1932

Abstract

Cadherins are the principal adhesion proteins at intercellular junctions and function as the biochemical Velcro that binds cells together. Besides this mechanical function, cadherin complexes are also mechanotransducers that sense changes in tension and trigger adaptive reinforcement of intercellular junctions. The assembly and regulation of cadherin adhesions are central to their mechanical functions, and new evidence is presented for a comprehensive model of cadherin adhesion, which is surprisingly more complex than previously appreciated. Recent findings also shed new light on mechanisms that regulate cadherin junction assembly, adhesion, and mechanotransduction. We further describe recent evidence for cadherin-based mechanotransduction, and the rudiments of the molecular mechanism, which involves α-catenin and vinculin as key elements. Potential roles of a broader cast of possible force-sensitive partners are considered, as well as known and speculative biological consequences of adhesion and force transduction at cadherin-mediated junctions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100913-013212
2014-10-06
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/30/1/annurev-cellbio-100913-013212.html?itemId=/content/journals/10.1146/annurev-cellbio-100913-013212&mimeType=html&fmt=ahah

Literature Cited

  1. Aono S, Nakagawa S, Reynolds AB, Takeichi M. 1999. p120ctn acts as an inhibitory regulator of cadherin function in colon carcinoma cells. J. Cell Biol. 145:551–62 [Google Scholar]
  2. Barry A, Tabdili H, Muhamed I, Wu J, Shashikanth N. et al. 2014. α-Catenin cytomechanics: role in cadherin-dependent adhesion and mechanotransduction. J. Cell Sci. 15:1779–91 [Google Scholar]
  3. Berx G, Becker KF, Höfler H, van Roy F. 1998. Mutations of the human E-cadherin (CDH1) gene. Hum. Mutat. 12:226–37 [Google Scholar]
  4. Berx G, van Roy F. 2009. Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb. Perspect. Biol. 1:a003129 [Google Scholar]
  5. Borghi N, Sorokina M, Shcherbakova OG, Weis WI, Pruitt BL. et al. 2012. E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. Proc. Natl. Acad. Sci. USA 109:12568–73 [Google Scholar]
  6. Braga VM. 2002. Cell-cell adhesion and signalling. Curr. Opin. Cell Biol. 14:546–56 [Google Scholar]
  7. Carisey A, Tsang R, Greiner AM, Nijenhuis N, Heath N. et al. 2013. Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Curr. Biol. 23:271–81 [Google Scholar]
  8. Cavey M, Rauzi M, Lenne PF, Lecuit T. 2008. A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453:751–56 [Google Scholar]
  9. Chesla SE, Selvaraj P, Zhu C. 1998. Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys. J. 75:1553–72 [Google Scholar]
  10. Chien YH, Jiang N, Li F, Zhang F, Zhu C, Leckband D. 2008. Two stage cadherin kinetics require multiple extracellular domains but not the cytoplasmic region. J. Biol. Chem. 283:1848–56 [Google Scholar]
  11. Choi HJ, Pokutta S, Cadwell GW, Bobkov AA, Bankston LA. et al. 2012. αE-catenin is an autoinhibited molecule that coactivates vinculin. Proc. Natl. Acad. Sci. USA 109:8576–81 [Google Scholar]
  12. Chopra A, Tabdanov E, Patel H, Janmey PA, Kresh JY. 2011. Cardiac myocyte remodeling mediated by N-cadherin-dependent mechanosensing. Am. J. Physiol. Heart Circ. Physiol. 300:H1252–66 [Google Scholar]
