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Dynamics and functions of E-cadherin complexes in epithelial cell and tissue morphogenesis

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Abstract

Cell–cell adhesion is at the center of structure and dynamics of epithelial tissue. E-cadherin–catenin complexes mediate Ca2+-dependent trans-homodimerization and constitute the kernel of adherens junctions. Beyond the basic function of cell–cell adhesion, recent progress sheds light the dynamics and interwind interactions of individual E-cadherin–catenin complex with E-cadherin superclusters, contractile actomyosin and mechanics of the cortex and adhesion. The nanoscale architecture of E-cadherin complexes together with cis-interactions and interactions with cortical actomyosin adjust to junctional tension and mechano-transduction by reinforcement or weakening of specific features of the interactions. Although post-translational modifications such as phosphorylation and glycosylation have been implicated, their role for specific aspects of in E-cadherin function has remained unclear. Here, we provide an overview of the E-cadherin complex in epithelial cell and tissue morphogenesis focusing on nanoscale architectures by super-resolution approaches and post-translational modifications from recent, in particular in vivo, studies. Furthermore, we review the computational modelling in E-cadherin complexes and highlight how computational modelling has contributed to a deeper understanding of the E-cadherin complexes.

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References

  • Aberle H, Butz S, Stappert J, Weissig H, Kemler R, Hoschuetzky H (1994) Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J Cell Sci 107:3655–3663

    Article  CAS  PubMed  Google Scholar 

  • Adhikari S, Moran J, Weddle C, Hinczewski M (2018) Unraveling the mechanism of the cadherin-catenin-actin catch bond. PLoS Comput Biol 14:e1006399

    Article  PubMed  PubMed Central  Google Scholar 

  • Arbore C, Sergides M, Gardini L, Bianchi G, Kashchuk A, Pertici I, Bianco P, Pavone F, Capitanio M (2022) α-catenin switches between a slip and an asymmetric catch bond with F-actin to cooperatively regulate cell junction fluidity. Nat Commun 13:1146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armstrong NJ, Painter KJ, Sherratt JA (2006) A continuum approach to modelling cell–cell adhesion. J Theor Biol 243:98–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates M, Huang B, Dempsey GT, Zhuang X (2007) Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science 317:1749–1753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertocchi C, Wang Y, Ravasio A, Hara Y, Wu Y, Sailov T, Baird MA, Davidson MW, Zaidel-Bar R, Toyama Y (2017) Nanoscale architecture of cadherin-based cell adhesions. Nat Cell Biol 19:28–37

    Article  CAS  PubMed  Google Scholar 

  • Bertocchi C, Ravasio A, Ong HT, Toyama Y, Kanchanawong P (2019) Mechanical roles of vinculin/β-catenin interaction in adherens junction. bioRxiv. 7:770735

    Google Scholar 

  • Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642–1645

    Article  CAS  PubMed  Google Scholar 

  • Bian Y, Song C, Cheng K, Dong M, Wang F, Huang J, Sun D, Wang L, Ye M, Zou H (2014) An enzyme assisted RP-RPLC approach for in-depth analysis of human liver phosphoproteome. J Proteomics 96:253–262

    Article  CAS  PubMed  Google Scholar 

  • Blom K, Godec A (2021) Criticality in cell adhesion. Phys Rev X 11:031067

    CAS  Google Scholar 

  • Boggon TJ, Murray J, Chappuis-Flament S, Wong E, Gumbiner BM, Shapiro L (2002) C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296:1308–1313

    Article  CAS  PubMed  Google Scholar 

  • Boller K, Vestweber D, Kemler R (1985) Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells. J Cell Biol 100:327–332

    Article  CAS  PubMed  Google Scholar 

  • Bosch JA, Perrimon N (2022) Prime editing for precise genome engineering in Drosophila. In: Dahmann C (ed) Drosophila: methods and protocols. Springer, US, New York, pp 113–134

    Chapter  Google Scholar 

  • Braeutigam A, Simsek AN, Gompper G, Sabass B (2022) Generic self-stabilization mechanism for biomolecular adhesions under load. Nat Commun 13:1–9

    Article  Google Scholar 

  • Brasch J, Harrison OJ, Ahlsen G, Carnally SM, Henderson RM, Honig B, Shapiro L (2011) Structure and binding mechanism of vascular endothelial cadherin: a divergent classical cadherin. J Mol Biol 408:57–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brockhausen I, Narasimhan S, Schachter H (1988) The biosynthesis of highly branched N-glycans: studies on the sequential pathway and functional role of N-actylglucosaminyltransferases I, II, III, IV, V and VI. Biochimie 70:1521–1533

    Article  CAS  PubMed  Google Scholar 

  • Buckley CD, Tan J, Anderson KL, Hanein D, Volkmann N, Weis WI, Nelson WJ, Dunn AR (2014) The minimal cadherin-catenin complex binds to actin filaments under force. Science 346:1254211

    Article  PubMed  PubMed Central  Google Scholar 

  • Bulgakova NA, Brown NH (2016) Drosophila p120-catenin is crucial for endocytosis of the dynamic E-cadherin–Bazooka complex. J Cell Sci 129:477–482

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cabrera AJ, Gumbiner BM, Kwon YV (2021) The roles of distinct Ca2+ signaling mediated by Piezo and inositol triphosphate receptor (IP3R) in the remodeling of E-cadherin during cell dissemination. bioRxiv: 2021.2011. 2010.467957

  • Campbell BC, Paez-Segala MG, Looger LL, Petsko GA, Liu CF (2022) Chemically stable fluorescent proteins for advanced microscopy. Nat Methods 19:1–10

