Skip to main content

Adherens Junctions and Cadherins in Drosophila Development

  • Chapter
  • First Online:
Adherens Junctions: from Molecular Mechanisms to Tissue Development and Disease

Part of the book series: Subcellular Biochemistry ((SCBI,volume 60))

Abstract

Drosophila represents a paradigm for the analysis of the cellular, molecular and genetic mechanisms of development and is an ideal model system to study the contribution of Adherens Junctions (AJs) and their major components, cadherins, to morphogenesis. The combination of different techniques and approaches has allowed researchers to identify the requirements of these epithelial junctions in vivo in the context of a whole organism. The functional analysis of mutants for AJ core components, particularly for Drosophila DE-cadherin, has shown that AJs play critical roles in virtually all stages of development. For instance, AJs maintain tissue integrity while allowing the remodelling and homeostasis of many tissues. They control cell shape, contribute to cell polarity, facilitate cell–cell recognition during cell sorting, orient cell divisions, or regulate cell rearrangements, among other activities. Remarkably, these activities require a very fine control of the organisation and turnover of AJs during development. In addition, AJs engage in diverse and complex interactions with the cytoskeleton, signalling networks, intracellular trafficking machinery or polarity cues to perform these functions. Here, by summarising the requirements of AJs and cadherins during Drosophila morphogenesis, we illustrate the capital contribution of this model system to our knowledge of the mechanisms and biology of AJs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Bao S, Cagan R (2005) Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell 8:925–935

    PubMed  CAS  Google Scholar 

  • Bastock R, Johnston D St (2008) Drosophila oogenesis. Curr Biol 18:R1082–R1087

    PubMed  CAS  Google Scholar 

  • Baum B, Georgiou M (2011) Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 192:907–917

    PubMed  CAS  Google Scholar 

  • Beitel GJ, Krasnow MA (2000) Genetic control of epithelial tube size in the Drosophila tracheal system. Development 127:3271–3282

    PubMed  CAS  Google Scholar 

  • Bertet C, Sulak L, Lecuit T (2004) Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429:667–671

    PubMed  CAS  Google Scholar 

  • Bilder D, Schober M, Perrimon N (2003) Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat Cell Biol 5:53–58

    PubMed  CAS  Google Scholar 

  • Blanchard GB, Murugesu S, Adams RJ, Martinez-Arias A, Gorfinkiel N (2010) Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 137:2743–2752

    PubMed  CAS  Google Scholar 

  • Blankenship JT, Backovic ST, Sanny JS, Weitz O, Zallen JA (2006) Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev Cell 11:459–470

    PubMed  CAS  Google Scholar 

  • Bloor JW, Kiehart DP (2002) Drosophila RhoA regulates the cytoskeleton and cell-cell adhesion in the developing epidermis. Development 129:3173–3183

    PubMed  CAS  Google Scholar 

  • Boettner B, Harjes P, Ishimaru S, Heke M, Fan HQ, Qin Y, Van Aelst L, Gaul U (2003) The AF-6 homolog canoe acts as a Rap1 effector during dorsal closure of the Drosophila embryo. Genetics 165:159–169

    PubMed  CAS  Google Scholar 

  • Boyle M, DiNardo S (1995) Specification, migration and assembly of the somatic cells of the Drosophila gonad. Development 121:1815–1825

    PubMed  CAS  Google Scholar 

  • Boyle M, Bonini N, DiNardo S (1997) Expression and function of clift in the development of somatic gonadal precursors within the Drosophila mesoderm. Development 124:971–982

    PubMed  CAS  Google Scholar 

  • 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 300:710–721

    PubMed  CAS  Google Scholar 

  • Butler LC, Blanchard GB, Kabla AJ, Lawrence NJ, Welchman DP, Mahadevan L, Adams RJ, Sanson B (2009) Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nat Cell Biol 11:859–864

    PubMed  CAS  Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster, 2nd edn. Springer-Verlag, Berlin

    Google Scholar 

  • Cavey M, Lecuit T (2009) Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harb Perspect Biol 1:a002998

    PubMed  Google Scholar 

  • Cavey M, Rauzi M, Lenne PF, Lecuit T (2008) A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453:751–756

    PubMed  CAS  Google Scholar 

  • Cela C, Llimargas M (2006) Egfr is essential for maintaining epithelial integrity during tracheal remodelling in Drosophila. Development 133:3115–3125

    PubMed  CAS  Google Scholar 

  • Chihara T, Kato K, Taniguchi M, Ng J, Hayashi S (2003) Rac promotes epithelial cell rearrangement during tracheal tubulogenesis in Drosophila. Development 130:1419–1428

