decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc

Development

Volumn 125, Issue 18, 1998, Pages 3741-3751

  Hazelett, Dennis J ^a   Bourouis, Marc ^b   Walldorf, Uwe ^c   Treisman, Jessica E ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

Decapentaplegic; Drosophila, eye development; Eyegone; Eyes absent; Wingless, pattern formation, imaginal disc

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR;

ARTICLE; EYE DEVELOPMENT; GENE CONTROL; IMAGINAL DISC; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT PROTEINS; PHOTORECEPTORS, INVERTEBRATE; PROTO-ONCOGENE PROTEINS; RETINA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

ERINACEIDAE; HEXAPODA; INSECTA;

EID: 0031658111     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (104)

1. Azpiazu, N., Lawrence, P.A., Vincent, J.-P., and Frasch, M. (1996). Segmentation and specification of the Drosophila mesoderm. Genes Dev. 10, 3183-3194.
2. Baker, N. E. (1987). Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila, and the spatial distribution of a transcript in embryos. EMBO J. 6, 1765-1774.
3. Baker, N. E. (1988). Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development 102, 489-497.
4. Basler, K., and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214.
5. Blackman, R. K., Sanicola, M., Raftery, L. A., Gillevet, T. and Gelbart, W. M. (1991). An extensive 3′ cis-regulatory region directs the imaginal disc expression of decapentaplegic, a member of the TGF-β family in Drosophila. Development 111, 657-665.
6. Bonini, N. M., Leiserson, W. M. and Benzer, S. (1993). The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72, 379-395.
7. Bonini, N. M., Bui, Q.T., Gray-Board, G.L., and Warrick, J.M. (1997). The Drosophila eyes absent gene directs ectopic eye formation in a pathway conserved between flies and vertebrates. Development 124, 4819-4826.
8. Brand, A., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
9. Brook, W. J., and Cohen, S.M. (1996). Antagonistic interactions between windless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila leg. Science 273, 1373-1377.
10. Brown, N. L., Sattler, C.A., Paddock, S.W., and Carroll, S.B. (1995). Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell 80, 879-887.
11. Brummel, T. J., Twombly, V., Marques, G., Wrana, J. L., Newfeld, S. J., Attisano, L., Massague, J., O'Connor, M. B. and Gelbart, W. M. (1994). Characterization and relationship of dpp receptors encoded by the saxophone and thick reins genes in Drosophila. Cell 78, 251-262.
12. Burke, R., and Basler, K. (1996). Hedgehog-dependent patterning in the Drosophila eye can occur in the absence of dpp signaling. Dev. Biol. 179, 360-368.
13. Cadigan, K. M., and Nusse, R. (1997). Wnt signaling: a common theme in animal development. Genes Dev. 11, 3286-3305.
14. Campbell, G., Weaver, T. and Tomlinson, A. (1993). Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74, 1113-1123.
15. Chanut, F., and Heberlein, U. (1997). Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124, 559-567.
16. Chen, R., Amoui, M., Zhang, Z., and Mardon, G. (1997). Dachshund and eyes absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila. Cell 91, 893-904.
17. Cheyette, B. N. R., Green, P. J., Martin, K., Garren, H., Hartenstein, V. and Zipursky, S. L. (1994). The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12, 977-996.
18. Cohen, B., Sincox, A.A., and Cohen, S.M. (1993). Allocation of the imaginal primordia in the Drosophila embryo. Development, 597-608.
19. Cross, D. A. E., Alessi, D.R., Cohen, P., Andjelkovich, M., and Hemmings, B.A. (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
20. Diaz-Benjumea, F. J., Cohen, B. and Cohen, S. M. (1994). Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372, 175-179.
21. DiNardo, S., Heemskerk, J., Dougan, S., and O'Farrell, P. H. (1994). The making of a maggot: patterning the Drosophila embryonic epidermis. Curr. Opin. Genet. Dev. 4, 529-534.
22. Dominguez, M., and Hafen, E. (1997). Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev. 11, 3254-3264.
23. Emori, Y., and Saigo, K. (1993). Distinct expression of two Drosophila homologs of fibroblast growth factor receptors in imaginal discs. FEBS Lett. 332, 111-114.
24. Ferguson, E. L., and Anderson, K. V. (1992). Localized enhancement and repression of the activity of the TGF-beta family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114, 583-597.
