Eyelid antagonizes wingless signaling during Drosophila development and has homology to the bright family of DNA-binding proteins

Genes and Development

Volumn 11, Issue 15, 1997, Pages 1949-1962

  Treisman, Jessica E ^a,b   Luk, Alvin ^c   Rubin, Gerald M ^b   Heberlein, Ulrike ^c  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bright; DNA binding; Drosophila; Eye development; Segmentation; Wingless

Indexed keywords

DNA BINDING PROTEIN;

ARTICLE; DNA BINDING; DROSOPHILA; EYE DEVELOPMENT; GENE EXPRESSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY;

EID: 0030861293     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.11.15.1949     Document Type: Article

References (106)

1. Artavanis-Tsakonas, S., K. Matsuno, and M.E. Fortini. 1995. Notch signaling. Science 268: 225-232.
2. Axelrod, J.D., K. Matsuno, S. Artavanis-Tsakonas, and N. Perrimon. 1996. Interaction between wingless and Notch signaling pathways mediated by dishevelled. Science 271: 1826-1832.
3. Baker, N.E. 1988. Embryonic and imaginai requirements for wingless, a segment-polarity gene in Drosophila. Dev. Biol. 125: 96-108.
4. Behrens, J., J.P. von Kries, M. Kuhl, L. Bruhn, D. Wedlich, R. Grosschedl, and W. Birchmeier. 1996. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382: 638-642.
5. Bejsovec, A. and A. Martinez-Arias. 1991. Roles of wingless in patterning the larval epidermis of Drosophila. Development 113: 471-485.
6. Bhanot, P., M. Brink, C.H. Samos, J.-C. Hsieh, Y. Wang, J.P. Macke, D. Andrew, J. Nathans, and R. Nusse. 1996. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382: 225-230.
7. Binari, R. and N. Perrimon. 1994. Stripe-specific regulation of pair-rule genes by hopscotch, a putative Jak family tyrosine kinase in Drosophila. Genes & Dev. 8: 300-312.
8. Blackman, R.K., M. Sanicola, L.A. Raftery, T. Gillevet, and W.M. Gelbart. 1991. An extensive 3′ cis-regulatory region directs the imaginai disc expression of decapentaplegic, a member of the TGF-β family in Drosophila. Development 111: 657-665.
9. Blair, S.S. 1992. shaggy (zeste-white 3) and the formation of supernumerary bristle precursors in the developing wing blade of Drosophila. Dev. Biol. 152: 263-278.
10. Bourouis, M., P. Heitzler, M, El Messal, and P. Simpson. 1989. Mutant Drosophila embryos in which all cells adopt a neural fate. Nature 341: 442-444.
11. Bourouis, M., P. Moore, L. Ruel, Y. Grau, P. Heitzler, and P. Simpson. 1990. An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2+ subfamily. EMBO J. 9: 2877-2884.
12. Brown, N.L., C.A. Sattler, S.W. Paddock, and S.B. Carroll. 1995. Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell 80: 879-887.
13. Brunner, E., O. Peter, L. Schweizer, and K. Basler. 1997. pangolin encodes a Lef-1 homolog that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature 385: 829-833.
14. Burke, R. and K. Basler. 1996. Hedgehog-dependent patterning in the Drosophila eye can occur in the absence of dpp signaling. Dev. Biol 179: 360-368.
15. Campbell, G., T. Weaver, and A. Tomlinson. 1993. Axis specification in the developing Drosophila appendage: The role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74: 1113-1123.
16. Chanut, F. and U. Heberlein. 1997. Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124: 559-567.
17. Chou, T.B. and N. Perrimon. 1992. Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131: 643-653.
18. Cohen, B., A.A. Sincox, and S.M. Cohen. 1993. Allocation of the imaginai primordia in the Drosophila embryo. Development 117: 597-608.
19. Couso, J.P. and A. Martinez-Arias. 1994. Notch is required for wingless signaling in the epidermis of Drosophila. Cell 79: 259-272.
20. Couso, J.P., M. Bate, and A. Martinez-Arias. 1993. A wingless-dependent polar coordinate system in Drosophila imaginai discs. Science 259: 484-489.
21. Couso, J.P., S.A. Bishop, and A. Martinez-Arias. 1994. The wingless signaling pathway and the patterning of the wing margin in Drosophila. Development 120: 621-636.
22. Couso, J.P., E. Knust, and A. Martinez-Arias. 1995. Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr. Biol. 5: 1437-1448.
23. Coyle-Thompson, C.A. and U. Banerjee. 1993. The strawberry notch gene functions with Notch in common developmental pathways. Development 119: 377-395.
