The Drosophila T-box transcription factor Midline functions within the Notch-Delta signaling pathway to specify sensory organ precursor cell fates and regulates cell survival within the eye imaginal disc

Mechanisms of Development

Volumn 130, Issue 11-12, 2013, Pages 577-601

  Das, Sudeshna ^a   Chen, Q Brent ^a   Saucier, Joseph D ^a   Drescher, Brandon ^a   Zong, Yan ^a   Morgan, Sarah ^a   Forstall, John ^a   Meriwether, Andrew ^a   Toranzo, Randy ^a   Leal, Sandra M ^a  

^a UNIVERSITY OF SOUTHERN MISSISSIPPI   (United States)

Author keywords

Apoptosis; Delta; Midline; Notch; Sensory organ precursor cell; Tbx20

Indexed keywords

NOTCH RECEPTOR; T BOX TRANSCRIPTION FACTOR;

APOPTOSIS; ARTICLE; CELL FATE; CELL SURVIVAL; CELL VIABILITY; CENTRAL NERVOUS SYSTEM; DROSOPHILA; EPIDERMIS; EPITHELIUM CELL; EYE DEVELOPMENT; EYE IMAGINAL DISC DEVELOPMENT; GENE EXPRESSION; GENETIC CONSERVATION; HEART; HUMAN; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SENSE ORGAN; VISUAL SYSTEM;

MUS; VERTEBRATA;

APOPTOSIS; DELTA; MIDLINE; NOTCH; SENSORY ORGAN PRECURSOR CELL; TBX20;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BODY PATTERNING; CELL SURVIVAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMAGINAL DISCS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LARVA; MEMBRANE PROTEINS; MICE; NERVE TISSUE PROTEINS; PUPA; RECEPTORS, NOTCH; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS;

EID: 84887608590     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2013.08.001     Document Type: Article

References (116)