    Article  Google Scholar 

  • Carvalho S, Catarino TA, Dias AM, Kato M, Almeida A, Hessling B, Figueiredo J, Gärtner F, Sanches JM, Ruppert T, Miyoshi E, Pierce M, Carneiro F, Kolarich D, Seruca R, Yamaguchi Y, Taniguchi N, Reis CA, Pinho SS (2016) Preventing E-cadherin aberrant N-glycosylation at Asn-554 improves its critical function in gastric cancer. Oncogene 35:1619–1631

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chan EH, Shivakumar PC, Clément R, Laugier E, Lenne P-F (2017) Patterned cortical tension mediated by N-cadherin controls cell geometric order in the Drosophila eye. elife 6:e22796

    Article  PubMed  PubMed Central  Google Scholar 

  • Chandran R, Kale G, Philippe J-M, Lecuit T, Mayor S (2021) Distinct actin-dependent nanoscale assemblies underlie the dynamic and hierarchical organization of E-cadherin. Curr Biol 31:1726–1736

    Article  Google Scholar 

  • Chandran L, Backer W, Schleutker R, Kong D, Beati SA, Luschnig S, Müller H-AJ (2023) Src42A is required for E-cadherin dynamics at cell junctions during Drosophila axis elongation. Development 150:dev201119

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Xie Z-R, Wu Y (2014) Computational modeling of the interplay between cadherin-mediated cell adhesion and Wnt signaling pathway. PLoS ONE 9:e100702

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen F, Tillberg PW, Boyden ES (2015) Expansion microscopy. Science 347:543–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C-L, Wang S-H, Chan P-C, Shen M-R, Chen H-C (2016a) Phosphorylation of E-cadherin at threonine 790 by protein kinase Cδ reduces β-catenin binding and suppresses the function of E-cadherin. Oncotarget 7:37260

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen J, Newhall J, Xie Z-R, Leckband D, Wu Y (2016b) A computational model for kinetic studies of cadherin binding and clustering. Biophys J 111:1507–1518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y-J, Huang J, Huang L, Austin E, Hong Y (2017) Phosphorylation potential of Drosophila E-cadherin intracellular domain is essential for development and adherens junction biosynthetic dynamics regulation. Development 144:1242–1248

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Brasch J, Harrison OJ, Bidone TC (2021) Computational model of E-cadherin clustering under force. Biophys J 120:4944–4954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng J, Allgeyer ES, Richens JH, Dzafic E, Palandri A, Lewków B, Sirinakis G, St Johnston D (2021) A single-molecule localization microscopy method for tissues reveals nonrandom nuclear pore distribution in Drosophila. J Cell Sci 134:jcs259570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chihara D, Nance J (2012) An E-cadherin-mediated hitchhiking mechanism for C. elegans germ cell internalization during gastrulation. Development 139:2547–2556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi H-J, Huber AH, Weis WI (2006) Thermodynamics of β-catenin-ligand interactions: the roles of the N-and C-terminal tails in modulating binding affinity. J Biol Chem 281:1027–1038

    Article  CAS  PubMed  Google Scholar 

  • Choi H-J, Loveless T, Lynch AM, Bang I, Hardin J, Weis WI (2015) A conserved phosphorylation switch controls the interaction between cadherin and β-catenin in vitro and in vivo. Dev Cell 33:82–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choudhary D, Narui Y, Neel BL, Wimalasena LN, Klanseck CF, De-la-Torre P, Chen C, Araya-Secchi R, Tamilselvan E, Sotomayor M (2020) Structural determinants of protocadherin-15 mechanics and function in hearing and balance perception. Proc Natl Acad Sci USA 117:24837–24848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Civera M, Vasile F, Potenza D, Colombo C, Parente S, Vettraino C, Prosdocimi T, Parisini E, Belvisi L (2019) Exploring E-cadherin-peptidomimetics interaction using NMR and computational studies. PLoS Comput Biol 15:e1007041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke DN, Miller PW, Lowe CJ, Weis WI, Nelson WJ (2016) Characterization of the cadherin–catenin complex of the sea anemone Nematostella vectensis and implications for the evolution of metazoan cell–cell adhesion. Mol Biol Evol 33:2016–2029

    Article  PubMed  PubMed Central  Google Scholar 

  • Dallon J, Newren E, Hansen MD (2009) Using a mathematical model of cadherin-based adhesion to understand the function of the actin cytoskeleton. Phys Rev E Stat Nonlin Soft Matter Phys 79:031918

    Article  CAS  PubMed  Google Scholar 

  • Davis MA, Ireton RC, Reynolds AB (2003) A core function for p120-catenin in cadherin turnover. J Cell Biol 163:525–534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desai R, Sarpal R, Ishiyama N, Pellikka M, Ikura M, Tepass U (2013) Monomeric α-catenin links cadherin to the actin cytoskeleton. Nat Cell Biol 15:261–273

    Article  CAS  PubMed  Google Scholar 

  • Dorland YL, Malinova TS, Van Stalborch A-MD, Grieve AG, Van Geemen D, Jansen NS, de Kreuk B-J, Nawaz K, Kole J, Geerts D (2016) The F-BAR protein pacsin2 inhibits asymmetric VE-cadherin internalization from tensile adherens junctions. Nat Commun 7:1–18

    Article  Google Scholar 

  • Doro F, Colombo C, Alberti C, Arosio D, Belvisi L, Casagrande C, Fanelli R, Manzoni L, Parisini E, Piarulli U (2015) Computational design of novel peptidomimetic inhibitors of cadherin homophilic interactions. Org Biomol Chem 13:2570–2573

    Article  CAS  PubMed  Google Scholar 

  • Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI (2005) α-catenin is a molecular switch that binds E-cadherin-β-catenin and regulates actin-filament assembly. Cell 123:903–915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engl W, Arasi B, Yap L, Thiery J, Viasnoff V (2014) Actin dynamics modulate mechanosensitive immobilization of E-cadherin at adherens junctions. Nat Cell Biol 16:584–591