24. de Celis, J.F. and M. Ruiz-Gomez. 1995. groucho and hedgehog regulate engrailed expression in the anterior compartment of the Drosophila wing. Development 121: 3467-3476.
25. de Celis, J.F., A. Garcia-Bellido, and S.J. Bray. 1996. Activation and function of Notch at the dorsal-ventral boundary of the wing imaginai disc. Development 122: 359-369.
26. Delidakis, C., A. Preiss, D.A. Hartley, and S. Artavanis-Tsakonas. 1991. Two genetically and molecularly distinct functions involved in early neurogenesis reside within the Enhancer of split locus of Drosophila melanogaster. Genetics 129: 803-823.
27. Desplan, C., J. Theis, and P.H. O'Farrell. 1988. The sequence specificity of homeodomain-DNA interaction. Cell 54: 1081-1090.
28. Diaz-Benjumea, F.J. and S.M. Cohen. 1995. Serrate signals through Notch to establish a wingless-dependent organizer at the dorsal-ventral compartment boundary of the Drosophila wing. Development 121: 4215-4225.
29. DiNardo, S., E. Sher, J. Heemskerk-Jongens, J.A. Kassis, and P.H. O'Farrell. 1988. Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature 332: 604-609.
30. DiNardo, S., J. Heemskerk, S. Dougan, and P.H. O'Farrell. 1994. The making of a maggot: Patterning the Drosophila embryonic epidermis. Curr. Opin. Genet. Dev. 4: 529-534.
31. Doherty, D., G. Feger, S. Younger-Shepherd, L.Y. Jan, and Y.N. Jan. 1996. Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation. Genes & Dev. 10: 421-434.
32. Dougan, S. and S. DiNardo. 1992. Drosophila wingless generates cell type diversity among engrailed expressing cells. Nature 360: 347-350.
33. Ferguson, E.L. and K.V. Anderson. 1992a. decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71: 451-461.
34. _. 1992b. 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.
35. Garcia-Bellido, A., P. Ripoll, and G. Morata. 1973. Developmental compartmentalization of the wing disc of Drosophila. Nature New Biol 245: 251-253.
36. Golic, K. 1991. Site-specific recombination between homologous chromosomes in Drosophila. Science 252: 958-961.
37. Gregory, S.L., D. Kortschak, B. Kalionis, and R. Saint. 1996. Characterization of the dead ringer gene identifies a novel, highly conserved family of sequence-specific DNA-binding proteins. Mol. Cell Biol. 16: 792-799.
38. Grimm, S. and G.O. Pflugfelder. 1996. Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless. Science 271: 1601-1604.
39. Han, K. and J.L. Manley. 1993. Transcriptional repression by the Drosophila even-skipped protein: Definition of a minimal repression domain. Genes & Dev. 7: 491-503.
40. Hayashi, S., B. Rubinfeld, B. Souza, P. Polakis, E. Wieschaus, and A.J. Levine. 1997. A Drosophila homolog of the tumor suppressor gene adenomatous polyposis coli down-regulates β-catenin but its zygotic expression is not essential for the regulation of Armadillo. Proc. Natl. Acad. Sci. 94: 242-247.
41. Heberlein, U., T. Wolff, and G.M. Rubin. 1993. The TGFβ homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75: 913-926.
42. Heberlein, U., C.M. Singh, A.Y. Luk, and T.J. Donohoe. 1995. Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373: 709-711.
43. Heemskerk, J., S. DiNardo, R. Kostriken, and P.H. O'Farrell. 1991. Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature 352: 404-410.
44. Herrscher, R.F., M.H. Kaplan, D.L. Lelsz, C. Das, R. Scheuermann, and P.W. Tucker. 1995. The immunoglobulin heavychain matrix-associating regions are bound by Bright: A B cell-specific trans-activator that describes a new DNA-binding protein family. Genes & Dev. 9: 3067-3082.
45. Hou, X.S., M.B. Melnick, and N. Perrimon. 1996. marelle acts downstream of the Drosophila HOP/JAK kinase and encodes protein similar to the mammalian STATs. Cell 84: 411-419.
46. Huber, O., R. Korn, J. McLaughlin, M. Ohsugi, B.G. Herrmann, and R. Kemler. 1996. Nuclear localization of β-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59: 3-10.
47. Immergluck, K., P.A. Lawrence, and M. Bienz. 1990. Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 62: 261-268.
48. Karim, F.D., H.C. Chang, M. Therrien, D.A. Wassarman, T. Laverty, and G.M. Rubin. 1996. A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics 143: 315-329.
49. Kassis, J. A. 1990. Spatial and temporal control elements of the Drosophila engrailed gene. Genes & Dev. 4: 433-443.
