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Ghost in the Machine: The Peripodial Epithelium

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Molecular Genetics of Axial Patterning, Growth and Disease in Drosophila Eye

Abstract

A fundamental feature of early animal development is that fate specification and the morphogenesis of one tissue is often induced by signals emanating from a neighboring population of cells. H. Spemann and H. Mangold introduced this concept when they showed that a transplanted blastopore lip of an early gastrulating newt could induce the formation of a full axis after it was transplanted into a second newt species. C.H. Waddington later demonstrated that the process of induction is not restricted to amphibians but rather is a general mechanism that applies broadly to many different organisms including mammals. Extirpation and transplantation studies of the vertebrate eye and lens indicate that these two tissues influence aspects of each other’s development. Likewise, several studies have shown that the development of the developing eye field in Drosophila is influenced by an overlying tissue called the peripodial epithelium. While the vertebrate lens and the peripodial epithelium of the Drosophila eye-antennal disc are non-homologous structures, these two tissues use common elements such as the Pax6 transcription factor and the TGFβ/BMP4 signaling pathway to influence the growth, specification, and patterning of the adjacent retinas. In this chapter, we will describe what is known about the role that the peripodial epithelium plays in the development of the eye-antennal disc of Drosophila.

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References

  • Abzhanov A, Holtzman S, Kaufman TC (2001) The Drosophila proboscis is specified by two Hox genes, proboscipedia and Sex combs reduced, via repression of leg and antennal appendage genes. Development 128:2803–2814

    CAS  PubMed  Google Scholar 

  • Adler PN, MacQueen M (1984) Cell proliferation and DNA replication in the imaginal wing disc of Drosophila melanogaster. Dev Biol 103:28–37

    Article  CAS  PubMed  Google Scholar 

  • Agnes F, Suzanne M, Noselli S (1999) The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development 126:5453–5462

    CAS  PubMed  Google Scholar 

  • Amore G, Casares F (2010) Size matters: the contribution of cell proliferation to the progression of the specification Drosophila eye gene regulatory network. Dev Biol 344:569–577

    Article  CAS  PubMed  Google Scholar 

  • Atkins M, Mardon G (2009) Signaling in the third dimension: the peripodial epithelium in eye disc development. Dev Dyn 238:2139–2148

    Article  PubMed  PubMed Central  Google Scholar 

  • Auerbach C (1936). The development of the legs, wings, and halteres in wild type and some mutant strains of Drosophila melanogaster. Trans R Soc Edin LVIII, Part III, No 27

    Google Scholar 

  • Baena-Lopez LA, Pastor-Pareja JC, Resino J (2003) Wg and Egfr signalling antagonise the development of the peripodial epithelium in Drosophila wing discs. Development 130:6497–6506

    Article  CAS  PubMed  Google Scholar 

  • Baker LR, Weasner BM, Nagel A, Neuman SD, Bashirullah A, Kumar JP (2018) Eyeless/Pax6 initiates eye formation non-autonomously from the peripodial epithelium. Development 145(15):dev163329

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baker NE (1988) Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev Biol 125:96–108

    Article  CAS  PubMed  Google Scholar 

  • Baker WK (1978) A fine-structure gynandromorph fate map of the Drosophila head. Genetics 88:743–754

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beadle GW, Ephrussi B (1935) Transplantation in Drosophila. Proc Natl Acad Sci USA 21:642–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beadle GW, Ephrussi B (1936a) Development of eye colors in Drosophila: transplantation experiments with suppressor of vermilion. Proc Natl Acad Sci USA 22:536–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beadle GW, Ephrussi B (1936b) The differentiation of eye pigments in Drosophila as studied by transplantation. Genetics 21:225–247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beadle GW, Ephrussi B (1937) Development of eye colors in Drosophila: diffusible substances and their interrelations. Genetics 22:76–86

