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Catching the Next Wave: Patterning of the Drosophila Eye by the Morphogenetic Furrow

  • Justin P. KumarEmail author
Chapter

Abstract

In 1864, August Weismann published the first drawing of the insect eye–antennal disc complex. In this image, he drew a line within the eye and described it as the border between the eye and antennal portions of the disc complex. One hundred and twelve years later, Donald Ready, Thomas Hanson, and Seymour Benzer demonstrated that this line, which they called the morphogenetic furrow, is actually the leading edge of a differentiating wave that traverses the eye disc of the fruit fly, Drosophila melanogaster, and transforms a field of undifferentiated and nonpatterned cells into an ordered array of periodically spaced ommatidia or unit eyes. In the 36 years since this seminal discovery, dozens of papers have focused on elucidating the molecular mechanisms that underlie the initiation and progression of the furrow as well as the many cellular changes that cells undergo as they enter, temporarily reside, and then exit the furrow. This review will summarize what is currently known about the cellular architecture of the furrow and the mechanisms that control its birth and propagation across the eye primordium. This chapter will also discuss the means by which the initiation of the furrow is restricted to a single point along the posterior margin.

Keywords

Posterior Margin Imaginal Disc Morphogenetic Furrow Cell Cycle Synchronization Posterior Center 
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.

Notes

Acknowledgments

I would like to thank everyone who has contributed to our understanding of the mechanisms that regulate the initiation and progression of the morphogenetic furrow. I would like to also apologize to anyone whose work is not cited here. This work was supported by a grant from the National Eye Institute (R01 EY4863) to Justin P. Kumar.

