Identification of novel regulators of atonal expression in the developing Drosophila retina

Genetics

Volumn 180, Issue 4, 2008, Pages 2095-2110

  Melicharek, David ^a   Shah, Arpit ^b   DiStefano, Ginnene ^a   Gangemi, Andrew J ^b   Orapallo, Andrew ^b   Vrailas Mortimer, Alysia D ^c   Marenda, Daniel R ^a  

^a DREXEL UNIVERSITY   (United States)

^b UNIVERSITY OF THE SCIENCES   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSECT PROTEIN; PROTEIN ATONAL; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; CHEMICAL MUTAGENESIS; CONTROLLED STUDY; DAUGHTERLESS GENE; DROSOPHILA; ENHANCER REGION; GENE IDENTIFICATION; GENE MUTATION; GENETIC ANALYSIS; HEDGEHOG GENE; KISMET GENE; LILLIPUTIAN GENE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; RETINA DEVELOPMENT; ROUGHENED EYE GENE; TEMPERATURE SENSITIVITY; TRANSCRIPTION REGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DNA HELICASES; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; NERVE TISSUE PROTEINS; PHENOTYPE; RETINA; TRANSCRIPTION FACTORS;

MAMMALIA; VERTEBRATA;

EID: 61749104678     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.093302     Document Type: Article

References (98)