    CAS  PubMed  PubMed Central  Google Scholar 

  • Becker HJ (1957) Uber Rontgenmossaikflecken und Defektmutationen am Auge von Drosophila und die Entwicklungsphysiologie des Auges. Z Induk Abst Vererb Lehre 88:333–373

    CAS  Google Scholar 

  • Bessa J, Casares F (2005) Restricted teashirt expression confers eye-specific responsiveness to Dpp and Wg signals during eye specification in Drosophila. Development 132:5011–5020

    Article  CAS  PubMed  Google Scholar 

  • Birmingham L (1942) Boundaries of differentiation of cephalic imaginal discs in Drosophila. J Exp Zool 91:345–363

    Article  Google Scholar 

  • 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 111:657–665

    CAS  PubMed  Google Scholar 

  • Bras-Pereira C, Bessa J, Casares F (2006) Odd-skipped genes specify the signaling center that triggers retinogenesis in Drosophila. Development 133:4145–4149

    Article  CAS  PubMed  Google Scholar 

  • Bryant PJ (1975) Pattern formation int he imaginal wing discof Drosophila melanogaster: fate map, regeneration and duplication. J Exp Zool 193:49–78

    Article  CAS  PubMed  Google Scholar 

  • Chadwick R, Jones B, Jack T, McGinnis W (1990) Ectopic expression from the Deformed gene triggers a dominant defect in Drosophila adult head development. Dev Biol 141:130–140

    Article  CAS  PubMed  Google Scholar 

  • Chanut F, Heberlein U (1997) Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124:559–567

    CAS  PubMed  Google Scholar 

  • 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 131:3839–3847

    Article  CAS  PubMed  Google Scholar 

  • Chen TY (1929) On the development of imaginal buds in normal and mutant Drosophila melanogaster. J Morph 47:135–199

    Article  Google Scholar 

  • Cho KO, Chern J, Izaddoost S, Choi KW (2000) Novel signaling from the peripodial membrane is essential for eye disc patterning in Drosophila. Cell 103:331–342

    Article  CAS  PubMed  Google Scholar 

  • Chouinard S, Kaufman TC (1991) Control of expression of the homeotic labial (lab) locus of Drosophila melanogaster: evidence for both positive and negative autogenous regulation. Development 113:1267–1280

    CAS  PubMed  Google Scholar 

  • Crampton GC (1942) The external morphology of the Diptera, Vol 47 (State Geological and Natural History Survey of Connecticut: State of Connecticut Public Document)

    Google Scholar 

  • Curtiss J, Mlodzik M (2000) Morphogenetic furrow initiation and progression during eye development in Drosophila: the roles of decapentaplegic, hedgehog and eyes absent. Development 127:1325–1336

    CAS  PubMed  Google Scholar 

  • Deak I (1980) A model linking segmentation, compartmentalization and regeneration in Drosophila development. J Theor Biol 84:477–504

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Benjumea FJ, Cohen B, Cohen SM (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372:175–179

    Article  CAS  PubMed  Google Scholar 

  • Diederich RJ, Pattatucci AM, Kaufman TC (1991) Developmental and evolutionary implications of labial, Deformed and engrailed expression in the Drosophila head. Development 113:273–281

    CAS  PubMed  Google Scholar 

  • Dominguez M, Casares F (2005) Organ specification-growth control connection: new in-sights from the Drosophila eye-antennal disc. Dev Dyn 232:673–684

    Article  CAS  PubMed  Google Scholar 

  • Dominguez M, Hafen E (1997) Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev 11:3254–3264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eassa YE (1953) The development of imaginal buds in the head of Pieris brassicae Linn. (Lepidoptera). Trans R Entomol Soc Lond 104:39–51

    Article  Google Scholar 

  • 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 133:4721–4729

    Article  CAS  PubMed  Google Scholar 

  • Ephrussi B, Beadle GW (1937a) Development of eye colors in Drosophila: production and release of cn substance by the eyes of different eye color mutants. Genetics 22:479–483

