Bar homeodomain proteins are anti-proneural in the Drosophila eye: Transcriptional repression of atonal by Bar prevents ectopic retinal neurogenesis

Development

Volumn 130, Issue 24, 2003, Pages 5965-5974

  Lim, Janghoo ^a   Choi, Kwang Wook ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Atonal; Bar homeodomain protein; Drosophila eye; Proneural; Retinal neurogenesis

Indexed keywords

DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; NOTCH RECEPTOR; PROTEIN ATONAL; PROTEIN BARH1; PROTEIN BARH2; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CLONE; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; GENE LOSS; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; MUTANT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA DEVELOPMENT; RETINA NERVE CELL; TRANSCRIPTION REGULATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYONIC STRUCTURES; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MORPHOGENESIS; NERVE TISSUE PROTEINS; NEURONS; PHOTORECEPTORS, INVERTEBRATE; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION FACTORS;

INVERTEBRATA; MAMMALIA; VERTEBRATA;

EID: 0346258169     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00818     Document Type: Article

References (67)

1. Artavanis-Tsakonas S., Rand, M. D. and Lake, R. J. (1999). Notch signaling: cell fate control and signal integration in development. Science 284, 770-776.
2. Baker, N. E., Mlodzik, M. and Rubin, G. M. (1990). Spacing differentiation in the developing Drosophila eye: a fibrinogen-related lateral inhibitor encoded by scabrous. Science 250, 1370-1377.
3. Baker, N. E. and Yu, S.-Y. (1997). Proneural function of neurogenic genes in the developing Drosophila eye. Curr Biol. 7, 122-132.
4. Baker, N. E. and Yu, S.-Y. (1998). The R8-photoreceptor equivalence group in Drosophila: fate choice precedes regulated Delta transcription and is independent of Notch gene dose. Met h. Dev. 74, 3-14.
5. Baonza, A., Casci, T. and Freeman, M. (2001). A primary role for the epidermal growth factor receptor in ommatidial spacing in the Drosophila eye. Curr Biol. 11, 396-404.
6. Blackman, R. K., Sanicola, M., Raftery, L. A., Gillevet, T. and Gelbart, W. M. (1991). An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-β family in Drosophila. Development 111, 657-665.
7. Blair, I. P., Gibson, R. R., Bennett, C. L. and Chance, P. F. (2002). Search for genes involved in Joubert syndrome: evidence that one or more major loci are yet to be identified and exclusion of candidate genes EN1, EN2, FGF8, and BARHL1. Am. J. Med. Genet. 107, 190-196.
8. Borod, E. R. and Heberlein, U. (1998). Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina. Dev. Biol. 197, 187-197.
9. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
10. Brunet, J. F. and Ghysen, A. (1999). Deconstructing cell determination: proneural genes and neuronal identity. BioEssays 21, 313-318.
11. Bulfone, A., Menguzzato, E., Broccoli, V., Marchitiello, A., Gattuso, C., Mariani, M., Consalez, G. G. Martinez, S., Ballabio, A. and Banfi, S. (2000). Barhl1, a gene belonging to a new subfamily of mammalian homeobox genes, is expressed in migrating neurons of the CNS. Hum. Mol. Genet. 9, 1443-1452.
12. Carroll, S. B. and Whyte, J. S. (1989). The role of the hairy gene during Drosophila morphogenesis-stripes in imaginal discs. Genes Dev. 3, 905-916.
13. 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.
14. Chanut, F., Luk, A. and Heberlein, U. (2000). 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, 1203-1217.
15. Chen, C. K. and Chien, C. T. (1999). Negative regulation of atonal in proneural cluster formation of Drosophila R8 photoreceptors. Proc. Natl. Acad. Sci. USA 96, 5055-5060.
16. Chen, C.-H., von Kessler, D. P., Park, W., Wang. B., Ma, Y. and Beachy, P.A. (1999). Nuclear trafficking of Cubitus interruptus in the transcriptional regulation of hedgehog target gene expression. Cell 98, 305-316.
