Advertisement

Cell Morphogenesis: Tracing the Paths of Induction During Drosophila Ommatidial Development

  • Jennifer CurtissEmail author
Chapter

Abstract

The study of the Drosophila melanogaster eye began in earnest in the late 1980s and continues to this day. Hundreds of fine papers have been published along the way. Thus, some may ask why it is important to continue to study the Drosophila eye. After all, what can possibly be left to discover that would lead to substantial advances in the field of Developmental Biology? One answer, as has been pointed out numerous times before, is that the Drosophila eye is a remarkable system for studying the role of induction in cell fate specification. And, in spite of the attention shown to it in the past, there are substantial gaps in our knowledge of how even this relatively simple system develops. Filling these gaps promises to unlock mysteries that no one yet suspects exist, which will lead to discoveries no one can yet fathom.

Keywords

Notch Signaling Lateral Inhibition Pigment Cell Epidermal Growth Factor Receptor Signaling Cone Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Artavanis-Tsakonas S, Muskavitch MA (2010) Notch: the past, the present, and the future. Curr Top Dev Biol 92:1–29PubMedGoogle Scholar
  2. Axelson H (2004) Notch signaling and cancer: emerging complexity. Semin Cancer Biol 14:317–319PubMedGoogle Scholar
  3. Baker NE (2000) Notch signaling in the nervous system Pieces still missing from the puzzle. Bioessays 22:264–273PubMedGoogle Scholar
  4. Baker NE (2002) Notch and the patterning of ommatidial founder cells in the developing Drosophila eye. In: Moses K (ed) Results and problems in cell differentiation. Springer, Berlin, pp 35–58Google Scholar
  5. Baker NE, Yu SY (1997) Proneural function of neurogenic genes in the developing Drosophila eye. Curr Biol 7:122–132PubMedGoogle Scholar
  6. Baker NE, Zitron AE (1995) Drosophila eye development: Notch and Delta amplify a neurogenic pattern conferred on the morphogenetic furrow by scabrous. Mech Dev 49:173–189PubMedGoogle Scholar
  7. Baker NE, Yu S, Han D (1996) Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye. Curr Biol 6:1290–1301PubMedGoogle Scholar
  8. Bang AG, Kintner C (2000) Rhomboid and Star facilitate presentation and processing of the Drosophila TGF-alpha homolog Spitz. Genes Dev 14:177–186PubMedGoogle Scholar
  9. Bao S (2010) Two themes on the assembly of the Drosophila eye. Curr Top Dev Biol 93:85–127PubMedGoogle Scholar
  10. Bao S, Cagan R (2005) Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell 8:925–935PubMedGoogle Scholar
  11. Bao S, Fischbach KF, Corbin V, Cagan RL (2010) Preferential adhesion maintains separation of ommatidia in the Drosophila eye. Dev Biol 344:948–956PubMedGoogle Scholar
  12. Baonza A, Casci T, Freeman M (2001) A primary role for the epidermal growth factor receptor in ommatidial spacing in the Drosophila eye. Curr Biol 11:396–404PubMedGoogle Scholar
  13. Baonza A, Freeman M (2001) Notch signaling and the initiation of neural development in the Drosophila eye. Development 128:3889–3898PubMedGoogle Scholar
  14. Basler K, Christen B, Hafen E (1991) Ligand-independent activation of the sevenless receptor tyrosine kinase changes the fate of cells in the developing Drosophila eye. Cell 64:1069–1081PubMedGoogle Scholar
  15. Basler K, Hafen E (1988) Sevenless and Drosophila eye development: a tyrosine kinase controls cell fate. Trends Genet 4:74–79PubMedGoogle Scholar
  16. Basler K, Yen D, Tomlinson A, Hafen E (1990) Reprogramming cell fate in the developing Drosophila retina: transformation of R7 cells by ectopic expression of rough. Genes Dev 4:728–739PubMedGoogle Scholar
  17. Batterham P, Crew JR, Sokac AM, Andrews JR, Pasquini GM, Davies AG, Stocker RF, Pollock JA (1996) Genetic analysis of the lozenge gene complex in Drosophila melanogaster: adult visual system phenotypes. J Neurogenet 10:193–220PubMedGoogle Scholar
  18. Behan KJ, Nichols CD, Cheung TL, Farlow A, Hogan BM, Batterham P, Pollock JA (2002) Yan regulates Lozenge during Drosophila eye development. Dev Genes Evol 212:267–276PubMedGoogle Scholar
  19. Bergmann A, Agapite J, McCall K, Steller H (1998) The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95:331–341PubMedGoogle Scholar
  20. Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517–530PubMedGoogle Scholar
  21. Bessa J, Gebelein B, Pichaud F, Casares F, Mann RS (2002) Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes Dev 16:2415–2427PubMedGoogle Scholar
  22. Bhattacharya A, Baker NE (2009) The HLH protein Extramacrochaetae is required for R7 cell and cone cell fates in the Drosophila eye. Dev Biol 327:288–300PubMedGoogle Scholar
  23. Bhattacharya A, Baker NE (2011) A network of broadly expressed HLH genes regulates tissue-specific cell fates. Cell 147:881–892PubMedGoogle Scholar
  24. Bhattacharya A, Baker NE (2012) The role of the bHLH protein hairy in morphogenetic furrow progression in the developing Drosophila eye. PLoS One 7:e47503PubMedGoogle Scholar
  25. Biggs WH, Zavitz KH, Dickson B, van der Straten A, Brunner D, Hafen E, Zipursky SL (1994) The Drosophila rolled locus encodes a MAP kinase required in the sevenless signal transduction pathway. EMBO J 13:1628–1635PubMedGoogle Scholar
  26. Bonini NM, Leiserson WM, Benzer S (1993) The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72:379–395PubMedGoogle Scholar
  27. Borod ER, Heberlein U (1998) Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina. Dev Biol 197:187–197PubMedGoogle Scholar
  28. Boulton SJ, Brook A, Staehling-Hampton K, Heitzler P, Dyson N (2000) A role for Ebi in neuronal cell cycle control. EMBO J 19:5376–5386PubMedGoogle Scholar
  29. Bowtell DD, Simon MA, Rubin GM (1988) Nucleotide sequence and structure of the sevenless gene of Drosophila melanogaster. Genes Dev 2:620–634PubMedGoogle Scholar
  30. Bray SJ (2006) Notch signaling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7:678–689PubMedGoogle Scholar