25. Fietz, M. J., Concordet, J. P., Barbosa, R., Johnson, R., Krauss, S., McMahon, A. P., Tabin, C., and Ingham, P. W. (1994). The hedgehog gene family in Drosophila and vertebrate development. Dev. Suppl. 36, 43-51.
26. Fortini, M. E., Simon, M.A., and Rubin, G.M. (1992). Signalling by the sevenless protein tyrosine kinase is mimicked by Ras1 activation. Nature 355, 559-561.
27. Frasch, M. (1995). Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374, 464-467.
28. Freeman, M. (1994). The spitz gene is required for photoreceptor determination in the Drosophila eye where it interacts with the EGF receptor. M.O.D. 48, 25-33.
29. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651-660.
30. Gomez-Skarmeta, J. L., del Corra,l R.D., de la Calle-Mustienes, E., Ferre-Marco, D., and Modolell, J. (1996). araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 85, 95-105.
31. Grimm, S., and Pflugfelder, G.O. (1996). Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless. Science 271, 1601-1604.
32. 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.
33. Halder, G., Callaerts, P., Flister, S., Walldorf, U., Kloter, U., and Gehring, W. J. (1998). Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development 125, 2181-2191.
34. Heberlein, U., Wolff, T. and Rubin, G. M. (1993). The TGFβ homolog dpp and the segment polarity gene hedgehog are required tor propagation of a morphogenetic wave in the Drosophila retina. Cell 75, 913-926.
35. Heberlein, U., Singh, C. M., Luk, A. Y. and Donohoe, T. J. (1995). Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373, 709-711.
36. Herbst, R., Carroll, P.M., Allard, J.D, Schilling, J., Raabe, T., and Simon, M.A. (1996). Daughter of sevenless is a substrate of the phosphotyrosine phosphatase Corkscrew and functions during sevenless signaling. Cell 85, 899-909.
37. Heslip, T. R., Theisen, H., Walker, H., and Marsh, J.L. (1997). SHAGGY and DISHEVELLED exert opposite effects on wingless and decapentaplegic expression and on positional identity in imaginal discs. Development 124, 1069-1078.
38. Hiromi, Y., and Gehring, W.J. (1987). Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50, 963-974.
39. Holley, S. A., Jackson, P.D., Sasai, Y., Lu, B., De Robertis, E.M., Hoffmann, F.M., and Ferguson, E.L. (1995). A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249-253.
40. Hunt, D. M. (1970). Lethal interactions of the eye-gone and eyeless mutants in Drosophila melanogaster. Genet. Res. 15, 29-34.
41. Jarman, A. P., Grau, Y., Jan, L. Y., and Jan, Y. N. (1993). atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73, 1307-1321.
42. Jarman, A. P., Grell, K. H., Ackerman, L., Jan, L. Y., and Jan, Y. N. (1994). atonal is the proneural gene for Drosophila photoreceptors. Nature 369, 398-400.
43. Jarman, A. P., Sun, Y., Jan, L. Y., and Jan, Y. N. (1995). Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 121, 2019-2030.
44. Jiang, J., and Struhl, G. (1996). Complementary and mutually exclusive activities of decapentaplegic and wingless organize axial patterning during Drosophila leg development. Cell 86, 401-410.
45. Jun, S., and Desplan, C. (1996). Cooperative interactions between paired domain and homeodomain. Development 122, 2639-2650.
46. Karim, F. D., and Rubin, G.M. (1998). Ectopic expression of activated Ras1 induces hyperplastic growth and increased cell death in Drosophila imaginal tissues. Development 125, 1-9.
47. Kassis, J. A., Noll, E., VanSickle, E. P., Odenwald, W. F. and Perrimon, N. (1992). Altering the insertional specificity of a Drosophila transposable element. Proc. Natl. Acad. Sci. USA 89, 1919-1923.
48. Kingsley, D. (1994). The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8, 133-146.
49. Lecuit, T., Brook, W. J., Ng, M., Sun, H., and Cohen, S. M. (1996). Two distinct mechanisms for long-range patterning by decapentaplegic in the Drosophila wing. Nature 381, 387-393.
50. Lecuit, T., and Cohen, S.M. (1997). Proximal-distal axis formation in the Drosophila leg. Nature 388, 139-145.
51. Lindsley, D., and Zimm, G. (1992). The Genome of Drosophila melanogaster. New York: Academic Press.
52. Ma, C., Zhou, Y., Beachy, P. A. and Moses, K. (1993). The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75, 927-938.
