Smoothened, thickveins and the genetic control of cell cycle and cell fate in the developing Drosophila eye

Mechanisms of Development

Volumn 123, Issue 2, 2006, Pages 151-165

  Vrailas, Alysia D ^a   Moses, Kevin ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Cell cycle; Compound eye; Decapentaplegic; Hedgehog; Morphogenetic furrow; Smoothened; Thickveins

Indexed keywords

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL FATE; CELL SPECIFICITY; CELL SURVIVAL; CELL TYPE; CLONE; EYE DEVELOPMENT; GENE MUTATION; GENETIC REGULATION; MOSAICISM; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; VEIN;

ANIMALS; CELL CYCLE; DROSOPHILA; DROSOPHILA PROTEINS; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MORPHOGENESIS; MOSAICISM; MUTATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

ANIMALIA; ERINACEIDAE;

EID: 32444441561     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2005.11.002     Document Type: Article

References (94)

1. K. Arora, M.B. O'Connor, and R. Warrior BMP signaling in Drosophila embryogenesis Ann. NY Acad. Sci. 785 1996 80 97
2. P. Aza-Blanc, F.-A. Ramirez-Weber, M.-P. Laget, C. Schwartz, and T.B. Kornberg Proteolysis that is inhibited by Hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor Cell 89 1997 1043 1053
3. N.E. Baker Cell proliferation, survival, and death in the Drosophila eye Semin. Cell Dev. Biol. 12 2001 499 507
4. N.E. Baker, and S. Yu Proneural function of neurogenic genes in the developing Drosophila eye Curr. Biol. 7 1997 122 132
5. N.E. Baker, S. Yu, and D. Han Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye Curr. Biol. 6 1996 1290 1301
6. A. Baonza, and M. Freeman Control of cell proliferation in the Drosophila eye by notch signaling Dev. Cell 8 2005 529 539
7. R.K. Blackman, M. Sanicola, L.A. Raftery, T. Gillevet, and W.M. Gelbart An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-ß family in Drosophila Development 111 1991 657 665
8. K. Blochinger, R. Bodmer, L.Y. Jan, and Y.N. Jan Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos Genes Dev. 4 1990 1322 1331
9. K. Blochlinger, L.Y. Jan, and Y.N. Jan Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila Development 117 1993 441 450
10. E.R. Borod, and U. Heberlein Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina Dev. Biol. 197 1998 187 197
11. R. Burke, and K. Basler Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing Development 122 1996 2261 2269
12. R. Burke, and K. Basler Hedgehog-dependent patterning in the Drosophila eye can occur in the absence of Dpp signaling Dev. Biol. 179 1996 360 368
13. R.L. Cagan, H. Krämer, A.C. Hart, and S.L. Zipursky The bride of sevenless and sevenless interaction: internalization of a transmembrane ligand Cell 69 1992 393 399
14. G. Campbell, H. Göring, T. Lin, E. Spana, S. Andersson, C.Q. Doe, and A. Tomlinson RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila Development 120 1994 2957 2966
15. F. Chanut, and U. Heberlein Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina Development 124 1997 559 567
16. F. Chanut, A. Luk, and U. Heberlein A screen for dominant modifiers of ro(Dom), a mutation that disrupts morphogenetic furrow progression in Drosophila, identifies groucho and hairless as regulators of atonal expression Genetics 156 2000 1203 1217
17. R. Chen, G. Halder, Z. Zhang, and G. Mardon Signaling by the TGF-ß homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila Development 126 1999 935 943
18. K.O. Cho, and K.W. Choi Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye Nature 396 1998 272 276
19. Y.H. Chou, and C.T. Chien Scabrous controls ommatidial rotation in the Drosophila compound eye Dev. Cell 3 2002 839 850
20. M.T. Cooper, and S.J. Bray Frizzled regulation of notch signaling polarizes cell fate in the Drosophila eye Nature 397 1999 526 530