  31. Brown KE, Baonza A, Freeman M (2006) Epithelial cell adhesion in the developing Drosophila retina is regulated by Atonal and the EGF receptor pathway. Dev Biol 300:710–721PubMedGoogle Scholar
  32. Brown KE, Kerr M, Freeman M (2007) The EGFR ligands Spitz and Keren act cooperatively in the Drosophila eye. Dev Biol 307:105–113PubMedGoogle Scholar
  33. Brown NL, Sattler CA, Paddock SW, Carroll SB (1995) Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell 80:879–887PubMedGoogle Scholar
  34. Brown NL, Paddock SW, Sattler CA, Cronmiller C, Thomas BJ, Carroll SB (1996) Daughterless is required for Drosophila photoreceptor cell determination, eye morphogenesis, and cell cycle progression. Dev Biol 179:65–78PubMedGoogle Scholar
  35. Brunner D, Dücker K, Oellers N, Hafen E, Scholz H, Klämbt C (1994a) The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature 370:386–389Google Scholar
  36. Brunner D, Oellers N, Szabad J, Biggs WH, Zipursky SL, Hafen E (1994b) A gain-of-function mutation in Drosophila MAP kinase activates multiple receptor tyrosine kinase signaling pathways. Cell 76:875–888Google Scholar
  37. Cagan RL, Ready DF (1989a) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3:1099–1112Google Scholar
  38. Cagan RL, Ready DF (1989b) The emergence of order in the Drosophila pupal retina. Dev Biol 136:346–362Google Scholar
  39. Campuzano S (2001) Emc, a negative HLH regulator with multiple functions in Drosophila development. Oncogene 20:8299–8307PubMedGoogle Scholar
  40. Carthew RW (2007) Pattern formation in the Drosophila eye. Curr Opin Genet Dev 17:309–313PubMedGoogle Scholar
  41. Chang HC, Solomon NM, Wassarman DA, Karim FD, Therrien M, Rubin GM, Wolff T (1995) Phyllopod functions in the fate determination of a subset of photoreceptors in Drosophila. Cell 80:463–472PubMedGoogle Scholar
  42. Charlton-Perkins M, Cook TA (2010) Building a fly eye: terminal differentiation events of the retina, corneal lens, and pigmented epithelia. Curr Top Dev Biol 93:129–173PubMedGoogle Scholar
  43. Charlton-Perkins M, Whitaker SL, Fei Y, Xie B, Li-Kroeger D, Gebelein B, Cook T (2011) Prospero and Pax2 combinatorially control neural cell fate decisions by modulating Ras- and Notch-dependent signaling. Neural Dev 6:20PubMedGoogle Scholar
  44. Chen CK, Chien CT (1999) Negative regulation of atonal in proneural cluster formation of Drosophila R8 photoreceptors. Proc Natl Acad Sci U S A 96:5055–5060PubMedGoogle Scholar
  45. Cheyette BN, Green PJ, Martin K, Garren H, Hartenstein V, Zipursky SL (1994) The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12:977–996PubMedGoogle Scholar
  46. Cook T, Pichaud F, Sonneville R, Papatsenko D, Desplan C (2003) Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev Cell 4:853–864PubMedGoogle Scholar
  47. Cooper MT, Bray SJ (1999) Frizzled regulation of Notch signaling polarizes cell fate in the Drosophila eye. Nature 397:526–530PubMedGoogle Scholar
  48. Cooper MT, Bray SJ (2000) R7 photoreceptor specification requires Notch activity. Curr Biol 10:1507–1510PubMedGoogle Scholar
  49. Coyle-Thompson CA, Banerjee U (1993) The strawberry notch gene functions with Notch in common developmental pathways. Development 119:377–395PubMedGoogle Scholar
  50. Crew JR, Batterham P, Pollock JA (1997) Developing compound eye in lozenge mutants of Drosophila: lozenge expression in the R7 equivalence group. Dev Genes Evol 206:481–493Google Scholar
  51. Cubas P, Celis JF de, Campuzano S, Modolell J (1991) Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev 5:996–1008PubMedGoogle Scholar
  52. Cubas P, Modolell J (1992) The extramacrochaetae gene provides information for sensory organ patterning. EMBO J 11:3385–3393PubMedGoogle Scholar
  53. Culí J, Modolell J (1998) Proneural gene self-stimulation in neural precursors: an essential mechanism for sense organ development that is regulated by Notch signaling. Genes Dev 12:2036–2047PubMedGoogle Scholar
  54. Curtiss J, Mlodzik M (2000) Morphogenetic furrow initiation and progression during eye development in Drosophila: the roles of decapentaplegic, hedgehog and eyes absent. Development 127:1325–1336PubMedGoogle Scholar
  55. Daga A, Karlovich CA, Dumstrei K, Banerjee U (1996) Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1. Genes Dev 10:1194–1205PubMedGoogle Scholar
  56. del Alamo D, Mlodzik M (2006) Frizzled/PCP-dependent asymmetric neuralized expression determines R3/R4 fates in the Drosophila eye. Dev Cell 11:887–894PubMedGoogle Scholar
  57. del Alamo D, Mlodzik M (2008) Self-modulation of Notch signaling during ommatidial development via the Roughened eye transcriptional repressor. Development 135:2895–2904PubMedGoogle Scholar
  58. Dickson B, Sprenger F, Hafen E (1992a) Prepattern in the developing Drosophila eye revealed by an activated torso–sevenless chimeric receptor. Genes Dev 6:2327–2339Google Scholar
  59. Dickson B, Sprenger F, Morrison D, Hafen E (1992b) Raf functions downstream of Ras1 in the Sevenless signal transduction pathway. Nature 360:600–603Google Scholar
  60. Dickson BJ, Domínguez M, van der Straten A, Hafen E (1995) Control of Drosophila photoreceptor cell fates by phyllopod, a novel nuclear protein acting downstream of the Raf kinase. Cell 80:453–462PubMedGoogle Scholar
  61. Distefano GM, Gangemi AJ, Khandelwal PJ, Saunders AJ, Marenda DR (2012) Drosophila lilliputian is required for proneural gene expression in retinal development. Dev Dyn 241:553–562PubMedGoogle Scholar
  62. Dokucu ME, Zipursky SL, Cagan RL (1996) Atonal, rough and the resolution of proneural clusters in the developing Drosophila retina. Development 122:4139–4147PubMedGoogle Scholar
  63. Domingos PM, Brown S, Barrio R, Ratnakumar K, Frankfort BJ, Mardon G, Steller H, Mollereau B (2004a) Regulation of R7 and R8 differentiation by the spalt genes. Dev Biol 273:121–133Google Scholar
  64. Domingos PM, Mlodzik M, Mendes CS, Brown S, Steller H, Mollereau B (2004b) Spalt transcription factors are required for R3/R4 specification and establishment of planar cell polarity in the Drosophila eye. Development 131:5695–5702Google Scholar