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ephrussi B, Beadle GW (1937b) Development of eye colors in Drosophila: transplantation experiments on the interaction of vermilion with other eye colors. Genetics 22:65–75

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferris GF (1950) External morphoogy of the adult. In: Demerec M (ed) Biology of Drosophila. Wiley, New York, pp 368–419

    Google Scholar 

  • Firth LC, Baker NE (2007) Spitz from the retina regulates genes transcribed in the second mitotic wave, peripodial epithelium, glia and plasmatocytes of the Drosophila eye imaginal disc. Dev Biol 307:521–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fristrom D, Frstrom JW (1993) The metamorphic development of the adult epidermis. In: Bate M, Martinez Arias A (eds) The Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 467–516

    Google Scholar 

  • Gibson MC, Lehman DA, Schubiger G (2002) Lumenal transmission of decapentaplegic in Drosophila imaginal discs. Dev Cell 3:451–460

    Article  CAS  PubMed  Google Scholar 

  • Gibson MC, Schubiger G (1999) Hedgehog is required for activation of engrailed during regeneration of fragmented Drosophila imaginal discs. Development 126:1591–1599

    CAS  PubMed  Google Scholar 

  • Gibson MC, Schubiger G (2000) Peripodial cells regulate proliferation and patterning of Drosophila imaginal discs. Cell 103:343–350

    Article  CAS  PubMed  Google Scholar 

  • 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 10:1051–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadorn E (1968) Transdetermination in cells. Sci Amer 219:110–172

    Article  CAS  PubMed  Google Scholar 

  • Hadorn E (1978) Transdetermination. In: Ashburner M, Wright (eds) The genetics and biology of Drosphila, vol 2c. Academic Press, New York, pp 555–617

    Google Scholar 

  • Halder G, Callaerts P, Flister S, Walldorf U, Kloter U, Gegring WJ (1998) Eyeless initiates the expression of both sine oculis and eyes absent during drosophila compound eye development. Development 125:2181–2191

    CAS  PubMed  Google Scholar 

  • Hallsson JH, Haflidadottir BS, Stivers C, Odenwald W, Arnheiter H, Pignoni F, Steingrimsson E (2004) The basic helix-loop-helix leucine zipper transcription factor Mitf is conserved in Drosophila and functions in eye development. Genetics 167:233–241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haynie JL, Bryant PJ (1986) Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster. J Exp Zool 237:293–308

    Article  CAS  PubMed  Google Scholar 

  • 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 125:3741–3751

    CAS  PubMed  Google Scholar 

  • Heberlein U, Borod ER, Chanut FA (1998) Dorsoventral patterning in the Drosophila retina by wingless. Development 125:567–577

    CAS  PubMed  Google Scholar 

  • 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 75:913–926

    Article  CAS  PubMed  Google Scholar 

  • Hursh DA, Stultz BG, Park SY (2016) Jun N-terminal kinase signaling makes a face. Fly 10:195–203

    Article  PubMed  PubMed Central  Google Scholar 

  • Jorgensen EM, Garber RL (1987) Function and misfunction of the two promoters of the Drosophila Antennapedia gene. Genes Dev 1:544–555

    Article  CAS  PubMed  Google Scholar 

  • Jurgens J, Hartenstein V (1993) The terminal regions of the body pattern. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 687–746

    Google Scholar 

  • Kooh PJ, Fehon RG, Muskavitch MA (1993) Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development 117:493–507

    CAS  PubMed  Google Scholar 

  • Kumar JP (2010) Retinal determination the beginning of eye development. Curr Top Dev Biol 93:1–28

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar JP (2011) My what big eyes you have: how the Drosophila retina grows. Dev Neurobiol 71:1133–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar JP (2013) Catching the next wave: patterning of the Drosophila eye by the morphogentic furrow. In: Singh A (ed) Molecular genetics of axial patterning, growth, and disease in the Drosophila eye. Springer, New York, pp 75–97

