Abstract
Over a brief few days, thousands of cells in the Drosophila eye are organized to generate a precisely patterned functional organ. Eye morphogenesis requires coordinated cell fate specification and differentiation, local cell movements, niche acquisition, and apoptosis to remove surplus cells. The eye has provided a superb model tissue for studies of the molecular bases of these events and the past decade has been punctuated with studies on the adhesion molecules at play as the fly eye develops. Because of its structure—a neuroepithelium composed of several discrete and easily discernable cell types—the eye provides unique opportunities to examine the roles of adhesion between cells as a complex organ is generated. Indeed, dynamic adhesion plays a significant role in orchestrating, regulating, and driving eye morphogenesis.
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
Bao S, Fischbach KF, Corbin V, Cagan RL (2010) Preferential adhesion maintains separation of ommatidia in the Drosophila eye. Dev Biol 344:948–956
Brown KE, Freeman M (2003) Egfr signalling defines a protective function for ommatidial orientation in the Drosophila eye. Development 130:5401–5412
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
Cagan R (2009) Principles of Drosophila eye differentiation. Curr Top Dev Biol 89:115–135
Cagan RL (2011) The Drosophila nephrocyte. Curr Opin Nephrol Hypertens 20:409–415
Cagan RL, Ready DF (1989) The emergence of order in the Drosophila pupal retina. Dev Biol 136:346–362
Chang LH, Chen P, Lien MT, Ho YH, Lin CM, Pan YT, Wei SY, Hsu JC (2011) Differential adhesion and actomyosin cable collaborate to drive Echinoid-mediated cell sorting. Development 138:3803–3812
Choi KW, Benzer S (1994) Rotation of photoreceptor clusters in the developing Drosophila eye requires the nemo gene. Cell 78:125–136
Chou YH, Chien CT (2002) Scabrous controls ommatidial rotation in the Drosophila compound eye. Dev Cell 3:839–850
Chu D, Pan H, Wan P, Wu J, Luo J, Zhu H, Chen J (2012) AIP1 acts with cofilin to control actin dynamics during epithelial morphogenesis. Development 139:3561–3571
Cooper MT, Bray SJ (1999) Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 397:526–530
Cordero JB, Larson DE, Craig CR, Hays R, Cagan R (2007) Dynamic Decapentaplegic signaling regulates patterning and adhesion in the Drosophila pupal retina. Development 134:1861–1871
De Graeve FM, Van de Bor V, Ghiglione C, Cerezo D, Jouandin P, Ueda R, Shashidhara LS, Noselli S (2012) Drosophila apc regulates delamination of invasive epithelial clusters. Dev Biol 368:76–85
Djiane A, Shimizu H, Wilkin M, Mazleyrat S, Jennings MD, Avis J, Bray S, Baron M (2011) Su(dx) E3 ubiquitin ligase-dependent and -independent functions of polychaetoid, the Drosophila ZO-1 homologue. J Cell Biol 192:189–200
Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI (2005) Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123:903–915
Duguay D, Foty RA, Steinberg MS (2003) Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev Biol 253:309–323
Escudero LM, Bischoff M, Freeman M (2007) Myosin II regulates complex cellular arrangement and epithelial architecture in Drosophila. Dev Cell 13:717–729
Fanto M, Mlodzik M (1999) Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397:523–526
Faul C, Asanuma K, Yanagida-Asanuma E, Kim K, Mundel P (2007) Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 17:428–437
Fetting JL, Spencer SA, Wolff T (2009) The cell adhesion molecules Echinoid and Friend of Echinoid coordinate cell adhesion and cell signaling to regulate the fidelity of ommatidial rotation in the Drosophila eye. Development 136:3323–3333
Fiehler RW, Wolff T (2007) Drosophila Myosin II, Zipper, is essential for ommatidial rotation. Dev Biol 310:348–362
Furuse M, Tsukita S (2006) Claudins in occluding junctions of humans and flies. Trends Cell Biol 16:181–188
Gaengel K, Mlodzik M (2003) Egfr signaling regulates ommatidial rotation and cell motility in the Drosophila eye via MAPK/Pnt signaling and the Ras effector Canoe/AF6. Development 130:5413–5423
