eye development by controlling factors essential for optic vesicle morphogenesis. Development 137, 725–734.
Torres, M., Gomez-Pardo, E., and Gruss, P. (1996). Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122, 3381–3391.
Toy, J., Yang, J.M., Leppert, G.S., and Sundin, O.H. (1998). The optx2 homeobox gene is expressed in early precursors of the eye and activates retina-specific genes. Proc. Natl. Acad. Sci. USA 95, 10643–10648.
Van Raay, T.J., and Vetter, M.L. (2004). Wnt/frizzled signaling during vertebrate retinal development. Dev. Neurosci. 26, 352–358.
Van Raay, T.J., Moore, K.B., Iordanova, I., Steele, M., Jamrich, M., Harris, W.A., and Vetter, M.L. (2005). Frizzled 5 signaling governs the neural potential of progenitors in the developing Xenopus retina. Neuron 46, 23–36.
Vogel-Hopker, A., Momose, T., Rohrer, H., Yasuda, K., Ishihara, L., and Rapaport, D.H. (2000). Multiple functions of fibroblast growth factor-8 (FGF-8). in chick eye development. Mech. Dev. 94, 25–36.
Waschek, J.A., Dicicco-Bloom, E., Nicot, A., and Lelievre, V. (2006). Hedgehog signaling: new targets for GPCRs coupled to cAMP and protein kinase A. Ann. N Y Acad. Sci. 1070, 120–128
Westenskow, P., Piccolo, S., and Fuhrmann, S. (2009). Betacatenin controls differentiation of the retinal pigment epithelium in the mouse optic cup by regulating Mitf and Otx2 expression. Development 136, 2505–2510.
Westenskow, P.D., McKean, J.B., Kubo, F., Nakagawa, S., and Fuhrmann, S. (2010). Ectopic Mitf in the embryonic chick retina by co-transfection of beta-catenin and Otx2. Invest. Ophthalmol. Vis. Sci. 51, 5328–5335.
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.
Zhao, S., and Overbeek, P.A. (1999). Tyrosinase-related protein 2 promoter targets transgene expression to ocular and neural crest-derived tissues. Dev. Biol. 216, 154–163.
Zhao, S., Hung, F.C., Colvin, J.S., White, A., Dai, W., Lovicu, F.J., Ornitz, D.M., and Overbeek, P.A. (2001). Patterning the optic neuroepithelium by FGF signaling and Ras activation. Development 128, 5051–5060.
Zhou, X., Hollemann, T., Pieler, T., and Gruss, P. (2000). Cloning and expression of xSix3, the Xenopus homologue of murine Six3. Mech. Dev. 91, 327–330.
Zuber, M.E., Perron, M., Philpott, A., Bang, A., and Harris, W.A. (1999). Giant eyes in Xenopus laevis by overexpression of XOptx2. Cell 98, 341–352.
Zuber, M.E., Gestri, G., Viczian, A.S., Barsacchi, G., and Harris, W.A. (2003). Specification of the vertebrate eye by a network of eye field transcription factors. Development 130, 5155–5167.
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Kim, HT., Kim, J.W. Compartmentalization of vertebrate optic neuroephithelium: External cues and transcription factors. Mol Cells 33, 317–324 (2012). https://doi.org/10.1007/s10059-012-0030-5
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DOI: https://doi.org/10.1007/s10059-012-0030-5