    PubMed  CAS  Google Scholar 

  • Choi W, Jung KC, Nelson KS, Bhat MA, Beitel GJ, Peifer M, Fanning AS (2011) The single Drosophila ZO-1 protein Polychaetoid regulates embryonic morphogenesis in coordination with Canoe/afadin and Enabled. Mol Biol Cell 22:2010–2030

    PubMed  CAS  Google Scholar 

  • Cox RT, Kirkpatrick C, Peifer M (1996) Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis. J Cell Biol 134:133–148

    PubMed  CAS  Google Scholar 

  • Dansereau DA, Lasko P (2008) The development of germline stem cells in Drosophila. Methods Mol Biol 450:3–26

    PubMed  CAS  Google Scholar 

  • Dawes-Hoang RE, Parmar KM, Christiansen AE Phelps CB, Brand AH, Wieschaus EF (2005) folded gastrulation, cell shape change and the control of myosin localization. Development 132:4165–4178

    PubMed  CAS  Google Scholar 

  • DeGennaro M, Hurd TR, Siekhaus DE, Biteau B, Jasper H, Lehmann R (2011) Peroxiredoxin stabilization of DE-cadherin promotes primordial germ cell adhesion. Dev Cell 20:233–243

    PubMed  CAS  Google Scholar 

  • Doe CQ (1992) Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116:855–863

    PubMed  CAS  Google Scholar 

  • Dumstrei K, Wang F, Hartenstein V (2003) Role of DE-cadherin in neuroblast proliferation, neural morphogenesis, and axon tract formation in Drosophila larval brain development. J Neurosci 23:3325–3335

    PubMed  CAS  Google Scholar 

  • Eichenberger-Glinz S (1979) Intercellular junctions during development and in tissue cultures of Drosophila melanogaster: an electron-microscopic study. Wilhelm Roux’s Arch Dev Biol 186:333–349

    Google Scholar 

  • Fiehler RW, Wolff T (2007) Drosophila Myosin II, Zipper, is essential for ommatidial rotation. Dev Biol 310:348–362

    PubMed  CAS  Google Scholar 

  • Fox DT, Homem CC, Myster SH, Wang F, Bain EE, Peifer M (2005) Rho1 regulates Drosophila adherens junctions independently of p120ctn. Development 132:4819–4831

    PubMed  CAS  Google Scholar 

  • Franke JD, Montague RA, Kiehart DP (2005) Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr Biol 15:2208–2221

    PubMed  CAS  Google Scholar 

  • Fulga TA, Rorth P (2002) Invasive cell migration is initiated by guided growth of long cellular extensions. Nat Cell Biol 4:715–719

    PubMed  CAS  Google Scholar 

  • Fung S, Wang F, Spindler SR, Hartenstein V (2009) Drosophila E-cadherin and its binding partner Armadillo/ beta-catenin are required for axonal pathway choices in the developing larval brain. Dev Biol 332:371–382

    PubMed  CAS  Google Scholar 

  • Geisbrecht ER, Montell DJ (2002) Myosin VI is required for E-cadherin-mediated border cell migration. Nat Cell Biol 4:616–620

    PubMed  CAS  Google Scholar 

  • Georgiou M, Marinari E, Burden J, Baum B (2008) Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol 18:1631–1638

    PubMed  CAS  Google Scholar 

  • Ghabrial A, Luschnig S, Metzstein MM, Krasnow MA (2003) Branching morphogenesis of the Drosophila tracheal system. Annu Rev Cell Dev Biol 19:623–647

    PubMed  CAS  Google Scholar 

  • Gho M, Schweisguth F (1998) Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature 393:178–181

    PubMed  CAS  Google Scholar 

  • Gho M, Bellaiche Y, Schweisguth F (1999) Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development 126:3573–3584

    PubMed  CAS  Google Scholar 

  • Godt D, Tepass U (1998) Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395:387–391

    PubMed  CAS  Google Scholar 

  • Gonzalez-Reyes A, Johnston D St (1998) The Drosophila AP axis is polarised by the cadherin-mediated positioning of the oocyte. Development 125:3635–3644

    PubMed  CAS  Google Scholar 

  • Gorfinkiel N, Arias AM (2007) Requirements for adherens junction components in the interaction between epithelial tissues during dorsal closure in Drosophila. J Cell Sci 120:3289–3298

    PubMed  CAS  Google Scholar 

  • Gorfinkiel N, Blanchard GB, Adams RJ, Martinez Arias A (2009) Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development 136:1889–1898

    PubMed  CAS  Google Scholar 

  • Grammont M (2007) Adherens junction remodeling by the Notch pathway in Drosophila melanogaster oogenesis. J Cell Biol 177:139–150

    PubMed  CAS  Google Scholar 

  • Grawe F, Wodarz A, Lee B, Knust E, Skaer H (1996) The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions. Development 122:951–959