17. Crew, J. R., Batterham, P. and Pollock, J. A. (1997). Developing compound eye in lozenge mutants of Drosophila: Lozenge expression in the R7 equivalence goup. Dev. Genes Evol. 206, 481-493.
18. Cubas, P., de Celis, J. F., Campuzano, S. and Modolell, J. (1991). Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev. 5, 996-1008.
19. Dietrich,U.and Campos-Ortega,J.A. (1984). The expression of neurogenic loci in imaginal epidermal cells of Drosophila melanogaster. J. Neurogenet. 1, 315-322.
20. Dokucu, M. E., Zipursky, S. L. and Cagan, R. L. (1996). Atonal, Rough and the resolution of proneural clusters in the developing Drosophila retina. Development 122, 4139-4147.
21. Dominguez, M. (1999). Dual role for Hedgehog in the regulation of the proneural gene atonal during ommatidia development. Development 126, 2345-2353.
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. Edelman, D. B., Meech, R. and Jones, F. S. (2000). The homeodomain protein Barx2 contains activator and repressor domains and interacts with members of the CREB family. J. Biol. Chem. 275, 21737-21745.
24. Epps, J. L., Jones, J. B. and Tanda, S. (1997). oroshigane, a new segment polarity gene of Drosophila melanogaster, functions in hedgehog signal transduction. Genetics 145, 1041-1052.
25. Flores, G. V., Daga, A., Kalhor, H. R. and Banerjee, U. (1998). Lozenge is expressed in pluripotent precursor cells and patterns multiple cell types in the Drosophila eye through the control of cell-specific transcription factors. Development 125, 3681-3687.
26. Frankfort, B. J. and Mardon, G. (2002). R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129, 1295-1306.
27. Frankfort, B. J., Nolo, R., Zhang, Z., Bellen, H. J. and Mardon, G. (2001). senseless repression of rough is required for R8 photoreceptor differentiation in the developing Drosophilo eye. Neuron 32, 403-414.
28. Ghysen, A. and Dambly-Chaudiere, C. (1988). From DNA to form: the achaete-scute complex. Genes Dev. 2, 495-501.
29. Greenwood, S. and Struhl, G. (1999). Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway. Development 126, 5795-5808.
30. Hassan, B. A., Bermingham, N. A., He, Y., Sun, Y., Jan, Y. N., Zoghbi, H. Y. and Bellen, H. J. (2000). atonal regulates neurite arborization but does not act as a proneural gene in the Drosophila brain. Neuron 25, 549-561.
31. 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, 131-145.
32. Hayashi, T. and Saigo, K. (2001). Diversification of cell types in the Drosophila eye by differential expression of prepattern genes. Mech. Dev. 108, 13-27.
33. Heberlein, U., Wolff, T. and Rubin, G. M. (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.
34. Heitzler, P., Bourouis, M., Ruel, L., Carteret, C. and Simpson, P. (1996). Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signalling in Drosophila. Development 122, 161-171.
35. Higashijima, S.-i., 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.
36. Hjalt, T. A. and Murray, J. C. (1999). The human BARX2 gene: genomic structure, chromosomal localization, and single nucleotide polymorphisms. Genomics 62, 456-459.
37. Ingham, P. W. (1998). Transducing Hedgehog: the story so far. EMBO J. 17, 3505-3511.
38. Izaddoost, S., Nam, S.-C., Bhat, M. A., Bellen, H. J. and Choi, K.-W. (2002). Drosophila Crumbs is a positional cue in photoreceptor adherens junctions and rhabdomeres. Nature 416, 178-183.
39. Jarman, A. P., Grell, E. H., Ackerman, L., Jan, L. Y. and Jan, Y. N. (1994). atonal is the proneural gene for Drosophila photoreceptors. Nature 369, 398-400.
40. 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.
41. Jiménez, G., Paroush, Z. and Ish-Horowicz, D. (1997). Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed. Genes Dev. 11, 3072-3082.
42. Jones, F. S., Kioussi, C., Cupertino, D. W., Kallunki, P., Holst, B. D. and Edelman, G. M. (1997). Barx2, a new homeobox gene of the Bar class, is expressed in neural and craniofacial structures during development. Proc. Natl. Acad. Sci. USA 94, 2632-2637.