References

  1. Bach EA, Vincent S, Zeidler MP, Perrimon N (2003) A sensitized genetic screen to identify novel regulators and components of the Drosophila janus kinase/signal transducer and activator of transcription pathway. Genetics 165:1149–1166PubMedGoogle Scholar
  2. Baker NE, Yu S, Han D (1996) Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye. Curr Biol 6:1290–1301PubMedCrossRefGoogle Scholar
  3. Basler K, Hafen E (1989) Dynamics of Drosophila eye development and temporal requirements of sevenless expression. Development 107:723–731PubMedGoogle Scholar
  4. Basler K, Struhl G (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368:208–214PubMedCrossRefGoogle Scholar
  5. Becker HJ (1957) Uber Rontgenmossaikflecken und Defektmutationen am Auge von Drosophila und die Entwicklungsphysiologie des Auges. Z Induk Abst Vererb Lehre 88:333–373Google Scholar
  6. Benlali A, Draskovic I, Hazelett DJ, Treisman JE (2000) act up controls actin polymerization to alter cell shape and restrict Hedgehog signaling in the Drosophila eye disc. Cell 101:271–281PubMedCrossRefGoogle Scholar
  7. Bessa J, Gebelein B, Pichaud F, Casares F, Mann RS (2002) Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes Dev 16:2415–2427PubMedCrossRefGoogle Scholar
  8. Bhattacharya A, Baker NE (2009) The HLH protein Extramacrochaetae is required for R7 cell and cone cell fates in the Drosophila eye. Dev Biol 327:288–300PubMedCrossRefGoogle Scholar
  9. Blackman RK, Sanicola M, Raftery LA, Gillevet T, Gelbart WM (1991) An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-b family in Drosophila. Development 111:657–665PubMedGoogle Scholar
  10. Bonini NM, Leiserson WM, Benzer S (1993) The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72:379–395PubMedCrossRefGoogle Scholar
  11. Borod ER, Heberlein U (1998) Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina. Dev Biol 197:187–197PubMedCrossRefGoogle Scholar
  12. Brennan CA, Ashburner M, Moses K (1998) Ecdysone pathway is required for furrow progression in the developing Drosophila eye. Development 125:2653–2664PubMedGoogle Scholar
  13. Brown NL, Sattler CA, Markey DR, Carroll SB (1991) hairy gene function in the Drosophila eye: normal expression is dispensable but ectopic expression alters cell fates. Development 113:1245–1256PubMedGoogle Scholar
  14. Brown NL, Sattler CA, Paddock SW, Carroll SB (1995) Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell 80:879–887PubMedCrossRefGoogle Scholar
  15. Burke R, Basler K (1996) Hedgehog-dependent patterning in the Drosophila eye can occur in the absence of Dpp signaling. Dev Biol 179:360–368PubMedCrossRefGoogle Scholar
  16. Cagan RL, Ready DF (1989a) The emergence of order in the Drosophila pupal retina. Dev Biol 136:346–362CrossRefGoogle Scholar
  17. Cagan RL, Ready DF (1989b) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3:1099–1112CrossRefGoogle Scholar
  18. Campos-Ortega JA, Hofbauer A (1977) Cell clones and pattern formation on the lineage of photoreceptor cells in the compound eye of Drosophila. Roux Arch Dev Biol 181:227–245CrossRefGoogle Scholar
  19. Capdevila J, Estrada MP, Sanchez-Herrero E, Guerrero I (1994) The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO 13:71–82Google Scholar
  20. Chanut F, Heberlein U (1997a) Retinal morphogenesis in Drosophila: hints from an eye-specific decapentaplegic allele. Dev Genet 20:197–207CrossRefGoogle Scholar
  21. Chanut F, Heberlein U (1997b) Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124:559–567Google Scholar
  22. Chanut F, Luk A, 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 156:1203–1217PubMedGoogle Scholar
  23. Chao JL, Tsai YC, Chiu SJ, Sun YH (2004) Localized Notch signal acts through eyg and upd to promote global growth in Drosophila eye. Development 131:3839–3847PubMedCrossRefGoogle Scholar
  24. Chen R, Halder G, Zhang Z, Mardon G (1999) Signaling by the TGF-b homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila. Development 126:935–943PubMedGoogle Scholar
  25. 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 12:977–996PubMedCrossRefGoogle Scholar
  26. Cho KO, Choi KW (1998) Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396:272–276PubMedCrossRefGoogle Scholar