  13. Chtcheglova LA, Waschke J, Wildling L, Drenckhahn D, Hinterdorfer P. 2007. Nano-scale dynamic recognition imaging on vascular endothelial cells. Biophys. J. 93:L11–13 [Google Scholar]
  14. Ciatto C, Bahna F, Zampieri N, VanSteenhouse HC, Katsamba PS. et al. 2010. T-cadherin structures reveal a novel adhesive binding mechanism. Nat. Struct. Mol. Biol. 17:339–47 [Google Scholar]
  15. Colombelli J, Besser A, Kress H, Reynaud EG, Girard P. et al. 2009. Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J. Cell Sci. 122:1665–79 [Google Scholar]
  16. Conway DE, Breckenridge MT, Hinde E, Gratton E, Chen CS, Schwartz MA. 2013. Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1. Curr. Biol. 23:1024–30 [Google Scholar]
  17. Dames SA, Bang E, Haussinger D, Ahrens T, Engel J, Grzesiek S. 2008. Insights into the low adhesive capacity of human T-cadherin from the NMR structure of its N-terminal extracellular domain. J. Biol. Chem. 283:23485–95 [Google Scholar]
  18. de Rooij J, Kerstens A, Danuser G, Schwartz MA, Waterman-Storer CM. 2005. Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J. Cell Biol. 171:153–64 [Google Scholar]
  19. Dembo M, Torney DC, Saxman K, Hammer D. 1988. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. R. Soc. Lond. B Biol. Sci. 234:55–83 [Google Scholar]
  20. 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. 15:261–73 [Google Scholar]
  21. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S. et al. 2011. Role of YAP/TAZ in mechanotransduction. Nature 474:179–83 [Google Scholar]
  22. Ehrlicher AJ, Nakamura F, Hartwig JH, Weitz DA, Stossel TP. 2011. Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Nature 478:260–63 [Google Scholar]
  23. El-Amraoui A, Petit C. 2013. Cadherin defects in inherited human diseases. Prog. Mol. Biol. Transl. Sci. 116361–84 [Google Scholar]
  24. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677–89 [Google Scholar]
  25. Evans E, Ritchie K. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541–55 [Google Scholar]
  26. Evans EA, Calderwood DA. 2007. Forces and bond dynamics in cell adhesion. Science 316:1148–53 [Google Scholar]
  27. Gjorevski N, Nelson CM. 2010. Endogenous patterns of mechanical stress are required for branching morphogenesis. Integr. Biol. 2:424–34 [Google Scholar]
  28. Granados-Riveron JT, Brook JD. 2012. The impact of mechanical forces in heart morphogenesis. Circ. Cardiovasc. Genet. 5:132–42 [Google Scholar]
  29. Gumbiner BM. 2005. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6:622–34 [Google Scholar]
  30. Hahn C, Schwartz MA. 2009. Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10:53–62 [Google Scholar]
  31. Harrison OJ, Bahna F, Katsamba PS, Jin X, Brasch J. et al. 2010. Two-step adhesive binding by classical cadherins. Nat. Struct. Mol. Biol. 17:348–57 [Google Scholar]
  32. Harrison OJ, Jin X, Hong S, Bahna F, Ahlsen G. et al. 2011. The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 19:244–56 [Google Scholar]
  33. Haussinger D, Ahrens T, Sass HJ, Pertz O, Engel J, Grzesiek S. 2002. Calcium-dependent homoassociation of E-cadherin by NMR spectroscopy: changes in mobility, conformation and mapping of contact regions. J. Mol. Biol. 324:823–39 [Google Scholar]
  34. Higashida C, Kiuchi T, Akiba Y, Mizuno H, Maruoka J. et al. 2013. F- and G-actin homeostasis regulates mechanosensitive actin nucleation by formins. Nat. Cell Biol. 15:395–405 [Google Scholar]