1. AGNEL, M., S. KERRIDGE, C. VOLA and R. GRIFFIN-SHEA, 1989 Two transcripts from the rotund region of Drosophila show positional specificities in imaginal disc tissues. Genes Dev. 3: 85-95.
2. ASHBURNER, M., 1989 Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. BAKER, N. E., M. MLODZIK and G. M. RUBIN, 1990 Spacing differentiation in the developing Drosophila eye: a fibrinogen-related lateral inhibitor encoded by scabrous. Science 250: 1370-1377.
4. BAKER, N. E., and G. M. RUBIN, 1989 Effect on eye development of dominant mutations in Drosophila homologue of the EGF receptor. Nature 340: 150-153.
5. BAKER, N. E., and G. M. RUBIN, 1992 Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs. Dev. Biol. 150: 381-396.
6. BAKER, N. E., S. YU and D. HAN, 1996 Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye. Curr. Biol. 6: 1290-1301.
7. BASLER, K., and E. HAFEN, 1989 Dynamics of Drosophila eye development and temporal requirements of sevenless expression. Development 107: 723-731.
8. BELL, A. E., 1954 New mutants report. Drosoph. Inf. Serv. 28: 73.
9. BONINI, N. M., W. M. LEISERSON and S. BENZER, 1993 The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72: 379-395.
10. BOROD, E. R., and U. HEBERLEIN, 1998 Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina. Dev. Biol. 197: 187-197.
11. BROWN, N. L., S. KANEKAR, M. L. VETTER, P. K. TUCKER, D. L. GEMZA et al., 1998 Math5 encodes a murine basic helix-loop-helix transcription factor expressed during early stages of retinal neurogenesis. Development 125: 4821-4833.
12. BROWN, N. L., S. W. PADDOCK, C. A. SATTLER, C. CRONMILLER, B. J. THOMAS et al., 1996 daughterless is required for Drosophila photoreceptor cell determination, eye morphogenesis, and cell cycle progression. Dev. Biol. 179: 65-78.
13. BROWN, N. L., S. PATEL, J. BRZEZINSKI and T. GLASER, 2001 Math5 is required for retinal ganglion cell and optic nerve formation. Development 128: 2497-2508.
14. BRUMBY, A. M., C. B. ZRALY, J. A. HORSFIELD, J. SECOMBE, R. SAINT et al., 2002 Drosophila cyclin E interacts with components of the Brahma complex. EMBO J. 21: 3377-3389.
15. CAMPOS-ORTEGA, J. A., and A. HOFBAUER, 1977 Cell clones and pattern formation: on the lineage of photoreceptor cells in the compound eye of Drosophila. Roux's Arch. Dev. Biol. 181: 227-245.
16. CHEN, C.-K., and C.-T. CHIEN, 1999 Negative regulation of atonal in proneural cluster formation of Drosophila R8 photoreceptors. Proc. Natl. Acad. Sci. USA 96: 5055-5060.
17. COLLINS, R. T., T. FURUKAWA, N. TANESE and J. E. TREISMAN, 1999 Osa associates with the Brahma chromatin remodeling complex and promotes the activation of some target genes. EMBO J. 18: 7029-7040.
18. DAUBRESSE, G., R. DEURING, L. MOORE, O. PAPOULAS, I. ZAKRAJSEK et al., 1999 The Drosophila kismet gene is related to chromatin-remodeling factors and is required for both segmentation and segment identity. Development 126: 1175-1187.
19. DINGWALL, A. K., S. J. BEEK, C. M. MCCALLUM, J. W. TAMKUN, G. V. KALPANA et al., 1995 The Drosophila snr1 and brm proteins are related to yeast SWI/SNF proteins and are components of a large protein complex. Mol. Biol. Cell 6: 777-791.
20. DOMINGUEZ, M., 1999 Dual role for Hedgehog in the regulation of the proneural gene atonal during ommatidia development. Development 126: 2345-2353.
21. DOROQUEZ, D. B., and I. REBAY, 2006 Signal integration during development: mechanisms of EGFR and Notch pathway function and cross-talk. Crit. Rev. Biochem. Mol. Biol. 41: 339-385.
22. ELFRING, L. K., C. DANIEL, O. PAPOULAS, R. DEURING, M. SARTE et al., 1998 Genetic analysis of brahma: the Drosophila homolog of the yeast chromatin remodeling factor SWI2/SNF2. Genetics 148: 251-265.
23. FRANKFORT, B. J., and G. MARDON, 2002 R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129: 1295-1306.
24. FRANKFORT, B. J., R. NOLO, Z. ZHANG, H. BELLEN and G. MARDON, 2001 senseless Repression of rough is required for R8 photoreceptor differentiation in the developing Drosophila eye. Neuron 32: 403-414.