    PubMed  CAS  Google Scholar 

  • Grzeschik NA, Knust E (2005) IrreC/rst-mediated cell sorting during Drosophila pupal eye development depends on proper localisation of DE-cadherin. Development 132:2035–2045

    PubMed  CAS  Google Scholar 

  • Haag TA, Haag NP, Lekven AC, Hartenstein V (1999) The role of cell adhesion molecules in Drosophila heart morphogenesis: faint sausage, shotgun/DE-cadherin, and laminin A are required for discrete stages in heart development. Dev Biol 208:56–69

    PubMed  CAS  Google Scholar 

  • Hackney JF, Pucci C, Naes E, Dobens L (2007) Ras signaling modulates activity of the ecdysone receptor EcR during cell migration in the Drosophila ovary. Dev Dyn 236:1213–1226

    PubMed  CAS  Google Scholar 

  • Harris KP, Tepass U (2008) Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. J Cell Biol 183:1129–1143

    PubMed  CAS  Google Scholar 

  • Harris TJ, Peifer M (2004) Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila. J Cell Biol 167:135–147

    PubMed  CAS  Google Scholar 

  • Harris TJ, Peifer M (2005) The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila. J Cell Biol 170:813–823

    PubMed  CAS  Google Scholar 

  • Harris TJ, Sawyer JK, Peifer M (2009) How the cytoskeleton helps build the embryonic body plan: models of morphogenesis from Drosophila. Curr Top Dev Biol 89:55–85

    PubMed  CAS  Google Scholar 

  • Hartenstein V, Younossi-Hartenstein A, Lekven A (1994) Delamination and division in the Drosophila neurectoderm: spatiotemporal pattern, cytoskeletal dynamics, and common control by neurogenic and segment polarity genes. Dev Biol 165:480–499

    PubMed  CAS  Google Scholar 

  • Hayashi T, Carthew RW (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431:647–652

    PubMed  CAS  Google Scholar 

  • Heisenberg CP (2009) Dorsal closure in Drosophila: cells cannot get out of the tight spot. Bioessays 31:1284–1287

    PubMed  CAS  Google Scholar 

  • Homem CC, Peifer M (2008) Diaphanous regulates myosin and adherens junctions to control cell contractility and protrusive behavior during morphogenesis. Development 135:1005–1018

    PubMed  CAS  Google Scholar 

  • Horne-Badovinac S, Bilder D (2005) Mass transit: epithelial morphogenesis in the Drosophila egg chamber. Dev Dyn 232:559–574

    PubMed  CAS  Google Scholar 

  • Hummel T, Zipursky SL (2004) Afferent induction of olfactory glomeruli requires N-cadherin. Neuron. 42:77–88

    PubMed  CAS  Google Scholar 

  • Hunter C, Wieschaus E (2000) Regulated expression of nullo is required for the formation of distinct apical and basal adherens junctions in the Drosophila blastoderm. J Cell Biol 150:391–401

    PubMed  CAS  Google Scholar 

  • Huynh JR, Johnston D St (2004) The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 14:R438–R449

    PubMed  CAS  Google Scholar 

  • Inaba M, Yuan H, Salzmann V, Fuller MT, Yamashita YM (2010) E-cadherin is required for centrosome and spindle orientation in Drosophila male germline stem cells. PLoS One 5:e12473

    PubMed  Google Scholar 

  • Irvine KD, Wieschaus E (1994) Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development 120:827–841

    PubMed  CAS  Google Scholar 

  • Iwai Y, Usui T, Hirano S, Steward R, Takeichi M, Uemura T (1997) Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron. 19:77–89

    PubMed  CAS  Google Scholar 

  • Iwai Y, Hirota Y, Ozaki K, Okano H, Takeichi M, Uemura T (2002) DN-cadherin is required for spatial arrangement of nerve terminals and ultrastructural organization of synapses. Mol Cell Neurosci. 19:375–388

    PubMed  CAS  Google Scholar 

  • Izaddoost S, Nam SC, Bhat MA, Bellen HJ, Choi KW (2002) Drosophila Crumbs is a positional cue in photoreceptor adherens junctions and rhabdomeres. Nature 416:178–183

    PubMed  CAS  Google Scholar 

  • Jacinto A, Wood W, Balayo T, Turmaine M, Martinez-Arias A , Martin P (2000) Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr Biol 10:1420–1426

    PubMed  CAS  Google Scholar 

  • Jacinto A, Wood W, Woolner S, Hiley C, Turner L, Wilson C, Martinez-Arias A, Martin P (2002a) Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr Biol 12:1245–1250

    CAS  Google Scholar 

  • Jacinto A, Woolner S, Martin P (2002b) Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev Cell 3:9–19