  35. Hirata H, Tatsumi H, Sokabe M. 2008. Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J. Cell Sci. 121:2795–804 [Google Scholar]
  36. Hong S, Troyanovsky RB, Troyanovsky SM. 2011. Cadherin exits the junction by switching its adhesive bond. J. Cell Biol. 192:1073–83 [Google Scholar]
  37. Hong S, Troyanovsky RB, Troyanovsky SM. 2013. Binding to F-actin guides cadherin cluster assembly, stability, and movement. J. Cell Biol. 201:131–43 [Google Scholar]
  38. Hsu JC, Koo H, Harunaga JS, Matsumoto K, Doyle AD, Yamada KM. 2013. Region-specific epithelial cell dynamics during branching morphogenesis. Dev. Dyn. 242:1066–77 [Google Scholar]
  39. Hu J, Lipowsky R, Weikl TR. 2013. Binding constants of membrane-anchored receptors and ligands depend strongly on the nanoscale roughness of membranes. Proc. Natl. Acad. Sci. USA 110:15283–88 [Google Scholar]
  40. Huang J, Zarnitsyna VI, Liu B, Edwards LJ, Jiang N. et al. 2010. The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464:932–36 [Google Scholar]
  41. Huveneers S, de Rooij J. 2013. Mechanosensitive systems at the cadherin-F-actin interface. J. Cell Sci. 126:403–13 [Google Scholar]
  42. Huveneers S, Oldenburg J, Spanjaard E, van der Krogt G, Grigoriev I. et al. 2012. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J. Cell Biol. 196:641–52 [Google Scholar]
  43. Huynh J, Nishimura N, Rana K, Peloquin JM, Califano JP. et al. 2011. Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci. Transl. Med. 3:112ra22 [Google Scholar]
  44. Hynes RO. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:673–87 [Google Scholar]
  45. Imamura Y, Itoh M, Maeno Y, Tsukita S, Nagafuchi A. 1999. Functional domains of α-catenin required for the strong state of cadherin-based cell adhesion. J. Cell Biol. 144:1311–22 [Google Scholar]
  46. Ishiyama N, Ikura M. 2012. The three-dimensional structure of the cadherin-catenin complex. Sub-Cell. Biochem. 60:39–62 [Google Scholar]
  47. Ishiyama N, Tanaka N, Abe K, Yang YJ, Abbas YM. et al. 2013. An autoinhibited structure of α-catenin and its implications for vinculin recruitment to adherens junctions. J. Biol. Chem. 288:15913–25 [Google Scholar]
  48. 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. 2009:67–80 [Google Scholar]
  49. Jasaitis A, Estevez M, Heysch J, Ladoux B, Dufour S. 2012. E-cadherin-dependent stimulation of traction force at focal adhesions via the Src and PI3K signaling pathways. Biophys. J. 103:175–84 [Google Scholar]
  50. Jeanes A, Gottardi CJ, Yap AS. 2008. Cadherins and cancer: How does cadherin dysfunction promote tumor progression?. Oncogene 276920–29 [Google Scholar]
  51. Jiang N, Huang J, Edwards LJ, Liu B, Zhang Y. et al. 2011. Two-stage cooperative T cell receptor-peptide major histocompatibility complex-CD8 trimolecular interactions amplify antigen discrimination. Immunity 34:13–23 [Google Scholar]
  52. Kasza KE, Zallen JA. 2011. Dynamics and regulation of contractile actin-myosin networks in morphogenesis. Curr. Opin. Cell Biol. 2330–38 [Google Scholar]
  53. Kim NG, Koh E, Chen X, Gumbiner BM. 2011. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc. Natl. Acad. Sci. USA 10811930–35 [Google Scholar]