21. J. Curtiss, and M. Mlodzik Morphogenetic furrow initiation and progression during eye development in Drosophila: the roles of decapentaplegic, hedgehog and eyes absent Development 127 2000 1325 1336
22. J.F. de Celis Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing Development 124 1997 1007 1018
23. J.F. de Celis Pattern formation in the Drosophila wing: the development of the veins BioEssays 25 2003 443 451
24. R. Derynck, Y. Zhang, and X.H. Feng Smads: transcriptional activators of TGF-beta responses Cell 95 1998 737 740
25. M.E. Dokucu, L.S. Zipursky, and R.L. Cagan Atonal, rough and the resolution of proneural clusters in the developing Drosophila retina Development 122 1996 4139 4147
26. M. Dominguez Dual role for Hedgehog in the regulation of the proneural gene atonal during ommatidia development Development 126 1999 2345 2553
27. M. Domínguez, and E. Hafen Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye Genes Dev. 11 1997 3254 3264
28. M. Dominguez, J.D. Wasserman, and M. Freeman Multiple functions for the EGF receptor in Drosophila eye development Curr. Biol. 8 1998 1039 1048
29. M. Duman-Scheel, L. Weng, S. Xin, and W. Du Hedgehog regulates cell growth and proliferation by inducing cyclin D and cyclin E Nature 417 2002 299 304
30. R.G. Fehon, P.J. Kooh, I. Rabay, C.L. Regan, T. Xu, M.A.T. Muskavitch, and S. Artavanis-Tsakonas Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila Cell 61 1990 523 534
31. R.L. Finley Jr, B.J. Thomas, S.L. Zipursky, and R. Brent Isolation of Drosophila cyclin D, a protein expressed in the morphogenetic furrow before entry into S phase Proc. Natl Acad. Sci. USA 93 1996 3011 3015
32. L.C. Firth, and N.E. Baker Extracellular signals responsible for spatially regulated proliferation in the differentiating Drosophila eye Dev. Cell 8 2005 541 551
33. B.J. Frankfort, and G. Mardon R8 development in the Drosophila eye: a paradigm for neural selection and differentiation Development 129 2002 1295 1306
34. B.J. Frankfort, R. Nolo, Z. Zhang, H. Bellen, and G. Mardon Senseless repression of rough is required for R8 photoreceptor differentiation in the developing Drosophila eye Neuron 32 2001 403 414
35. W. Fu, and N.E. Baker Deciphering synergistic and redundant roles of hedgehog, decapentaplegic and delta that drive the wave of differentiation in Drosophila eye development Development 130 2003 5229 5239
36. M.C. Gibson, and N. Perrimon Extrusion and death of DPP/BMP-compromised epithelial cells in the developing Drosophila wing Science 307 2005 1785 1789
37. S. Greenwood, and G. Struhl Progression of the morphogenetic furrow in the Drosophila eye: the roles of hedgehog, decapentaplegic and the raf pathway Development 126 1999 5795 5808
38. U. Heberlein, and K. Moses Mechanisms of Drosophila retinal morphogenesis: the virtues of being progressive Cell 81 1995 987 990
39. U. Heberlein, T. Wolff, and G.M. Rubin The TGFß homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina Cell 75 1993 913 926
40. U. Heberlein, C.M. Singh, A.Y. Luk, and T.J. Donohoe Growth and differentiation in the Drosophila eye coordinated by hedgehog Nature 373 1995 709 711
41. S.-I. Higashijima, T. Kojima, T. Michiue, S. Ishimaru, Y. Emori, and K. Saigo 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 1992 50 60
42. J. Horsfield, A. Penton, J. Secombe, F.M. Hoffman, and H. Richardson Decapentaplegic is required for arrest in G1 phase during Drosophila eye development Development 125 1998 5069 5078
43. A.P. Jarman, E.H. Grell, L. Ackerman, L.Y. Jan, and Y.N. Jan Atonal is the proneural gene for Drosophila photoreceptors Nature 369 1994 398 400
44. L.A. Johnston, and B.A. Edgar Wingless and notch regulate cell-cycle arrest in the developing Drosophila wing Nature 394 1998 82 84