    CAS  Google Scholar 

  • Jenkins AB, McCaffery JM, Van Doren M (2003) Drosophila E-cadherin is essential for proper germ cell-soma interaction during gonad morphogenesis. Development 130:4417–4426

    PubMed  CAS  Google Scholar 

  • Jiang L, Rogers SL, Crews ST (2007) The Drosophila Dead end Arf-like3 GTPase controls vesicle trafficking during tracheal fusion cell morphogenesis. Dev Biol 311:487–499

    PubMed  CAS  Google Scholar 

  • Jung AC, Ribeiro C, Michaut L, Certa U, Affolter M (2006) Polychaetoid/ZO-1 is required for cell specification and rearrangement during Drosophila tracheal morphogenesis. Curr Biol 16:1224–1231

    PubMed  CAS  Google Scholar 

  • Kakihara K, Shinmyozu K, Kato K, Wada H, Hayashi S (2008) Conversion of plasma membrane topology during epithelial tube connection requires Arf-like 3 small GTPase in Drosophila. Mech Dev 125:325–336

    PubMed  CAS  Google Scholar 

  • Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149:471–490

    PubMed  CAS  Google Scholar 

  • Kolsch V, Seher T, Fernandez-Ballester GJ, Serrano L, Leptin M. (2007) Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 315:384–386

    PubMed  Google Scholar 

  • Krahn MP, Klopfenstein DR, Fischer N, Wodarz A (2010) Membrane targeting of Bazooka/PAR-3 is mediated by direct binding to phosphoinositide lipids. Curr Biol 20:636–642

    PubMed  CAS  Google Scholar 

  • Kunwar PS, Sano H, Renault AD, Barbosa V, Fuse N, Lehmann R (2008) Tre1 GPCR initiates germ cell transepithelial migration by regulating Drosophila melanogaster E-cadherin. J Cell Biol 183:157–168

    PubMed  CAS  Google Scholar 

  • Laplante C, Nilson LA (2006) Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila. Development 133:3255–3264

    PubMed  CAS  Google Scholar 

  • Laplante C, Nilson LA (2011) Asymmetric distribution of Echinoid defines the epidermal leading edge during Drosophila dorsal closure. J Cell Biol 192:335–348

    PubMed  CAS  Google Scholar 

  • Le Borgne R, Bellaiche Y, Schweisguth F (2002) Drosophila E-cadherin regulates the orientation of asymmetric cell division in the sensory organ lineage. Curr Biol 12:95–104

    PubMed  CAS  Google Scholar 

  • Lecuit T (2004) Junctions and vesicular trafficking during Drosophila cellularization. J Cell Sci 117:3427–3433

    PubMed  CAS  Google Scholar 

  • Lee CH, Herman T, Clandinin TR, Lee R, Zipursky SL (2001) N-cadherin regulates target specificity in the Drosophila visual system. Neuron 30:437–450

    PubMed  CAS  Google Scholar 

  • Lee M, Lee S, Zadeh AD, Kolodziej PA (2003) Distinct sites in E-cadherin regulate different steps in Drosophila tracheal tube fusion. Development 130:5989–5999

    PubMed  CAS  Google Scholar 

  • Lee S, Kolodziej PA (2002) The plakin Short Stop and the RhoA GTPase are required for E-cadherin-dependent apical surface remodeling during tracheal tube fusion. Development 129:1509–1520

    PubMed  CAS  Google Scholar 

  • Leibfried A, Fricke R, Morgan MJ, Bogdan S, Bellaiche Y (2008) Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr Biol 18:1639–1648

    PubMed  CAS  Google Scholar 

  • Leptin M, Grunewald B (1990) Cell shape changes during gastrulation in Drosophila. Development 110:73–84

    PubMed  CAS  Google Scholar 

  • Levayer R, Pelissier-Monier A, Lecuit T (2011) Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat Cell Biol 13:734

    CAS  Google Scholar 

  • Levine B, Hackney JF, Bergen A, Dobens L, Truesdale 3rd A, Dobens L (2010) Opposing interactions between Drosophila cut and the C/EBP encoded by slow border cells direct apical constriction and epithelial invagination. Dev Biol 344:196–209

    PubMed  CAS  Google Scholar 

  • Li MA, Alls JD, Avancini RM, Koo K, Godt D (2003) The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat Cell Biol 5:994–1000

    PubMed  CAS  Google Scholar 

  • Lin HP, Chen HM, Wei SY, Chen LY, Chang LH, Sun YJ, Huang SY, Hsu JC (2007) Cell adhesion molecule Echinoid associates with unconventional myosin VI/Jaguar motor to regulate cell morphology during dorsal closure in Drosophila. Dev Biol 311:423–433