    Article  Google Scholar 

  • Fan X, She Y-M, Bagshaw RD, Callahan JW, Schachter H, Mahuran DJ (2005) Identification of the hydrophobic glycoproteins of Caenorhabditis elegans. Glycobiology 15:952–964

    Article  CAS  PubMed  Google Scholar 

  • Figueroa A, Kotani H, Toda Y, Mazan-Mamczarz K, Mueller EC, Otto A, Disch L, Norman M, Ramdasi RM, Keshtgar M, Gorospe M, Fujita Y (2009) Novel roles of hakai in cell proliferation and oncogenesis. Mol Biol Cell 20:3533–3542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fletcher AG, Osterfield M, Baker RE, Shvartsman SY (2014) Vertex models of epithelial morphogenesis. Biophys J 106:2291–2304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HEM, Behrens J, Sommer T, Birchmeier W (2002) Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat Cell Biol 4:222–231

    Article  CAS  PubMed  Google Scholar 

  • Gemp IM, Carthew RW, Hilgenfeldt S (2011) Cadherin-dependent cell morphology in an epithelium: constructing a quantitative dynamical model. PLoS Comput Biol 7:e1002115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong EY, Park E, Lee K (2010) Hakai acts as a coregulator of estrogen receptor alpha in breast cancer cells. Cancer Sci 101:2019–2025

    Article  CAS  PubMed  Google Scholar 

  • Grimm JB, Muthusamy AK, Liang Y, Brown TA, Lemon WC, Patel R, Lu R, Macklin JJ, Keller PJ, Ji N (2017) A general method to fine-tune fluorophores for live-cell and in vivo imaging. Nat Methods 14:987–994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillaume E, Comunale F, Do Khoa N, Planchon D, Bodin S, Gauthier-Rouvière C (2013) Flotillin microdomains stabilize cadherins at cell–cell junctions. J Cell Sci 126:5293–5304

    CAS  PubMed  Google Scholar 

  • Gustafsson N, Culley S, Ashdown G, Owen DM, Pereira PM, Henriques R (2016) Fast live-cell conventional fluorophore nanoscopy with ImageJ through super-resolution radial fluctuations. Nat Commun 7:1–9

    Article  Google Scholar 

  • Hale R, Brittle AL, Fisher KH, Monk NA, Strutt D (2015) Cellular interpretation of the long-range gradient of Four-jointed activity in the Drosophila wing. elife 4:e05789

    Article  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison OJ, Jin X, Hong S, Bahna F, Ahlsen G, Brasch J, Wu Y, Vendome J, Felsovalyi K, Hampton CM (2011) The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 19:244–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He M, Ye W, Wang W-J, Sison ES, Jan YN, Jan LY (2017) Cytoplasmic Cl− couples membrane remodeling to epithelial morphogenesis. Proc Natl Acad Sci USA 114:E11161–E11169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helenius A, Aebi M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73:1019–1049

    Article  CAS  PubMed  Google Scholar 

  • Hell SW, Wichmann J (1994) Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett 19:780–782

    Article  CAS  PubMed  Google Scholar 

  • Heuzé ML, Narayana GHNS, d’Alessandro J, Cellerin V, Dang T, Williams DS, Van Hest JC, Marcq P, Mège R-M, Ladoux B (2019) Myosin II isoforms play distinct roles in adherens junction biogenesis. elife 8:e46599

    Article  PubMed  PubMed Central  Google Scholar 

  • Hill E, Broadbent ID, Chothia C, Pettitt J (2001) Cadherin superfamily proteins in Caenorhabditis elegans and Drosophila melanogaster. J Mol Biol 305:1011–1024

    Article  CAS  PubMed  Google Scholar 

  • Hong S, Troyanovsky RB, Troyanovsky SM (2010) Spontaneous assembly and active disassembly balance adherens junction homeostasis. Proc Natl Acad Sci USA 107:3528–3533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huff J (2015) The Airyscan detector from ZEISS: confocal imaging with improved signal-to-noise ratio and super-resolution. Nat Methods 12:i–ii

    Article  CAS  Google Scholar 

  • Hyafil F, Morello D, Babinet C, Jacob F (1980) A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos. Cell 21:927–934

    Article  CAS  PubMed  Google Scholar 

  • Hyafil F, Babinet C, Jacob F (1981) Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell 26:447–454

    Article  CAS  PubMed  Google Scholar 

  • Indra I, Hong S, Troyanovsky R, Kormos B, Troyanovsky S (2013) The adherens junction: a mosaic of cadherin and nectin clusters bundled by actin filaments. J Invest Dermatol 133:2546–2554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iyer KV, Piscitello-Gómez R, Paijmans J, Jülicher F, Eaton S (2019) Epithelial viscoelasticity is regulated by mechanosensitive E-cadherin turnover. Curr Biol 29:578–591

    Article  CAS  PubMed  Google Scholar 

  • Jamal BT, Nita-Lazar M, Gao Z, Amin B, Walker J, Kukuruzinska MA (2009) N-glycosylation status of E-cadherin controls cytoskeletal dynamics through the organization of distinct β-catenin-and γ-catenin-containing AJs. Cell Health Cytoskelet 2009:67

    PubMed  PubMed Central  Google Scholar 

  • Jeong H, Clark S, Goehring A, Dehghani-Ghahnaviyeh S, Rasouli A, Tajkhorshid E, Gouaux E (2022) Structures of the TMC-1 complex illuminate mechanosensory transduction. Nature 610:796–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jolly MK, Rizvi MS, Kumar A, Sinha P (2014) Mathematical modeling of sub-cellular asymmetry of fat-dachsous heterodimer for generation of planar cell polarity. PLoS ONE 9:e97641

