Evolution of eyes and photoreceptor cell types

International Journal of Developmental Biology

Volumn 47, Issue 7-8, 2003, Pages 563-571

  Arendt, Detlev ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Evolution; Eye; Opsin; Photoreceptor; Retinal ganglion cell

Indexed keywords

OPSIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX6;

BIODIVERSITY; CELL TYPE; COMPARATIVE STUDY; EVOLUTION; EYE DEVELOPMENT; GENE EXPRESSION; GENETIC CONSERVATION; LENS EPITHELIUM; MOLECULAR BIOLOGY; NONHUMAN; PHOTORECEPTOR CELL; PIGMENT CELL; PRIORITY JOURNAL; REVIEW; STEM CELL;

AMACRINE CELLS; ANIMALS; EVOLUTION, MOLECULAR; EYE; EYE PROTEINS; HOMEODOMAIN PROTEINS; MODELS, BIOLOGICAL; OPSIN; PAIRED BOX TRANSCRIPTION FACTORS; PHOTORECEPTORS, INVERTEBRATE; PHOTORECEPTORS, VERTEBRATE; REPRESSOR PROTEINS; RETINA; RETINAL GANGLION CELLS; VARIATION (GENETICS);

ANIMALIA; BILATERIA; VERTEBRATA;

EID: 1642512344     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (112)

1. ANDREWS, G.L., YUN, K., RUBENSTEIN, J.L. and MASTICK, G.S. (2003). Dlx transcription factors regulate differentiation of dopaminergic neurons of the ventral thalamus. Mol. Cell. Neurosci. 23: 107-20.
2. ARENDT, D., TESSMAR, K., DE CAMPOS-BAPTISTA, M.I., DORRESTEIJN, A. and WITTBRODT, J. (2002). Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development 129: 1143-54.
3. ARENDT, D. and WITTBRODT, J. (2001). Reconstructing the eyes of Urbilateria. Phil. Trans. Roy. Soc. Lond. B 356: 1545-1563.
4. BARBER, V.C., EVANS, E.M. and LAND, M.F. (1967). The fine structure of the eye of the mollusc Pecten maximus. Z. Zellforsch. 76: 295-312.
5. BARBER, V.C. and WRIGHT, D.E. (1969). The fine structure of the eye and optic tentacle of the mollusc Cardium edule. J. Ultrastruct. Res. 26: 515-528.
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. Investigative Ophthalm. Vis. Sci. 38: 1293-1303.
7. BELENKY, M.A., SMERASKI, C.A., PROVENCIO, I., SOLLARS, P.J. and PICKARD, G.E. (2003). Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J. Comp. Neurol. 460: 380-93.
8. BELLINGHAM, J., WHITMORE, D., PHILP, A.R., WELLS, D.J. and FOSTER, R.G. (2002). Zebrafish melanopsin: isolation, tissue localisation and phylogenetic position. Brain Res. Mol. Brain Res. 107: 128-36.
9. BERMINGHAM, N.A., HASSAN, B.A., WANG, V.Y., FERNANDEZ, M., BANFI, S., BELLEN, H.J., FRITZSCH, B. and ZOGHBI, H.Y. (2001). Proprioceptor pathway development is dependent on Math1. Neuron 30: 411-22.
10. BOSSING, T., UDOLPH, G., DOE, C.Q. and TECHNAU, G.M. (1996). The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 179: 41-64.
11. 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.
12. CALLAERTS, P., MUNOZ-MARMOL, A.M., GLARDON, S., CASTILLO, E., SUN, H., Li, W.H., GEHRING, W.J. and SALO, E. (1999). Isolation and expression of a Pax6 gene in the regenerating and intact Planarian Dugesia(G)tigrina. Proc. Nat. Acad. Sci. USA 96: 558-563.
13. CARL, M., LOOSLI, F. and WITTBRODT, J. (2002). Six3 inactivation reveals its essential role for the formation and patterning of the vertebrate eye. Development 129: 4057-63.
14. CEPKO, C.L. (1999). The roles of intrinsic and extrinsic cues and bHLH genes in the determination of retinal cell fates. Curr. Opin. Neurobiol. 9: 37-46.
