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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
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
Bastock R, Johnston D St (2008) Drosophila oogenesis. Curr Biol 18:R1082–R1087
Baum B, Georgiou M (2011) Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 192:907–917
Beitel GJ, Krasnow MA (2000) Genetic control of epithelial tube size in the Drosophila tracheal system. Development 127:3271–3282
Bertet C, Sulak L, Lecuit T (2004) Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429:667–671
Bilder D, Schober M, Perrimon N (2003) Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat Cell Biol 5:53–58
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
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
Bloor JW, Kiehart DP (2002) Drosophila RhoA regulates the cytoskeleton and cell-cell adhesion in the developing epidermis. Development 129:3173–3183
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
Boyle M, DiNardo S (1995) Specification, migration and assembly of the somatic cells of the Drosophila gonad. Development 121:1815–1825
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
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
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
Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster, 2nd edn. Springer-Verlag, Berlin
Cavey M, Lecuit T (2009) Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harb Perspect Biol 1:a002998
Cavey M, Rauzi M, Lenne PF, Lecuit T (2008) A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453:751–756
Cela C, Llimargas M (2006) Egfr is essential for maintaining epithelial integrity during tracheal remodelling in Drosophila. Development 133:3115–3125
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
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
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
Dansereau DA, Lasko P (2008) The development of germline stem cells in Drosophila. Methods Mol Biol 450:3–26
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
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
Doe CQ (1992) Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116:855–863
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
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
Fiehler RW, Wolff T (2007) Drosophila Myosin II, Zipper, is essential for ommatidial rotation. Dev Biol 310:348–362
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
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
Fulga TA, Rorth P (2002) Invasive cell migration is initiated by guided growth of long cellular extensions. Nat Cell Biol 4:715–719
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
Geisbrecht ER, Montell DJ (2002) Myosin VI is required for E-cadherin-mediated border cell migration. Nat Cell Biol 4:616–620
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
Ghabrial A, Luschnig S, Metzstein MM, Krasnow MA (2003) Branching morphogenesis of the Drosophila tracheal system. Annu Rev Cell Dev Biol 19:623–647
Gho M, Schweisguth F (1998) Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature 393:178–181
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
Godt D, Tepass U (1998) Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395:387–391
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
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
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
Grammont M (2007) Adherens junction remodeling by the Notch pathway in Drosophila melanogaster oogenesis. J Cell Biol 177:139–150
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
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
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
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
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
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
Harris TJ, Peifer M (2005) The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila. J Cell Biol 170:813–823
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
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
Hayashi T, Carthew RW (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431:647–652
Heisenberg CP (2009) Dorsal closure in Drosophila: cells cannot get out of the tight spot. Bioessays 31:1284–1287
Homem CC, Peifer M (2008) Diaphanous regulates myosin and adherens junctions to control cell contractility and protrusive behavior during morphogenesis. Development 135:1005–1018
Horne-Badovinac S, Bilder D (2005) Mass transit: epithelial morphogenesis in the Drosophila egg chamber. Dev Dyn 232:559–574
Hummel T, Zipursky SL (2004) Afferent induction of olfactory glomeruli requires N-cadherin. Neuron. 42:77–88
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
Huynh JR, Johnston D St (2004) The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 14:R438–R449
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
Irvine KD, Wieschaus E (1994) Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development 120:827–841
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
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
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
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
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
Jacinto A, Woolner S, Martin P (2002b) Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev Cell 3:9–19
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
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
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
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
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
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
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
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
Laplante C, Nilson LA (2006) Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila. Development 133:3255–3264
Laplante C, Nilson LA (2011) Asymmetric distribution of Echinoid defines the epidermal leading edge during Drosophila dorsal closure. J Cell Biol 192:335–348
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
Lecuit T (2004) Junctions and vesicular trafficking during Drosophila cellularization. J Cell Sci 117:3427–3433
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
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
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
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
Leptin M, Grunewald B (1990) Cell shape changes during gastrulation in Drosophila. Development 110:73–84
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
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
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
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