  54. Kitagawa M, Natori M, Murase S, Hirano S, Taketani S, Suzuki ST. 2000. Mutation analysis of cadherin-4 reveals amino acid residues of EC1 important for the structure and function. Biochem. Biophys. Res. Commun. 271:358–63 [Google Scholar]
  55. Kobielak A, Fuchs E. 2004. α-Catenin: at the junction of intercellular adhesion and actin dynamics. Nat. Rev. Mol. Cell Biol. 5:614–25 [Google Scholar]
  56. Kris AS, Kamm RD, Sieminski AL. 2008. VASP involvement in force-mediated adherens junction strengthening. Biochem. Biophys. Res. Commun. 375:134–38 [Google Scholar]
  57. Ladoux B, Anon E, Lambert M, Rabodzey A, Hersen P. et al. 2010. Strength dependence of cadherin-mediated adhesions. Biophys. J. 98:534–42 [Google Scholar]
  58. Lampugnani MG, Resnati M, Raiteri M, Pigott R, Pisacane A. et al. 1992. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118:1511–22 [Google Scholar]
  59. Langer MD, Guo HB, Shashikanth N, Pierce M, Leckband D. 2012. N-glycosylation alters cadherin-mediated intercellular binding kinetics. J. Cell Sci. 125:2478–85 [Google Scholar]
  60. Le Clainche C, Dwivedi SP, Didry D, Carlier MF. 2010. Vinculin is a dually regulated actin filament barbed end-capping and side-binding protein. J. Biol. Chem. 285:23420–32 [Google Scholar]
  61. le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N. et al. 2010. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II–dependent manner. J. Cell Biol. 189:1107–15 [Google Scholar]
  62. Leckband D, Israelachvili J. 2001. Intermolecular forces in biology. Q. Rev. Biophys. 34:105–267 [Google Scholar]
  63. Leckband D, Prakasam A. 2006. Mechanism and dynamics of cadherin adhesion. Annu. Rev. Biomed. Eng. 8:259–87 [Google Scholar]
  64. Leckband D, Sivasankar S. 2012a. Biophysics of cadherin adhesion. Sub-Cell. Biochem. 60:63–88 [Google Scholar]
  65. Leckband D, Sivasankar S. 2012b. Cadherin recognition and adhesion. Curr. Opin. Cell Biol. 24:620–27 [Google Scholar]
  66. Leckband DE, le Duc Q, Wang N, de Rooij J. 2011. Mechanotransduction at cadherin-mediated adhesions. Curr. Opin. Cell Biol. 23:523–30 [Google Scholar]
  67. Lecuit T, Lenne PF, Munro E. 2011. Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 27:157–84 [Google Scholar]
  68. Levayer R, Lecuit T. 2013. Oscillation and polarity of E-cadherin asymmetries control actomyosin flow patterns during morphogenesis. Dev. Cell 26:162–75 [Google Scholar]
  69. Li F, Leckband D. 2006. Dynamic strength of molecularly bonded surfaces. J. Chem. Phys. 125:194702 [Google Scholar]
  70. Liu Z, Tan JL, Cohen DM, Yang MT, Sniadecki NJ. et al. 2010. Mechanical tugging force regulates the size of cell-cell junctions. Proc. Natl. Acad. Sci. USA 107:9944–49 [Google Scholar]
  71. Liwosz A, Lei T, Kukuruzinska MA. 2006. N-glycosylation affects the molecular organization and stability of E-cadherin junctions. J. Biol. Chem. 281:23138–49 [Google Scholar]
  72. Lu P, Weaver VM, Werb Z. 2012. The extracellular matrix: a dynamic niche in cancer progression. J. Cell Biol. 196:395–406 [Google Scholar]
  73. Maddugoda MP, Crampton MS, Shewan AM, Yap AS. 2007. Myosin VI and vinculin cooperate during the morphogenesis of cadherin cell cell contacts in mammalian epithelial cells. J. Cell Biol. 178:529–40 [Google Scholar]
  74. Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C. 2003. Direct observation of catch bonds involving cell-adhesion molecules. Nature 423:190–93 [Google Scholar]