    PubMed  CAS  Google Scholar 

  • Llimargas M, Casanova J (2010) Apical constriction and invagination: a very self-reliant couple. Dev Biol 344:4–6

    PubMed  CAS  Google Scholar 

  • Lu B, Roegiers F, Jan LY, Jan YN (2001) Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature 409:522–525

    PubMed  CAS  Google Scholar 

  • Maeda K, Takemura M, Umemori M, Adachi-Yamada T (2008) E-cadherin prolongs the moment for interaction between intestinal stem cell and its progenitor cell to ensure Notch signaling in adult Drosophila midgut. Genes Cells 13:1219–1227

    PubMed  CAS  Google Scholar 

  • Manning G, Krasnow MA (1993) Development of the Drosophila tracheal system. In: Bate M, Martínez-Arias A (eds) The development of Drosophila melanogaster, Vol I. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 609–685

    Google Scholar 

  • Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus EF (2010) Integration of contractile forces during tissue invagination. J Cell Biol 188:735–749

    PubMed  CAS  Google Scholar 

  • Mathews WR, Ong D, Milutinovich AB, Van Doren M (2006) Zinc transport activity of Fear of Intimacy is essential for proper gonad morphogenesis and DE-cadherin expression. Development 133:1143–1153

    PubMed  CAS  Google Scholar 

  • Matsuo T, Takahashi K, Suzuki E, Yamamoto D (1999) The Canoe protein is necessary in adherens junctions for development of ommatidial architecture in the Drosophila compound eye. Cell Tissue Res 298:397–404

    PubMed  CAS  Google Scholar 

  • Mazumdar A, Mazumdar M (2002) How one becomes many: blastoderm cellularization in Drosophila melanogaster. Bioessays 24:1012–1022

    PubMed  CAS  Google Scholar 

  • McCrea PD, Turck CW, Gumbiner B (1991) A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 254:1359–1361

    PubMed  CAS  Google Scholar 

  • McGill MA, McKinley RF, Harris TJ (2009) Independent cadherin-catenin and Bazooka clusters interact to assemble adherens junctions. J Cell Biol 185:787–796

    PubMed  CAS  Google Scholar 

  • Medina E, Williams J, Klipfell E, Zarnescu D, Thomas G, Le Bivic A (2002) Crumbs interacts with moesin and beta(Heavy)-spectrin in the apical membrane skeleton of Drosophila. J Cell Biol 158:941–951

    PubMed  CAS  Google Scholar 

  • Medioni C, Astier M, Zmojdzian M , Jagla K, Semeriva M (2008) Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation. J Cell Biol 182:249–261

    PubMed  CAS  Google Scholar 

  • Melani M, Simpson KJ, Brugge JS, Montell D (2008) Regulation of cell adhesion and collective cell migration by hindsight and its human homolog RREB1. Curr Biol 18:532–537

    PubMed  CAS  Google Scholar 

  • Millo H, Leaper K, Lazou V, Bownes M (2004) Myosin VI plays a role in cell-cell adhesion during epithelial morphogenesis. Mech Dev 121:1335–1351

    PubMed  CAS  Google Scholar 

  • Mirkovic I, Mlodzik M (2006) Cooperative activities of drosophila DE-cadherin and DN-cadherin regulate the cell motility process of ommatidial rotation. Development 133:3283–3293

    PubMed  CAS  Google Scholar 

  • Mlodzik M (1999) Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and cross-talk. EMBO J 18:6873–6879

    PubMed  CAS  Google Scholar 

  • Montell DJ (2003) Border-cell migration: the race is on. Nat Rev Mol Cell Biol 4:13–24

    PubMed  CAS  Google Scholar 

  • Montell DJ (2006) The social lives of migrating cells in Drosophila. Curr Opin Genet Dev 16:374–383

    PubMed  CAS  Google Scholar 

  • Murray MJ, Davidson CM, Hayward NM, Brand AH (2006) The Fes/Fer non-receptor tyrosine kinase cooperates with Src42 A to regulate dorsal closure in Drosophila. Development 133:3063–3073

    PubMed  CAS  Google Scholar 

  • Niewiadomska P, Godt D, Tepass U (1999) DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J Cell Biol 144:533–547

    PubMed  CAS  Google Scholar 

  • O’Keefe DD, Prober DA, Moyle PS, Rickoll WL, Edgar BA (2007) Egfr/Ras signaling regulates DE-cadherin/Shotgun localization to control vein morphogenesis in the Drosophila wing. Dev Biol 311:25–39

    PubMed  Google Scholar 

  • Oda H, Tsukita S (1999) Dynamic features of adherens junctions during Drosophila embryonic epithelial morphogenesis revealed by a Dalpha-catenin-GFP fusion protein. Dev Genes Evol 209:218–225