1. Adam J.C., Montell D.J. A role of extra macrochaetae downstream of Notch in follicle cell differentiation. Development 2004, 131:5971-5980.
2. Affolter M., Nellen D., Nussbaumer U., Basler K. Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TBF beta homologs during Drosophila embryogenesis. Development 1994, 120:3105-3117.
3. Artavanis-Tsakonas S., Matsuno K., Fortini M.E. Notch signaling. Science 1995, 268:225-232.
4. Bainbridge S.P., Bownes M. Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morph. 1981, 65:57-80.
5. Baker N.E., Zitron A.E. Drosophila eye development: Notch and Delta amplify a neurogenic pattern conferred on the morphogenetic furrow by scabrous. Mech. Dev. 1995, 49:173-189.
6. Bao S. Two themes on the assembly of the Drosophila eye. Invertebrate and Vertebrate Eye Development 2010, 85-117. Academic Press, Elsevier Inc., San Diego CA. R.L. Cagan, T.A. Reh (Eds.).
7. Baonza A., Garcia-Bellido A. Dual role of extramacrochaetae in cell proliferation and cell differentiation during wing morphogenesis in Drosophila. Mech. Dev. 1999, 80:133-146.
8. Baonza A., deCelis J.F., Garcia-Bellida A. Relationships between extramacrochaetae and Notch signaling in Drosophila wing development. Development 2000, 127:2383-2393.
9. Blochlinger K.R., Bodmer R., Jan L.Y., Jan Y.N. Patterns of expression of Cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Nature 1990, 333:629-635.
10. Bhattacharya A., Baker N.E. A network of broadly expressed HLH genes regulates tissue-specific cell fates. Cell 2011, 147:881-892.
11. Blair S. Genetic mosaic techniques for studying Drosophila development. Development 2003, 130:5065-5072.
12. Bossuyt W., De Geest N., Aerts S., Leenaerts I., Marynen P., Hassan B.A. The atonal proneural transcription factor links differentiation and tumor formation in Drosophila. PLoS Biol. 2009, 7(2):e40.
13. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
14. Brown N.L., Sattler C.A., Markey D.R., Carroll S.B. Hairy gene function in the Drosophila eye: normal expression is dispensable but ectopic expression alters cell fates. Development 1991, 113:1245-1256.
15. Buescher M., Svendsen P.C., Tio M., Miskolczi-McCallum C., Tear G., Brook W.J., Chia W. Drosophila T box proteins break the symmetry of hedgehog-dependent activation of wingless. Curr. Bio. 2004, 14:1694-1702.
16. Buescher M., Tio M., Tear G., Overton P.M., Brook W.J., Chia W. Functions of the segment polarity genes midline and H15 in Drosophila melanogaster neurogenesis. Dev. Biol. 2006, 292:418-429.
17. Cadigan K.M., Nusse R. Wingless signaling in the Drosophila eye and embryonic epidermis. Development 1996, 122:2801-2812.
18. Cadigan K.M., Jou A.D., Nusse R. Wingless blocks bristle formation and morphogenetic furrow progression in the eye through repression of Daughterless. Development 2002, 129:3393-3402.
19. Cagan R.L., Ready D.F. Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev. 1989, 3:1099-1112.
20. Cagan R.L., Ready D.F. The emergence of order in the Drosophila pupal retina. Dev. Biol. 1989, 136:346-362.
21. Cagan R.L., Kramer H., Hart A.C., Zipursky S.L. The bride of sevenless and sevenless interaction: internalization of a transmembrane ligand. Cell 1992, 69:393-399.
22. Carlson H., Ota S., Song Y., Chen Y., Hurlin P.J. Tbx3 impinges on the p53 pathway to suppress apoptosis, facilitate cell transformation and block myogenic differentiation. Oncogene 2002, 21:3827-3835.
23. Carroll S.B., Whyte J.S. The role of the hairy gene during Drosophila morphogenesis: stripes in imaginal discs. Development 1989, 3:905-916.
24. Chandrasekaran V., Beckendorf S.K. Senseless is necessary for survival of embryonic salivary glands in Drosophila. Development 2003, 130:4719-4728.
25. Chen P., Nordstrom W., Gish B., Abrams J.M. Grim, a novel cell death gene in Drosophila. Genes Dev. 1996, 10:1773-1782.
26. Copeland J.M., Bosdet I., Freeman J.D., Guo M., Gorski S.M., Hay B.A. Echinus, required for interommatidial cell sorting and cell death in the Drosophila pupal retina, encodes a protein with homology to ubiquitin-specific proteases. BMC Dev. Bio. 2007, 7:82.
27. Cubas P., de Celis J.F., Campuzano S., Modolell J. Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila wing imaginal disc. Genes Dev. 1991, 5:996-1008.
28. Cutforth T., Gaul U. The genetics of visual system development in Drosophila: specification, connectivity and asymmetry. Curr. Opin. Neurobiol. 1997, 7:48-54.
29. DeStrooper B., Annaert W., Cupers P., Saftig P., Craessaerts K., Mumm J.S., Schroeter E.H., Schrijvers V., Wolfe M.S., Ray W.J., Goate A., Kopan R. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 1999, 398:518-522.