53. Ma, C., and Moses, K. (1995). wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. Development 121, 2279-2289.
54. Mardon, G., Solomon, N. M. and Rubin, G. M. (1994). dachsund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120, 3473-3486.
55. Masucci, J. D., Miltenberger, R. J., and Hoffmann, F. M. (1990). Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal discs is regulated by 3′ cis-regulatory elements. Genes Dev. 4, 2011-2023.
56. Nellen, D., Burke, R., Struhl, G., and Basler, K. (1996). Direct and long-range action of a dpp morphogen gradient. Cell 85, 357-368.
57. Newfeld, S. J., Chartoff, E.H., Graff, J.M., Melton, D.A., and Gelbart, W.M. (1996). Mothers against dpp encodes a conserved cytoplasmic protein required in dpp/TGF-β responsive cells. Development 122, 2099-2108.
58. O'Keefe, L., Dougan, S.T., Gabay, L., Raz, E., Shilo, B.-Z., and DiNardo, S. (1997). Spitz and Wingless, emanating from distinct borders, cooperate to establish cell fate across the Engrailed domain in the Drosophila epidermis. Development 124, 4837-4845.
59. Olivier, J. P., Raabe, T., Henkemeyer, M., Dickson, B., Mbamalu, G., Margolis, B., Schlessinger, J., Hafen, E., and Pawson, T. (1993). A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73, 179-191.
60. Pai, C.-Y., Kuo, T.-S., Jaw, T.J., Kurant, E., Chen, C.-T., Bessarab, D.A., Salzberg, A., and Sun, Y.H. (1998). The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, Extradenticle, and suppresses eye development in Drosophila. Genes Dev. 12, 435-446.
61. 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.
62. Peifer, M., and Wieschaus, E. (1990). The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglohin. Cell 63, 1167-1176.
63. Peifer, M., Sweeton, D., Casey, M., and Wieschaus, E. (1994). wingless signal and zeste-white 3 kinase trigger opposing changes in the intracellular distribution of armadillo. Development 120, 369-380.
64. Penton, A., and Hoffmann, F.M. (1996). Decapentaplegic restricts the domain of wingless during Drosophila limb patterning. Nature 382, 162-165.
65. Penton, A., Selleck, S.B., and Hoffmann, F.M. (1997). Regulation of cell cycle synchronization by decapentaplegic during Drosophila eye development. Science 275, 203-206.
66. Pflugfelder, G. O., Roth, H., and Poeck, B. (1992). A homology domain shared between Drosophila optomotor-blind and mouse Brachyury is involved in DNA binding. Biochem. Biophys. Res. Commun. 186, 98-925.
67. Piccolo, S., Sasai, Y., Lu, B., and De Robertis, E.M. (1996). Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589-598.
68. Pignoni, F., Hu, B., Zavitz, K.H., Xiao, J., Garrity, P.A., and Zipursky, S.L. (1997). The eye specification proteins so and eya form a complex and regulate multiple steps in Drosophila eye development. Cell 91, 881-892.
69. Pignoni, F., and Zipursky S. L. (1997). Induction of Drosophila eye development by Decapentaplegic. Development 124, 271-278.
70. Pirrotta, V. (1988). Vectors for P-mediated transformation in Drosophila. Biotechnology 10, 437-456.
71. 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 Aniridia in humans. Science 265, 785-789.
72. Raabe, T., Riesgo-Escovar, J., Liu, X., Bausenwein, B.S., Deak, P., Maroy, P., and Hafen, E. (1996). DOS, a novel pleckstrin homology domain-containing protein required for signal transduction between sevenless and Ras1 in Drosophila. Cell 85, 911-920.
73. Raftery, L. A., Twombly, V., Wharton, K., and Gelbart, W.M. (1995). Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics 139, 241-254.
74. Ready, D. F., Hanson, T. E. and Benzer, S. (1976). Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53, 217-240.
75. Riese, J., Yu, X., Munnerlyn, A., Eresh, S., Hsu, S.-C., Grosschedl, R., and Bienz, M. (1997). LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88, 777-788.
76. Robinow, S., and White, K. (1991). Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22, 443-461.
77. Rogge, R. D., Karlovich, C.A., and Banerjee, U. (1991). Genetic dissection of a neurodevelopmental pathway: Son of sevenless functions downstream of the sevenless and EGF receptor tyrosine kinases. Cell 64, 39-48.
78. Royet, J., and Finkelstein, R. (1997). Establishing primordia in the Drosophila eye-antennal imaginal disc: the roles of decapentaplegic, wingless and hedgehog. Development 124, 4793-4800.