  65. Domínguez M (1999) Dual role for Hedgehog in the regulation of the proneural gene atonal during ommatidia development. Development 126:2345–2353PubMedGoogle Scholar
  66. Domínguez M, Hafen E (1997) Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev 11:3254–3264PubMedGoogle Scholar
  67. Domínguez M, Wasserman JD, Freeman M (1998) Multiple functions of the EGF receptor in Drosophila eye development. Curr Biol 8:1039–1048PubMedGoogle Scholar
  68. Dong X, Tsuda L, Zavitz KH, Lin M, Li S, Carthew RW, Zipursky SL (1999) ebi regulates epidermal growth factor receptor signaling pathways in Drosophila. Genes Dev 13:954–965PubMedGoogle Scholar
  69. Doroquez DB, Orr-Weaver TL, Rebay I (2007) Split ends antagonizes the Notch and potentiates the EGFR signaling pathways during Drosophila eye development. Mech Dev 124:792–806PubMedGoogle Scholar
  70. Doroquez DB, Rebay I (2006) Signal integration during development: mechanisms of EGFR and Notch pathway function and cross-talk. Crit Rev Biochem Mol Biol 41:339–385PubMedGoogle Scholar
  71. Ellis HM, Spann DR, Posakony JW (1990) Extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins. Cell 61:27–38PubMedGoogle Scholar
  72. Fanto M, Mayes CA, Mlodzik M (1998) Linking cell-fate specification to planar polarity: determination of the R3/R4 photoreceptors is a prerequisite for the interpretation of the Frizzled mediated polarity signal. Mech Dev 74:51–58PubMedGoogle Scholar
  73. Fanto M, Mlodzik M (1999) Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397:523–526PubMedGoogle Scholar
  74. Fehon RG, Johansen K, Rebay I, Artavanis-Tsakonas S (1991) Complex cellular and subcellular regulation of notch expression during embryonic and imaginal development of Drosophila: implications for notch function. J Cell Biol 113:657–669PubMedGoogle Scholar
  75. Firth LC, Baker NE (2009) Retinal determination genes as targets and possible effectors of extracellular signals. Dev Biol 327:366–375PubMedGoogle Scholar
  76. Flores GV, Daga A, Kalhor HR, 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 125:3681–3687PubMedGoogle Scholar
  77. Flores GV, Duan H, Yan H, Nagaraj R, Fu W, Zou Y, Noll M, Banerjee U (2000) Combinatorial signaling in the specification of unique cell fates. Cell 103:75–85PubMedGoogle Scholar
  78. Fortini ME (2009) Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 16:633–647PubMedGoogle Scholar
  79. Fortini ME, Simon MA, Rubin GM (1992) Signaling by the sevenless protein tyrosine kinase is mimicked by Ras1 activation. Nature 355:559–561PubMedGoogle Scholar
  80. Frankfort BJ, Mardon G (2002) R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129:1295–1306PubMedGoogle Scholar
  81. Frankfort BJ, Mardon G (2004) Senseless represses nuclear transduction of Egfr pathway activation. Development 131:563–570PubMedGoogle Scholar
  82. Frankfort BJ, Nolo R, Zhang Z, Bellen H, Mardon G (2001) Senseless repression of rough is required for R8 photoreceptor differentiation in the developing Drosophila eye. Neuron 32:403–414PubMedGoogle Scholar
  83. Frankfort BJ, Pepple KL, Mamlouk M, Rose MF, Mardon G (2004) Senseless is required for pupal retinal development in Drosophila. Genesis 38:182–194PubMedGoogle Scholar
  84. Freeman M (1994a) Misexpression of the Drosophila argos gene, a secreted regulator of cell determination. Development 120:2297–2304Google Scholar
  85. Freeman M (1994b) The spitz gene is required for photoreceptor determination in the Drosophila eye where it interacts with the EGF receptor. Mech Dev 48:25–33Google Scholar
  86. Freeman M (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87:651–660PubMedGoogle Scholar
  87. Freeman M (1997) Cell determination strategies in the Drosophila eye. Development 124:261–270PubMedGoogle Scholar
  88. Freeman M (2002) A fly’s eye view of EGF receptor signaling. EMBO J 21:6635–6642PubMedGoogle Scholar
  89. Freeman M, Kimmel BE, Rubin GM (1992a) Identifying targets of the rough homeobox gene of Drosophila: evidence that rhomboid functions in eye development. Development 116:335–346Google Scholar
  90. Freeman M, Klämbt C, Goodman CS, Rubin GM (1992b) The argos gene encodes a diffusible factor that regulates cell fate decisions in the Drosophila eye. Cell 69:963–975Google Scholar
  91. Fu W, Baker NE (2003) Deciphering synergistic and redundant roles of Hedgehog, Decapentaplegic and Delta that drive the wave of differentiation in Drosophila eye development. Development 130:5229–5239PubMedGoogle Scholar
  92. Fu W, Noll M (1997) The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye. Genes Dev 11:2066–2078PubMedGoogle Scholar
  93. Gabay L, Scholz H, Golembo M, Klaes A, Shilo BZ, Klämbt C (1996) EGF receptor signaling induces pointed P1 transcription and inactivates Yan protein in the Drosophila embryonic ventral ectoderm. Development 122:3355–3362PubMedGoogle Scholar
  94. Gabay L, Seger R, Shilo BZ (1997) In situ activation pattern of Drosophila EGF receptor pathway during development. Science 277:1103–1106PubMedGoogle Scholar
  95. Garcàa-Bellido A, de Celis JF (2009) The complex tale of the achaete-scute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics 182:631–639Google Scholar
  96. Garrell J, Modolell J (1990) The Drosophila extramacrochaetae locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein. Cell 61:39–48PubMedGoogle Scholar
  97. Golembo M, Raz E, Shilo BZ (1996a) The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm. Development 122:3363–3370Google Scholar
  98. Golembo M, Schweitzer R, Freeman M, Shilo BZ (1996b) Argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 122:223–230Google Scholar
  99. Goyal L, McCall K, Agapite J, Hartwieg E, Steller H (2000) Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J 19:589–597PubMedGoogle Scholar
  100. Greenblatt DY, Vaccaro AM, Jaskula-Sztul R, Ning L, Haymart M, Kunnimalaiyaan M, Chen H (2007) Valproic acid activates notch-1 signaling and regulates the neuroendocrine phenotype in carcinoid cancer cells. Oncologist 12:942–951PubMedGoogle Scholar