    Chapter  Google Scholar 

  • Kumar K, Ouweneel WJ, Faber J (1979) Differentiation capacities of the labial imaginal disc of Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 186:51–64

    Article  Google Scholar 

  • Kumar SR, Patel H, Tomlinson A (2015) Wingless mediated apoptosis: How cone cells direct the death of peripheral ommatidia in the developing Drosophila eye. Dev Biol 407:183–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee H, Stultz BG, Hursh DA (2007) The Zic family member, odd-paired, regulates the Drosophila BMP, decapentaplegic, during adult head development. Development 134:1301–1310

    Article  CAS  PubMed  Google Scholar 

  • Legent K, Treisman JE (2008) Wingless signaling in Drosophila eye development. Methods Mol Biol 469:141–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim HY, Tomlinson A (2006) Organization of the peripheral fly eye: the roles of Snail family transcription factors in peripheral retinal apoptosis. Development 133:3529–3537

    Article  CAS  PubMed  Google Scholar 

  • Lim J, Choi KW (2004) Drosophila eye disc margin is a center for organizing long-range planar polarity. Genesis 39:26–37

    Article  PubMed  Google Scholar 

  • 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 121:2279–2289

    CAS  PubMed  Google Scholar 

  • 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 75:927–938

    Article  CAS  PubMed  Google Scholar 

  • Madhaven MM, Schneiderman HA (1977) Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during the larval development of Drosophila melanogaster. Wilhelm Roux Arch Dev Biol 183:269–305

    Article  Google Scholar 

  • Manseau L, Baradaran A, Brower D, Budhu A, Elefant F, Phan H, Philp AV, Yang M, Glover D, Kaiser K et al (1997) GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev Dyn 209:310–322

    Article  CAS  PubMed  Google Scholar 

  • Mardon G, Solomon NM, Rubin GM (1994) Dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120:3473–3486

    CAS  PubMed  Google Scholar 

  • Martinez-Arias A, Ingham PW, Scott MP, Akam ME (1987) The spatial and temporal deployment of Dfd and Scr transcripts throughout development of Drosophila. Development 100:673–683

    CAS  PubMed  Google Scholar 

  • 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 4:2011–2023

    Article  CAS  PubMed  Google Scholar 

  • Mathi SK, Larsen E (1988) Patterns of cell division in imaginal discs of Drosophila. Tissue Cell 20:461–472

    Article  CAS  PubMed  Google Scholar 

  • Maurel-Zaffran C, Treisman JE (2000) Pannier acts upstream of wingless to direct dorsal eye disc development in Drosophila. Development 127:1007–1016

    CAS  PubMed  Google Scholar 

  • McClure KD, Schubiger G (2005) Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs. Development 132:5033–5042

    Article  CAS  PubMed  Google Scholar 

  • Merrill VK, Diederich RJ, Turner FR, Kaufman TC (1989) A genetic and developmental analysis of mutations in labial, a gene necessary for proper head formation in Drosophila melanogaster. Dev Biol 135:376–391

    Article  CAS  PubMed  Google Scholar 

  • Merrill VK, Turner FR, Kaufman TC (1987) A genetic and developmental analysis of mutations in the Deformed locus in Drosophila melanogaster. Dev Biol 122:379–395

    Article  CAS  PubMed  Google Scholar 

  • Milner MJ (1977) The eversion and differentiation of Drosophila melanogaster leg and wing imaginal discs cultured in vitro with an optimal concentration of beta-ecdysone. J Embryol Exp Morphol 37:105–117

    CAS  PubMed  Google Scholar 

  • Milner MJ, Bleasby AJ, Kelly SL (1984a) The role of the peripodial membrane of leg and wing imaginal discs of Drosophila melanogaster during evagination and differentiation in vitro. Wilhelm Roux’s Arch Dev Biol 193:180–186