79. Ruberte, E., Marty, T., Nellen, D., Affolter, M., and Basler, K. (1995). An absolute requirement for both the type II and type I receptors, punt and thick veins, for Dpp signaling in vivo. Cell 80, 889-897.
80. Schmidt, J., Francois, V., Bier, E., and Kimelman, D. (1995). Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning. Development 121, 4319-4328.
81. Schnepp, B., Grumbling, G., Donaldson, T., and Simcox, A. (1996). Vein is a novel component in the Drosophila epidermal growth factor receptor pathway with similarity to the neuregulins. Genes Dev. 10, 2302-2313.
82. Schweitzer, R., Howes, R., Smith, R., Shilo, B.Z., and Freeman, M. (1995a). Inhibition of Drosophila EGF receptor activation by the secreted protein Argos. Nature 376, 699-702.
83. Schweitzer, R., Shaharabany, M., Seger, R., and Shilo, B.-Z. (1995b). Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev. 9, 1518-1529.
84. Sekelsky, J. J., Newfeld, S.J., Raftery, L.A., Chartoff, E.H., and Gelbart, W.M. (1995). Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139, 1347-1358.
85. Serikaku, M. A., and O'Tousa, J.E. (1994). sine oculis is a homeohox gene required for Drosophila visual system development. Genetics 138, 1137-1150.
86. Shen, W., and Mardon, G. (1997). Ectopic eye development in Drosophila induced by directed dachshund expression. Development 124, 45-52.
87. Simcox, A. A., Grumbling, G., Schnepp, B., Bennington-Mathias, C., Hersperger, E., and Shearn, A. (1996). Molecular, phenotypic, and expression analysis of vein, a gene required for growth of the Drosophila wing disc. Dev. Biol. 177, 475-489.
88. Simon, M. A., Bowtell, D.D., Dodson, G.S., Laverty, T.R., and Rubin, G.M. (1991). Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling hy the sevenless protein tyrosine kinase. Cell 67, 701-716.
89. Simon, M. A., Dodson, G.S., and Rubin, G.M. (1993). An SH3-SH2-SH3 protein is required lor p21Ras1 activation and binds to sevenless and Sos proteins in vitro. Cell 73, 169-177.
90. Staehling-Hampton, K., Jackson, P. D., Clark, M. J., Brand, A. H., and Hoffmann, F. M. (1994). Specificity of none morphogenetic protein-related factors: cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A. Cell Growth and Diff. 5, 585-593.
91. Stambolic, V., and Woodgett, J.R. (1994). Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem. J. 303, 701-704.
92. Strutt, D. I., Wiersdorff, V., and Mlodzik, M. (1995). Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A. Nature 373, 705-709.
93. Strutt, D. I., and Mlodzik, M. (1997). Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disc. Development 124, 3233-3240.
94. Szuts, D., Freeman, M., and Bienz, M. (1997). Antagonism between EGFR and Wingless signalling in the larval cuticle of Drosophila. Development 124, 3209-3219.
95. Theisen, H., Haerry, T.E., O'Connor, M.B., and Marsh, J.L. (1996). Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. Development 122, 3939-3948.
96. Tio, M., Ma, C., and Moses, K. (1994). spitz, a Drosophila homolog of transforming growth factor-alpha, is required in the founding photoreceptor cells of the compound eye facets. Mechan. Dev. 48, 13-23.
97. Tio, M., and Moses, K. (1997). The Drosophila TGFalpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124, 343-351.
98. Treisman, J. E., and Rubin, G. M. (1995). wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121, 3519-3527.
99. van de Wetering, M., Cavallo, R., Dooijes, D., van Beest, M., van Es, J., Loureiro, J., Ympa, A., Hursh, D., Jones, T., Bejsovec, A., Peifer, M., Mortin, M., and Clevers, H. (1997). Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789-800.
100. Vincent, J. P., Girdham, C.H., and O'Farrell, P.H. (1994). A cell-autonomous, ubiquitous marker for the analysis of Drosophila genetic-mosaics. Dev. Biol. 164, 328-331.
101. Wiersdorff, V., Lecuit, T., Cohen, S.M., and Mlodzik, M. (1996). Mad acts downstream of dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 122, 2153-2162.
102. Xie, T., Finelli, A., and Padgett, R.W. (1994). The Drosophila saxophone gene: a serine-threonine kinase receptor of the TGF-β superfamily. Science 263, 1756-1759.
103. Xu, T., and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
104. Zecca, M., Basler, K., and Struhl, G. (1996). Direct and long-range action of a wingless morphogen gradient. Cell 87, 833-844.