25. FREEMAN, M., 1997 Cell determination strategies in the Drosophila eye. Development 124: 261-270.
26. FREEMAN, M., 1998 Complexity of EGF receptor signaling revealed in Drosophila. Curr. Opin. Genet. Dev. 8: 407-411.
27. FUERST, P. G., S. M. RAUCH and R. W. BURGESS, 2007 Defects in eye development in transgenic mice overexpressing the heparan sulfate proteoglycan agrin. Dev. Biol. 303: 165-180.
28. GREENWOOD, S., and G. STRUHL, 1999 Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway. Development 126: 5795-5808.
29. GU, Y., Y. SHEN, R. A. GIBBS and D. L. NELSON, 1996 Identification of FMR2, a novel gene associated with the FRAXE CCG repeat and CpG island. Nat. Genet. 13: 109-113.
30. GU, Y., and D. L. NELSON, 2003 FMR2 function: insight from a mouse knockout model. Cytogenet. Genome Res. 100: 129-139.
31. HASSAN, B. A., and H. J. BELLEN, 2000 Doing the MATH: Is the mouse a good model for fly development? Genes Dev. 14: 1852-1865.
32. 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.
33. HIGSON, T. S., J. E. TESSIATORE, S. A. BENNETT, R. C. DERK and M. A. KOTARSKI, 1993 The molecular organization of the Star/asteroid region, a region necessary for proper eye development in Drosophila melanogaster. Genome 36: 356-366.
34. HSIUNG, F., and K. MOSES, 2002 Retinal development in Drosophila: specifying the first neuron. Hum. Mol. Genet. 11: 1207-1214.
35. HUFNAGEL, R. B., A. N. RIESENBERG, S. M. SAUL and N. L. BROWN, 2007 Conserved regulation of Math5 and Math1 revealed by Math5-GFP transgenes. Mol. Cell. Neurosci. 36: 435-448.
36. HUTCHESON, D. A., and M. L. VETTER, 2001 The bHLH factors Xath5 and XNeuroD can upregulate the expression of Xbrn3d, a POU-homeodomain transcription factor. Dev. Biol. 232: 327-338.
37. INGHAM, P. W., and A. P. MCMAHON, 2001 Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15: 3059-3087.
38. JANODY, F., J. D. LEE, N. JAHREN, D. J. HAZELET, A. BANLALI et al., 2004 A mosaic genetic screen reveals distinct roles for trithorax and Polycomb group genes in Drosophila eye development. Genetics 166: 187-200.
39. JANODY, F., Z. MARTIROSYAN, A. BENLALI and J. E. TREISMAN, 2003 Two subunits of the Drosophila mediator complex act together to control cell affinity. Development 130: 3691-3701.
40. JARMAN, A. P., Y. GRAU, L. Y. JAN and Y. N. JAN, 1993 atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73: 1307-1321.
41. JARMAN, A. P., E. H. GRELL, L. ACKERMAN, L. Y. JAN and Y. N. JAN, 1994 atonal is the proneural gene for Drosophila photoreceptors. Nature 369: 398-400.
42. JARMAN, A. P., Y. SUN, L. Y. JAN and Y. N. JAN, 1995 Role of the proneural gene, atonal, in formation of the Drosophila chordotonal organs and photoreceptors. Development 121: 2019-2030.
43. KENNISON, J. A., and J. W. TAMKUN, 1988 Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc. Natl. Acad. Sci. USA 85: 8136-8140.
44. KOPHENGNAVONG, T., J. E. MICHNOWICZ and T. K. BLACKWELL, 2000 Establishment of distinct MyoD, E2A, and twist DNA binding specificities by different basic region-DNA conformations. Mol. Cell. Biol. 20: 261-272.
45. KUMAR, J., and K. MOSES, 1997 Transcription factors in eye development: A gorgeous mosaic? Genes Dev. 11: 2023-2028.
46. KUMAR, J. P., F. HSIUNG, M. POWERS and K. MOSES, 2003 Nuclear translocation of activated MAP kinase is developmentally regulated in the developing Drosophila eye. Development 130: 3703-3714.
47. KUZIN, B., S. TILLIB, Y. SEDKOV, L. MIZROKHI and A. MAZO, 1994 The Drosophila trithorax gene encodes a chromosomal protein and directly regulates the region-specific homeotic gene fork head. Genes Dev. 8: 2478-2490.
48. LE, T. T., E. WROBLEWSKI, S. PATEL, A. N. RIESENBERG and N. L. BROWN, 2006 Math5 is required for both early retinal neuron differentiation and cell cycle progression. Dev. Biol. 295: 764-778.
49. LEE, E.-C., X. HU, S.-Y. YU and N. E. BAKER, 1996 The scabrous gene encodes a secreted glycoprotein dimer and regulates proneural development in Drosophila eyes. Mol. Cell. Biol. 16: 1179-1188.
50. LEE, J. J., D. P. VON KESSLER, S. PARKS and P. A. BEACHY, 1992 Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71: 33-50.