15. CHEN, S., WANG, Q.L., NIE, Z., SUN, H., LENNON, G., COPELAND, N.G., GILBERT, D.J., JENKINS, N.A. and ZACK, D.J. (1997). Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19: 1017-30.
16. CHOW, R.L., SNOW, B., NOVAK, J., LOOSER, J., FREUND, C., VIDGEN, D., PLODER, L. and McInnes, R.R. (2001). Vsx1, a rapidly evolving paired-like homeobox gene expressed in cone bipolar cells. Mech. Dev. 109: 315-22.
17. 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.
18. COOK, T., PICHAUD, F., SONNEVILLE, R., PAPATSENKO, D. and DESPLAN, C. (2003). Distinction between Color Photoreceptor Cell Fates Is Controlled by Prospero in Drosophila. Dev. Cell 4: 853-64.
19. CZERNY, T., HALDER, G., KLOTER, U., SOUABNI, A., GEHRING, W.J. and BUSSLINGER, M. (1999). twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol. Cell 3: 297-307.
20. DANIEL, A., DUMSTREI, K., LENGYEL, J.A. and HARTENSTEIN, V. (1999). The control of cell fate in the embryonic visual system by atonal, tailless and EGFR signaling. Development 126: 2945-54.
21. DARWIN, C. (1859). "On the Origin of Species by Means of Natural Selection: or the Preservation of Favoured Races in the Struggle for Life. " John Murray, London.
22. DAVIS, R.J., TAVSANLI, B.C., DITTRICH, C., WALLDORF, U. and MARDON, G. (2003). Drosophila retinal homeobox (drx) is not required for establishment of the visual system, but is required for brain and clypeus development. Dev. Biol. 259: 272-87.
23. DE MELO, J., QIU, X., DU, G., CRISTANTE, L. and EISENSTAT, D.D. (2003). Dlx1, Dlx2, Pax6, Bm3b and Chx10 homeobox gene expression defines the retinal ganglion and inner nuclear layers of the developing and adult mouse retina. J. Comp. Neurol. 461: 187-204.
24. DESCHET, K., BOURRAT, F., RISTORATORE, F., CHOURROUT, D. and JOLY, J.-S. (1999). Expression of the medaka (Oryzias latipes) OI-Rx3 paired-like gene in two diencephalic derivatives, the eye and the hypothalamus. Mech. Dev. 83: 179-182.
25. DRIVENES, O., SOVIKNES, A.M., EBBESSON, L.O., FJOSE, A., SEO, H.C. and HELVIK, J.V. (2003). Isolation and characterization of two teleost melanopsin genes and their differential expression within the inner retina and brain. J. Comp. Neurol. 456: 84-93.
26. DYER, M.A., LIVESEY, F.J., CEPKO, C.L. and OLIVER, G. (2003). Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nat. Genet. 34: 53-8.
27. EAKIN, R. (1968). "Evolution of photoreceptors." Appleton-Century-Crofts, New York.
28. EAKIN, R.M. (1982). Continuity and diversity in photoreceptors. In "Visual cells in Evolution" (J. A. Westfall, Ed.), pp. 91-105. Raven Press, New York.
29. EAKIN, R.M. and BRANDENBURGER, J.L. (1980). Unique eye of probable evolutionary significance. Science 211: 1189-1190.
30. EGGERT, T., HAUCK, B., HILDEBRANDT, N., GEHRING, W.J. and WALLDORF, U. (1998). Isolation of a Drosophila homolog of the vertebrate homeobox gene Rx and its possible role in brain and eye development. Proc. Nat. Acad. Sci. USA 95: 2343-2348.
31. ERKMAN, L., YATES, P.A., MCLAUGHLIN, T., MCEVILLY, R.J., WHISENHUNT, T., O'CONNELL, S.M., KRONES, A.I., KIRBY, M.A., RAPAPORT, D.H., BERMINGHAM, J.R., O'LEARY, D.D. and ROSENFELD, M.G. (2000). A POU domain transcription factor-dependent program regulates axon pathfinding in the vertebrate visual system. Neuron 28: 779-92.