    Article  PubMed  PubMed Central  Google Scholar 

  • Jolly MK, Ware KE, Xu S, Gilja S, Shetler S, Yang Y, Wang X, Austin RG, Runyambo D, Hish AJ, DeWitt SB, George JT, Kreulen RT, Boss MK, Lazarides AL, Kerr DL, Gerber DG, Sivaraj D, Armstrong AJ, Dewhirst MW et al (2019) E-cadherin represses anchorage-independent growth in sarcomas through both signaling and mechanical mechanismse-cadherin represses anchorage-independent growth. Mol Cancer Res 17:1391–1402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones SA, Shim S-H, He J, Zhuang X (2011) Fast, three-dimensional super-resolution imaging of live cells. Nat Methods 8:499–505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jülicher F, Grill SW, Salbreux G (2018) Hydrodynamic theory of active matter. Rep Prog Phys 81:076601

    Article  PubMed  Google Scholar 

  • Jungmann R, Avendaño MS, Dai M, Woehrstein JB, Agasti SS, Feiger Z, Rodal A, Yin P (2016) Quantitative super-resolution imaging with qPAINT. Nat Methods 13:439–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaido M, Wada H, Shindo M, Hayashi S (2009) Essential requirement for RING finger E3 ubiquitin ligase Hakai in early embryonic development of Drosophila. Genes Cells 14:1067–1077

    Article  CAS  PubMed  Google Scholar 

  • Kaji H, Saito H, Yamauchi Y, Shinkawa T, Taoka M, Hirabayashi J, Kasai K-i, Takahashi N, Isobe T (2003) Lectin affinity capture, isotope-coded tagging and mass spectrometry to identify N-linked glycoproteins. Nat Biotechnol 21:667–672

    Article  CAS  PubMed  Google Scholar 

  • Kale GR, Yang X, Philippe J-M, Mani M, Lenne P-F, Lecuit T (2018) Distinct contributions of tensile and shear stress on E-cadherin levels during morphogenesis. Nat Commun 9:1–16

    Article  CAS  Google Scholar 

  • Katsamba P, Carroll K, Ahlsen G, Bahna F, Vendome J, Posy S, Rajebhosale M, Price S, Jessell T, Ben-Shaul A (2009) Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. Proc Natl Acad Sci USA 106:11594–11599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura A, Terao M, Kato A, Hanafusa T, Murota H, Katayama I, Miyoshi E (2012) Upregulation of N-acetylglucosaminyltransferase-V by heparin-binding EGF-like growth factor induces keratinocyte proliferation and epidermal hyperplasia. Exp Dermatol 21:515–519

    Article  CAS  PubMed  Google Scholar 

  • Kobielak A, Fuchs E (2004) α-catenin: at the junction of intercellular adhesion and actin dynamics. Nat Rev Mol Cell Biol 5:614–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong D, Großhans J (2022) Optochemical control of cell contractility in embryos Drosophila. In: Dahmann C (ed) Drosophila: methods and protocols. Springer, US, New York, pp 285–299

    Chapter  Google Scholar 

  • Kong D, Lv Z, Häring M, Lin B, Wolf F, Großhans J (2019) In vivo optochemical control of cell contractility at single-cell resolution. EMBO Rep 20:e47755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornfeld R, Kornfeld S (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54:631–664

    Article  CAS  PubMed  Google Scholar 

  • Kovacs EM, Goodwin M, Ali RG, Paterson AD, Yap AS (2002) Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr Biol 12:379–382

    Article  CAS  PubMed  Google Scholar 

  • Krueger D, De Renzis S (2022) Optogenetic methods to control tissue mechanics in Drosophila. In: Dahmann C (ed) Drosophila: methods and protocols. Springer, US, New York, pp 269–283

    Chapter  Google Scholar 

  • Kumar A, Rizvi MS, Athilingam T, Parihar SS, Sinha P (2020) Heterophilic cell–cell adhesion of atypical cadherins fat and dachsous regulate epithelial cell size dynamics during Drosophila thorax morphogenesis. Mol Biol Cell 31:546–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsen ISB, Narimatsu Y, Joshi HJ, Siukstaite L, Harrison OJ, Brasch J, Goodman KM, Hansen L, Shapiro L, Honig B (2017) Discovery of an O-mannosylation pathway selectively serving cadherins and protocadherins. Proc Natl Acad Sci USA 114:11163–11168

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Clainche C, Carlier M-F (2008) Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 88:489–513

    Article  PubMed  Google Scholar 

  • Le Garrec JF, Lopez P, Kerszberg M (2006) Establishment and maintenance of planar epithelial cell polarity by asymmetric cadherin bridges: a computer model. Dev Dyn 235:235–246

    Article  PubMed  Google Scholar 

  • Leckband D, De Rooij J (2014) Cadherin adhesion and mechanotransduction. Annu Rev Cell Dev Biol 30:291–315

    Article  CAS  PubMed  Google Scholar 

  • Lecuit T, Lenne P-F, Munro E (2011) Force generation, transmission, and integration during cell and tissue morphogenesis. Annu Rev Cell Dev Biol 27:157–184

    Article  CAS  PubMed  Google Scholar 

  • Levayer R, Lecuit T (2013) Oscillation and polarity of E-cadherin asymmetries control actomyosin flow patterns during morphogenesis. Dev Cell 26:162–175

    Article  CAS  PubMed  Google Scholar 

  • Li D, Shao L, Chen B-C, Zhang X, Zhang M, Moses B, Milkie DE, Beach JR, Hammer JA III, Pasham M (2015) Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics. Science 349:aab3500

    Article  PubMed  PubMed Central  Google Scholar 

  • Li JXH, Tang VW, Brieher WM (2020) Actin protrusions push at apical junctions to maintain E-cadherin adhesion. Proc Natl Acad Sci USA 117:432–438

    Article  CAS  PubMed  Google Scholar 

  • Li JXH, Tang VW, Boateng KA, Brieher WM (2021) Cadherin puncta are interdigitated dynamic actin protrusions necessary for stable cadherin adhesion. Proc Natl Acad Sci USA 118:e2023510118