Gemp IM, Carthew RW, Hilgenfeldt S (2011) Cadherin-dependent cell morphology in an epithelium: constructing a quantitative dynamical model. PLoS Comput Biol 7:e1002115
Goodrich LV, Strutt D (2011) Principles of planar polarity in animal development. Development 138:1877–1892
Grillo-Hill BK, Wolff T (2009) Dynamic cell shapes and contacts in the developing Drosophila retina are regulated by the Ig cell adhesion protein hibris. Dev Dyn 238:2223–2234
Gumbiner BM (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6:622–634
Hayashi T, Carthew RW (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431:647–652
Hilgenfeldt S, Erisken S, Carthew RW (2008) Physical modeling of cell geometric order in an epithelial tissue. Proc Natl Acad Sci U S A 105:907–911
Ho YH, Lien MT, Lin CM, Wei SY, Chang LH, Hsu JC (2010) Echinoid regulates Flamingo endocytosis to control ommatidial rotation in the Drosophila eye. Development 137:745–754
Hohne M, Lorscheider J, Bardeleben A von, Dufner M, Scharf MA, Godel M, Helmstadter M, Schurek EM, Zank S, Gerke P et al (2011) The BAR domain protein PICK1 regulates cell recognition and morphogenesis by interacting with Neph proteins. Mol Cell Biol 31:3241–3251
Huber AH, Weis WI (2001) The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell 105:391–402
Johnson RI, Seppa MJ, Cagan RL (2008) The Drosophila CD2AP/CIN85 orthologue Cindr regulates junctions and cytoskeleton dynamics during tissue patterning. J Cell Biol 180:1191–1204
Johnson RI, Sedgwick A, D’Souza-Schorey C, Cagan RL (2011) Role for a Cindr-Arf6 axis in patterning emerging epithelia. Mol Biol Cell 22:4513–4526
Johnson RI, Bao S, Cagan RL (2012) Interactions between Drosophila IgCAM adhesion receptors and Cindr, the Cd2ap/Cin85 ortholog. Dev Dyn 241:1933–1943
Kafer J, Hayashi T, Maree AF, Carthew RW, Graner F (2007) Cell adhesion and cortex contractility determine cell patterning in the Drosophila retina. Proc Natl Acad Sci U S A 104:18549–18554
Knust E (2007) Photoreceptor morphogenesis and retinal degeneration: lessons from Drosophila. Curr Opin Neurobiol 17:541–547
Krejci A, Bernard F, Housden BE, Collins S, Bray SJ (2009) Direct response to Notch activation: signaling crosstalk and incoherent logic. Sci Signal 2:ra1
Kumar JP (2012) Building an ommatidium one cell at a time. Dev Dyn 241:136–149
Larson DE, Liberman Z, Cagan RL (2008) Cellular behavior in the developing Drosophila pupal retina. Mech Dev 125:223–232
Larson DE, Johnson RI, Swat M, Cordero JB, Glazier JA, Cagan RL (2010) Computer simulation of cellular patterning within the Drosophila pupal eye. PLoS Comput Biol 6:e1000841
Maung SM, Jenny A (2011) Planar cell polarity in Drosophila. Organogenesis 7:165–179
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
Mirkovic I, Gault WJ, Rahnama M, Jenny A, Gaengel K, Bessette D, Gottardi CJ, Verheyen EM, Mlodzik M (2011) Nemo kinase phosphorylates beta-catenin to promote ommatidial rotation and connects core PCP factors to E-cadherin-beta-catenin. Nat Struct Mol Biol 18:665–672
Miyashita Y, Ozawa M (2007) Increased internalization of p120-uncoupled E-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein. J Biol Chem282:11540–11548
Muller HA (2000) Genetic control of epithelial cell polarity: lessons from Drosophila. Dev Dyn 218:52–67
Munoz-Soriano V, Belacortu Y, Durupt FC, Munoz-Descalzo S, Paricio N (2011) Mtl interacts with members of Egfr signaling and cell adhesion genes in the Drosophila eye. Fly (Austin) 5:88–101
Nagaraj R, Banerjee U (2007) Combinatorial signaling in the specification of primary pigment cells in the Drosophila eye. Development 134:825–831
Nelson WJ (2008) Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem Soc Trans 36:149–155
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, Gonzalez-Nino E, Burnett M, Dylla L, Lambeth SM, Licon E, Amesoli C, Edgar BA, Curtiss J (2009) Rap1 maintains adhesion between cells to affect Egfr signaling and planar cell polarity in Drosophila. Dev Biol 333:143–160