30. Dichtel-Danjoy M.L., Ma D., Dourlen P., Chatelain G., Napoletano F., Robin M., Corbet M., Levet C., Hafsi H., Hainaut P., Ryoo H.D., Bourdon J.C., Mollereau B. Drosophila p53 isoforms differentially regulate apoptosis and apoptosis-induced proliferation. Cell Death Differ. 2013, 20:108-116.
31. Diederich R.J., Matsuno K., Hing H., Artavanis-Tsakonas S. Cytosolic interaction between deltex and Notch ankyrin repeats implicates deltex in the Notch signaling pathway. Development 1994, 120:473-481.
32. Dokucu M.E., Zipursky S.L., Cagan R.L. Atonal, Rough and the resolution of proneural clusters in the developing Drosophila retina. Development 1996, 122:4139-4147.
33. Doroquez D.B., Rebay I. Signal integration during development: mechanisms of EGFR and Notch pathway function and cross-talk. Crit. Rev. Biochem. Mol. Biol. 2006, 41:339-385.
34. Ellis H.M., Spann D.R., Posakony J.W. Extramacrochaetae, a negative regulator of sensory organ development in Drosophila defines a new class of helix-loop-helix proteins. Cell 1990, 61:27-38.
35. Ellis M.C., O'Neill E.M., Rubin G.M. Expression of Drosophila glass protein and evidence for negative regulation of its activity in non-neuronal cells by another DNA-binding protein. Development 1993, 119:855-865.
36. Fehon R.G., Kooh P.J., Rebay I., Artavanis-Tsakonas S. Complex cellular and subcellular regulation of Notch expression during embryonic and imaginal development of Drosophila: Implications for Notch function. J. Cell Biol. 1991, 113:657-669.
37. Frankfort B.J., Mardon G. R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 2002, 129:1295-1306.
38. Frankfort B.J., Pepple K.L., Mamlouk M., Rose M.F., Mardon G. Senseless is required for pupal retinal development in Drosophila. Genesis 2004, 38:182-194.
39. Freeman M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 1996, 87:651-660.
40. Freeman M. Cell determination strategies in the Drosophila eye. Development 1997, 124:261-270.
41. Garrell J., Modolell J. The Drosophila extra-macro-chaetae locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein. Cell 1990, 61:39-48.
42. Go M.J., Eastman D.S., Artavanis-Tsakonas S. Cell proliferation control by Notch signaling in Drosophila development. Development 1998, 125:2031-2040.
43. Grether M.E., Abrams J.M., Agapite J., White K., Stellar H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 1995, 9:1694-1708.
44. Guo M., Jan L.Y., Jan Y.N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 1996, 17:27-41.
45. Hagedorn E.J., Bayraktor J.L., Kandachar V.R., Bai T., Englert D.M., Chang H.C. Drosophila melanogaster auxin regulates the internalization of Delta to control activity of the Notch signaling pathway. J. Cell Bio. 2006, 173:443-452.
46. Hay B.A., Wolff T., Rubin G.M. Expression of Baculovirus P35 prevents cell death in Drosophila. Development 1994, 120:2121-2129.
47. Heberlein U., Wolff T., Rubin G.M. The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 1993, 75:913-926.
48. Jafar-Nejad H., Acar M., Nolo R., Lacin H., Pan H., Parkhurst S.M., Bellon H.J. Senseless acts as a binary switch during sensory organ precursor selection. Genes Dev. 2003, 17:2966-2978.
49. Jahangiri L., Nelson A.C., Wardle F.C. A cis-regulatory module upstream of deltaC regulated by Ntla and Tbx16 drives expression in the tailbud, presomitic mesoderm and somites. Dev. Biol. 2012, 371:110-120.
50. Jarman A.P., Grau Y., Jan L.Y., Jan Y.N. atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 1993, 73:1307-1321.
51. Jarman A.P., Grell E.H., Acherman L., Jan L.Y., Jan Y.N. Atonal is the proneural gene for Drosophila photoreceptors. Nature 1994, 369:398-400.
52. Jarman A.P., Sun Y., Jan L.Y., Jan Y.N. Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 1995, 121:2019-2030.
53. Jones B.W., Fetter R.D., Tear G., Goodman C.S. Glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 1995, 82:1013-1023.
54. Koto A., Kuranaga E., Miura M. Apoptosis ensures spacing pattern formation of Drosophila sensory organs. Curr. Biol. 2011, 21:2780287.
55. Kraus F., Haenig B., Kispert A. Cloning and expression analysis of the mouse T-box gene Tbx20. Mech. Dev. 2001, 100:87-91.
56. Kumar J.P. Building an ommatidium one cell at a time. Dev. Dyn. 2012, 241:136-149.
57. LaCount D.J., Hanson S.F., Schneider C.L., Friesen P.D. Caspase inhibitor P35 and inhibitor of apoptosis Op-IAP block in vivo proteolytic activation of an effector caspase at different steps. J. Biol. Chem. 2000, 275:15657-15664.
58. Lai E.C., Orgogozo V. A hidden program in Drosophila peripheral neurogenesis revealed: fundamental principles underlying sensory organ diversity. Dev. Biol. 2004, 269:1-17.