    Article  PubMed  PubMed Central  Google Scholar 

  • Lickert H, Bauer A, Kemler R, Stappert J (2000) Casein kinase II phosphorylation of E-cadherin increases E-cadherin/β-catenin interaction and strengthens cell-cell adhesion. J Biol Chem 275:5090–5095

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Cao Q-H, Lu D-J, Luo B, Lu X-F, Luo R-C, Wang X-G (2015) TMEM16A overexpression contributes to tumor invasion and poor prognosis of human gastric cancer through TGF-β signaling. Oncotarget 6:11585

    Article  PubMed  PubMed Central  Google Scholar 

  • Liwosz A, Lei T, Kukuruzinska MA (2006) N-glycosylation affects the molecular organization and stability of E-cadherin junctions. J Biol Chem 281:23138–23149

    Article  CAS  PubMed  Google Scholar 

  • Lv Z, Zhang N, Zhang X, Großhans J, Kong D (2022) The lateral epidermis actively counteracts pulling by the amnioserosa during dorsal closure. Front Cell Dev Biol 10:865397

    Article  PubMed  PubMed Central  Google Scholar 

  • Maître J-L, Berthoumieux H, Krens SFG, Salbreux G, Jülicher F, Paluch E, Heisenberg C-P (2012) Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338:253–256

    Article  PubMed  Google Scholar 

  • Mangeol P, Massey-Harroche D, Le Bivic A, Lenne P-F (2019) Nectins rather than E-cadherin anchor the actin belts at cell-cell junctions of epithelia. bioRxiv. 107:809343

    Google Scholar 

  • Maraspini R, Wang C-H, Honigmann A (2019) Optimization of 2D and 3D cell culture to study membrane organization with STED microscopy. J Phys D Appl Phys 53:014001

    Article  Google Scholar 

  • McEwen AE, Maher MT, Mo R, Gottardi CJ (2014) E-cadherin phosphorylation occurs during its biosynthesis to promote its cell surface stability and adhesion. Mol Biol Cell 25:2365–2374

    Article  PubMed  PubMed Central  Google Scholar 

  • Mège RM, Ishiyama N (2017) Integration of cadherin adhesion and cytoskeleton at adherens junctions. Cold Spring Harb Perspect Biol 9:a028738

    Article  PubMed  PubMed Central  Google Scholar 

  • Metzcar J, Wang Y, Heiland R, Macklin P (2019) A review of cell-based computational modeling in cancer biology. JCO Clin Cancer Inform 2:1–13

    Article  Google Scholar 

  • Mukherjee M, Chow SY, Yusoff P, Seetharaman J, Ng C, Sinniah S, Koh XW, Asgar NFM, Li D, Yim D (2012) Structure of a novel phosphotyrosine-binding domain in Hakai that targets E-cadherin. EMBO J 31:1308–1319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller H, Wieschaus E (1996) armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J Cell Biol 134:149–163

    Article  PubMed  Google Scholar 

  • Murakawa H, Togashi H (2015) Continuous models for cell–cell adhesion. J Theor Biol 374:1–12

    Article  CAS  PubMed  Google Scholar 

  • Myster SH, Cavallo R, Anderson CT, Fox DT, Peifer M (2003) Drosophila p120 catenin plays a supporting role in cell adhesion but is not an essential adherens junction component. J Cell Biol 160:433–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narasimhan S (1982) Control of glycoprotein synthesis. UDP-GlcNAc: glycopeptide beta 4-N-acetylglucosaminyltransferase III, an enzyme in hen oviduct which adds GlcNAc in beta 1–4 linkage to the beta-linked mannose of the trimannosyl core of N-glycosyl oligosaccharides. J Biol Chem 257:10235–10242

    Article  CAS  PubMed  Google Scholar 

  • Naser AN, Guiler W, Lu Q, Chen YH (2022) Nanoarchitecture and molecular interactions of epithelial cell junction proteins revealed by super-resolution microscopy. Ann NY Acad Sci 1516:175–187

    Article  CAS  PubMed  Google Scholar 

  • National Academies of Sciences, Engineering, and Medicine (2022) Physics of Life. The National Academies Press. https://doi.org/10.17226/26403

    Book  Google Scholar 

  • Nestor-Bergmann A, Blanchard GB, Hervieux N, Fletcher AG, Étienne J, Sanson B (2022) Adhesion-regulated junction slippage controls cell intercalation dynamics in an apposed-cortex adhesion model. PLoS Comput Biol 18:e1009812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishiguchi S, Yagi A, Sakai N, Oda H (2016) Divergence of structural strategies for homophilic E-cadherin binding among bilaterians. J Cell Sci 129:3309–3319

    CAS  PubMed  Google Scholar 

  • Nyberg KG, Carthew RW (2022) CRISPR-/Cas9-mediated precise and efficient genome editing in Drosophila. In: Dahmann C (ed) Drosophila. Methods in molecular biology, vol 2540. Humana, New York, pp 135–156

    Google Scholar 

  • Oda H, Tsukita S (1999) Nonchordate classic cadherins have a structurally and functionally unique domain that is absent from chordate classic cadherins. Dev Biol 216:406–422

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Pai LM, Kirkpatrick C, Blanton J, Oda H, Takeichi M, Peifer M (1996) Drosophila alpha-catenin and E-cadherin bind to distinct regions of Drosophila Armadillo. J Biol Chem 271:32411–32420

    Article  CAS  PubMed  Google Scholar 

  • Palovuori R, Eskelinen S (2000) Role of vinculin in the maintenance of cell-cell contacts in kidney epithelial MDBK cells. Eur J Cell Biol 79:961–974