50. Kassis, J.A., E. Noll, E.P. VanSickle, W.F. Odenwald, and N. Perrimon. 1992. Altering the insertional specificity of a Drosophila transposable element. Proc. Natl. Acad. Sci. 89: 1919-1923.
51. Kim, J., K.D. Irvine, and S.B. Carroll. 1995. Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82: 795-802.
52. Kimmel, B.E., U. Heberlein, and G.M. Rubin. 1990. The homeodomain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes & Dev. 4: 712-727.
53. Klingensmith, J. and R. Nusse. 1994. Signaling by wingless in Drosophila. Dev. Biol. 166: 396-414.
54. Klingensmith, J., R. Nusse, and N. Perrimon. 1994. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes & Dev. 8: 118-130.
55. Ma, C. and K. Moses. 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.
56. Ma, C., Y. Zhou, P.A. Beachy, and K. Moses. 1993. The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75: 927-938.
57. Masucci, J.D., R.J. Miltenberger, and F.M. Hoffmann. 1990. Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal discs is regulated by 3′ cis-regulatory elements. Genes & Dev. 4: 2011-2023.
58. Mlodzik, M., N.E. Baker, and G.M. Rubin. 1990. Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes & Dev. 4: 1848-1861.
59. Molenaar, M., M. van de Wetering, M. Oosterwegel, J. Peterson-Maduro, S. Godsave, V. Korinek, J. Roose, O. Destree, and H. Clevers. 1996. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 86: 391-399.
60. Murata, G. and P. Ripoll. 1975. Minutes: Mutants autonomously affecting cell division rate in Drosophila. Dev. Biol. 42: 211-221.
61. Morata, G. and P.A. Lawrence. 1977. The development of wingless, a homeotic mutation of Drosophila. Dev. Biol. 56: 227-240.
62. Neumann, C.J. and S.M. Cohen. 1996. Distinct mitogenic and cell specification functions of wingless in different regions of the wing. Development 122: 1781-1789.
63. Ng, M., F.J. Diaz-Benjumea, J.-P. Vincent, J. Wu, and S.M. Cohen. 1996. Specification of the wing by localized expression of wingless protein. Nature 381: 316-318.
64. Noordemeer, J., J. Klingensmith, N. Perrimon, and R. Nusse. 1994. dishevelled and armadillo act in the Wingless signaling pathway in Drosophila. Nature 367: 80-83.
65. Nusse, R. and H.H. Varmus. 1992. Wnt genes. Cell 69: 1073-1087.
66. Orsulic, S. and M. Peifer. 1996. An in vivo structure-function study of armadillo, the beta-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for wingless signaling. J. Cell Biol. 134: 1283-1300.
67. Paroush, Z.F., R.L. Finley Jr., T. Kidd, S.M. Wainwright, P.W. Ingham, R. Brent, and D. Ish-Horowicz. 1994. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell 79: 805-815.
68. Peifer, M. and E. Wieschaus. 1990. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell 63: 1167-1176.
69. Peifer, M., D. Sweeton, M. Casey, and E. Wieschaus. 1994a. wingless signal and zeste-white 3 kinase trigger opposing changes in the intracellular distribution of armadillo. Development 120: 369-380.
70. Peifer, M., L.-M. Pai, and M. Casey. 1994b. Phosphorylation of the Drosophila adherens junction protein armadillo: Roles for wingless signal and zeste-white 3 kinase. Dev. Biol. 166: 543-556.
71. Perrimon, N. and D. Smouse. 1989. Multiple functions of a Drosophila homeotic gene, zeste-white3, during segmentation and neurogenesis. Dev. Biol. 135: 287-305.
72. Phillips, R.G. and J.R.S. Whittle. 1993. wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development. Development 118: 427-438.
73. Pignoni, F. and S.L. Zipursky. 1997. Induction of Drosophila eye development by Decapentaplegic. Development 124: 271-278.
74. Ready, D.F., T.E. Hanson, and S. Benzer. 1976. Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53: 217-240.
75. Riese, J., X. Yu, A. Munnerlyn, S. Eresh, S.-C. Hsu, R. Grosschedl, and M. Bienz. 1997. LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88: 777-788.
76. Robinow, S. and K. White. 1991. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22: 443-461.
77. Ronchi, E., J.E. Treisman, N. Dostatni, G. Struhl, and C. Desplan. 1993. Down-regulation of the Drosophila morphogen bicoid by the torso receptor-mediated signal transduction cascade. Cell 74: 347-355.
78. Royet, J. and R. Finkelstein. 1996. hedgehog, wingless and orthodenticle specify adult head development in Drosophila. Development 122: 1849-1858.