    PubMed  CAS  Google Scholar 

  • Oda H, Uemura T, Shiomi K, Nagafuchi A, Tsukita S, Takeichi M (1993) Identification of a Drosophila homologue of alpha-catenin and its association with the armadillo protein. J Cell Biol 121:1133–1140

    PubMed  CAS  Google Scholar 

  • Oda H, Uemura T, Harada Y, Iwai Y, Takeichi M (1994) A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion. Dev Biol 165:716–726

    PubMed  CAS  Google Scholar 

  • Oda H, Uemura T, Takeichi M (1997) Phenotypic analysis of null mutants for DE-cadherin and Armadillo in Drosophila ovaries reveals distinct aspects of their functions in cell adhesion and cytoskeletal organization. Genes Cells 2:29–40

    PubMed  CAS  Google Scholar 

  • Oda H, Tsukita S, Takeichi M (1998) Dynamic behavior of the cadherin-based cell-cell adhesion system during Drosophila gastrulation. Dev Biol 203:435–450

    PubMed  CAS  Google Scholar 

  • Ohlstein B, Spradling A (2007) Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 315:988–992

    PubMed  CAS  Google Scholar 

  • Pacquelet A, Rorth P (2005) Regulatory mechanisms required for DE-cadherin function in cell migration and other types of adhesion. J Cell Biol 170:803–812

    PubMed  CAS  Google Scholar 

  • Peifer M (1993) The product of the Drosophila segment polarity gene armadillo is part of a multi-protein complex resembling the vertebrate adherens junction. J Cell Sci 105(Pt 4):993–1000

    PubMed  CAS  Google Scholar 

  • Peifer M, Wieschaus E (1990) The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell 63:1167–1176

    PubMed  CAS  Google Scholar 

  • Peifer M, Orsulic S, Sweeton D, Wieschaus E (1993) A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development 118:1191–207

    PubMed  CAS  Google Scholar 

  • Pellikka M, Tanentzapf G, Pinto M, Smith C, McGlade CJ, Ready DF, Tepass U (2002) Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416:143–149

    PubMed  CAS  Google Scholar 

  • Pilot F, Philippe JM, Lemmers C, Lecuit T (2006) Spatial control of actin organization at adherens junctions by a synaptotagmin-like protein Btsz. Nature 442:580–584

    PubMed  CAS  Google Scholar 

  • Pirraglia C, Walters J, Myat MM (2010) Pak1 control of E-cadherin endocytosis regulates salivary gland lumen size and shape. Development 137:4177–4189

    PubMed  CAS  Google Scholar 

  • Poodry CA, Schneiderman HA (1970) The ultrastructure of the developing leg of Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 166:1–44

    Google Scholar 

  • Prakash S, Caldwell JC, Eberl DF, Clandinin TR (2005) Drosophila N-cadherin mediates an attractive interaction between photoreceptor axons and their targets. Nat Neurosci 8:443–450

    PubMed  CAS  Google Scholar 

  • Rauzi M, Lenne PF, Lecuit T (2010) Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468:1110–1114

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rhyu M.S, Jan LY, Jan YN (1994) Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76:477–491

    PubMed  CAS  Google Scholar 

  • Ribeiro C, Neumann M, Affolter M (2004) Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr Biol 14:2197–2207

    PubMed  CAS  Google Scholar 

  • Roegiers F, Younger-Shepherd S, Jan LY, Jan YN (2001) Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage. Nat Cell Biol 3:58–67

    PubMed  CAS  Google Scholar 

  • Rugendorff A, Younossi-Hartenstein AY, Hartenstein V (1994) Embryonic origin and differentiation of the Drosophila heart. Roux’s Arch Dev Biol 203

    Google Scholar 

  • Samakovlis C, Hacohen N, Manning G, Sutherland DC, Guillemin K, Krasnow MA (1996a) Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122:1395–1407

    CAS  Google Scholar 

  • Samakovlis C, Manning G, Steneberg P, Hacohen N, Cantera R, Krasnow MA (1996b) Genetic control of epithelial tube fusion during Drosophila tracheal development. Development 122:3531–3536

    CAS  Google Scholar 

  • Santiago-Martinez E, Soplop NH, Patel R, Kramer SG (2008) Repulsion by Slit and Roundabout prevents Shotgun/E-cadherin-mediated cell adhesion during Drosophila heart tube lumen formation. J Cell Biol 182:241–248

    PubMed  CAS  Google Scholar 

  • Sawyer JK, Harris NJ, Slep KC, Gaul U, Peifer M (2009) The Drosophila afadin homologue Canoe regulates linkage of the actin cytoskeleton to adherens junctions during apical constriction. J Cell Biol 186:57–73