Ooshio T, Fujita N, Yamada A, Sato T, Kitagawa Y, Okamoto R, Nakata S, Miki A, Irie K, Takai Y (2007) Cooperative roles of Par-3 and afadin in the formation of adherens and tight junctions. J Cell Sci 120:2352–2365
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
Reiter C, Schimansky T, Nie Z, Fischbach KF (1996) Reorganization of membrane contacts prior to apoptosis in the Drosophila retina: the role of the IrreC-rst protein. Development 122:1931–1940
Schwabe T, Gontang AC, Clandinin TR (2009) More than just glue: the diverse roles of cell adhesion molecules in the Drosophila nervous system. Cell Adh Migr 3:36–42
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
Singh J, Mlodzik M (2012) Hibris, a Drosophila nephrin homolog, is required for presenilin-mediated Notch and APP-like cleavages. Dev Cell 23:82–96
Staley BK, Irvine KD (2012) Hippo signaling in Drosophila: recent advances and insights. Dev Dyn 241:3–15
Steinberg MS (1970) Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J Exp Zool 173:395–433
Steinberg MS (2007) Differential adhesion in morphogenesis: a modern view. Curr Opin Genet Dev 17:281–286
Steinberg MS, Takeichi M (1994) Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc Natl Acad Sci U S A 91:206–209
Strutt H, Strutt D (2003) EGF signaling and ommatidial rotation in the Drosophila eye. Curr Biol 13:1451–1457
Takahashi K, Nakanishi H, Miyahara M, Mandai K, Satoh K, Satoh A, Nishioka H, Aoki J, Nomoto A, Mizoguchi A et al (1999) Nectin/PRR: an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J Cell Biol 145:539–549
Tepass U, Harris KP (2007) Adherens junctions in Drosophila retinal morphogenesis. Trends Cell Biol 17(1):26–35
Tepass U, Tanentzapf G, Ward R, Fehon R (2001) Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35:747–784
Thoreson MA, Anastasiadis PZ, Daniel JM, Ireton RC, Wheelock MJ, Johnson KR, Hummingbird DK, Reynolds AB (2000) Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion. J Cell Biol 148:189–202
Tossidou I, Teng B, Drobot L, Meyer-Schwesinger C, Worthmann K, Haller H, Schiffer M (2010) CIN85/RukL is a novel binding partner of nephrin and podocin and mediates slit diaphragm turnover in podocytes. J Biol Chem 285:25285–25295
Verdier V, Guang Chao C, Settleman J (2006) Rho-kinase regulates tissue morphogenesis via non-muscle myosin and LIM-kinase during Drosophila development. BMC Dev Biol 6:38
Vidal M, Wells S, Ryan A, Cagan R (2005) ZD6474 suppresses oncogenic RET isoforms in a Drosophila model for type 2 multiple endocrine neoplasia syndromes and papillary thyroid carcinoma. Cancer Res 65:3538–3541
Wei SY, Escudero LM, Yu F, Chang LH, Chen LY, Ho YH, Lin CM, Chou CS, Chia W, Modolell J et al (2005) Echinoid is a component of adherens junctions that cooperates with DE-Cadherin to mediate cell adhesion. Dev Cell 8:493–504
Weis WI, Nelson WJ (2006) Re-solving the cadherin-catenin-actin conundrum. J Biol Chem 281:35593–35597
Winter CG, Wang B, Ballew A, Royou A, Karess R, Axelrod JD, Luo L (2001) Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105:81–91
Xiao K, Garner J, Buckley KM, Vincent PA, Chiasson CM, Dejana E, Faundez V, Kowalczyk AP (2005) p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. Mol Biol Cell16:5141–5151
Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ (2005) Deconstructing the cadherin-catenin-actin complex. Cell 123:889–901
Yap AS, Crampton MS, Hardin J (2007) Making and breaking contacts: the cellular biology of cadherin regulation. Curr Opin Cell Biol 19:508–514
Acknowledgments
I am grateful to Mark Hellerman, Ursula Weber, and Jun Wu for very helpful comments on this chapter.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Johnson, R. (2013). Cell Adhesion During Drosophila Eye Development. In: Singh, A., Kango-Singh, M. (eds) Molecular Genetics of Axial Patterning, Growth and Disease in the Drosophila Eye. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8232-1_7
Download citation
DOI: https://doi.org/10.1007/978-1-4614-8232-1_7
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-8231-4
Online ISBN: 978-1-4614-8232-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)