    Article  CAS  PubMed  Google Scholar 

  • Patel SD, Ciatto C, Chen CP, Bahna F, Rajebhosale M, Arkus N, Schieren I, Jessell TM, Honig B, Price SR (2006) Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell 124:1255–1268

    Article  CAS  PubMed  Google Scholar 

  • Pettitt J (2005) The cadherin superfamily. In: The C. elegans Research Community (eds) WormBook. doi/https://doi.org/10.1895/wormbook.1.50.1, http://www.wormbook.org/

  • Piedra J, Miravet S, Castaño J, Pálmer HG, Heisterkamp N, García de Herreros A, Duñach M (2003) p120 Catenin-associated Fer and Fyn tyrosine kinases regulate β-catenin Tyr-142 phosphorylation and β-catenin-α-catenin Interaction. Mol Cell Biol 23:2287–2297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinheiro D, Hannezo E, Herszterg S, Bosveld F, Gaugue I, Balakireva M, Wang Z, Cristo I, Rigaud SU, Markova O, Bellaïche Y (2017) Transmission of cytokinesis forces via E-cadherin dilution and actomyosin flows. Nature 545:103–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinho SS, Seruca R, Gärtner F, Yamaguchi Y, Gu J, Taniguchi N, Reis CA (2011) Modulation of E-cadherin function and dysfunction by N-glycosylation. Cell Mol Life Sci 68:1011–1020

    Article  CAS  PubMed  Google Scholar 

  • Quang B-AT, Mani M, Markova O, Lecuit T, Lenne P-F (2013) Principles of E-cadherin supramolecular organization in vivo. Curr Biol 23:2197–2207

    Article  Google Scholar 

  • Ramis-Conde I, Drasdo D, Anderson AR, Chaplain MA (2008) Modeling the influence of the E-cadherin-β-catenin pathway in cancer cell invasion: a multiscale approach. Biophys J 95:155–165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raza Q, Choi JY, Li Y, O’Dowd RM, Watkins SC, Chikina M, Hong Y, Clark NL, Kwiatkowski AV (2019) Evolutionary rate covariation analysis of E-cadherin identifies Raskol as a regulator of cell adhesion and actin dynamics in Drosophila. PLoS Genet 15:e1007720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhee J, Buchan T, Zukerberg L, Lilien J, Balsamo J (2007) Cables links Robo-bound Abl kinase to N-cadherin-bound β-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat Cell Biol 9:883–892

    Article  CAS  PubMed  Google Scholar 

  • Roy Choudhury A, Großhans J, Kong D (2021) Ion channels in epithelial dynamics and morphogenesis. Cells 10:2280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3:793–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sahl SJ, Hell SW, Jakobs S (2017) Fluorescence nanoscopy in cell biology. Nat Rev Mol Cell Biol 18:685–701

    Article  CAS  PubMed  Google Scholar 

  • Said R, Wang H, Pernier J, Narassimprakash H, Roméro S, Gautreau AM, Mège R-M, Le Clainche C (2022) The adherens junction proteins α-catenin, vinculin and VASP cooperate to promote actin assembly. bioRxiv. 261:10915

    Google Scholar 

  • Sakakibara S, Mizutani K, Sugiura A, Sakane A, Sasaki T, Yonemura S, Takai Y (2020) Afadin regulates actomyosin organization through αE-catenin at adherens junctions. J Cell Biol 219:e201907079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schermelleh L, Carlton PM, Haase S, Shao L, Winoto L, Kner P, Burke B, Cardoso MC, Agard DA, Gustafsson MG (2008) Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320:1332–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schermelleh L, Ferrand A, Huser T, Eggeling C, Sauer M, Biehlmaier O, Drummen GPC (2019) Super-resolution microscopy demystified. Nat Cell Biol 21:72–84

    Article  CAS  PubMed  Google Scholar 

  • Schmidt A, Finegan T, Häring M, Kong D, Fletcher AG, Alam Z, Grosshans J, Wolf F, Peifer M (2023) Polychaetoid/ZO-1 strengthens cell junctions under tension while localizing differently than core adherens junction proteins. Mol Biol Cell 34:8

    Google Scholar 

  • Schwientek T, Mandel U, Roth U, Müller S, Hanisch FG (2007) A serial lectin approach to the mucin-type O-glycoproteome of Drosophila melanogaster S2 cells. Proteomics 7:3264–3277

    Article  CAS  PubMed  Google Scholar 

  • Sefton M, Johnson MH, Clayton L (1992) Synthesis and phosphorylation of uvomorulin during mouse early development. Development 115:313–318

    Article  CAS  PubMed  Google Scholar 

  • Serre JM, Lucas B, Martin SC, Heier JA, Shao X, Hardin J (2022) C elegans srGAP is an α-catenin M domain-binding protein that strengthens cadherin-dependent adhesion during morphogenesis. Development 149:dev200775

    Article  PubMed  PubMed Central  Google Scholar 

  • Serres M, Filhol O, Lickert H, Grangeasse C, Chambaz EM, Stappert J, Vincent C, Schmitt D (2000) The disruption of adherens junctions is associated with a decrease of E-cadherin phosphorylation by protein kinase CK2. Exp Cell Res 257:255–264

    Article  CAS  PubMed  Google Scholar 

  • Shafraz O, Rübsam M, Stahley SN, Caldara AL, Kowalczyk AP, Niessen CM, Sivasankar S (2018) E-cadherin binds to desmoglein to facilitate desmosome assembly. elife 7:e37629

    Article  PubMed  PubMed Central  Google Scholar 

  • Shao L, Kner P, Rego EH, Gustafsson MG (2011) Super-resolution 3D microscopy of live whole cells using structured illumination. Nat Methods 8:1044–1046

    Article  CAS  PubMed  Google Scholar 

  • Shen Y, Hirsch DS, Sasiela CA, Wu WJ (2008) Cdc42 regulates E-cadherin ubiquitination and degradation through an epidermal growth factor receptor to Src-mediated pathway. J Biol Chem 283:5127–5137