    PubMed  CAS  Google Scholar 

  • Sawyer JM, Harrell JR, Shemer G, Sullivan-Brown J, Roh-Johnson M, Goldstein B (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341:5–19

    PubMed  CAS  Google Scholar 

  • Seppa MJ, Johnson RI, Bao S, Cagan RL (2008) Polychaetoid controls patterning by modulating adhesion in the Drosophila pupal retina. Dev Biol 318:1–16

    PubMed  CAS  Google Scholar 

  • Shaye DD, Casanova J, Llimargas M (2008) Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nat Cell Biol 10:964–970

    PubMed  CAS  Google Scholar 

  • Shindo M, Wada H, Kaido M, Tateno M, Aigaki T, Tsuda L, Hayashi S (2008) Dual function of Src in the maintenance of adherens junctions during tracheal epithelial morphogenesis. Development 135:1355–1364

    PubMed  CAS  Google Scholar 

  • Sokac AM, Wieschaus E (2008) Zygotically controlled F-actin establishes cortical compartments to stabilize furrows during Drosophila cellularization. J Cell Sci 121:1815–1824

    PubMed  CAS  Google Scholar 

  • Solon J, Kaya-Copur A, Colombelli J, Brunner D (2009) Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137:1331–1342

    PubMed  Google Scholar 

  • Song X, Xie T (2002) DE-cadherin-mediated cell adhesion is essential for maintaining somatic stem cells in the Drosophila ovary. Proc Natl Acad Sci U S A 99:14813–14818

    PubMed  CAS  Google Scholar 

  • Song X, Zhu CH, Doan C, Xie T (2002) Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 296:1855–1857

    PubMed  CAS  Google Scholar 

  • Strutt H, Strutt D (1999) Polarity determination in the Drosophila eye. Curr Opin Genet Dev 9:442–446

    PubMed  CAS  Google Scholar 

  • Sweeton D, Parks S, Costa M, Wieschaus E (1991) Gastrulation in Drosophila: the formation of the ventral furrow and posterior midgut invaginations. Development 112:775–789

    PubMed  CAS  Google Scholar 

  • Takahashi K, Matsuo T, Katsube T, Ueda R, Yamamoto D (1998) Direct binding between two PDZ domain proteins Canoe and ZO-1 and their roles in regulation of the jun N-terminal kinase pathway in Drosophila morphogenesis. Mech Dev 78:97–111

    PubMed  CAS  Google Scholar 

  • Takahashi M, Takahashi F, Ui-Tei K, Kojima T, Saigo K (2005) Requirements of genetic interactions between Src42 A, armadillo and shotgun, a gene encoding E-cadherin, for normal development in Drosophila. Development 132:2547–2559

    PubMed  CAS  Google Scholar 

  • Tanaka H, Takasu E, Aigaki T, Kato K, Hayashi S, Nose A (2004) Formin3 is required for assembly of the F-actin structure that mediates tracheal fusion in Drosophila. Dev Biol 274:413–425

    PubMed  CAS  Google Scholar 

  • Tanaka-Matakatsu M, Uemura T, Oda H, Takeichi M, Hayashi S (1996) Cadherin-mediated cell adhesion and cell motility in Drosophila trachea regulated by the transcription factor Escargot. Development 122:3697–3705

    PubMed  CAS  Google Scholar 

  • Tanentzapf G, Smith C, McGlade J, Tepass U (2000) Apical, lateral, and basal polarization cues contribute to the development of the follicular epithelium during Drosophila oogenesis. J Cell Biol 151:891–904

    PubMed  CAS  Google Scholar 

  • Tanentzapf G, Tepass U (2003) Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat Cell Biol 5:46–52

    PubMed  CAS  Google Scholar 

  • Tepass U (1996) Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev Biol 177:217–225

    PubMed  CAS  Google Scholar 

  • Tepass U, Harris KP (2007) Adherens junctions in Drosophila retinal morphogenesis. Trends Cell Biol 17:26–35

    PubMed  CAS  Google Scholar 

  • Tepass U, Hartenstein V (1994a) Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm. Development 120:579–590

    CAS  Google Scholar 

  • Tepass U, Hartenstein V (1994b) The development of cellular junctions in the Drosophila embryo. Dev Biol 161:563–596

    CAS  Google Scholar 

  • Tepass U, Gruszynski-DeFeo E, Haag TA, Omatyar L, Torok T, Hartenstein V (1996) shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev 10:672–685

    PubMed  CAS  Google Scholar 

  • Tepass U, Godt D, Winklbauer R (2002) Cell sorting in animal development: signalling and adhesive mechanisms in the formation of tissue boundaries. Curr Opin Genet Dev 12:572–582