32. FERNALD, R.D. (1997). The evolution of eyes. Brain Behav. Evol. 50: 253-9.
33. FERNALD, R.D. (2000). Evolution of eyes. Curr. Opin. Neurobiol. 10: 444-50.
34. FISCHER, A. and BRÖKELMANN, J. (1966). Das Auge von Platynereis dumerilii (Polychaeta). Sein Feinbau im ontogenetischen und adaptiven Wandel. Z. Zellforsch. 71: 217-244.
35. FRANKFORT, B.J. and MARDON, G. (2002). R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129: 1295-1306.
36. FURUKAWA, T., MORROW, E.M. and CEPKO, C.L. (1997a). Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91: 531-41.
37. FURUKAWA, T., MORROW, E.M. and CEPKO, C.L. (1997b). Crx, a Novel Otx-Like Homeobox Gene, Shows Photoreceptor-Specific Expression and Regulates Photoreceptor Differentiation. Cell 91: 531-541.
38. GEHRING, W. and ROSBASH, M. (2003). The co-evolution of blue-light photoreception and circadian rhythms. Proc. Natl. Acad. Sci. in press
39. GEHRING, W.J. and IKEO, K. (1999). Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet. 15: 371-7.
40. GHANBARI, H., SEO, H. C., FJOSE, A. and BRANDLI, A.W. (2001). Molecular cloning and embryonic expression of Xenopus Six homeobox genes. Mech. Dev. 101: 271-7.
41. GLARDON, S., HOLLAND, L.Z., GEHRING, W.J. and HOLLAND, N.D. (1998). Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax6): insights into eye and photoreceptor evolution. Development 125: 2701-2710.
42. HALDER, G., CALLAERTS, P. and GEHRING, W.J. (1995). Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267: 1788-1792.
43. HARTMANN, B., LEE, P.N., KANG, Y.Y., TOMAREV, S., DE COUET, H.G. and CALLAERTS, P. (2003). Pax6 in the sepiolid squid Euprymna scolopes: evidence for a role in eye, sensory organ and brain development. Mech. Dev. 120: 177-83.
44. HATAKEYAMA, J., TOMITA, K., INOUE, T. and KAGEYAMA, R. (2001). Roles of homeobox and bHLH genes in specification of a retinal cell type. Development Suppl. 128: 1313-22.
45. HATTAR, S., LIAO, H. W., TAKAO, M., BERSON, D.M. and YAU, K.W. (2002). Melanopsin-containing retinal ganglion cells: architecture, projections and intrinsic photosensitivity. Science 295: 1065-70.
46. HAYASHI, T., KOJIMA, T. and SAIGO, K. (1998). Specification of primary pigment cell and outer photoreceptor fates by BarH1 homeobox gene in the developing Drosophila eye. Dev. Biol. 200: 131-45.
47. HEANUE, T.A., RESHEF, R., DAVIS, R.J., MARDON, G., Oliver, G., TOMAREV, S., LASSAR, A.B. and TABIN, C.J. (1999). Synergistic regulation of vertebrate muscle development by Dach2, Eya2 and Six1, homologs of genes required for Drosophila eye formation. Genes Dev. 13: 3231-43.
48. HIGASHIJIMA, S., KOJIMA, T., MICHIUE, T., ISHIMARU, S., EMORI, Y. and SAIGO, K. (1992). Dual Bar homeo box genes of Drosophila required in two photoreceptor cells, R1 and R6 and primary pigment cells for normal eye development. Genes Dev. 6: 50-60.
49. HSIUNG, F. and MOSES, K. (2002). Retinal development in Drosophila: specifying the first neuron. Hum. Mol. Genet. 11: 1207-14.
50. HUTCHESON, D.A. and VETTER, M.L. (2001). The bHLH factors Xath5 and XNeuroD can upregulate the expression of XBm3d, a POU-homeodomain transcription factor. Dev. Biol. 232: 327-38.