51. LEWIS, E. B., 1945 The relation of repeats to position effect in Drosophila melanogaster. Genetics 30: 137-166.
52. LI, Y., and N. E. BAKER, 2001 Proneural enhancement by Notch overcomes Suppressor-of-Hairless repressor function in the developing Drosophila eye. Curr. Biol. 11: 330-338.
53. LIM, J., O. K. LEE, Y. C. HSU, A. SINGH and K. W. CHOI, 2007 Drosophila TRAP230/240 are essential coactivators for Atonal in retinal neurogenesis. Dev. Biol. 308: 322-330.
54. LIM, J., H. JAFAR-NEJAD, Y. C. HSU and K. W. CHOI, 2008 Novel function of the class I bHLH protein Daughterless in the negative regulation of proneural gene expression in the Drosophila eye. EMBO Rep. (in press).
55. LUM, L., and P. A. BEACHY, 2004 The Hedgehog response network: sensors, switches, and routers. Science 304: 1755-1759.
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. MA, C., H. LIU, Y. ZHOU and K. MOSES, 1996 Identification and characterization of autosomal genes that interact with glass in the developing Drosophila eye. Genetics 142: 1199-1213.
58. MARENDA, D. R., C. B. ZRALY, Y. FENG, S. EGAN and A. K. DINGWALL, 2003 The Drosophila SNR1 (SNF5/INI1) subunit directs essential developmental functions of the Brahma chromatin remodeling complex. Mol. Cell. Biol. 23: 289-305.
59. MASSARI, M. E., and C. MURRE, 2000 Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20: 429-440.
60. 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.
61. MOLLEREAU, B., and P. M. DOMINGOS, 2005 Photoreceptor differentiation in Drosophila: from immature neurons to functional photoreceptors. Dev. Dyn. 232: 585-592.
62. MOSES, K., 1991 The role of transcription factors in the developing Drosophila eye. Trends Genet. 7: 250-255.
63. MOSES, K., 2003 Drosophila eye: progressive neural development, in Encyclopedia of Life Sciences. John Wiley & Sons, Chichester, UK.
64. MULLER, D., S. J. KUGLER, A. PREISS, D. MAIER and A. C. NAGEL, 2005 Genetic modifier screens on Hairless gain-of-function phenotypes reveal genes involved in cell differentiation, cell growth and apoptosis in Drosophila melanogaster. Genetics 171: 1137-1152.
65. NEUFELD, T. P., A. F. DE LA CRUZ, L. A. JOHNSTON and B. A. EDGAR, 1998a Coordination of growth and cell division in the Drosophila wing. Cell 93: 1183-1193.
66. NEUFELD, T. P., A. H. TANG and G. M. RUBIN, 1998b A genetic screen to identify components of the sina signaling pathway in Drosophila eye development. Genetics 148: 277-286.
67. NEWSOME, T. P., B. ASLING and B. J. DICKSON, 2000 Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127: 851-860.
68. NÜSSLEIN-VOLHARD, C., and E. WIESCHAUS, 1980 Mutations affecting segment number and polarity in Drosophila. Nature 287: 795-801.
69. PERRON, M., and W. A. HARRIS, 2000 Determination of vertebrate retinal progenitor cell fate by the Notch pathway and basic helix-loop-helix transcription factors. Cell. Mol. Life Sci. 57: 215-223.
70. PERRON, M., S. KANEKAR, M. L. VETTER and W. A. HARRIS, 1998 The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. Dev. Biol. 199: 185-200.
71. READY, D. F., T. E. HANSON and S. BENZER, 1976 Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53: 217-240.
72. ROCH, F., F. SERRAS, F. J. CIFUENTES, M. COROMINAS, B. ALSINA et al., 1998 Screening of larval/pupal P-element induced lethals on the second chromosome in Drosophila melanogaster: clonal analysis and morphology of imaginal discs. Mol. Gen. Genet. 257: 103-112.
73. SANLAVILLE, D., and A. VERLOES, 2007 CHARGE syndrome: an update. Eur. J. Hum. Genet. 15: 389-399.
74. SAUL, S. M., J. A. BRZEZINSKI, IV, R. A. ALTSCHULER, S. E. SHORE, D. D. RUDOLPH et al., 2008 Math5 expression and function in the central auditory system. Mol. Cell. Neurosci. 37: 153-169.
75. SCHIMMENTI, L. A., J. DE LA CRUZ, R. A. LEWIS, J. D. KARKERA, G. S. MANLIGAS et al., 2003 Novel mutation in sonic hedgehog in non-syndromic colobomatous microphthalmia. Am. J. Med. Genet. A 116A: 215-221.
76. SMITH, J. E., III, and C. CRONMILLER, 2001 The Drosophila daughterless gene autoregulates and is controlled by both positive and negative cis regulation. Development 128: 4705-4714.