    PubMed  CAS  Google Scholar 

  • Ting CY, Yonekura S, Chung P, Hsu SN, Robertson HM, Chiba A, Lee CH (2005) Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents. Development 132:953–963

    PubMed  CAS  Google Scholar 

  • Uemura T, Oda H, Kraut R, Hayashi S, Kotaoka Y, Takeichi M (1996) Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev 10:659–671

    PubMed  CAS  Google Scholar 

  • Van Doren M, Mathews WR, Samuels M, Moore LA, Broihier HT, Lehmann R (2003) fear of intimacy encodes a novel transmembrane protein required for gonad morphogenesis in Drosophila. Development 130:2355–2364

    PubMed  Google Scholar 

  • Voog J, D’Alterio C, Jones DL (2008) Multipotent somatic stem cells contribute to the stem cell niche in the Drosophila testis. Nature 454:1132–1136

    PubMed  CAS  Google Scholar 

  • Wang F, Dumstrei K, Haag T, Hartenstein V (2004) The role of DE-cadherin during cellularization, germ layer formation and early neurogenesis in the Drosophila embryo. Dev Biol 270:350–363

    PubMed  CAS  Google Scholar 

  • Wang H, Singh SR, Zheng Z, Oh SW, Chen X, Edwards K, Hou SX (2006) Rap-GEF signaling controls stem cell anchoring to their niche through regulating DE-cadherin-mediated cell adhesion in the Drosophila testis. Dev Cell 10:117–126

    PubMed  CAS  Google Scholar 

  • Warner SJ, Longmore GD (2009a) Cdc42 antagonizes Rho1 activity at adherens junctions to limit epithelial cell apical tension. J Cell Biol 187:119–133

    CAS  Google Scholar 

  • Warner SJ, Longmore GD (2009b) Distinct functions for Rho1 in maintaining adherens junctions and apical tension in remodeling epithelia. J Cell Biol 185:1111–1125

    CAS  Google Scholar 

  • Wei SY, Escudero LM, Yu F, Chang LH, Chen LY, Ho YH, Lin CM, Chou CS, Chia W, Modolell J, Hsu JC (2005) Echinoid is a component of adherens junctions that cooperates with DE-Cadherin to mediate cell adhesion. Dev Cell 8:493–504

    PubMed  CAS  Google Scholar 

  • White P, Aberle H, Vincent JP (1998) Signaling and adhesion activities of mammalian beta-catenin and plakoglobin in Drosophila. J Cell Biol 140:183–195

    PubMed  CAS  Google Scholar 

  • Wolff T, Ready DF (1993) Pattern formation in the Drosophila retina. In: The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press. Vol. 2:1277–1325

    Google Scholar 

  • Wu X, Tanwar PS, Raftery LA (2008) Drosophila follicle cells: morphogenesis in an eggshell. Semin Cell Dev Biol 19:271–282

    PubMed  CAS  Google Scholar 

  • Xie T (2008) Germline stem cell niches

    Google Scholar 

  • Yamashita YM (2010) Cell adhesion in regulation of asymmetric stem cell division. Curr Opin Cell Biol 22:605–610

    PubMed  CAS  Google Scholar 

  • Yamashita YM, Mahowald AP, Perlin JR, Fuller MT (2007) Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518–521

    PubMed  CAS  Google Scholar 

  • Yonekura S, Xu L, Ting CY, Lee CH (2007) Adhesive but not signaling activity of Drosophila N-cadherin is essential for target selection of photoreceptor afferents. Dev Biol 304:759–770

    PubMed  CAS  Google Scholar 

  • Zallen JA, Wieschaus E (2004) Patterned gene expression directs bipolar planar polarity in Drosophila. Dev Cell 6:343–355

    PubMed  CAS  Google Scholar 

  • Zhu H, Luo L (2004) Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42:63–75

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the members of Llimargas lab and K. Campbell for critical reading of the manuscript and R. Rycroft for corrections. Work in our lab is supported by funds from the Ministerio de Ciencia e Innovación (BFU2009-09041/BMC) and AGAUR-Generalitat de Catalunya (2009-SGR1333) to ML, and from Programme Consolider 2007 (CSD2007-00008) project. A.L. acknowledges a contract from the “Juan de la Cierva” programme. We apologize to those authors whose work we were unable to cite due to space restrictions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marta Llimargas .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Letizia, A., Llimargas, M. (2012). Adherens Junctions and Cadherins in Drosophila Development. In: Harris, T. (eds) Adherens Junctions: from Molecular Mechanisms to Tissue Development and Disease. Subcellular Biochemistry, vol 60. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4186-7_11

Download citation

Publish with us

Policies and ethics