  27. Cohen SM (1993) Imaginal disc development. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 747–841Google Scholar
  28. Corrigall D, Walther RF, Rodriguez L, Fichelson P, Pichaud F (2007) Hedgehog signaling is a principal inducer of Myosin-II-driven cell ingression in Drosophila epithelia. Dev Cell 13:730–742PubMedCrossRefGoogle Scholar
  29. 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
  30. Czerny T, Halder G, Kloter U, Souabni A, Gehring WJ, Busslinger M (1999) twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol Cell 3:297–307PubMedCrossRefGoogle Scholar
  31. Dietrich W (1909) Die Fazettenaugen der Dipteren. Z Wiss Zool 92:465–539Google Scholar
  32. 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
  33. Dominguez M (1999) Dual role for hedgehog in the regulation of the proneural gene atonal during ommatidia development. Development 126:2345–2353PubMedGoogle Scholar
  34. Dominguez M, Celis JF de (1998) A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396:276–278PubMedCrossRefGoogle Scholar
  35. Dominguez M, Hafen E (1997) Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev 11:3254–3264PubMedCrossRefGoogle Scholar
  36. Edgar BA, O’Farrell PH (1989) Genetic control of cell division patterns in the Drosophila embryo. Cell 57:177–187PubMedCrossRefGoogle Scholar
  37. Ekas LA, Baeg GH, Flaherty MS, Ayala-Camargo A, Bach EA (2006) JAK/STAT signaling promotes regional specification by negatively regulating wingless expression in Drosophila. Development 133:4721–4729PubMedCrossRefGoogle Scholar
  38. 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 61:27–38PubMedCrossRefGoogle Scholar
  39. Fan SS, Ready DF (1997) Glued participates in distinct microtubule-based activities in Drosophila eye development. Development 124:1497–1507PubMedGoogle Scholar
  40. Firth LC, Bhattacharya A, Baker NE (2010). Cell cycle arrest by a gradient of Dpp signaling during Drosophila eye development. BMC Dev Biol 10:28PubMedCrossRefGoogle Scholar
  41. Fischer-Vize JA, Mosley KL (1994) Marbles mutants: uncoupling cell determination and nuclear migration in the developing Drosophila eye. Development 120:2609–2618PubMedGoogle Scholar
  42. Frankfort BJ, Mardon G (2002) R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129:1295–1306PubMedGoogle Scholar
  43. 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 32:403–414PubMedCrossRefGoogle Scholar
  44. Freeman M (1994) The spitz gene is required for photoreceptor determination in the Drosophila eye where it interacts with the EGF receptor. Mech Dev 48:25–33PubMedCrossRefGoogle Scholar
  45. Freeman M (1996) Reiterative use of the EGF Receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87:651–660PubMedCrossRefGoogle Scholar
  46. Freeman M (1997) Cell determination strategies in the Drosophila eye. Development 124:261–270PubMedGoogle Scholar
  47. 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 61:39–48PubMedCrossRefGoogle Scholar
  48. Gonzalez F, Swales L, Bejsovec A, Skaer H, Martinez Arias A (1991) Secretion and movement of wingless protein in the epidermis of the Drosophila embryo. Mech Dev 35:43–54PubMedCrossRefGoogle Scholar
  49. 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
  50. Gutierrez-Avino FJ, Ferres-Marco D, Dominguez M (2009) The position and function of the Notch-mediated eye growth organizer: the roles of JAK/STAT and four-jointed. EMBO Rep 10:1051–1058PubMedCrossRefGoogle Scholar
  51. Hazelett DJ, Bourouis M, Walldorf U, Treisman JE (1998) decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development 125:3741–3751PubMedGoogle Scholar
  52. 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
  53. Heberlein U, Singh CM, Luk AY, Donohoe TJ (1995) Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373:709–711PubMedCrossRefGoogle Scholar
  54. Heberlein U, Wolff T, Rubin GM (1993) The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75:913–926PubMedCrossRefGoogle Scholar
  55. Heemskerk J, DiNardo S (1994) Drosophila hedgehog acts as a morphogen in cellular patterning. Cell 76:449–460PubMedCrossRefGoogle Scholar