    Article  CAS  PubMed  Google Scholar 

  • Sheppard L, Green DG, Lerchbaumer G, Rothenberg KE, Fernandez-Gonzalez R, Tepass U (2022) The α-catenin mechanosensing M region is required for cell adhesion during tissue morphogenesis. J Cell Biol 222:e202108091

    Article  PubMed  PubMed Central  Google Scholar 

  • Shewan AM, Maddugoda M, Kraemer A, Stehbens SJ, Verma S, Kovacs EM, Yap AS (2005) Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell–cell contacts. Mol Biol Cell 16:4531–4542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slováková J, Sikora M, Arslan FN, Caballero-Mancebo S, Krens SG, Kaufmann WA, Merrin J, Heisenberg C-P (2022) Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells. Proc Natl Acad Sci USA 119:e2122030119

    Article  PubMed  PubMed Central  Google Scholar 

  • Smutny M, Cox HL, Leerberg JM, Kovacs EM, Conti MA, Ferguson C, Hamilton NA, Parton RG, Adelstein RS, Yap AS (2010) Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat Cell Biol 12:696–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smyrek I, Mathew B, Fischer S, Lissek S, Becker S, Stelzer E (2019) E-cadherin, actin, microtubules and FAK dominate different spheroid formation phases and important elements of tissue integrity. Biol Open 8:bio037051

    CAS  PubMed  Google Scholar 

  • Sokabe T, Fukumi-Tominaga T, Yonemura S, Mizuno A, Tominaga M (2010) The TRPV4 channel contributes to intercellular junction formation in keratinocytes. J Biol Chem 285:18749–18758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stappert J, Kemler R (1994) A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated. Cell Commun Adhes 2:319–327

    Article  CAS  Google Scholar 

  • Takeichi M (1991) Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251:1451–1455

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tepass U, Gruszynski-DeFeo E, Haag TA, Omatyar L, Török 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

    Article  CAS  PubMed  Google Scholar 

  • Thompson CJ, Su Z, Vu VH, Wu Y, Leckband DE, Schwartz DK (2020) Cadherin clusters stabilized by a combination of specific and nonspecific cis-interactions. elife 9:e59035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson CJ, Vu VH, Leckband DE, Schwartz DK (2021) Cadherin cis and trans interactions are mutually cooperative. Proc Natl Acad Sci USA 118:e2019845118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Troyanovsky RB, Sergeeva AP, Indra I, Chen C-S, Kato R, Shapiro L, Honig B, Troyanovsky SM (2021) Sorting of cadherin–catenin-associated proteins into individual clusters. Proc Natl Acad Sci USA 118:e2105550118

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Uozumi N, Yanagidani S, Miyoshi E, Ihara Y, Sakuma T, Gao C-X, Teshima T, Fujii S, Shiba T, Taniguchi N (1996) Purification and cDNA cloning of porcine brain GDP-L-Fuc: N-acetyl-β-D-glucosaminide α1→ 6fucosyltransferase. J Biol Chem 271:27810–27817

    Article  CAS  PubMed  Google Scholar 

  • Van Roy F, Berx G (2008) The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 65:3756–3788

    Article  CAS  PubMed  Google Scholar 

  • Vanderleest TE, Smits CM, Xie Y, Jewett CE, Blankenship JT, Loerke D (2018) Vertex sliding drives intercalation by radial coupling of adhesion and actomyosin networks during Drosophila germband extension. elife 7:e34586

    Article  PubMed  PubMed Central  Google Scholar 

  • Vargas DA, Sun M, Sadykov K, Kukuruzinska MA, Zaman MH (2016) The integrated role of Wnt/β-catenin, N-glycosylation, and E-cadherin-mediated adhesion in network dynamics. PLoS Comput Biol 12:e1005007

    Article  PubMed  PubMed Central  Google Scholar 

  • Verma S, Shewan AM, Scott JA, Helwani FM, den Elzen NR, Miki H, Takenawa T (2004) Arp2/3 activity is necessary for efficient formation of E-cadherin adhesive contacts. J Biol Chem 279:34062–34070

    Article  CAS  PubMed  Google Scholar 

  • Vicidomini G, Moneron G, Han KY, Westphal V, Ta H, Reuss M, Engelhardt J, Eggeling C, Hell SW (2011) Sharper low-power STED nanoscopy by time gating. Nat Methods 8:571–573

    Article  CAS  PubMed  Google Scholar 

  • Vu V, Light T, Sullivan B, Greiner D, Hristova K, Leckband D (2021) P120 catenin potentiates constitutive E-cadherin dimerization at the plasma membrane and regulates trans binding. Curr Biol 31:3017-3027.e7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker D, Georgopoulos NT, Southgate J (2010) Anti-social cells: predicting the influence of E-cadherin loss on the growth of epithelial cell populations. J Theor Biol 262:425–440

    Article  CAS  PubMed  Google Scholar 

  • Wang Y-C, Khan Z, Kaschube M, Wieschaus EF (2012) Differential positioning of adherens junctions is associated with initiation of epithelial folding. Nature 484:390–393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Allgeyer ES, Sirinakis G, Zhang Y, Hu K, Lessard MD, Li Y, Diekmann R, Phillips MA, Dobbie IM (2021) Implementation of a 4Pi-SMS super-resolution microscope. Nat Protoc 16:677–727

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Jiang J, Yang X, Zhou G, Wang L, Xiao B (2022) Tethering Piezo channels to the actin cytoskeleton for mechanogating via the cadherin-β-catenin mechanotransduction complex. Cell Rep 38:110342