  75. Maruthamuthu V, Sabass B, Schwarz US, Gardel ML. 2011. Cell-ECM traction force modulates endogenous tension at cell-cell contacts. Proc. Natl. Acad. Sci. USA 108:4708–13 [Google Scholar]
  76. McLachlan RW, Yap AS. 2007. Not so simple: the complexity of phosphotyrosine signaling at cadherin adhesive contacts. J. Mol. Med. 85:545–54 [Google Scholar]
  77. Nagar B, Overduin M, Ikura M, Rini JM. 1996. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380:360–64 [Google Scholar]
  78. Ng MR, Besser A, Danuser G, Brugge JS. 2012. Substrate stiffness regulates cadherin-dependent collective migration through myosin-II contractility. J. Cell Biol. 199:545–63 [Google Scholar]
  79. Nguyen TN, Uemura A, Shih W, Yamada S. 2010. Zyxin-mediated actin assembly is required for efficient wound closure. J. Biol. Chem. 285:35439–45 [Google Scholar]
  80. Nieset JE, Redfield AR, Jin F, Knudsen KA, Johnson KR, Wheelock MJ. 1997. Characterization of the interactions of α-catenin with α-actinin and β-catenin/plakoglobin. J. Cell Sci. 110:Pt. 81013–22 [Google Scholar]
  81. Niessen CM, Leckband D, Yap AS. 2011. Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation. Physiol. Rev. 91:691–731 [Google Scholar]
  82. Nita-Lazar M, Noonan V, Rebustini I, Walker J, Menko AS, Kukuruzinska MA. 2009. Overexpression of DPAGT1 leads to aberrant N-glycosylation of E-cadherin and cellular discohesion in oral cancer. Cancer Res. 69:5673–80 [Google Scholar]
  83. Nita-Lazar M, Rebustini I, Walker J, Kukuruzinska MA. 2010. Hypoglycosylated E-cadherin promotes the assembly of tight junctions through the recruitment of PP2A to adherens junctions. Exp. Cell Res. 316:1871–84 [Google Scholar]
  84. Pacquelet A, Rorth P. 2005. Regulatory mechanisms required for DE-cadherin function in cell migration and other types of adhesion. J. Cell Biol. 170:803–12 [Google Scholar]
  85. Petrova YI, Spano MJ, Gumbiner BM. 2012. Conformational epitopes at cadherin binding sites and p120-catenin phosphorylation regulate cell adhesion. Mol. Biol. Cell 23:2092–108 [Google Scholar]
  86. Prakasam A, Chien YH, Maruthamuthu V, Leckband DE. 2006. Calcium site mutations in cadherin: impact on adhesion and evidence of cooperativity. Biochemistry 45:6930–39 [Google Scholar]
  87. Rakshit S, Zhang Y, Manibog K, Shafraz O, Sivasankar S. 2012. Ideal, catch, and slip bonds in cadherin adhesion. Proc. Natl. Acad. Sci. USA 109:18815–20 [Google Scholar]
  88. Rangarajan ES, Izard T. 2012. The cytoskeletal protein α-catenin unfurls upon binding to vinculin. J. Biol. Chem. 287:18492–99 [Google Scholar]
  89. Rangarajan ES, Izard T. 2013. Dimer asymmetry defines α-catenin interactions. Nat. Struct. Mol. Biol. 20:188–93 [Google Scholar]
  90. Ranscht B, Dours-Zimmermann MT. 1991. T-cadherin, a novel cadherin cell adhesion molecule in the nervous system lacks the conserved cytoplasmic region. Neuron 7:391–402 [Google Scholar]
  91. Rauzi M, Lenne PF, Lecuit T. 2010. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468:1110–14 [Google Scholar]
  92. Roh-Johnson M, Shemer G, Higgins CD, McClellan JH, Werts AD. et al. 2012. Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science 335:1232–35 [Google Scholar]
  93. Sarpal R, Pellikka M, Patel RR, Hui FYW, Godt D, Tepass U. 2012. Mutational analysis supports a core role for Drosophila α-catenin in adherens junction function. J. Cell Sci. 125:233–45 [Google Scholar]