  56. Held LI (2002) Imaginal discs: the genetic and cellular logic of pattern formation. Developmental and cell biology series, vol 39. Cambridge Press, Cambridge, p 460CrossRefGoogle Scholar
  57. Horsfield J, Penton A, Secombe J, Hoffman FM, Richardson H (1998) decapentaplegic is required for arrest in G1 phase during Drosophila eye development. Development 125:5069–5078PubMedGoogle Scholar
  58. Houalla T, Hien Vuong D, Ruan W, Suter B, Rao Y (2005) The Ste20-like kinase misshapen functions together with Bicaudal-D and dynein in driving nuclear migration in the developing drosophila eye. Mech Dev 122:97–108PubMedCrossRefGoogle Scholar
  59. Ives P (1950) New mutant report: bar-3. Dros Info Serv 24:58Google Scholar
  60. Jarman AP, Grell EH, Ackerman L, Jan LY, Jan YN (1994) atonal is the proneural gene for Drosophila photoreceptors. Nature 369:398–400PubMedCrossRefGoogle Scholar
  61. 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
  62. Jones NA, Kuo YM, Sun YH, Beckendorf SK (1998) The Drosophila Pax gene eye gone is required for embryonic salivary duct development. Development 125:4163–4174PubMedGoogle Scholar
  63. Jun S, Wallen RV, Goriely A, Kalionis B, Desplan C (1998) Lune/eye gone, a Pax-like protein, uses a partial paired domain and a homeodomain for DNA recognition. Proc Natl Acad Sci U S A 95:13720–13725PubMedCrossRefGoogle Scholar
  64. Jurgens G, Hartenstein V (1993) The terminal regions of the body plan. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 687–746Google Scholar
  65. Kango-Singh M, Singh A, Henry Sun Y (2003) Eyeless collaborates with Hedgehog and Decapentaplegic signaling in Drosophila eye induction. Dev Biol 256:49–60PubMedCrossRefGoogle Scholar
  66. Kenyon KL, Ranade SS, Curtiss J, Mlodzik M, Pignoni F (2003) Coordinating proliferation and tissue specification to promote regional identity in the Drosophila head. Dev Cell 5:403–414PubMedCrossRefGoogle Scholar
  67. Kimberly EL, Hardin J (1998) Bottle cells are required for the initiation of primary invagination in the sea urchin embryo. Dev Biol 204:235–250PubMedCrossRefGoogle Scholar
  68. Kumar JP (2010) Retinal determination the beginning of eye development. Curr Top Dev Biol 93:1–28PubMedCrossRefGoogle Scholar
  69. Kumar JP (2011) My what big eyes you have: how the Drosophila retina grows. Dev Neurobiol 71:1133–1152PubMedCrossRefGoogle Scholar
  70. Kumar JP (2012) Building an ommatidium one cell at a time. Dev Dyn 241:136–149PubMedCrossRefGoogle Scholar
  71. Kumar JP, Moses K (2001a) EGF receptor and Notch signaling act upstream of Eyeless/Pax6 to control eye specification. Cell 104:687–697CrossRefGoogle Scholar
  72. Kumar JP, Moses K (2001b) The EGF receptor and notch signaling pathways control the initiation of the morphogenetic furrow during Drosophila eye development. Development 128:2689–2697Google Scholar
  73. 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
  74. Lebovitz RM, Ready DF (1986) Ommatidial development in Drosophila eye disc fragments. Dev Biol 117:663–671PubMedCrossRefGoogle Scholar
  75. Lee JJ, Kessler DP von, Parks S, Beachy PA (1992) Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71:33–50PubMedCrossRefGoogle Scholar
  76. Lopes CS, Casares F (2009) hth maintains the pool of eye progenitors and its downregulation by Dpp and Hh couples retinal fate acquisition with cell cycle exit. Dev Biol 339:78–88PubMedCrossRefGoogle Scholar
  77. Ma C, Liu H, Zhou Y, Moses K (1996) Identification and characterization of autosomal genes that interact with glass in the developing Drosophila eye. Genetics 142:1199–1213PubMedGoogle Scholar
  78. Ma C, Moses K (1995) wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. Development 121:2279–2289PubMedGoogle Scholar
  79. Ma C, Zhou Y, Beachy PA, Moses K (1993) The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75:927–938PubMedCrossRefGoogle Scholar
  80. Massague J (1996) TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 85:947–950PubMedCrossRefGoogle Scholar
  81. Massague J, Polyak K (1995) Mammalian antiproliferative signals and their targets. Curr Opin Genet Dev 5:91–96PubMedCrossRefGoogle Scholar