51. JANG, C.C., CHAO, J.L., JONES, N., YAO, L.C., BESSARAB, D.A., KUO, Y.M., JUN, S., DESPLAN, C., BECKENDORF, S.K. and SUN, Y.H. (2003). Two Pax genes, eye gone and eyeless, act cooperatively in promoting Drosophila eye development. Development 130: 2939-2951.
52. JEAN, D., EWAN, K. and GRUSS, P. (1998). Molecular Regulators Involved in Vertebrate Eye Development. Mech. Dev. 76: 3-18.
53. JESSELL, T.M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1: 20-9.
54. KAWAKAMI, K., OHTO, H., TAKIZAWA, T. and SAITO, T. (1996). Identification and expression of six family genes in mouse retina. FEBS Letters 393: 259-263.
55. 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: 725-36.
56. KOJIMA, D., MANO, H. and FUKADA, Y. (2000). Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J. Neurosci. 20: 2845-51.
57. KRUPNICK, J.G., GUREVICH, V.V. and BENOVIC, J.L. (1997). Mechanism of quenching of phototransduction. Binding competition between arrestin and transducin for phosphorhodopsin. J. Biol. Chem. 272: 18125-31.
58. KUMAR, J. and MOSES, K. (1997). Transcription factors in eye development: a gorgeous mosaic? Genes and Development 11: 2023-2028.
59. KUMAR, J. P. and MOSES, K. (2001). Eye specification in Drosophila: perspectives and implications. Semin. Cell Dev. Biol. 12: 469-74.
60. LAGUTIN, O.V., ZHU, C.C., KOBAYASHI, D., TOPCZEWSKI, J., SHIMAMURA, K., PUELLES, L., RUSSELL, H.R., Mckinnon, P.J., SOLNICA-KREZEL, L. and OLIVER, G. (2003). Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 17: 368-79.
61. LIU, W., KHARE, S.L., LIANG, X., PETERS, M.A., LIU, X., CEPKO, C.L. and XIANG, M. (2000). All Brn3 genes can promote retinal ganglion cell differentiation in the chick. Development - Suppl. 127: 3237-47.
62. 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: 1649-54.
63. LIVESEY, F.J. and CEPKO, C.L. (2001). Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2: 109-18.
64. LOOSLI, F., KMITA-CUNISSE, M. and GEHRING, W.J. (1996). Isolation of a Pax-6 homolog from the ribbonworm Lineus sanguineus. Proc. Nat. Acad. Sci. USA 93: 2658-63.
65. LOOSLI, F., KOSTER, R.W., CARL, M., KRONE, A. and WITTBRODT, J. (1998). Six3, a medaka homologue of the Drosophila homeobox gene sine oculis is expressed in the anterior embryonic shield and the developing eye. Mech. Dev. 74: 159-64.
66. LOOSLI, F., WINKLER, S., BURGTORF, C., WURMBACH, E., ANSORGE, W., HENRICH, T., GRABHER, C., ARENDT, D., CARL, M., KRONE, A., GRZEBISZ, E. and WITTBRODT, J. (2001). Medaka eyeless is the key factor linking retinal determination and eye growth. Development 128: 4035-44.
67. LOPEZ, J.M., MORENO, N. and GONZALEZ, A. (2002). Localization of choline acetyltransferase in the developing and adult retina of Xenopus laevis. Neurosci. Lett. 330: 61-4.
68. LOPEZ-RIOS, J., TESSMAR, K., LOOSLI, F., WITTBRODT, J. and BOVOLENTA, P. (2003). Six3 and Six6 activity is modulated by members of the groucho family. Development 130: 185-95.
69. LOTT, J.S., WILDE, J.I., CARNE, A., EVANS, N. and FINDLAY, J.B. (1999). The ordered visual transduction complex of the squid photoreceptor membrane. Mol. Neurobiol. 20: 61-80.
70. MARQUARDT, T., ASHERY-PADAN, R. and REJEWSKI, N., SCARDIGLI, R., GUILLEMOT, F. and GRUSS, P. (2001). Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105: 43-55.
71. MARTINEZ MORALES, J., SIGNORE, M., ACAMPORA, D., SIMEONE, A. and BOVOLENTA, P. (2000). Otx genes are required for tissue specification in the developing eye Development 128(11): 2019-2030.