    Article  CAS  PubMed  Google Scholar 

  • Watabe-Uchida M, Uchida N, Imamura Y, Nagafuchi A, Fujimoto K, Uemura T, Vermeulen S, Van Roy F, Adamson ED, Takeichi M (1998) α-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells. J Cell Biol 142:847–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wombacher R, Heidbreder M, Van De Linde S, Sheetz MP, Heilemann M, Cornish VW, Sauer M (2010) Live-cell super-resolution imaging with trimethoprim conjugates. Nat Methods 7:717–719

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Vendome J, Shapiro L, Ben-Shaul A, Honig B (2011) Transforming binding affinities from three dimensions to two with application to cadherin clustering. Nature 475:510–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Y, Kanchanawong P, Zaidel-Bar R (2015) Actin-delimited adhesion-independent clustering of E-cadherin forms the nanoscale building blocks of adherens junctions. Dev Cell 32:139–154

    Article  CAS  PubMed  Google Scholar 

  • Yao M, Qiu W, Liu R, Efremov AK, Cong P, Seddiki R, Payre M, Lim CT, Ladoux B, Mege R-M (2014) Force-dependent conformational switch of α-catenin controls vinculin binding. Nat Commun 5:4525

    Article  CAS  PubMed  Google Scholar 

  • Yap AS, Niessen CM, Gumbiner BM (1998) The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn. J Cell Biol 141:779–789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yap AS, Gomez GA, Parton RG (2015) Adherens junctions revisualized: organizing cadherins as nanoassemblies. Dev Cell 35:12–20

    Article  CAS  PubMed  Google Scholar 

  • Yonemura S, Itoh M, Nagafuchi A, Tsukita S (1995) Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. J Cell Sci 108:127–142

    Article  CAS  PubMed  Google Scholar 

  • Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M (2010) α-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12:533–542

    Article  CAS  PubMed  Google Scholar 

  • Yoshida C, Takeichi M (1982) Teratocarcinoma cell adhesion: identification of a cell-surface protein involved in calcium-dependent cell aggregation. Cell 28:217–224

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura M, Nishikawa A, Ihara Y, Si T, Taniguchi N (1995) Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc Natl Acad Sci USA 92:8754–8758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Q, Kim T, Rajagopal V (2022) Role of actin filaments and cis binding in cadherin clustering and patterning. PLoS Comput Biol 18:e1010257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu-Kemp H-C, Szymanski RA, Cortes DB, Gadda NC, Lillich ML, Maddox AS, Peifer M (2021) Micron-scale supramolecular myosin arrays help mediate cytoskeletal assembly at mature adherens junctions. J Cell Biol 221:e202103074

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaidel-Bar R (2013) Cadherin adhesome at a glance. J Cell Sci 126:373–378

    Article  CAS  PubMed  Google Scholar 

  • Zhai B, Villén J, Beausoleil SA, Mintseris J, Gygi SP (2008) Phosphoproteome analysis of Drosophila melanogaster embryos. J Proteome Res 7:1675–1682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Zhang Y, Ten Hagen KG (2008) A mucin-type O-glycosyltransferase modulates cell adhesion during Drosophila development. J Biol Chem 283:34076–34086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Sivasankar S, Nelson WJ, Chu S (2009) Resolving cadherin interactions and binding cooperativity at the single-molecule level. Proc Natl Acad Sci USA 106:109–114

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Kong D, Reichl L, Vogt N, Wolf F, Großhans J (2014) The glucosyltransferase Xiantuan of the endoplasmic reticulum specifically affects E-Cadherin expression and is required for gastrulation movements in Drosophila. Dev Biol 390:208–220

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Liang Y, Xu Z, Wang L, Zhou F, Li Z, Jin J, Yang Y, Fang Z, Hu Y (2008) N-Glycosylation affects the adhesive function of E-Cadherin through modifying the composition of adherens junctions (AJs) in human breast carcinoma cell line MDA-MB-435. J Cell Biochem 104:162–175

    Article  CAS  PubMed  Google Scholar 

  • Zhou F, Su J, Fu L, Yang Y, Zhang L, Wang L, Zhao H, Zhang D, Li Z, Zha X (2008) Unglycosylation at Asn-633 made extracellular domain of E-cadherin folded incorrectly and arrested in endoplasmic reticulum, then sequentially degraded by ERAD. Glycoconj J 25:727–740

    Article  CAS  PubMed  Google Scholar 

  • Zhu W, Leber B, Andrews DW (2001) Cytoplasmic O-glycosylation prevents cell surface transport of E-cadherin during apoptosis. EMBO J 20:5999–6007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu B, Chappuis-Flament S, Wong E, Jensen IE, Gumbiner BM, Leckband D (2003) Functional analysis of the structural basis of homophilic cadherin adhesion. Biophys J 84:4033–4042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zielinska DF, Gnad F, Schropp K, Wiśniewski JR, Mann M (2012) Mapping N-glycosylation sites across seven evolutionarily distant species reveals a divergent substrate proteome despite a common core machinery. Mol Cell 46:542–548

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the grants of the Deutsche Forschungsgemeinschaft (GR1945/10-1and GR1945/10-2 to JG)

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  1. Na Zhang and Matthias Häring share co-first authorship.

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  1. Department of Biology, Philipps University, 35043, Marburg, Germany

    Na Zhang, Jörg Großhans & Deqing Kong

  2. Göttingen Campus Institute for Dynamics of Biological Networks (CIDBN), Georg August University Göttingen, 37073, Göttingen, Germany

    Matthias Häring, Fred Wolf, Jörg Großhans & Deqing Kong

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NZ, MH and DK: wrote the manuscript and drew the figures; FW: helped improve the writing; JG and DK improved and revised the manuscript.

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Zhang, N., Häring, M., Wolf, F. et al. Dynamics and functions of E-cadherin complexes in epithelial cell and tissue morphogenesis. Mar Life Sci Technol 5, 585–601 (2023). https://doi.org/10.1007/s42995-023-00206-w

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