  82. Masucci JD, Miltenberger RJ, Hoffmann FM (1990) Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal disks is regulated by 3’ cis-regulatory elements. Genes Dev 4:2011–2023PubMedCrossRefGoogle Scholar
  83. Mohler J (1988) Requirements for hedgehog, a segmental polarity gene, in patterning larval and adult cuticle of Drosophila. Genetics 120:1061–1072PubMedGoogle Scholar
  84. Mosley-Bishop KL, Li Q, Patterson L, Fischer JA (1999) Molecular analysis of the klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye. Curr Biol 9:1211–1220PubMedCrossRefGoogle Scholar
  85. Mozer BA (2001) Dominant Drop mutants are gain-of-function alleles of the muscle segment homeobox gene (msh) whose overexpression leads to the arrest of eye development. Dev Biol 233:380–393PubMedCrossRefGoogle Scholar
  86. Padgett RW, St Johnston RD, Gelbart WM (1987) A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-beta family. Nature 325:81–84PubMedCrossRefGoogle Scholar
  87. Pan D, Rubin GM (1995) cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80:543–552PubMedCrossRefGoogle Scholar
  88. Panganiban GE, Rashka KE, Neitzel MD, Hoffmann FM (1990a) Biochemical characterization of the Drosophila dpp protein, a member of the transforming growth factor beta family of growth factors. Mol Cell Biol 10:2669–2677Google Scholar
  89. Panganiban GE, Reuter R, Scott MP, Hoffmann FM (1990b) A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development 110:1041–1050Google Scholar
  90. Papayannopoulos V, Tomlinson A, Panin VM, Rauskolb C, Irvine KD (1998) Dorsal-ventral signaling in the Drosophila eye. Science 281:2031–2034PubMedCrossRefGoogle Scholar
  91. Patterson K, Molofsky AB, Robinson C, Acosta S, Cater C, Fischer JA (2004) The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. Mol Biol Cell 15(2):600–610PubMedCrossRefGoogle Scholar
  92. Pauli T, Seimiya M, Blanco J, Gehring WJ (2005) Identification of functional sine oculis motifs in the autoregulatory element of its own gene, in the eyeless enhancer and in the signalling gene hedgehog. Development 132:2771–2782PubMedCrossRefGoogle Scholar
  93. Peng HW, Slattery M, Mann RS (2009) Transcription factor choice in the Hippo signaling pathway: homothorax and yorkie regulation of the microRNA bantam in the progenitor domain of the Drosophila eye imaginal disc. Genes Dev 23:2307–2319PubMedCrossRefGoogle Scholar
  94. Penton A, Selleck SB, Hoffmann FM (1997) Regulation of cell cycle synchronization by decapentaplegic during Drosophila eye development. Science 275:203–206PubMedCrossRefGoogle Scholar
  95. 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—4078Google Scholar
  96. Pfeiffer S, Vincent JP (1999) Signalling at a distance: transport of Wingless in the embryonic epidermis of Drosophila. Semin Cell Dev Biol 10:303–309PubMedCrossRefGoogle Scholar
  97. Pignoni F, Zipursky SL (1997) Induction of Drosophila eye development by Decapentaplegic. Development 124:271–278PubMedGoogle Scholar
  98. Quiring R, Walldorf U, Kloter U, Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans (see comments). Science 265(5173):785–789PubMedCrossRefGoogle Scholar
  99. Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240PubMedCrossRefGoogle Scholar
  100. Richardson H, O’Keefe LV, Marty T, Saint R (1995) Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc. Development 121:3371–3379PubMedGoogle Scholar
  101. Rogers EM, Brennan CA, Mortimer NT, Cook S, Morris AR, Moses K (2005) Pointed regulates an eye-specific transcriptional enhancer in the Drosophila hedgehog gene, which is required for the movement of the morphogenetic furrow. Development 132:4833–4843PubMedCrossRefGoogle Scholar
  102. Royet J, Finkelstein R (1996) hedgehog, wingless and othrodenticle specify adult head development in Drosophila. Development 122:1849–1858PubMedGoogle Scholar
  103. Royet J, Finkelstein R (1997) Establishing primordia in the Drosophila eye-antennal imaginal disc: the role of decapentaplegic, wingless and hedgehog. Development 124:4793–4800PubMedGoogle Scholar
  104. Serikaku MA, O’Tousa JE (1994) sine oculis is a homeobox gene required for Drosophila visual system development. Genetics 138:1137–1150PubMedGoogle Scholar