72. 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.
73. MAYEENUDDIN, L.H. and MITCHELL, J. (2001). cDNA cloning and characterization of a novel squid rhodopsin kinase encoding multiple modular domains. Vis. Neurosci. 18: 907-15.
74. MAYEENUDDIN, L.H. and MITCHELL, J. (2003). Squid visual arrestin: cDNA cloning and calcium-dependent phosphorylation by rhodopsin kinase (SQRK). J. Neurochem. 85: 592-600.
75. MEYER-ROCHOW, V.B. and STEWART, D. (1996). Review of larval and postlarval eye ultrastructure in the lamprey (Cyclostomata) with special emphasis on Geotria australis (Gray). Microsc. Res. Tech. 35: 431-44.
76. NILSSON, D.-E. (1996). Eye ancestry: old genes for new eyes. Curr. Biol. 6: 39-42.
77. PATTERSON, K.D., CLEAVER, O., GERBER, W.V., WHITE, F.G. and KRIEG, P.A. (2000). Distinct expression patterns for two Xenopus Bar homeobox genes. Dev. Gen. Evol. 210: 140-4.
78. 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.
79. PICHAUD, F. and DESPLAN, C. (2002). Pax genes and eye organogenesis. Curr. Opin. Genet. Dev. 12: 430-4.
80. PINEDA, D., GONZALEZ, J., CALLAERTS, P., IKEO, K., GEHRING, W.J. and SALO, E. (2000). Searching for the prototypic eye genetic network: Sine oculisis essential for eye regeneration in planarians. Proc. Nat. Acad. Sci. USA 97: 4525-4529.
81. POGGI, L., CARL, M., VIGNALI, R., BARSACCHI, G. and WITTBRODT, J. (2002). Expression of a medaka (Oryzias latipes) Bar homologue in the differentiating central nervous system and retina. Mech. Dev. 114: 193-6.
82. PROVENCIO, I., RODRIGUEZ, I.R., JIANG, G., HAYES, W.P., MOREIRA, E.F. and ROLLAG, M.D. (2000). A novel human opsin in the inner retina. J. Neurosci. 20: 600-5.
83. PROVENCIO, I., ROLLAG, M.D. and CASTRUCCI, A.M. (2002). Photoreceptive net in the mammalian retina. Nature 415: 493.
84. QUIRING, R., WALLDORF, U., KLOTER, U. and GEHRING, W.J. (1994). Homology of the eyeless gene of drosophila to the small eye gene in mice and aniddia in humans. Science 265: 785-789.
85. ROLLAG, M.D., BERSON, D.M. and PROVENCIO, I. (2003). Melanopsin, ganglion-cell photoreceptors and mammalian photoentrainment. J. Biol. Rhythms 18: 227-34.
86. SAITO, T., SAWAMOTO, K., OKANO, H. and ERSON, D.J. and MIKOSHIBA, K. (1998). Mammalian BarH homologue is a potential regulator of neural bHLH genes. Dev. Biol. 199: 216-25.
87. SALO, E., PINEDA, D., MARSAL, M., GONZALEZ, J., GREMIGNI, V. and BATISTONI, R. (2002). Genetic network of the eye in Platyhelminthes: expression and functional analysis of some players during planarian regeneration. Gene 287: 67-74.
88. SALVINI-PLAWEN, L.V. and MAYR, E. (1977). "On the evolution of photoreceptors and eyes." Plenum, New York.
89. SCHMIDT, H., RICKERT, C., BOSSING, T., VEF, O., URBAN, J., TECHNAU, G.M., UDOLPH, G. and DOE, C.Q. (1997). The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 189: 186-204.
90. SEIMIYA, M. and GEHRING, W.J. (2000). The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development 127: 1879-1886.
91. SERIKAKU, M.A. and O'TOUSA, J.E. (1994). sine oculis is a homeobox gene required for Drosophila visual system development. Genetics 138: 1137-50.