    Article  Google Scholar 

  • Milner MJ, Bleasby AJ, Pyott A (1983) The role of the peripodial membrane in the morphogenesis fo the eye-antennal disc of Drosophila melanogaster. Wilhelm Rouxs Arch Dev Biol 192:164–170

    Article  CAS  Google Scholar 

  • Milner MJ, Bleasby AJ, Pyott A (1984b) Cell interactions during the fusionin vitro of Drosophila eye-antennal imaginal discs. Wilhelm Roux’s Arch Dev Biol 193:406–413

    Article  Google Scholar 

  • Milner MJ, Haynie JL (1979) Fusion of Drosophila eye-antennal imaginal discs during differentiation in vitro. Wilhelm Roux’s Arch Dev Biol 185:363–370

    Article  Google Scholar 

  • Morata G, Lawrence PA (1979) Development of the eye-antenna imaginal disc of Drosophila. Dev Biol 70:355–371

    Article  CAS  PubMed  Google Scholar 

  • Nardi JB, Norby SW, Magee-Adams SM (1987) Cellular events within peripodial epithelia that accompany evagination of Manduca wing discs: conversion of cuboidal epithelia to columnar epithelia. Dev Biol 119:20–26

    Article  Google Scholar 

  • Nusinow D, Greenberg L, Hatini V (2008) Reciprocal roles for bowl and lines in specifying the peripodial epithelium and the disc proper of the Drosophila wing primordium. Development 135:3031–3041

    Article  CAS  PubMed  Google Scholar 

  • Oros SM, Tare M, Kango-Singh M, Singh A (2010) Dorsal eye selector pannier (pnr) suppresses the eye fate to define dorsal margin of the Drosophila eye. Dev Biol 346:258–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouweneel WJ (1970) Normal and abnormal determination in the imaginal discs of Drosophila, with special reference to the eye discs. Acta Embryol Exp 1:95–119

    CAS  Google Scholar 

  • Pallavi SK, Shashidhara LS (2003) Egfr/Ras pathway mediates interactions between peripodial and disc proper cells in Drosophila wing discs. Development 130:4931–4941

    Article  CAS  PubMed  Google Scholar 

  • Pallavi SK, Shashidhara LS (2005) Signaling interactions between squamous and columnar epithelia of the Drosophila wing disc. J Cell Sci 118:3363–3370

    Article  CAS  PubMed  Google Scholar 

  • Park SY, Stultz BG, Hursh DA (2015) Dual role of Jun N-terminal kinase activity in bone morphogenetic protein-mediated Drosophila ventral head development. Genetics 201:1411–1426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pastor-Pareja JC, Grawe F, Martin-Blanco E, Garcia-Bellido A (2004) Invasive cell behavior during Drosophila imaginal disc eversion is mediated by the JNK signaling cascade. Dev Cell 7:387–399

    Article  CAS  PubMed  Google Scholar 

  • 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 132:2771–2782

    Article  CAS  PubMed  Google Scholar 

  • Pereira PS, Pinho S, Johnson K, Couso JP, Casares F (2006) A 3′ cis-regulatory region controls wingless expression in the Drosophila eye and leg primordia. Dev Dyn 235:225–234

    Article  CAS  PubMed  Google Scholar 

  • Pignoni F, Hu B, Zavitz KH, Xiao J, Garrity PA, Zipursky SL (1997) The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development. Cell 91:881–891

    Article  CAS  PubMed  Google Scholar 

  • Pilkington RW (1942) Facet mutants of Drosophila. Proc Zool Soc Lond Ser A 3:199–222

    Google Scholar 

  • Poodry CA, Schneiderman HA (1970) The ultrastructure of the developing leg of Drosophila melanogaster. Wilhelm Roux’ Archiv fur Entwicklungsmechanik der Organismen 166:1–44

    Article  PubMed  Google Scholar 

  • Ramirez-Weber FA, Kornberg TB (1999) Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97:599–607

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Weber FA, Kornberg TB (2000) Signaling reaches to new dimensions in Drosophila imaginal discs. Cell 103:189–192