79. Rubinfeld, B., B. Souza, I. Albert, O. Muller, S.H. Chamberlain, R.H. Masiarz, S. Munemitsu, and P. Polakis. 1993. Association of the APC gene product with beta-catenin. Science 262: 1731-1734.
80. Rubinfeld, B., I. Albert, E. Porfiri, C. Fiol, S. Munemitsu, and P. Polakis. 1996. Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science 272: 1023-1026.
81. Rulifson, E.J. and S.S. Blair. 1995. Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development 121: 2813-2824.
82. Rulifson, E.J., C.A. Micchelli, J.D. Axelrod, N. Perrimon, and S.S. Blair. 1996. wingless refines its own expression domain on the Drosophila wing margin. Nature 384: 72-74.
83. Rushlow, C.A., A. Hogan, S.M. Pinchin, K.M. Howe, M. Lardelli, and D. Ish-Horowicz. 1989. The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J. 8: 3095-3103.
84. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual, second ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
85. Siegfried, E. and N. Perrimon. 1994. Drosophila wingless: A paradigm for the function and mechanism of Wnt signaling. BioEssays 16: 395-404.
86. Siegfried, E., L.A. Perkins, T.M. Capaci, and N. Perrimon. 1990. Putative protein kinase product of the Drosophila segment-polarity gene zeste-white3. Nature 345: 825-829.
87. Siegfried, E., T.B. Chou, and N. Perrimon. 1992. wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71: 1167-1179.
88. Siegfried, E., E.L. Wilder, and N. Perrimon. 1994. Components of wingless signaling in Drosophila. Nature 367: 76-80.
89. Simpson, P., W. El Messal, J. Moscoso del Prado, and P. Ripoll. 1988. Stripes of positional homologies across the wing blade of Drosophila melanogaster. Development 103: 391-401.
90. Spradling, A.C., D.M. Stern, I. Kiss, J. Roote, T. Laverty, and G.M. Rubin. 1995. Gene disruptions using P transposable elements: An integral component of the Drosophila genome project. Proc. Natl. Acad. Sci. 92: 10824-10830.
91. Struhl, G. and K. Basler. 1993. Organizing activity of wingless protein in Drosophila. Cell 72: 527-540.
92. Su, L.K., B. Vogelstein, and K.W. Kinzler. 1993. Association of the APC tumor suppressor protein with catenins. Science 262: 1734-1737.
93. Tamkun, J.W., R. Deuring, M.P. Scott, M. Kissinger, A.M. Pattatucci, T.C. Kaufman, and J.A. Kennison. 1992. brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68: 561-572.
94. Theisen, H., J. Purcell, M. Bennett, D. Kansagara, A. Syed, and J.L. Marsh. 1994. dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120: 347-360.
95. Treisman, J.E. and G.M. Rubin. 1995. wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121: 3519-3527.
96. Treisman, J.E., Z. Lai, and G.M. Rubin. 1995. shortsighted acts in the decapentaplegic pathway in Drosophila eye development and has homology to a mouse TGF-β responsive gene. Development 121: 2835-2845.
97. Tomlinson, A. and D.F. Ready. 1987. Cell fate in the Drosophila ommatidium. Dev. Biol. 123: 264-275.
98. van de Wetering, M., R. Cavallo, D. Dooijes, M. van Beest, J. van Es, J. Loureiro, A. Ympa, D. Hursh, T. Jones, A. Bejsovec, M. Peifer, M. Mortin, and H. Clevers. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88: 789-800.
99. Vincent, J.P., C.H. Girdham, and P.H. O'Farrell. 1994. A cell-autonomous, ubiquitous marker for the analysis of Drosophila genetic mosaics. Dev. Biol. 164: 328-331.
100. Wiersdorff, V., T. Lecuit, S.M. Cohen, and M. Mlodzik. 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.
101. Wilder, E.L. and N. Perrimon. 1995. Dual functions of wingless in the Drosophila leg imaginal disc. Development 121: 477-488.
102. Williams, J.A., S.W. Paddock, and S.B. Carroll. 1993. Pattern formation in a secondary field: A hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. Development 117: 571-584.
103. Xu, T. and G.M. Rubin. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223-1237.
104. Yan, R., S. Small, C. Desplan, C.R. Dearolf, and J.E. Darnell. 1996. Identification of a Stat gene that functions in Drosophila development. Cell 84: 421-430.
105. Yanagawa, S., F. van Leeuwen, A. Wodarz, J. Klingensmith, and R. Nusse. 1995. The Dishevelled protein is modified by Wingless signaling in Drosophila. Genes & Dev. 9: 1087-1097.
106. Zecca, M., K. Basler, and G. Struhl. 1996. Direct and long-range action of a wingless morphogen gradient. Cell 87: 833-844.