  101. Greenwood S, Struhl G (1999) Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway. Development 126:5795–5808PubMedGoogle Scholar
  102. Grether ME, Abrams JM, Agapite J, White K, Steller H (1995) The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev 9:1694–1708PubMedGoogle Scholar
  103. Guenther MG, Lane WS, Fischle W, Verdin E, Lazar MA, Shiekhattar R (2000) A core SMRT corepressor complex containing HDAC3 and TBL1, a WD40-repeat protein linked to deafness. Genes Dev 14:1048–1057PubMedGoogle Scholar
  104. Guichard A, Biehs B, Sturtevant MA, Wickline L, Chacko J, Howard K, Bier E (1999) rhomboid and Star interact synergistically to promote EGFR/MAPK signaling during Drosophila wing vein development. Development 126:2663–2676PubMedGoogle Scholar
  105. Hafen E, Basler K, Edstroem JE, Rubin GM (1987) Sevenless, a cell-specific homeotic gene of Drosophila, encodes a putative transmembrane receptor with a tyrosine kinase domain. Science 236:55–63PubMedGoogle Scholar
  106. Halder G, Callaerts P, Flister S, Walldorf U, Kloter U, Gehring WJ (1998) Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development 125:2181–2191PubMedGoogle Scholar
  107. Hart AC, Krämer H, Van Vactor DL, Paidhungat M, Zipursky SL (1990) Induction of cell fate in the Drosophila retina: the bride of sevenless protein is predicted to contain a large extracellular domain and seven transmembrane segments. Genes Dev 4:1835–1847PubMedGoogle Scholar
  108. Hayashi T, Kojima T, Saigo K (1998) Specification of primary pigment cell and outer photoreceptor fates by BarH1 homeobox gene in the developing Drosophila eye. Dev Biol 200:131–145PubMedGoogle Scholar
  109. Hayashi T, Xu C, Carthew RW (2008) Cell-type-specific transcription of prospero is controlled by combinatorial signaling in the Drosophila eye. Development 135:2787–2796PubMedGoogle Scholar
  110. Heberlein U, Mlodzik M, Rubin GM (1991) Cell-fate determination in the developing Drosophila eye: role of the rough gene. Development 112:703–712PubMedGoogle Scholar
  111. Heberlein U, Hariharan IK, Rubin GM (1993) Star is required for neuronal differentiation in the Drosophila retina and displays dosage-sensitive interactions with Ras1. Dev Biol 160:51–63PubMedGoogle Scholar
  112. Heberlein U, Singh CM, Luk AY, Donohoe TJ (1995) Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373:709–711PubMedGoogle Scholar
  113. Higashijima S, Kojima T, Michiue T, Ishimaru S, Emori Y, Saigo K (1992a) 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 6:50–60Google Scholar
  114. Higashijima S, Michiue T, Emori Y, Saigo K (1992b) Subtype determination of Drosophila embryonic external sensory organs by redundant homeo box genes BarH1 and BarH2. Genes Dev 6:1005–1018Google Scholar
  115. Hsiung F, Moses K (2002) Retinal development in Drosophila: specifying the first neuron. Hum Mol Genet 11:1207–1214PubMedGoogle Scholar
  116. Jackson Behan K, Fair J, Singh S, Bogwitz M, Perry T, Grubor V, Cunningham F, Nichols CD, Cheung TL, Batterham P, Pollock JA (2005) Alternative splicing removes an Ets interaction domain from Lozenge during Drosophila eye development. Dev Genes Evol 215:423–435PubMedGoogle Scholar
  117. Jarman AP, Grau Y, Jan LY, Jan YN (1993) Atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307–1321PubMedGoogle Scholar
  118. Jarman AP, Grell EH, Ackerman L, Jan LY, Jan YN (1994) Atonal is the proneural gene for Drosophila photoreceptors. Nature 369:398–400PubMedGoogle Scholar
  119. Jarman AP, Sun Y, Jan LY, Jan YN (1995) Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 121:2019–2030PubMedGoogle Scholar
  120. Jemc J, Rebay I (2007) Identification of transcriptional targets of the dual-function transcription factor/phosphatase eyes absent. Dev Biol 310:416–429PubMedGoogle Scholar
  121. Jenny A (2010) Planar cell polarity signaling in the Drosophila eye. Curr Top Dev Biol 93:189–227PubMedGoogle Scholar
  122. Kao HY, Ordentlich P, Koyano-Nakagawa N, Tang Z, Downes M, Kintner CR, Evans RM, Kadesch T (1998) A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev 12:2269–2277PubMedGoogle Scholar
  123. Kauffmann RC, Li S, Gallagher PA, Zhang J, Carthew RW (1996) Ras1 signaling and transcriptional competence in the R7 cell of Drosophila. Genes Dev 10:2167–2178PubMedGoogle Scholar
  124. Kimmel BE, Heberlein U, Rubin GM (1990) The homeo domain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes Dev 4:712–727PubMedGoogle Scholar
  125. Kolodkin AL, Pickup AT, Lin DM, Goodman CS, Banerjee U (1994) Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila. Development 120:1731–1745PubMedGoogle Scholar
  126. Kooh PJ, Fehon RG, Muskavitch MA (1993) Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development 117:493–507PubMedGoogle Scholar
  127. Kopan R, Ilagan MX (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:216–233PubMedGoogle Scholar
  128. Krämer H, Cagan RL, Zipursky SL (1991) Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature 352:207–212PubMedGoogle Scholar
  129. Kumar JP (2009) The molecular circuitry governing retinal determination. Biochim Biophys Acta 1789:306–314PubMedGoogle Scholar
  130. Kumar JP (2010) Retinal determination the beginning of eye development. Curr Top Dev Biol 93:1–28PubMedGoogle Scholar
  131. Kumar JP (2011) My what big eyes you have: how the Drosophila retina grows. Dev Neurobiol 71:1133–1152PubMedGoogle Scholar
  132. Kumar JP (2012) Building an ommatidium one cell at a time. Dev Dyn 241:136–149PubMedGoogle Scholar
  133. Kumar JP, Tio M, Hsiung F, Akopyan S, Gabay L, Seger R, Shilo BZ, Moses K (1998) Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125:3875–3885PubMedGoogle Scholar
  134. Kumar JP, Hsiung F, Powers MA, Moses K (2003) Nuclear translocation of activated MAP kinase is developmentally regulated in the developing Drosophila eye. Development 130:3703–3714PubMedGoogle Scholar
  135. Kurada P, White K (1998) Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95:319–329PubMedGoogle Scholar