43. Kanekar, S., Perron, M., Dorsky, R., Harris, W. A., Jan, L. Y., Jan, Y. N. and Vetter, M. L. (1997). Xath5 participates in a network of bHLH genes in the developing Xenopus retina. Neuron 19, 981-994.
44. Kqjima, T., Sato, M. and Saigo, K. (2000). Formation and specification of distal leg segments in Drosophila by dual Bar homeobox genes BarH1 and BarH2. Development 127, 769-778.
45. Kumar, J. P., Tio, M., Hsiung, F., Akopyan, S., Gabay, L., Seger, R., Shilo, B. Z., and Moses, K. (1998). Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125, 3875-3885.
46. Lee, E. C., Hu, X., Yu, S. Y. and Baker, N. E. (1996). The scabrous gene encodes a secreted glycoprotein dimer and regulates proneural development in Drosophila eyes. Mol. Cell. Biol. 16, 1179-1188.
47. 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.
48. Methot, N. and Basler, K. (1999). Hedgehog controls limb development by regulating the activities of distinct transcriptional activator and repressor forms of Cubitus interruptus. Cell 96, 819-831.
49. Mlodzik, M., Baker, N. E. and Rubin, G. M. (1990). Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes Dev. 4, 1848-1861.
50. Motzny, C. K. and Holmgren, R. (1995). The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech. Dev. 52, 137-150.
51. Nolo, R., Abbott, L. A. and Bellen, H. J. (2000). Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102, 349-362.
52. 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. Genes Evol. 210, 140-144.
53. Pellikka, M., Tanentzapf, G., Pinto, M., Smith, C., McGlade, C. J., Ready, D. F, and Tepass, U. (2002). Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416, 143-149.
54. Price, M. A. and Kalderon, D. (1999). Proteolysis of Cubitus interruptus in Drosophila requires phosphorylation by protein kinase A. Development 126, 4331-4339.
55. Romani, S., Campuzano, S., Macagno, E. R. and Modolell, J. (1989). Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development. Genes Dev. 3, 997-1007.
56. Saito, T., Sawamoto, K., Okano, H., Anderson, D. J. and Mikoshiba, K. (1998). Mammalian BarH homologue is potential regulator of neural bHLH genes. Dev. Biol. 199, 216-225.
57. Sato, M., Kojima, T., Michiue, T. and Saigo, K. (1999). Bar homeobox genes are latitudinal prepattern genes in the developing Drosophila notum whose expression is regulated by the concerted functions of decapentaplegic and wingless. Development 126, 1457-1466.
58. Schweisguth, F., Gho, M. and Lecourtois, M. (1996). Control of cell fate choices by lateral signaling in the adult peripheral nervous system of Drosophila melanogaster. Dev. Genet. 18, 28-39.
59. Skeath, J. B. and Carroll, S. B. (1991). Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 5, 984-995.
60. Smith, S. T. and Jaynes, J. B. (1996). A conserved region of engrailed, shared among all en-, gsc-, Nk1-, Nk2- and msh-class homeoproteins, mediates active transcriptional repression in vivo. Development 122, 3141-3150.
61. 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.
62. Sun, Y., Jan, L. Y. and Jan, Y. N. (1998). Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system. Development 125, 3731-3740.
63. Tomlinson, A. and Struhl, G. (2001). Delta/Notch and Boss/Sevenless signals act combinatorially to specify the Drosophila R7 photoreceptor. Mol. Cell 7, 487-495.
64. Treisman, J. E. (2001). Drosophila homologues of the transcriptional coactivation complex subunits TRAP240 and TRAP230 are required for identical processes in eye-antennal disc development. Development 128, 603-615.
65. 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, 24-29.
66. Wolff, T. and Ready, D. F. (1993). Pattern formation in the Drosophila retina. In The Development of Drosophila melanogaster (ed. Bate, M. and Martinez-Arias, A.), pp. 1277-1326. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
67. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.