Llimargas M, Casanova J (2010) Apical constriction and invagination: a very self-reliant couple. Dev Biol 344:4–6
Lu B, Roegiers F, Jan LY, Jan YN (2001) Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature 409:522–525
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
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
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
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
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
Mazumdar A, Mazumdar M (2002) How one becomes many: blastoderm cellularization in Drosophila melanogaster. Bioessays 24:1012–1022
McCrea PD, Turck CW, Gumbiner B (1991) A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 254:1359–1361
McGill MA, McKinley RF, Harris TJ (2009) Independent cadherin-catenin and Bazooka clusters interact to assemble adherens junctions. J Cell Biol 185:787–796
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
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
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
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
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
Mlodzik M (1999) Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and cross-talk. EMBO J 18:6873–6879
Montell DJ (2003) Border-cell migration: the race is on. Nat Rev Mol Cell Biol 4:13–24
Montell DJ (2006) The social lives of migrating cells in Drosophila. Curr Opin Genet Dev 16:374–383
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
Niewiadomska P, Godt D, Tepass U (1999) DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J Cell Biol 144:533–547
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
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
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
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
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
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
Ohlstein B, Spradling A (2007) Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 315:988–992
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
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
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
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
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
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
Pirraglia C, Walters J, Myat MM (2010) Pak1 control of E-cadherin endocytosis regulates salivary gland lumen size and shape. Development 137:4177–4189
Poodry CA, Schneiderman HA (1970) The ultrastructure of the developing leg of Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 166:1–44
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
Rauzi M, Lenne PF, Lecuit T (2010) Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468:1110–1114
Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240
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
Ribeiro C, Neumann M, Affolter M (2004) Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr Biol 14:2197–2207
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
Rugendorff A, Younossi-Hartenstein AY, Hartenstein V (1994) Embryonic origin and differentiation of the Drosophila heart. Roux’s Arch Dev Biol 203
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
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
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
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
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
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
Shaye DD, Casanova J, Llimargas M (2008) Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nat Cell Biol 10:964–970
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
Sokac AM, Wieschaus E (2008) Zygotically controlled F-actin establishes cortical compartments to stabilize furrows during Drosophila cellularization. J Cell Sci 121:1815–1824
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
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
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
Strutt H, Strutt D (1999) Polarity determination in the Drosophila eye. Curr Opin Genet Dev 9:442–446
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
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
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
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
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
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
Tanentzapf G, Tepass U (2003) Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat Cell Biol 5:46–52
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
Tepass U, Harris KP (2007) Adherens junctions in Drosophila retinal morphogenesis. Trends Cell Biol 17:26–35
Tepass U, Hartenstein V (1994a) Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm. Development 120:579–590
Tepass U, Hartenstein V (1994b) The development of cellular junctions in the Drosophila embryo. Dev Biol 161:563–596
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
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
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
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
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
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
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
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
Warner SJ, Longmore GD (2009a) Cdc42 antagonizes Rho1 activity at adherens junctions to limit epithelial cell apical tension. J Cell Biol 187:119–133
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
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
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
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
Wu X, Tanwar PS, Raftery LA (2008) Drosophila follicle cells: morphogenesis in an eggshell. Semin Cell Dev Biol 19:271–282
Xie T (2008) Germline stem cell niches
Yamashita YM (2010) Cell adhesion in regulation of asymmetric stem cell division. Curr Opin Cell Biol 22:605–610
Yamashita YM, Mahowald AP, Perlin JR, Fuller MT (2007) Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518–521
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
Zallen JA, Wieschaus E (2004) Patterned gene expression directs bipolar planar polarity in Drosophila. Dev Cell 6:343–355
Zhu H, Luo L (2004) Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42:63–75
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
Corresponding author
Editor information
Editors and Affiliations
Rights 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
DOI: https://doi.org/10.1007/978-94-007-4186-7_11
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-4185-0
Online ISBN: 978-94-007-4186-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)