The HLH protein Extramacrochaetae is required for R7 cell and cone cell fates in the Drosophila eye

Developmental Biology

Volumn 327, Issue 2, 2009, Pages 288-300

  Bhattacharya, Abhishek ^a   Baker, Nicholas E ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Cell fate specification; Drosophila eye; Extramacrochaetae; Eye development; Notch signaling; R7 cell

Indexed keywords

DROSOPHILA PROTEIN; NOTCH RECEPTOR; PROTEIN EXTRAMACROCHAETAE; UNCLASSIFIED DRUG;

ARTICLE; CELL FATE; CELL MATURATION; CONTROLLED STUDY; DROSOPHILA; EYE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CONE; SIGNAL TRANSDUCTION;

EID: 60549101866     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.11.037     Document Type: Article

References (73)

1. Adam J.C., and Montell D.J. A role for extra macrochaetae downstream of Notch in follicle cell differentiation. Development 131 (2004) 5971-5980
2. Alifragis P., Poortinga G., Parkhurst S.M., and Delidakis C. A network of interacting transcriptional regulators involved in Drosophila neural fate specification revealed by the yeast two-hybrid system. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 13099-13104
3. Alon U. Network motifs: theory and experimental approaches. Nature 450 (2007) 450-461
4. Aster J.C., Pear W.S., and Blacklow S.C. Notch signaling in leukemia. Ann. Rev. Pathol. 3 (2008) 587-613
5. Bai G., Sheng N., Xie Z., Bian W., Yokota Y., Benezra R., Kageyama R., Guillemot F., and Jing N. Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev. Cell 13 (2007) 283-297
6. Baker N.E. Notch and the patterning of ommatidial founder cells in the developing Drosophila eye. Results Probl. Cell Differ. 37 (2002) 35-58
7. Baker N.E., and Yu S. Proneural function of neurogenic genes in the developing Drosophila eye. Curr. Biol. 7 (1997) 122-132
8. Baker N.E., Yu S., and Han D. Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye. Curr. Biol. 6 (1996) 1290-1301
9. Baonza A., and Freeman M. Notch signalling and the initiation of neural development in the Drosophila eye. Development 128 (2001) 3889-3898
10. Baonza A., de Celis J.F., and Garcia-Bellido A. Relationships between extramacrochaetae and Notch signalling in Drosophila wing development. Development 127 (2000) 2383-2393
11. Blochlinger K., Jan L.Y., and Jan Y.N. Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development 117 (1993) 441-450
12. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
13. Bray S.J. Notch signalling: a simple pathway becomes complex. Nat. Rev., Mol. Cell Biol. 7 (2006) 678-689
14. Brown N.L., Sattler C.A., Paddock S.W., and Carroll S.B. Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell 80 (1995) 879-887
15. Brown N.L., Paddock S.W., Sattler C.A., Cronmiller C., Thomas B.J., and Carroll S.B. daughterless is required for Drosophila photoreceptor cell determination, eye morphogenesis, and cell cycle progression. Dev. Biol. 179 (1996) 65-78
16. Cagan R.L., and Ready D.F. Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev. 3 (1989) 1099-1112
17. Campuzano S. Emc, a negative HLH regulator with multiple functions in Drosophila development. Oncogene 20 (2001) 8299-8307
18. Castrillon D.H., Gonczy P., Alexander S., Rawson R., Eberhart C.G., Viswanathan S., DiNardo S., and Wasserman S.A. Towards a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135 (1993) 489-505
19. Cooper M.T., and Bray S.J. Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 397 (1999) 526-530
20. Cooper M.T., and Bray S.J. R7 photoreceptor specification requires Notch activity. Curr. Biol. 10 (2000) 1507-1510
21. de Celis J.F., Baonza A., and Garcia-Bellido A. Behavior of extramacrochaetae mutant cells in the morphogenesis of the Drosophila wing. Mech. Dev. 53 (1995) 209-221
22. de Celis J.F., de Celis J., Ligoxygakis P., Preiss A., Delidakis C., and Bray S. Functional relationships between Notch, Su(H) and the bHLH genes of the E(spl) complex: the E(spl) genes mediate only a subset of Notch activities during imaginal development. Development 122 (1996) 2719-2728