92. SHENG, G., THOUVENOT, E., SCHMUCKER, D., WILSON, D.S. and DESPLAN, C. (1997). Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila: evidence for a conserved function in photoreceptors. Genes Dev. 11: 1122-31.
93. SHIRASAKI, R. and PFAFF, S.L. (2002). Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25: 251-81.
94. SIMPSON, T.I. and PRICE, D.J. (2002). Pax6; a pleiotropic player in development. Bioessays 24: 1041-51.
95. TESSMAR, K., LOOSLI, F. and WITTBRODT, J. (2002). A screen for co-factors of Six3. Mech. Dev. 117: 103-13.
96. TESSMAR-RAIBLE, K. and ARENDT, D. (2003). Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr. Opin. Genet. Dev. 13(4): 331-340
97. THOR, S. and ERSSON, S.G., TOMLINSON, A. and THOMAS, J.B. (1999). A LIM-homeodomain combinatodal code for motor-neuron pathway selection. Nature 397: 76-80.
98. TOMAREV, S.I., CALLAERTS, P., KOS, L.,ZINOVIEVA, R., HALDER, G., GEHRING, W. and Piatigorsky, J. (1997). Squid Pax-6 and eye development. Proc. Natl. Acad. Sci. USA 94: 2421-6.
99. UMESONO, Y., WATANABE, K. and AGATA, K. (1999). Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev. Genes. Evol. 209: 31-9.
100. URBACH, R. and TECHNAU, G.M. (2003). Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130: 3621-37.
101. VANDENDRIES, E.R., JOHNSON, D. and REINKE, R. (1996). orthodenticle is required for photoreceptor cell development in the Drosophila eye. Dev. Biol. 173: 243-55.
102. VICZIAN, A. S., VIGNALI, R., ZUBER, M. E., BARSACCHI, G. and HARRIS, W.A. (2003). XOtx5b and XOtx2 regulate photoreceptor and bipolar fates in the Xenopus retina. Development 130: 1281-94.
103. WANG, S.W., GAN, L., MARTIN, S.E. and KLEIN, W.H. (2000). Abnormal polarization and axon outgrowth in retinal ganglion cells lacking the POU-domain transcription factor Brn-3b. Mol. Cell. Neurosci. 16: 141-56.
104. 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: 24-9.
105. WANG, S.W., MU, X., BOWERS, W.J., KIM, D.S., PLAS, D.J., CRAIR, M.C., FEDEROFF, H.J., GAN, L. and KLEIN, W.H. (2002). Brn3b/Brn3c double knockout mice reveal an unsuspected role for Brn3c in retinal ganglion cell axon outgrowth. Development 129: 467-77.
106. WAWERSIK, S. and MAAS, R.L. (2000). Vertebrate eye development as modeled in Drosophila. Hum. Mol. Genet. 9: 917-925.
107. WILSON, S.W. and RUBENSTEIN, J.L. (2000). Induction and dorsoventral patterning of the telencephalon. Neuron 28: 641-51.
108. WITKOVSKY, P. (2000). Photoreceptor classes and transmission at the photoreceptor synapse in the retina of the clawed frog, Xenopus laevis. Microsc. Res. Tech. 50: 338-46.
109. YASUHARA, O., TOOYAMA, I., AIMI, Y., BELLIER, J.P., HISANO, T., MATSUO, A., PARK, M. and KIMURA, H. (2003). Demonstration of cholinergic ganglion cells in rat retina: expression of an alternative splice variant of choline acetyltransferase. J. Neurosci 23: 2872-81.
110. YASUYAMA, K., KITAMOTO, T. and SALVATERRA, P.M. (1995). Localization of choline acetyltransferase-expressing neurons in the larval visual system of Drosophila melanogaster. Cell Tissue Res. 282: 193-202.
111. YASUYAMA, K. and MEINERTZHAGEN, I.A. (1999). Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. J. Comp. Neurol 412: 193-202.
112. ZHU, C.C., DYER, M.A., UCHIKAWA, M., KONDOH, H., LAGUTIN, O.V. and OLIVER, G. (2002). Six3-mediated auto repression and eye development requires its interaction with members of the Groucho-related family of co-repressors. Development 129: 2835-49.