77. SRINIVASAN, S., J. A. ARMSTRONG, R. DEURING, I. K. DAHLSVEEN, H. MCNEILL et al., 2005 The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA polymerase II. Development 132: 1623-1635.
78. ST PIERRE, S. E., M. I. GALINDO, J. P. COUSO and S. THOR, 2002 Control of Drosophila imaginal disc development by rotund and roughened eye: differentially expressed transcripts of the same gene encoding functionally distinct zinc finger proteins. Development 129: 1273-1281.
79. STARK, D. R., 2002 Hedgehog signalling: pulling apart Patched and Smoothened. Curr. Biol. 12: R437-R439.
80. SUN, Y., L. Y. JAN and Y. N. JAN, 1998 Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system. Development 125: 3731-3740.
81. SUZUKI, T., and K. SAIGO, 2000 Transcriptional regulation of atonal required for Drosophila larval eye development by concerted action of eyes absent, sine oculis and hedgehog signaling independent of fused kinase and cubitus interruptus. Development 127: 1531-1540.
82. TAMKUN, J. W., R. DEURING, M. P. SCOTT, M. KISSINGER, A. M. PATTATUCCI et al., 1992 brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/ SWI2. Cell 68: 561-572.
83. TANG, A. H., T. P. NEUFELD, G. M. RUBIN and H. A. MULLER, 2001 Transcriptional regulation of cytoskeletal functions and segmentation by a novel maternal pair-rule gene, lilliputian. Development 128: 801-813.
84. THERRIEN, M., D. K. MORRISON, A. M. WONG and G. M. RUBIN, 2000 A genetic screen for modifiers of a kinase suppressor of Ras-dependent rough eye phenotype in Drosophila. Genetics 156: 1231-1242.
85. TIO, M., and K. MOSES, 1997 The Drosophila TGFa homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124: 343-351.
86. TOMLINSON, A., and D. F. READY, 1987 Neuronal differentiation in the Drosophila ommatidium. Dev. Biol. 120: 366-376.
87. TREISMAN, J. E., A. LUK, G. M. RUBIN and U. HEBERLEIN, 1997 eyelid antagonizes wingless signaling during Drosophila development and has homology to the Bright family of DNA-binding proteins. Genes Dev. 11: 1949-1962.
88. VETTER, M. L., and N. L. BROWN, 2001 The role of basic helix-loop-helix genes in vertebrate retinogenesis. Semin. Cell Dev. Biol. 12: 491-498.
89. VRAILAS, A. D., D. R. MARENDA, S. E. COOK, M. A. POWERS, J. A. LORENZEN et al., 2006 smoothened and thickveins regulate Moleskin/Importin 7-mediated MAP kinase signaling in the developing Drosophila eye. Development 133: 1485-1494.
90. VRAILAS, A. D., and K. MOSES, 2006 Smoothened, thickveins and the genetic control of cell cycle and cell fate in the developing Drosophila eye. Mech. Dev. 123: 151-165.
91. WANG, S. W., B. S. KIM, K. DING, H. WANG, D. SUN et al., 2001 Requirement for math5 in the development of retinal ganglion cells. Genes Dev. 15: 24-29.
92. WHITE, N. M., and A. P. JARMAN, 2000 Drosophila atonal controls photoreceptor R8-specific properties and modulates both receptor tyrosine kinase and Hedgehog signalling. Development 127: 1681-1689.
93. WOLFF, T., and D. F. READY, 1993 Pattern formation in the Drosophila retina, pp. 1277-1325 in The Development of Drosophila melanogaster, edited by M. BATE and A. MARTINEZ- ARIAS. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
94. XU, T., and G. M. RUBIN, 1993 Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223-1237.
95. YAN, R. T., W. MA, L. LIANG and S. Z. WANG, 2005 bHLH genes and retinal cell fate specification. Mol. Neurobiol. 32: 157-171.
96. YANG, Z., K. DING, L. PAN, M. DENG and L. GAN, 2003 Math5 determines the competence state of retinal ganglion cell progenitors. Dev. Biol. 264: 240-254.
97. ZENG, C., S. YOUNGER-SHEPHERD, L. Y. JAN and Y. N. JAN, 1998 Delta and Serrate are redundant Notch ligands required for asymmetric cell divisions within the Drosophila sensory organ lineage. Genes Dev. 12: 1086-1091.
98. ZRALY, C. B., D. R. MARENDA, R. NANCHAL, G. CAVALLI, C. MUCHARDT et al., 2003 SNR1 is an essential subunit in a subset of Drosophila brm complexes, targeting specific functions during development. Dev. Biol. 253: 291-308.