    Article  CAS  PubMed  Google Scholar 

  • Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240

    Article  CAS  PubMed  Google Scholar 

  • Reinhardt CA, Hodgkin NM, Bryant PJ (1977) Wound healing in the imaginal discs of Drosophila. I. Scanning electron microscopy of normal and healing wing discs. Dev Biol 60:238–257

    Article  CAS  PubMed  Google Scholar 

  • Richard M, Bauer R, Tavosanis G, Hoch M (2017) The gap junction protein Innexin3 is required for eye disc growth in Drosophila. Dev Biol 425:191–207

    Article  CAS  PubMed  Google Scholar 

  • Richard M, Hoch M (2015) Drosophila eye size is determined by Innexin 2-dependent Decapentaplegic signalling. Dev Biol 408:26–40

    Article  CAS  PubMed  Google Scholar 

  • Roy S, Hsiung F, Kornberg TB (2011) Specificity of Drosophila cytonemes for distinct signaling pathways. Science 332:354–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Royet J, Finkelstein R (1996) Hedgehog, wingless and othrodenticle specify adult head development in Drosophila. Development 122:1849–1858

    CAS  PubMed  Google Scholar 

  • Royet J, Finkelstein R (1997) Establishing primordia in the Drosophila eye-antennal imaginal disc: the role of decapentaplegic, wingless and hedgehog. Development 124:4793–4800

    CAS  PubMed  Google Scholar 

  • Segal D, Gelbart WM (1985) Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics 109:119–143

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sen A, Stultz BG, Lee H, Hursh DA (2010) Odd paired transcriptional activation of decapentaplegic in the Drosophila eye/antennal disc is cell autonomous but indirect. Dev Biol 343:167–177

    Article  CAS  PubMed  Google Scholar 

  • Silver SJ, Rebay I (2005) Signaling circuitries in development: insights from the retinal determination gene network. Development 132:3–13

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Tare M, Puli OR, Kango-Singh M (2012) A glimpse into dorso-ventral patterning of the Drosophila eye. Dev Dyn 241:69–84

    Article  PubMed  Google Scholar 

  • Singh J, Mlodzik M (2012) Planar cell polarity signaling: coordination of cellular orientation across tissues. Wiley Interdiscip Rev Dev Biol 1:479–499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snodgrass RE (1935) The principles of insect morphology. McGraw-Hill, New York

    Google Scholar 

  • Spencer FA, Hoffmann FM, Gelbart WM (1982) Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28:451–461

    Article  CAS  PubMed  Google Scholar 

  • Sprey TE, Oldenhave M (1974) A detailed organ map of the wing disk of Calliphora erythrocephala. Neth J Zool 24:291–310

    Article  Google Scholar 

  • Struhl G (1981) A blastoderm fate map of compartments and segments of the Drosophila head. Dev Biol 84:386–396

    Article  CAS  PubMed  Google Scholar 

  • Stultz BG, Lee H, Ramon K, Hursh DA (2006) Decapentaplegic head capsule mutations disrupt novel peripodial expression controlling the morphogenesis of the Drosophila ventral head. Dev Biol 296:329–339

    Article  CAS  PubMed  Google Scholar 

  • Stultz BG, Park SY, Mortin MA, Kennison JA, Hursh DA (2012) Hox proteins coordinate peripodial decapentaplegic expression to direct adult head morphogenesis in Drosophila. Dev Biol 369:362–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stultz BG, Ray RP, Hursh DA (2005) Analysis of the shortvein cis-regulatory region of the decapentaplegic gene of Drosophila melanogaster. Genesis 42:181–192

    Article  CAS  PubMed  Google Scholar 

  • Sturtevant AH (1929) The claret mutant type of Drosophila simulans: a study of chromosome elimination and cell lineage. Z Wiss Zool Abt A 135:323–356