59. Leal S.M., Qian L., Lacin H., Bodmer R., Skeath J.B. Neuromancer1 and Neuromancer2 Regulate Cell Fate Specification in the Developing Embryonic CNS of Drosophila melanogaster. Dev. Biol. 2009, 325:138-150.
60. Lebestky T., Chang T., Hartenstein V., Banerjee U. Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 2000, 288:146-149.
61. Lee E., Hu X., Yu S., Baker N.E. The secreted glycoprotein scabrous regulates proneural development in the Drosophila eye. Mol. Cell. Biol. 1996, 16:1179-1188.
62. Li W.-Z., Li S.-L., Zheng H.Y., Zhang S.-P., Xue L. A broad expression profile of the GMR-Gal4 driver in Drosophila melanogaster. Genet. Mol. Res. 2012, 11:1997-2002.
63. Ligoxygakis P., Yu S.Y., Delidakis C., Baker N.E. A subset of notch functions during Drosophila eye development require Su(H) and the E(spl) gene complex. Development 1998, 125:2893-2900.
64. Lovicu F.J., McAvoy J.W., de longh R.U. Understanding the role of growth factors in embryonic development: insights from the lens. Philos. Trans. R. Soc. Lond. B 2011, 366:1204-1218.
65. Lyman D.F., Yedvobnick B. Drosophila Notch receptor activity suppresses Hairless function during adult external sensory organ development. Genetics 1995, 141:1491-1505.
66. Meins M., Henderson D.J., Bhattacharya S.S., Sowden J.C. Characterization of the human TBX20 gene, a new member of the T-box gene family closely related to the Drosophila H15 gene. Genomics 2000, 67:317-332.
67. Melicharek D., Shah A., DiStefano G., Gangemi A.J., Orapallo A., Vrailas-Mortimer A.D., Marenda D.A. Identification of novel regulators of atonal expression in the developing Drosophila retina. Genetics 2008, 180:2095-2110.
68. Mesquita D., Dekanty A., Milan M. A dp53-dependent mechanism involved in corrdinating tissue growth in Drosophila. PLoS Biol. 2010, 8:e10000566.
69. Miller D.T., Cagan R.L. Local induction of patterning and programmed cell death in the developing Drosophila retina. Development 1998, 125:2327-2335.
70. Mok L.P., Qin T., Bardot B., LeComte M., Homayouni A., Ahimou F., Wesley C. Delta activity independent of its activity as a ligand of Notch. BMC Dev. Biol. 2005, 5:6.
71. Mollereau B., Domingos P.M. Photoreceptor differentiation in Drosophila: from immature neurons to functional receptors. Dev. Dyn. 2005, 232:585-592.
72. Moses K., Ellis M.C., Rubin G.M. The glass gene encoded a zinc-finger protein required by Drosophila photoreceptor cells. Nature 1989, 340:531-536.
73. Muller D., Kugler S.J., Preiss A., Maier D., Nagel A.C. Genetic modifier screens on Hairless gain-of-function phenotypes reveal genes involved in cell differentiation, cell growth and apoptosis in Drosophila melanogaster. Genetics 2005, 171:1137-1152.
74. Muskavitch M.A. Delta-notch signaling and Drosophila cell fate choice. Dev. Biol. 1994, 166:415-430.
75. Nagaraj R., Banerjee U. Combinatorial signaling in the specification of primary pigment cells in the Drosophila eye. Development 2007, 134:825-831.
76. Nakao K., Campos-Ortega J.A. Persistent expression of genes of the enhancer of split complex suppresses neural development in Drosophila. Neuron 1996, 16:272-286.
77. Nolo R., Abbott L.A., Bellon H.J. Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 2000, 102:349-362.
78. Oda H., Uemura T., Harada Y., Iwai Y., Takeichi M. A Drosophila homolog of Cadherin associated with Armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 1994, 165:716-726.
79. Ohsako S., Hyer J., Panganiban G., Oliver I., Caudy M. Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev. 1994, 8:2743-2755.
80. Panin V.M., Papayannopoulos V., Wilson R., Irvine K.D. Fringe modulates Notch-ligand interactions. Nature 1997, 387:908-912.
81. Parks A.L., Turner F.R., Muskavitch M.A.T. Relationships between complex Delta expression and the specification of retinal cell fates during Drosophila eye development. Mech. Dev. 1995, 50:201-216.
82. Parody T.R., Muskavitch M.A. The pleiotropic function of Delta during postembryonic development of Drosophila melanogaster. Genetics 1993, 135:527-539.
83. Pennimpede T., Proske J., Konig A., Vidigal J.A., Morkel M., Bramsen J.B., Herrmann B.G., Wittler L. In vivo knockdown of Brachyury results in skeletal defects and urorectal malformations resembling caudal regression syndrome. Dev Biol. 2012, 372:55-67.
84. Pepple K.L., Atkins M., Venken K., Wellnitz K., Harding M., Franfort B., Mardon G. Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate. Development 2008, 135:4071-4079.
85. Pickup A.T., Lamka M.L., Sun Q., Yip M.L.R., Lipshitz H.D. Control of photoreceptor cell morphology, planar polarity and epithelial integrity during Drosophila eye development. Development 2002, 129:2247-2258.