  136. Lage P, Jan YN, Jarman AP (1997) Requirement for EGF receptor signaling in neural recruitment during formation of Drosophila chordotonal sense organ clusters. Curr Biol 7:166–175PubMedGoogle Scholar
  137. Lai ZC, Harrison SD, Karim F, Li Y, Rubin GM (1996) Loss of tramtrack gene activity results in ectopic R7 cell formation, even in a sina mutant background. Proc Natl Acad Sci U S A 93:5025–5030PubMedGoogle Scholar
  138. Lai, Z.-C., Fetchko, M, Li,Y (1997) Repression of Drosophila Photoreceptor Cell Fate Through Cooperative Action of Two Transcriptional Repressors Yan and Tramtrack. Genetics 147: 1131–1137PubMedGoogle Scholar
  139. Lai ZC, Li Y (1999) Tramtrack69 is positively and autonomously required for Drosophila photoreceptor development. Genetics 152:299–305PubMedGoogle Scholar
  140. Lai ZC, Rubin GM (1992) Negative control of photoreceptor development in Drosophila by the product of the yan gene, an ETS domain protein. Cell 70:609–620PubMedGoogle Scholar
  141. Lawrence PA, Green SM (1979) Cell lineage in the developing retina of Drosophila. Dev Biol 71:142–152PubMedGoogle Scholar
  142. Lee EC, Hu X, Yu SY, Baker NE (1996) The scabrous gene encodes a secreted glycoprotein dimer and regulates proneural development in Drosophila eyes. Mol Cell Biol 16:1179–1188PubMedGoogle Scholar
  143. Lee JR, Urban S, Garvey CF, Freeman M (2001) Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107:161–171PubMedGoogle Scholar
  144. Leong KG, Karsan A (2006) Recent insights into the role of Notch signaling in tumorigenesis. Blood 107:2223–2233PubMedGoogle Scholar
  145. Lesokhin AM, Yu SY, Katz J, Baker NE (1999) Several levels of EGF receptor signaling during photoreceptor specification in wild-type, Ellipse, and null mutant Drosophila. Dev Biol 205:129–144PubMedGoogle Scholar
  146. Li S, Li Y, Carthew RW, Lai ZC (1997) Photoreceptor cell differentiation requires regulated proteolysis of the transcriptional repressor Tramtrack. Cell 90:469–478PubMedGoogle Scholar
  147. Li J, Wang J, Nawaz Z, Liu JM, Qin J, Wong J (2000) Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. EMBO J 19:4342–4350PubMedGoogle Scholar
  148. Li X, Perissi V, Liu F, Rose DW, Rosenfeld MG (2002) Tissue-specific regulation of retinal and pituitary precursor cell proliferation. Science 297:1180–1183PubMedGoogle Scholar
  149. Li Y, Baker NE (2001) Proneural enhancement by Notch overcomes Suppressor-of-Hairless repressor function in the developing Drosophila eye. Curr Biol 11:330–338PubMedGoogle Scholar
  150. Ligoxygakis P, Yu SY, Delidakis C, Baker NE (1998) A subset of notch functions during Drosophila eye development require Su(H) and the E(spl) gene complex. Development 125:2893–2900PubMedGoogle Scholar
  151. Lim J, Choi KW (2003) Bar homeodomain proteins are anti-proneural in the Drosophila eye: transcriptional repression of atonal by Bar prevents ectopic retinal neurogenesis. Development 130:5965–5974PubMedGoogle Scholar
  152. Lim J, Choi KW (2004) Induction and autoregulation of the anti-proneural gene Bar during retinal neurogenesis in Drosophila. Development 131:5573–5580PubMedGoogle Scholar
  153. Lim J, Jafar-Nejad H, Hsu YC, Choi KW (2008) Novel function of the class I bHLH protein Daughterless in the negative regulation of proneural gene expression in the Drosophila eye. EMBO Rep 9:1128–1133PubMedGoogle Scholar
  154. Majumdar A, Nagaraj R, Banerjee U (1997) Strawberry notch encodes a conserved nuclear protein that functions downstream of Notch and regulates gene expression along the developing wing margin of Drosophila. Genes Dev 11:1341–1353PubMedGoogle Scholar
  155. Mankidy R, Hastings J, Thackeray JR (2003) Distinct phospholipase C-gamma-dependent signaling pathways in the Drosophila eye and wing are revealed by a new small wing allele. Genetics 164:553–563PubMedGoogle Scholar
  156. Marygold SJ, Walker C, Orme M, Leevers S (2011) Genetic characterization of ebi reveals its critical role in Drosophila wing growth Fly (Austin) 5Google Scholar
  157. Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20:429–440PubMedGoogle Scholar
  158. Mavromatakis YE, Tomlinson A (2012a) Stop and go: antagonistic signals in the specification of the Drosophila R7 photoreceptor viewed from an evolutionary perspective Fly (Austin) 6Google Scholar
  159. Mavromatakis YE, Tomlinson A (2012b) The role of the small GTPase Rap in Drosophila R7 photoreceptor specification. Proc Natl Acad Sci U S A 109:3844–3849Google Scholar
  160. Meier P, Silke J, Leevers SJ, Evan GI (2000) The Drosophila caspase DRONC is regulated by DIAP1. EMBO J 19:598–611PubMedGoogle Scholar
  161. Melicharek D, Shah A, DiStefano G, Gangemi AJ, Orapallo A, Vrailas-Mortimer AD, Marenda DR (2008) Identification of novel regulators of atonal expression in the developing Drosophila retina. Genetics 180:2095–2110PubMedGoogle Scholar
  162. Miller AC, Seymour H, King C, Herman TG (2008) Loss of seven-up from Drosophila R1/R6 photoreceptors reveals a stochastic fate choice that is normally biased by Notch. Development 135:707–715PubMedGoogle Scholar
  163. Miller AC, Lyons EL, Herman TG (2009) cis-Inhibition of Notch by endogenous Delta biases the outcome of lateral inhibition. Curr Biol 19:1378–1383PubMedGoogle Scholar
  164. Miller DT, Cagan RL (1998) Local induction of patterning and programmed cell death in the developing Drosophila retina. Development 125:2327–2335PubMedGoogle Scholar
  165. Mlodzik M, Hiromi Y, Weber U, Goodman CS, Rubin GM (1990) The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60:211–224PubMedGoogle Scholar
  166. Morante J, Desplan C, Celik A (2007) Generating patterned arrays of photoreceptors. Curr Opin Genet Dev 17:314–319PubMedGoogle Scholar
  167. Morey M, Yee SK, Herman T, Nern A, Blanco E, Zipursky SL (2008) Coordinate control of synaptic-layer specificity and rhodopsins in photoreceptor neurons. Nature 456:795–799PubMedGoogle Scholar
  168. Morillo SA, Braid LR, Verheyen EM, Rebay I (2012) Nemo phosphorylates Eyes absent and enhances output from the Eya-Sine oculis transcriptional complex during Drosophila retinal determination. Dev Biol 365:267–276PubMedGoogle Scholar