45. D. Kalderon Transducing the hedgehog signal Cell 103 2000 371 374
46. R.C. Kauffmann, S. Li, P.A. Gallagher, J. Zhang, and R.W. Carthew Ras1 signaling and transcriptional competence in the R7 cell of Drosophila Genes Dev. 10 1996 2167 2178
47. J.A. Knoblich, and C.F. Lehner Synergistic action of Drosophila cyclins A and B during the G2-M transition EMBO J. 12 1993 65 74
48. R.P. Kuhnlein, G. Frommer, M. Friedrich, M. Gonzalez-Gaitan, A. Weber, and J.F. Wagner-Bernholz Spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo EMBO J. 13 1994 168 179
49. J.J. Lee, D.P. von Kessler, S. Parks, and P.A. Beachy Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog Cell 71 1992 33 50
50. A.M. Lesokhin, S.Y. Yu, J. Katz, and N.E. Baker Several levels of EGF receptor signaling during photoreceptor specification in wild-type, Ellipse, and Null Mutant Drosophila Dev. Biol. 205 1999 129 144
51. W. Li, J.T. Ohlmeyer, M.E. Lane, and D. Kalderon Function of protein kinase a in Hedgehog signal transduction and Drosophila imaginal disc development Cell 80 1995 553 562
52. L. Lum, and P.A. Beachy The Hedgehog response network: sensors, switches, and routers Science 304 2004 1755 1759
53. L. Lum, C. Zhang, S. Oh, R.K. Mann, D.P. von Kessler, and J. Taipale Hedgehog signal transduction via smoothened association with a cytoplasmic complex scaffolded by atypical kinesin Costal-2 Mol. Cell. 12 2003 1261 1274
54. C. Ma, and K. Moses Wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye Development 121 1995 2279 2289
55. C. Ma, Y. Zhou, P.A. Beachy, and K. Moses The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye Cell 75 1993 927 938
56. C. Martin-Castellanos, and B.A. Edgar A characterization of the effects of Dpp signaling on cell growth and proliferation in the Drosophila wing Development 129 2002 1003 1013
57. B. Mollereau, M. Dominguez, R. Webel, N.J. Colley, B. Keung, J.F. de Celis, and C. Desplan Two-step process for photoreceptor formation in Drosophila Nature 412 2001 911 913
58. C.K. Motzny, and R. Holmgren The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways Mech. Dev. 52 1995 137 150
59. B.A. Mozer, and K. Easwarachandran Pattern formation in the absence of cell proliferation: tissue-specific regulation of cell cycle progression by string (stg) during Drosophila eye development Dev. Biol. 213 1999 54 69
60. J.L. Mullor, M. Calleja, J. Capdevila, and I. Guerrero Hedgehog activity, independent of decapentaplegic, participates in wing disc patterning Development 124 1997 1227 1237
61. C. Niehrs Mad connection to the nucleus Nature 381 1996 561 562
62. R. Nolo, L.A. Abbott, and H.J. Bellen Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila Cell 102 2000 349 362
63. E.M. O'Neill, I. Rebay, R. Tjian, and G.M. Rubin The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway Cell 78 1994 137 147
64. K.S. Pappu, R. Chen, B.W. Middlebrooks, C. Woo, U. Heberlein, and G. Mardon Mechanism of hedgehog signaling during Drosophila eye development Development 130 2003 3053 3062
65. A. Penton, S.B. Selleck, and F.M. Hoffmann Regulation of cell cycle synchronization by decapentaplegic during Drosophila eye development Science 275 1997 203 206
66. A. Perez-Garijo, F.A. Martin, and G. Morata Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila Development 131 2004 5591 5598
67. U. Persson, H. Izumi, S. Souchelnytskyi, S. Itoh, S. Grimsby, and U. Engstrom The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation Fed. Eur. Biochem. Soc. Letters 434 1998 83 87
68. F. Pignoni, and S.L. Zipursky Induction of Drosophila eye development by Decapentaplegic Development 124 1997 271 278
69. H. Qi, M.D. Rand, X. Wu, N. Sestan, W. Wang, and P. Rakic Processing of the Notch ligand delta by the metalloprotease Kuzbanian Science 283 1999 91 94