    Google Scholar 

  • Theisen H, Haerry TE, O'Connor MB, Marsh JL (1996) Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. Development 122:3939–3948

    CAS  PubMed  Google Scholar 

  • Tomlinson A (2003) Patterning the peripheral retina of the fly: decoding a gradient. Dev Cell 5:799–809

    Article  CAS  PubMed  Google Scholar 

  • Treisman JE, Rubin GM (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121:3519–3527

    CAS  PubMed  Google Scholar 

  • Tsai YC, Sun YH (2004) Long-range effect of upd, a ligand for Jak/STAT pathway, on cell cycle in Drosophila eye development. Genesis 39:141–153

    Article  CAS  PubMed  Google Scholar 

  • 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 306:760–771

    Article  CAS  PubMed  Google Scholar 

  • Usui K, Simpson P (2000) Cellular basis of the dynamic behavior of the imaginal thoracic discs during Drosophila metamorphosis. Dev Biol 225:13–25

    Article  CAS  PubMed  Google Scholar 

  • Voas MG, Rebay I (2004) Signal integration during development: Insights from the Drosophila eye. Dev Dyn 229:162–175

    Article  CAS  PubMed  Google Scholar 

  • Vogt M (1946) Zur labilen Determination der Imagin-alscheiben von Drosophila. I. Verhalten verschieden-altriger Imaginalanlagen bei operativer Defektsetzung. Biol Zbl 65:223–238

    Google Scholar 

  • Waddington CH (1941) The genetic control of wing development in Drosophila. J Genet 41:75–139

    Article  Google Scholar 

  • Wieschaus E, Gehring W (1976) Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Dev Biol 50:249–263

    Article  CAS  PubMed  Google Scholar 

  • Wirz J, Fessler LI, Gehring WJ (1986) Localization of the Antennapedia protein in Drosophila embryos and imaginal discs. EMBO J 5:3327–3334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, NY, pp 1277–1326

    Google Scholar 

  • Younossi-Hartenstein A, Tepass U, Hartenstein V (1993) Embryonic origin of the imaginal discs of the head of Drosophila melanogaster. Roux’s Arch Dev Biol 203:60–73

    Article  Google Scholar 

  • Zeitlinger J, Bohmann D (1999) Thorax closure in Drosophila: involvement of Fos and the JNK pathway. Development 126:3947–3956

    CAS  PubMed  Google Scholar 

  • Zhang T, Zhou Q, Pignoni F (2011) Yki/YAP, Sd/TEAD and Hth/MEIS control tissue specification in the Drosophila eye disc epithelium. PLoS One 6:e22278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We first thank every researcher that has worked on the peripodial epithelia of imaginal discs over the last century—Peter Bryant, John Haynie, Martin Milner, and Gerold Schubiger deserve special mention. We would also like to thank Alison Ordway and Alison Smith for their comments on an earlier draft of this chapter. This work is supported by a grant from the National Eye Institute (R01 EY014863) and funds from the Department of Biology, the College of Arts and Sciences, and the Office of the Vice Provost for Research at Indiana University to Justin P. Kumar.

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  1. Department of Biology, Indiana University, Bloomington, IN, USA

    Brandon P. Weasner, Bonnie M. Weasner & Justin P. Kumar

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  1. Brandon P. Weasner
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  2. Bonnie M. Weasner
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  3. Justin P. Kumar
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Correspondence to Justin P. Kumar .

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  1. Department of Biology, University of Dayton, Dayton, OH, USA

    Amit Singh

  2. Department of Biology Office: SC303C, University of Dayton, Dayton, OH, USA

    Madhuri Kango-Singh

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Weasner, B.P., Weasner, B.M., Kumar, J.P. (2020). Ghost in the Machine: The Peripodial Epithelium. In: Singh, A., Kango-Singh, M. (eds) Molecular Genetics of Axial Patterning, Growth and Disease in Drosophila Eye. Springer, Cham. https://doi.org/10.1007/978-3-030-42246-2_4

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