  169. Moses K, Ellis MC, Rubin GM (1989) The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature 340:531–536PubMedGoogle Scholar
  170. Moses K, Rubin GM (1991) Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev 5:583–593PubMedGoogle Scholar
  171. Nagaraj R, Banerjee U (2007) Combinatorial signaling in the specification of primary pigment cells in the Drosophila eye. Development 134:825–831PubMedGoogle Scholar
  172. Nolo R, Abbott LA, Bellen HJ (2000) Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102:349–362PubMedGoogle Scholar
  173. O’Neill EM, Rebay I, Tjian R, Rubin GM (1994) The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78:137–147PubMedGoogle Scholar
  174. Oberoi J, Fairall L, Watson PJ, Yang JC, Czimmerer Z, Kampmann T, Goult BT, Greenwood JA, Gooch JT, Kallenberger BC, Nagy L, Neuhaus D, Schwabe JW (2011) Structural basis for the assembly of the SMRT/NCoR core transcriptional repression machinery. Nat Struct Mol Biol 18:177–184PubMedGoogle Scholar
  175. Ohsako S, Hyer J, Panganiban G, Oliver I, Caudy M (1994) Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev 8:2743–2755PubMedGoogle Scholar
  176. Okabe M, Okano H (1997) Two-step induction of chordotonal organ precursors in Drosophila embryogenesis. Development 124:1045–1053PubMedGoogle Scholar
  177. Ou JP, Lin HY, Su KY, Yu SL, Tseng IH, Chen CJ, Hsu HC, Chan DC, Sophia Chen YL (2012) Potential therapeutic role of Z-isochaihulactone in lung cancer through induction of apoptosis via Notch signaling. Evid Based Complement Alternat Med 2012:809204PubMedGoogle Scholar
  178. Parks AL, Turner FR, Muskavitch MA (1995) Relationships between complex Delta expression and the specification of retinal cell fates during Drosophila eye development. Mech Dev 50:201–216PubMedGoogle Scholar
  179. Pepple KL, Atkins M, Venken K, Wellnitz K, Harding M, Frankfort B, Mardon G (2008) Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate. Development 135:4071–4079PubMedGoogle Scholar
  180. Perissi V, Aggarwal A, Glass CK, Rose DW, Rosenfeld MG (2004) A corepressor/coactivator exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors. Cell 116:511–526PubMedGoogle Scholar
  181. Perissi V, Scafoglio C, Zhang J, Ohgi KA, Rose DW, Glass CK, Rosenfeld MG (2008) TBL1 and TBLR1 phosphorylation on regulated gene promoters overcomes dual CtBP and NCoR/SMRT transcriptional repression checkpoints. Mol Cell 29:755–766PubMedGoogle Scholar
  182. Perissi V, Jepsen K, Glass CK, Rosenfeld MG (2010) Deconstructing repression: evolving models of co-repressor action. Nat Rev Genet 11:109–123PubMedGoogle Scholar
  183. Pickup AT, Banerjee U (1999) The role of star in the production of an activated ligand for the EGF receptor signaling pathway. Dev Biol 205:254–259PubMedGoogle Scholar
  184. Platta CS, Greenblatt DY, Kunnimalaiyaan M, Chen H (2008) Valproic acid induces Notch1 signaling in small cell lung cancer cells. J Surg Res 148:31–37Google Scholar
  185. Powell LM, Jarman AP (2008) Context dependence of proneural bHLH proteins. Curr Opin Genet Dev 18:411–417PubMedGoogle Scholar
  186. Quan XJ, Hassan BA (2005) From skin to nerve: flies, vertebrates and the first helix. Cell Mol Life Sci 62:2036–2049PubMedGoogle Scholar
  187. Ramos RG, Igloi GL, Lichte B, Baumann U, Maier D, Schneider T, Brandstätter JH, Fröhlich A, Fischbach KF (1993) The irregular chiasm C-roughest locus of Drosophila, which affects axonal projections and programmed cell death, encodes a novel immunoglobulin-like protein. Genes Dev 7:2533–2547PubMedGoogle Scholar
  188. Rawlins EL, White NM, Jarman AP (2003) Echinoid limits R8 photoreceptor specification by inhibiting inappropriate EGF receptor signaling within R8 equivalence groups. Development 130:3715–3724PubMedGoogle Scholar
  189. Read D, Manley JL (1992) Alternatively spliced transcripts of the Drosophila tramtrack gene encode zinc finger proteins with distinct DNA binding specificities. EMBO J 11:1035–1044PubMedGoogle Scholar
  190. Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240PubMedGoogle Scholar
  191. Rebay I, Rubin GM (1995) Yan functions as a general inhibitor of differentiation and is negatively regulated by activation of the Ras1/MAPK pathway. Cell 81:857–866PubMedGoogle Scholar
  192. Reich A, Shilo BZ (2002) Keren, a new ligand of the Drosophila epidermal growth factor receptor, undergoes two modes of cleavage. EMBO J 21:4287–4296PubMedGoogle Scholar
  193. Reinke R, Zipursky SL (1988) Cell-cell interaction in the Drosophila retina: the bride of sevenless gene is required in photoreceptor cell R8 for R7 cell development. Cell 55:321–330PubMedGoogle Scholar
  194. Reiter C, Schimansky T, Nie Z, Fischbach KF (1996) Reorganization of membrane contacts prior to apoptosis in the Drosophila retina: the role of the IrreC-rst protein. Development 122:1931–1940PubMedGoogle Scholar
  195. Rogge RD, Karlovich CA, Banerjee U (1991) Genetic dissection of a neurodevelopmental pathway: Son of sevenless functions downstream of the sevenless and EGF receptor tyrosine kinases. Cell 64:39–48PubMedGoogle Scholar
  196. Roignant JY, Treisman JE (2009) Pattern formation in the Drosophila eye disc. Int J Dev Biol 53:795–804PubMedGoogle Scholar
  197. Rosay P, Colas JF, Maroteaux L (1995) Dual organization of the Drosophila neuropeptide receptor NKD gene promoter. Mech Dev 51:329–339PubMedGoogle Scholar
  198. Sawamoto K, Taguchi A, Hirota Y, Yamada C, Jin M, Okano H (1998) Argos induces programmed cell death in the developing Drosophila eye by inhibition of the Ras pathway. Cell Death Differ 5:548PubMedGoogle Scholar
  199. Schlesinger A, Kiger A, Perrimon N, Shilo BZ (2004) Small wing PLCgamma is required for ER retention of cleaved Spitz during eye development in Drosophila. Dev Cell 7:535–545PubMedGoogle Scholar
  200. Schweitzer R, Howes R, Smith R, Shilo BZ, Freeman M (1995a) Inhibition of Drosophila EGF receptor activation by the secreted protein Argos. Nature 376:699–702Google Scholar