70. L.A. Raftery, and D.J. Sutherland TGF-beta family signal transduction in Drosophila development: from Mad to Smads Dev. Biol. 210 1999 251 268
71. D.F. Ready, T.E. Hanson, and S. Benzer Development of the Drosophila retina, a neurocrystalline lattice Dev. Biol. 53 1976 217 240
72. R. Reifegerste, and K. Moses Genetics of epithelial polarity and pattern in the Drosophila retina BioEssays 21 1999 275 285
73. H. Richardson, L.V. O'Keefe, T. Marty, and R. Saint Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc Development 121 1995 3371 3379
74. S. Robinow, and K. White The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages Dev. Biol. 126 1988 294 303
75. A.B. Rodrigues, E. Werner, and K. Moses Genetic and biochemical analysis of the role of Egfr in the morphogenetic furrow of the developing Drosophila eye Development 132 2005 4697 4707
76. H.D. Ryoo, T. Gorenc, and H. Steller Apoptotic cells can induce compensatory cell proliferation through the JNK and the wingless signaling pathways Dev. Cell 7 2004 491 501
77. B.V. Shyamala, and K.M. Bhat A positive role for patched-smoothened signaling in promoting cell proliferation during normal head development in Drosophila Development 129 2002 1839 1847
78. A. Srinivasan, K.A. Roth, R.O. Sayers, K.S. Shindler, A.M. Wong, L.C. Fritz, and K.J. Tomaselli In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system Cell Death Differ. 5 1998 1004 1016
79. M. Strigini, and S.M. Cohen A Hedgehog activity gradient contributes to AP axial patterning of the Drosophila wing Development 124 1997 4697 4705
80. D.I. Strutt, and M. Mlodzik The regulation of hedgehog and decapentaplegic during Drosophila eye imaginal disc development Mech. Dev. 58 1996 39 50
81. D.I. Strutt, V. Wiersdorff, and M. Mlodzik Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A Nature 373 1995 705 709
82. D.I. Strutt, U. Weber, and M. Mlodzik The role of RhoA in tissue polarity and frizzled signaling Nature 387 1997 292 295
83. H. Tanimoto, S. Itoh, P. ten Dijke, and T. Tabata Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs Mol. Cell 5 2000 59 71
84. M. Tio, and K. Moses The Drosophila TGFα homolog spitz acts in photoreceptor recruitment in the developing retina Development 124 1997 343 351
85. A. Tomlinson The cellular dynamics of pattern formation in the eye of Drosophila J. Embryol. Exp. Morph. 89 1985 313 331
86. A. Tomlinson Cellular interactions in the developing Drosophila eye Development 104 1988 183 193
87. A. Tomlinson, and D.F. Ready Neuronal differentiation in the Drosophila ommatidium Dev. Biol. 120 1987 366 376
88. J. Torres-Vazquez, R. Warrior, and K. Arora Schnurri is required for dpp-dependent patterning of the Drosophila wing Dev. Biol. 227 2000 388 402
89. M. Vervoort, M. Crozatier, D. Valle, and A. Vincent The COE transcription factor Collier is a mediator of short-range Hedgehog-induced patterning of the Drosophila wing Curr. Biol. 9 1999 632 639
90. M.G. Voas, and I. Rebay Signal integration during development: insights from the Drosophila eye Dev. Dyn. 229 2004 162 175
91. V. Wiersdorff, T. Lecuit, S.M. Cohen, and M. Mlodzik 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 1996 2153 2162
92. T. Wolff, and D.F. Ready The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave Development 113 1991 841 850
93. T. Wolff, and D.F. Ready Chapter 22: pattern formation in the Drosophila retina M. Bate A. Martinez-Arias The Development of Drosophila melanogaster vol. 2 1993 Cold Spring Harbor Laboratory Press 1277 1325
94. K. Yu, M.A. Sturtevant, B. Biehs, V. Francois, R.W. Padgett, R.K. Blackman, and E. Bier The Drosophila decapentaplegic and short gastrulation genes function antagonistically during adult wing vein development Development 122 1996 4033 4044