  105. Singh A, Choi KW (2003) Initial state of the Drosophila eye before dorsoventral specification is equivalent to ventral. Development 130:6351–6360PubMedCrossRefGoogle Scholar
  106. Struhl G (1981) A blastoderm fate map of compartments and segments of the Drosophila head. Dev Biol 84:386–396PubMedCrossRefGoogle Scholar
  107. Strutt DI, Mlodzik M (1997) Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disc. Development 124:3233–3240PubMedGoogle Scholar
  108. Strutt DI, Wiersdorff V, Mlodzik M (1995) Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A. Nature 373:705–709PubMedCrossRefGoogle Scholar
  109. Sun YH, Tsai CJ, Green MM, Chao JL, Yu CT, Jaw TJ, Yeh JY, Bolshakov VN (1995) White as a reporter gene to detect transcriptional silencers specifying position-specific gene expression during Drosophila melanogaster eye development. Genetics 141:1075–1086PubMedGoogle Scholar
  110. Swan A, Nguyen T, Suter B (1999) Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nat Cell Biol 1:444–449PubMedCrossRefGoogle Scholar
  111. Tabata T, Kornberg TB (1994) Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76:89–102PubMedCrossRefGoogle Scholar
  112. Tearle R, Tomlinson A, Saint R (1994) The dominant Drop eye mutations of Drosophila melanogaster define two loci implicated in normal eye development. Mol Gen Genet 244:426–434PubMedCrossRefGoogle Scholar
  113. Thomas BJ, Gunning DA, Cho J, Zipursky L (1994) Cell cycle progression in the developing Drosophila eye: roughex encodes a novel protein required for the establishment of G1. Cell 77:1003–1014PubMedCrossRefGoogle Scholar
  114. Thomas BJ, Zavitz KH, Dong X, Lane ME, Weigmann K, Finley RL Jr, Brent R, Lehner CF, Zipursky SL (1997) Roughex down-regulates G2 cyclins in G1. Genes Dev 11:1289–1298PubMedCrossRefGoogle Scholar
  115. 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 48:13–23PubMedCrossRefGoogle Scholar
  116. Tio M, Moses K (1997) The Drosophila TGF alpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124:343–351PubMedGoogle Scholar
  117. Tomlinson A (1985). The cellular dynamics of pattern formation in the eye of Drosophila. J Embryol Exp Morphol 89:313–331PubMedGoogle Scholar
  118. Tomlinson A, Ready DF (1987) Neuronal differentiation in the Drosophila ommatidium. Dev Biol 120:366–376PubMedCrossRefGoogle Scholar
  119. Treisman JE, Rubin GM (1995) Wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121:3519–3527PubMedGoogle Scholar
  120. Tsai YC, Sun YH (2004) Long-range effect of upd, a ligand for Jak/STAT pathway, on cell cycle in Drosophila eye development. Genesis 39:141–153PubMedCrossRefGoogle Scholar
  121. Tsai YC, Yao JG, Chen PH, Posakony JW, Barolo S, Kim J, Sun YH (2007) Upd/Jak/STAT signaling represses wg transcription to allow initiation of morphogenetic furrow in Drosophila eye development. Dev Biol 306:760–771PubMedCrossRefGoogle Scholar
  122. den Heuvel M van, Nusse R, Johnston P, Lawrence PA (1989) Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59:739–749CrossRefGoogle Scholar
  123. 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
  124. Waddington CH, Perry MM (1960) The ultrastructure of the developing eye of Drosophila. Proc Roy Soc Biol Sci 153:155–178CrossRefGoogle Scholar
  125. Wehrli M, Tomlinson A (1995) Epithelial planar polarity in the developing Drosophila eye. Development 121:2451–2459PubMedGoogle Scholar
  126. Wiersdorff V, Lecuit T, Cohen SM, Mlodzik M (1996) Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 122:2153–2162PubMedGoogle Scholar
  127. Wolff T, Ready DF (1991) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113:841–850PubMedGoogle Scholar
  128. Yao JG, Weasner BM, Wang LH, Jang CC, Weasner B, Tang CY, Salzer CL, Chen CH, Hay B, Sun YH et al (2008) Differential requirements for the Pax6(5a) genes eyegone and twin of eyegone during eye development in Drosophila. Dev Biol 315(2):535–551PubMedCrossRefGoogle Scholar
  129. Zelhof AC, Ghbeish N, Tsai C, Evans RM, McKeown M (1997) A role for ultraspiracle, the Drosophila RXR, in morphogenetic furrow movement and photoreceptor cluster formation. Development 124:2499–2506PubMedGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA

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