  201. Schweitzer R, Shaharabany M, Seger R, Shilo BZ (1995b) Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev 9:1518–1529Google Scholar
  202. Shi Y, Noll M (2009) Determination of cell fates in the R7 equivalence group of the Drosophila eye by the concerted regulation of D-Pax2 and TTK88. Dev Biol 331:68–77PubMedGoogle Scholar
  203. Shilo BZ (2005) Regulating the dynamics of EGF receptor signaling in space and time. Development 132:4017–4027PubMedGoogle Scholar
  204. Silver SJ, Rebay I (2005) Signaling circuitries in development: insights from the retinal determination gene network. Development 132:3–13PubMedGoogle Scholar
  205. Simon MA, Bowtell DD, Dodson GS, Laverty TR, Rubin GM (1991) Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67:701–716PubMedGoogle Scholar
  206. Singh J, Mlodzik M (2012) Hibris, a Drosophila nephrin homolog, is required for presenilin-mediated Notch and APP-like cleavages. Dev Cell 23:82–96PubMedGoogle Scholar
  207. Spencer SA, Cagan RL (2003) Echinoid is essential for regulation of Egfr signaling and R8 formation during Drosophila eye development. Development 130:3725–3733PubMedGoogle Scholar
  208. Spencer SA, Powell PA, Miller DT, Cagan RL (1998) Regulation of EGF receptor signaling establishes pattern across the developing Drosophila retina. Development 125:4777–4790PubMedGoogle Scholar
  209. Steele L, Sukhanova MJ, Xu J, Gordon GM, Huang Y, Yu L, Du W (2009) Retinoblastoma family protein promotes normal R8-photoreceptor differentiation in the absence of rhinoceros by inhibiting dE2F1 activity. Dev Biol 335:228–236PubMedGoogle Scholar
  210. Sukhanova MJ, Steele LJ, Zhang T, Gordon GM, Du W (2011) RBF and Rno promote photoreceptor differentiation onset through modulating EGFR signaling in the Drosophila developing eye. Dev Biol 359:190–198PubMedGoogle Scholar
  211. Sun Y, Jan LY, Jan YN (1998) Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system. Development 125:3731–3740PubMedGoogle Scholar
  212. Sundaram MV (2005) The love-hate relationship between Ras and Notch. Genes Dev 19:1825–1839PubMedGoogle Scholar
  213. Suzuki T, Saigo K 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 127:1531–1540PubMedGoogle Scholar
  214. Swanson CI, Evans NC, Barolo S (2010) Structural rules and complex regulatory circuitry constrain expression of a Notch- and EGFR-regulated eye enhancer. Dev Cell 18:359–370PubMedGoogle Scholar
  215. Takano A, Zochi R, Hibi M, Terashima T, Katsuyama Y (2011) Function of strawberry notch family genes in the zebrafish brain development. Kobe J Med Sci 56:E220–230PubMedGoogle Scholar
  216. Tanaka-Matakatsu M, Du W (2008) Direct control of the proneural gene atonal by retinal determination factors during Drosophila eye development. Dev Biol 313:787–801PubMedGoogle Scholar
  217. Tang AH, Neufeld TP, Kwan E, Rubin GM (1997) PHYL acts to down-regulate TTK88, a transcriptional repressor of neuronal cell fates, by a SINA-dependent mechanism. Cell 90:459–467PubMedGoogle Scholar
  218. Tepass U, Harris KP (2007) Adherens junctions in Drosophila retinal morphogenesis. Trends Cell Biol 17:26–35PubMedGoogle Scholar
  219. Thackeray JR, Gaines PC, Ebert P, Carlson JR (1998) Small wing encodes a phospholipase C-(gamma) that acts as a negative regulator of R7 development in Drosophila. Development 125:5033–5042PubMedGoogle Scholar
  220. Tio M, Ma C, Moses K (1994) Spitz, a Drosophila homolog of transforming growth factor-alpha, is required in the founding photoreceptor cells of the compound eye facets. Mech Dev 48:13–23PubMedGoogle Scholar
  221. Tio M, Moses K (1997) The Drosophila TGF alpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124:343–351PubMedGoogle Scholar
  222. Tomita A, Buchholz DR, Shi YB (2004) Recruitment of N-CoR/SMRT-TBLR1 corepressor complex by unliganded thyroid hormone receptor for gene repression during frog development. Mol Cell Biol 24:3337–3346PubMedGoogle Scholar
  223. Tomlinson A (1985) The cellular dynamics of pattern formation in the eye of Drosophila. J Embryol Exp Morphol 89:313–331PubMedGoogle Scholar
  224. Tomlinson A, Kimmel BE, Rubin GM (1988) Rough, a Drosophila homeobox gene required in photoreceptors R2 and R5 for inductive interactions in the developing eye. Cell 55:771–784PubMedGoogle Scholar
  225. Tomlinson A, Mavromatakis YE, Struhl G (2011) Three distinct roles for notch in Drosophila R7 photoreceptor specification. PLoS Biol 9:e1001132PubMedGoogle Scholar
  226. Tomlinson A, Ready DF (1986) Sevenless: a cell-specific homeotic mutation of the Drosophila eye. Science 231:400–402PubMedGoogle Scholar
  227. Tomlinson A, Ready DF (1987a) Cell fate in the Drosophila ommatidium. Dev Biol 123:264–275Google Scholar
  228. Tomlinson A, Ready DF (1987b) Neuronal differentiation in Drosophila ommatidium. Dev Biol 120:366–376Google Scholar
  229. Tomlinson A, Struhl G (1999) Decoding vectorial information from a gradient: sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye. Development 126:5725–5738PubMedGoogle Scholar
  230. Tomlinson A, Struhl G (2001) Delta/Notch and Boss/Sevenless signals act combinatorially to specify the Drosophila R7 photoreceptor. Mol Cell 7:487–495PubMedGoogle Scholar
  231. Tsruya R, Schlesinger A, Reich A, Gabay L, Sapir A, Shilo BZ (2002) Intracellular trafficking by Star regulates cleavage of the Drosophila EGF receptor ligand Spitz. Genes Dev 16:222–234PubMedGoogle Scholar
  232. Tsruya R, Wojtalla A, Carmon S, Yogev S, Reich A, Bibi E, Merdes G, Schejter E, Shilo BZ (2007) Rhomboid cleaves Star to regulate the levels of secreted Spitz. EMBO J 26:1211–1220PubMedGoogle Scholar
  233. Tsuda L, Nagaraj R, Zipursky SL, Banerjee U (2002) An EGFR/Ebi/Sno pathway promotes delta expression by inactivating Su(H)/SMRTER repression during inductive notch signaling. Cell 110:625–637PubMedGoogle Scholar
  234. Tsuda L, Kaido M, Lim YM, Kato K, Aigaki T, Hayashi S (2006) An NRSF/REST-like repressor downstream of Ebi/SMRTER/Su(H) regulates eye development in Drosophila. EMBO J 25:3191–3202PubMedGoogle Scholar