23. Doe C.Q., and Skeath J.B. Neurogenesis in the insect nervous system. Curr. Opin. Neurobiol. 6 (1996) 18-24
24. Dokucu M.E., Zipursky S.L., and Cagan R.L. Atonal, Rough and the resolution of proneural clusters in the developing Drosophila retina. Development 122 (1996) 4139-4147
25. Domingos P.M., Brown S., Barrio R., Ratnakumar K., Frankfort B.J., Mardon G., Steller H., and Mollereau B. Regulation of R7 and R8 differentiation by the spalt genes. Dev. Biol. 273 (2004) 121-133
26. Doroquez D.B., and Rebay I. Signal integration during development: mechanisms of EGFR and Notch pathway function and cross-talk. Crit. Rev. Biochem. Mol. Biol. 41 (2006) 339-385
27. Duffy J.B., Kania M.A., and Gergen J.P. Expression and function of the Drosophila gene runt in early stages of neural development. Development 113 (1991) 1223-1230
28. Ellis H.M. Embryonic expression and function of the Drosophila helix-loop-helix gene, extramacrochaetae. Mech. Dev. 47 (1994) 65-72
29. Ellis H.M., Spann D.R., and Posakony J.W. extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins. Cell 61 (1990) 27-38
30. Fanto M., and Mlodzik M. Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397 (1999) 523-526
31. Firth L.C., and Baker N.E. Spitz from the retina regulates genes transcribed in the second mitotic wave, peripodial epithelium, glia and plasmatocytes of the Drosophila eye imaginal disc. Dev. Biol. 307 (2007) 521-538
32. Firth L.C., Li W., Zhang H., and Baker N.E. Analyses of RAS regulation of eye development in Drosophila melanogaster. Methods Enzymol. 407 (2006) 711-721
33. Flores G.V., Duan H., Yan H., Nagaraj R., Fu W., Zou Y., Noll M., and Banerjee U. Combinatorial signaling in the specification of unique cell fates. Cell 103 (2000) 75-85
34. Fortini M.E., Rebay I., Caron L.A., and Artavanis-Tsakonas S. An activated Notch receptor blocks cell-fate commitment in the developing Drosophila eye. Nature 365 (1993) 555-557
35. Frankfort B.J., and Mardon G. R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129 (2002) 1295-1306
36. Fryer C.J., White J.B., and Jones K.A. Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol. Cell 16 (2004) 509-520
37. Fu W., and Noll M. The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye. Genes Dev. 11 (1997) 2066-2078
38. Fu W., and Baker N.E. 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
39. Fuerstenberg S., and Giniger E. Multiple roles for notch in Drosophila myogenesis. Dev. Biol. 201 (1998) 66-77
40. Garcia Alonso L.A., and Garcia-Bellido A. Extramacrochaetae, a trans-acting gene of the achaete-scute complex of Drosophila involved in cell communication. Roux's Arch. Dev. Biol. 197 (1988) 328-338
41. Garrell J., and Modolell J. The Drosophila extramacrochaetae locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein. Cell 61 (1990) 39-48
42. Hassan B., and Vassin H. Regulatory interactions during early neurogenesis in Drosophila. Dev. Genet. 18 (1996) 18-27
43. Heitzler P., Bourouis M., Ruel L., Carteret C., and Simpson P. 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 (1996) 161-171
44. Hinz U., Giebel B., and Campos-Ortega J.A. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76 (1994) 77-87
45. Iavarone A., and Lasorella A. Id proteins in neural cancer. Cancer Lett. 204 (2004) 189-196
46. Janody F., Lee J.D., Jahren N., Hazelett D.J., Benlali A., Miura G.I., Draskovic I., and Treisman J.E. A mosaic genetic screen reveals distinct roles for trithorax and polycomb group genes in Drosophila eye development. Genetics 166 (2004) 187-200
47. Jarman A.P., Grell E.H., Ackerman L., Jan L.Y., and Jan Y.N. atonal is the proneural gene for Drosophila photoreceptors. Nature 369 (1994) 398-400
48. Jennings B., Preiss A., Delidakis C., and Bray S. The Notch signalling pathway is required for Enhancer of split bHLH protein expression during neurogenesis in the Drosophila embryo. Development 120 (1994) 3537-3548