  94. Sawyer JK, Choi W, Jung KC, He L, Harris NJ, Peifer M. 2011. A contractile actomyosin network linked to adherens junctions by Canoe/afadin helps drive convergent extension. Mol. Biol. Cell 22:2491–508 [Google Scholar]
  95. 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 [Google Scholar]
  96. 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 [Google Scholar]
  97. Schepis A, Sepich D, Nelson WJ. 2012. αE-catenin regulates cell-cell adhesion and membrane blebbing during zebrafish epiboly. Development 139:537–46 [Google Scholar]
  98. Scott JA, Shewan AM, den Elzen NR, Loureiro JJ, Gertler FB, Yap AS. 2006. Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts. Mol. Biol. Cell 17:1085–95 [Google Scholar]
  99. Serra-Picamal X, Conte V, Vincent R, Anon E, Tambe DT. et al. 2012. Mechanical waves during tissue expansion. Nat. Phys. 8:628–34 [Google Scholar]
  100. Shan W, Yagita Y, Wang Z, Koch A, Fex Svenningsen A. et al. 2004. The minimal essential unit for cadherin-mediated intercellular adhesion comprises extracellular domains 1 and 2. J. Biol. Chem. 279:55914–23 [Google Scholar]
  101. Shapiro L, Weis WI. 2009. Structure and biochemistry of cadherins and catenins. Cold Spring Harb. Perspect. Biol. 1:1–22 [Google Scholar]
  102. Shemesh T, Bershadsky AD, Kozlov MM. 2005. Force-driven polymerization in cells: actin filaments and focal adhesions. J. Phys. Condens. Matter 17:S3913–S28 [Google Scholar]
  103. Shewan AM, Maddugoda M, Kraemer A, Stehbens SJ, Verma S. et al. 2005. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 16:4531–42 [Google Scholar]
  104. Shi Q, Maruthamuthu V, Leckband D. 2010. Allosteric cross-talk between cadherin ectodomains. Biophys. J. 99:95–104 [Google Scholar]
  105. Smith MA, Blankman E, Gardel ML, Luettjohann L, Waterman CM, Beckerle MC. 2010. A zyxin-mediated mechanism for actin stress fiber maintenance and repair. Dev. Cell 19:365–76 [Google Scholar]
  106. Sperry RB, Bishop NH, Bramwell JJ, Brodeur MN, Carter MJ. et al. 2010. Zyxin controls migration in epithelial-mesenchymal transition by mediating actin-membrane linkages at cell-cell junctions. J. Cell. Physiol. 222:612–24 [Google Scholar]
  107. Tabdili H, Langer M, Shi Q, Poh Y-C, Wang N, Leckband D. 2012. Cadherin-dependent mechanotransduction depends on ligand identity but not affinity. J. Cell Sci. 125:4362–71 [Google Scholar]
  108. Taguchi K, Ishiuchi T, Takeichi M. 2011. Mechanosensitive EPLIN-dependent remodeling of adherens junctions regulates epithelial reshaping. J. Cell Biol. 194:643–56 [Google Scholar]
  109. Takeichi M. 1990. Cadherins: a molecular family important in selective cell-cell adhesion. Annu. Rev. Biochem. 59:237–52 [Google Scholar]
  110. Tamura K, Shan WS, Hendrickson WA, Colman DR, Shapiro L. 1998. Structure-function analysis of cell adhesion by neural (N-)cadherin. Neuron 20:1153–63 [Google Scholar]
  111. Tang VW, Brieher WM. 2012. α-Actinin-4/FSGS1 is required for Arp2/3-dependent actin assembly at the adherens junction. J. Cell Biol. 196:115–30 [Google Scholar]
  112. Tepass U, Truong K, Gotd D, Ikura M, Peifer M. 2000. Cadherins in embryonic and neural morphogenesis. Nat. Rev. Mol. Cell Biol. 1:91–100 [Google Scholar]
  113. Thomas W. 2008. Catch bonds in adhesion. Annu. Rev. Biomed. Eng. 10:39–57 [Google Scholar]