86. Qi H., Rand M.D., Wu X., Sestan N., Wang W., Rakic P., Xu T., Artavanis-Tsakonas S. Processing of the notch ligand delta by the metalloprotease Kuzbanian. Science 1999, 283:91-94.
87. Qian L., Liu J., Bodmer R. Neuromancer TBX20-related genes (H15/midline) promote cell fate specification and morphogenesis of the Drosophila heart. Dev. Biol. 2005, 279:509-524.
88. Ready D.F., Hanson T.E., Benzer S. Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 1976, 53:217-240.
89. Rebeiz M., Miller S.W., Posakony J.W. Notch regulates numb: integration of conditional and autonomous cell fate specification. Development 2011, 138:215-225.
90. Riggleman B., Schedl P., Wieschaus E. Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell 1990, 63:549-560.
91. Robinow S., White K. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 1991, 22:443-461.
92. Rutkowski R., Hofmann K., Gartner A. Phylogeny and function of the invertebrate p53 superfamily. Cold Spring Harb. Perspect. Biol. 2010, 2:a001131. Epub.
93. Schroeter E.H., Kisslinger J.A., Kopan R. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 1998, 393:382-386.
94. Shiga Y., Tanaka-Matakatsu M., Hayashi S. A nuclear GFP/beta-galactosidase fusion protein as a marker of morphogenesis in living Drosophila. Dev. Growth Differ. 1996, 38:99-106.
95. Silver R.J., Rebay I. Signaling circuitries in development: insights from the retinal determination network. Development 2005, 132:3-13.
96. Skeath J.B., Carroll S.B. Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 1991, 5:984-995.
97. Skeath J.B., Doe C.Q. Sanpodo and Notch act in opposition to Numb to distinguish sibling fates in the Drosophila CNS. Development 1998, 125:1857-1865.
98. Smith J.E., Cronmiller C. The Drosophila daughterless gene autoregulates and is controlled by both negative and positive gene regulation. Development 2001, 128:4705-4714.
99. Svendsen P.C., Formaz-Preston A., Leal S.M., Brook W.J. The Tbx20 homologs midline and H15 specify ventral fate in the Drosophila melanogaster leg. Development 2009, 136:2689-2693.
100. Tomlinson A., Ready D.F. Cell fate in the Drosophila ommatidium. Dev. Biol. 1987, 123:264-275.
101. Tripathi B.J., Tripathi R.C., Livingston A.M., Borisuth N.S. The role of growth factors in the embryogenesis and differentiation of the eye. Am. J. Anat. 1991, 192:442-471.
102. Tsachaki M., Sprecher S.G. Genetic and developmental mechanisms underlying the formation of the Drosophila compound eye. Dev. Dyn. 2012, 241:40-56.
103. van Doren M., Ellis H.M., Posakony J.W. The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. Development 1994, 113:245-255.
104. Vuong L., Conley S.M., Al-Ubaidi M.R. Expression and role of p53 in the retina. Invest. Ophthalmol. Vis. Sci. 2012, 53:1362-1371.
105. Waddington C.H., Perry M.M. The ultrastructure of the developing eye of Drosophila. Proc. R. Soc. Biol. Sci. 1960, 153:155-178.
106. Walther R.F., Pichaud F. Immunofluorescent staining and imaging of the pupal and adult Drosophila visual system. Nat. Protoc. 2006, 1:2635-2642.
107. White K., Grether M.E., Abrams J.M., Young L., Farrell K., Steller H. Genetic control of programmed cell death in Drosophila. Science 1994, 264:677-683.
108. Wigglesworth V.B. The origin of the sensory neurons in an insect, Rhodnius prolixus (Hemiptera). Q. J. Microsc. Sci. 1953, 94:93-112.
109. Wolff T., Ready D.F. The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 1991, 113:841-850.
110. Wolff T., Ready D.F. Cell death in normal and rough eye mutants of Drosophila. Development 1991, 113:825-839.
111. Xu T., Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 1993, 117:1223-1237.
112. Yamaguchi M., Hirose F., Inoue Y.H., Shiraki M., Hayashi Y., Nishi Y., Matsukage A. Ectopic expression of human p53 inhibits entry into S phase and induces apoptosis in the Drosophila eye imaginal disc. Oncogene 1999, 18:6767-6775.
113. Yao K.M., Samson M.L., Reeves R., White K. Gene elav of Drosophila melanogaster: a prototype for neuronal-specific RNA binding protein gene family that is conserved in flies and humans. J. Neurobiol. 1993, 24:723-739.
114. Ye Y., Fortini M.E. Apoptotic activities of wild-type and Alzheimer's disease-related mutant presenilins in Drosophila melanogaster. J. Cell Biol. 1999, 146:1351-1364.
115. Younger-Shepherd S., Vaessin H., Bier E., Jan L.Y., Jan Y.N. Deadpan, an essential pan-neural gene encoding an HLH protein, acts as a denominator in Drosophila sex determination. Cell 1992, 70:911-922.
116. Yu S.Y., Yoo S.J., Yang L., Zapata C., Srinivasan A., Hay B.A. A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 2002, 129:3269-3278.