49. Jönsson F., and Knust E. Distinct functions of the Drosophila genes Serrate and Delta revealed by ectopic expression during wing development. Dev. Genes Evol. 206 (1996) 91-101
50. Kaminker J.S., Canon J., Salecker I., and Banerjee U. Control of photoreceptor axon target choice by transcriptional repression of Runt. Nat. Neurosci. 5 (2002) 746-750
51. Kanai M.I., Okabe M., and Hiromi Y. seven-up controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. Dev. Cell 8 (2005) 203-213
52. Karandikar U.C., Trott R.L., Yin J., Bishop C.P., and Bidwai A.P. Drosophila CK2 regulates eye morphogenesis via phosphorylation of E(spl)M8. Mech. Dev. 121 (2004) 273-286
53. Kauffmann R.C., Li S., Gallagher P.A., Zhang J., and Carthew R.W. Ras1 signaling and transcriptional competence in the R7 cell of Drosophila. Genes Dev. 10 (1996) 2167-2178
54. Kramatschek B., and Campos-Ortega J.A. Neuroectodermal transcription of the Drosophila neurogenic genes E(spl) and HLH-m5 is regulated by proneural genes. Development 120 (1994) 815-826
55. Kuhnlein R.P., Frommer G., Friedrich M., Gonzalez-Gaitan M., Weber A., Wagner-Bernholz J.F., Gehring W.J., Jackle H., and Schuh R. 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
56. Lehmann R., Jimenez F., Dietrich U., and Campos-Ortega J.A. On the phenotype and development of mutants of early neurogenesis in Drosophila melanogaster. Roux's Arch. Dev. Biol. 192 (1983) 62-74
57. Li Y., and Baker N.E. The roles of cis-inactivation by Notch ligands and of neuralized during eye and bristle patterning in Drosophila. BMC Dev. Biol. 4 (2004) 5
58. Massari M.E., and Murre C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20 (2000) 429-440
59. Mlodzik M., Hiromi Y., Weber U., Goodman C.S., and Rubin G.M. The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60 (1990) 211-224
60. Morata G., and Ripoll P. Minutes: mutants of Drosophila autonomously affecting cell division rate. Dev. Biol. 42 (1975) 211-221
61. Morel V., and Schweisguth F. Repression by suppressor of hairless and activation by Notch are required to define a single row of single-minded expressing cells in the Drosophila embryo. Genes Dev. 14 (2000) 377-388
62. Nagaraj R., Cannon J., and Banerjee U. Cell fate specification in the Drosophila eye. In: Moses K. (Ed). Drosophila Eye Development Vol. 37 (2002), Springer 73-88
63. Neufeld T.P., de la Cruz A.F., Johnston L.A., and Edgar B.A. Coordination of growth and cell division in the Drosophila wing. Cell 93 (1998) 1183-1193
64. Newsome T.P., Asling B., and Dickson B.J. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127 (2000) 851-860
65. Nolo R., Abbott L.A., and Bellen H.J. Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102 (2000) 349-362
66. Oellers N., Dehio M., and Knust E. bHLH proteins encoded by the Enhancer of split complex of Drosophila negatively interfere with transcriptional activation mediated by proneural genes. Mol. Gen. Genet. 244 (1994) 465-473
67. Pignoni F., and Zipursky S.L. Induction of Drosophila eye development by decapentaplegic. Development 124 (1997) 271-278
68. Rottgen G., Wagner T., and Hinz U. A genetic screen for elements of the network that regulates neurogenesis in Drosophila. Mol. Gen. Genet. 257 (1998) 442-451
69. Ruzinova M.B., and Benezra R. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13 (2003) 410-418
70. Tomlinson A., and Struhl G. Delta/Notch and Boss/Sevenless signals act combinatorially to specify the Drosophila R7 photoreceptor. Mol. Cell 7 (2001) 487-495
71. Van Doren M., Ellis H.M., and Posakony J.W. The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. Development 113 (1991) 245-255
72. Watt F.M., Estrach S., and Amber C.A. Epidermal Notch signalling: differentiation, cancer, and adhesion. Curr. Opin. Cell Biol. 20 (2008) 171-179
73. Xu T., and Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117 (1993) 1223-1237