  235. Urban S, Lee JR, Freeman M (2001) Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107:173–182PubMedGoogle Scholar
  236. Urban S, Lee JR, Freeman M (2002) A family of Rhomboid intramembrane proteases activates all Drosophila membrane-tethered EGF ligands. EMBO J 21:4277–4286PubMedGoogle Scholar
  237. Usui K, Goldstone C, Gibert JM, Simpson P (2008) Redundant mechanisms mediate bristle patterning on the Drosophila thorax. Proc Natl Acad Sci U S A 105:20112–20117PubMedGoogle Scholar
  238. Van Doren M, Ellis HM, Posakony JW (1991) The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. Development 113:245–255PubMedGoogle Scholar
  239. Van Doren M, Bailey AM, Esnayra J, Ede K, Posakony JW (1994) Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. Genes Dev 8:2729–2742PubMedGoogle Scholar
  240. Van Vactor DL, Cagan RL, Krämer H, Zipursky SL (1991) Induction in the developing compound eye of Drosophila: multiple mechanisms restrict R7 induction to a single retinal precursor cell. Cell 67:1145–1155PubMedGoogle Scholar
  241. Voas MG, Rebay I (2003) The novel plant homeodomain protein rhinoceros antagonizes Ras signaling in the Drosophila eye. Genetics 165:1993–2006PubMedGoogle Scholar
  242. Voas MG, Rebay I (2004) Signal integration during development: insights from the Drosophila eye. Dev Dyn 229:162–175PubMedGoogle Scholar
  243. Wang SL, Hawkins CJ, Yoo SJ, Müller HA, Hay BA (1999) The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 98:453–463Google Scholar
  244. Wasserman JD, Urban S, Freeman M (2000) A family of rhomboid-like genes: Drosophila rhomboid-1 and roughoid/rhomboid-3 cooperate to activate EGF receptor signaling. Genes Dev 14:1651–1663PubMedGoogle Scholar
  245. Weber U, Siegel V, Mlodzik M (1995) pipsqueak encodes a novel nuclear protein required downstream of seven-up for the development of photoreceptors R3 and R4. EMBO J 14:6247–6257PubMedGoogle Scholar
  246. Weber U, Paricio N, Mlodzik M (2000) Jun mediates Frizzled-induced R3/R4 cell fate distinction and planar polarity determination in the Drosophila eye. Development 127:3619–3629PubMedGoogle Scholar
  247. Weber U, Pataki C, Mihaly J, Mlodzik M (2008) Combinatorial signaling by the Frizzled/PCP and Egfr pathways during planar cell polarity establishment in the Drosophila eye. Dev Biol 316:110–123PubMedGoogle Scholar
  248. Weinmaster G, Fischer JA (2011) Notch ligand ubiquitylation: what is it good for? Dev Cell 21:134–144PubMedGoogle Scholar
  249. White NM, Jarman AP (2000) Drosophila atonal controls photoreceptor R8-specific properties and modulates both receptor tyrosine kinase and Hedgehog signaling. Development 127:1681–1689PubMedGoogle Scholar
  250. Wolff T, Ready DF (1991a) Cell death in normal and rough eye mutants of Drosophila. Development 113:825–839Google Scholar
  251. Wolff T, Ready DF (1991b) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113:841–850Google Scholar
  252. Wolff T, Ready DF (1993) Pattern formation in the Drosophila retina. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 1277–1325Google Scholar
  253. Xie B, Charlton-Perkins M, McDonald E, Gebelein B, Cook T (2007) Senseless functions as a molecular switch for color photoreceptor differentiation in Drosophila. Development 134:4243–4253PubMedGoogle Scholar
  254. Xiong WC, Montell C (1993) tramtrack is a transcriptional repressor required for cell fate determination in the Drosophila eye. Genes Dev 7:1085–1096PubMedGoogle Scholar
  255. Xu C, Kauffmann RC, Zhang J, Kladny S, Carthew RW (2000) Overlapping activators and repressors delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell 103:87–97PubMedGoogle Scholar
  256. Yamada T, Okabe M, Hiromi Y (2003) EDL/MAE regulates EGF-mediated induction by antagonizing Ets transcription factor Pointed. Development 130:4085–4096PubMedGoogle Scholar
  257. Yamamoto D, Nihonmatsu I, Matsuo T, Miyamoto H, Kondo S, Hirata K, Ikegami Y (1996) Genetic interactions of pokkuri with seven in absentia, tramtrack and downstream components of the sevenless pathway in R7 photoreceptor induction in Drosophila melanogaster. Rouxs Arch Dev Biol 205:215–224Google Scholar
  258. Yan H, Canon J, Banerjee U (2003) A transcriptional chain linking eye specification to terminal determination of cone cells in the Drosophila eye. Dev Biol 263:323–329PubMedGoogle Scholar
  259. Yang L, Baker NE (2001) Role of the EGFR/Ras/Raf pathway in specification of photoreceptor cells in the Drosophila retina. Development 128:1183–1191PubMedGoogle Scholar
  260. Yogev S, Schejter ED, Shilo BZ (2008) Drosophila EGFR signaling is modulated by differential compartmentalization of Rhomboid intramembrane proteases. EMBO J 27:1219–1230PubMedGoogle Scholar
  261. Yogev S, Rousso T, Schejter ED, Shilo BZ (2011) Versatility of EGF receptor ligand processing in insects. Dev Biol 357:17–20PubMedGoogle Scholar
  262. Yoon HG, Chan DW, Huang ZQ, Li J, Fondell JD, Qin J, Wong J (2003) Purification and functional characterization of the human N-CoR complex: the roles of HDAC3, TBL1 and TBLR1. EMBO J 22:1336–1346PubMedGoogle Scholar
  263. Yu SY, Yoo SJ, Yang L, Zapata C, Srinivasan A, Hay BA, Baker NE (2002) A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129:3269–3278PubMedGoogle Scholar
  264. Zhang J, Kalkum M, Chait BT, Roeder RG (2002) The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol Cell 9:611–623PubMedGoogle Scholar
  265. Zhang T, Ranade S, Cai CQ, Clouser C, Pignoni F (2006) Direct control of neurogenesis by selector factors in the fly eye: regulation of atonal by Ey and So. Development 133:4881–4889PubMedGoogle Scholar
  266. Zheng L, Carthew RW (2008) Lola regulates cell fate by antagonizing Notch induction in the Drosophila eye. Mech Dev 125:18–29PubMedGoogle Scholar
  267. Zheng Q, Qin H, Zhang H, Li J, Hou L, Wang H, Zhang X, Zhang S, Feng L, Liang Y, Han H, Yi D (2007) Notch signaling inhibits growth of the human lung adenocarcinoma cell line A549. Oncol Rep 17:847–852PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of BiologyNew Mexico State UniversityLas CrucesUSA

Personalised recommendations