  114. Thomas WA, Boscher C, Chu YS, Cuvelier D, Martinez-Rico C. et al. 2013. α-Catenin and vinculin cooperate to promote high E-cadherin-based adhesion strength. J. Biol. Chem. 288:4957–69 [Google Scholar]
  115. Troyanovsky RB, Sokolov E, Troyanovsky SM. 2003. Adhesive and lateral E-cadherin dimers are mediated by the same interface. Mol. Cell. Biol. 23:7965–72 [Google Scholar]
  116. Truong Quang BA, Mani M, Markova O, Lecuit T, Lenne PF. 2013. Principles of E-cadherin supramolecular organization in vivo. Curr. Biol. 23:2197–207 [Google Scholar]
  117. Tsuiji H, Xu L, Schwartz K, Gumbiner BM. 2007. Cadherin conformations associated with dimerization and adhesion. J. Biol. Chem. 282:12871–82 [Google Scholar]
  118. Twiss F, le Duc Q, Van Der Horst S, Tabdili H, Van Der Krogt G. et al. 2012. Vinculin-dependent cadherin mechanosensing regulates efficient epithelial barrier formation. Biol. Open 1:1128–40 [Google Scholar]
  119. Tzima E, Irani-Tehrani Kiosses M WB, Dejana E, Schultz DA. et al. 2005. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437:426–31 [Google Scholar]
  120. Valbuena A, Vera AM, Oroz J, Menéndez M, Carrión-Vázquez M. 2012. Mechanical properties of β-catenin revealed by single-molecule experiments. Biophys. J. 103:1744–52 [Google Scholar]
  121. Watabe-Uchida M, Uchida N, Imamura Y, Nagafuchi A, Fujimoto K. et al. 1998. α-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells. J. Cell Biol. 142:847–57 [Google Scholar]
  122. Weber GF, Bjerke MA, DeSimone DW. 2012. A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev. Cell 22:104–15 [Google Scholar]
  123. Wen KK, Rubenstein PA, DeMali KA. 2009. Vinculin nucleates actin polymerization and modifies actin filament structure. J. Biol. Chem. 284:30463–73 [Google Scholar]
  124. Wheelock MJ, Johnson KR. 2003. Cadherin-mediated cellular signaling. Curr. Opin. Cell Biol. 15:509–14 [Google Scholar]
  125. Wu Y, Jin X, Harrison O, Shapiro L, Honig BH, Ben-Shaul A. 2010. Cooperativity between trans and cis interactions in cadherin-mediated junction formation. Proc. Natl. Acad. Sci. USA 107:17592–97 [Google Scholar]
  126. 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 475:510–13 [Google Scholar]
  127. Yap AS, Kovacs EM. 2003. Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell Biol. 160:11–16 [Google Scholar]
  128. Yonemura S. 2011. A mechanism of mechanotransduction at the cell-cell interface. BioEssays 33:732–36 [Google Scholar]
  129. 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. 12:533–42 [Google Scholar]
  130. Zemljic-Harpf AE, Godoy J, Platoshyn O, Asfaw EK, Busija AR. et al. 2014. Vinculin directly binds zonula occludens-1 and is essential for stabilizing connexin 43 containing gap junctions in cardiac myocytes. J. Cell Sci. 127:1104–16 [Google Scholar]
  131. 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 106:109–14 [Google Scholar]
  132. Zhu C, Bao G, Wang N. 2000. Cell mechanics: mechanical response, cell adhesion, and molecular deformation. Annu. Rev. Biomed. Eng. 2:189–226 [Google Scholar]
  133. Ziegler WH, Liddington RC, Critchley DR. 2006. The structure and regulation of vinculin. Trends Cell Biol. 16:453–60 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100913-013212
Loading
/content/journals/10.1146/annurev-cellbio-100913-013212
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error