α-catenin, vinculin, and F-actin in strengthening E-cadherin cell-cell adhesions and mechanosensing

Cell Adhesion and Migration

Volumn 7, Issue 4, 2013, Pages 345-350

  Dufour, Sylvie ^a   Mège, René Marc ^b   Thiery, Jean Paul ^c,d  

^a INSTITUT CURIE   (France)

^b INSTITUT JACQUES MONOD   (France)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

Adhesion; Cadherin; Catenin; Cytoskeleton; Force; Mechanosensing; Strength; Vinculin

Indexed keywords

ACTIN; ALPHA CATENIN; F ACTIN; UVOMORULIN; VINCULIN;

CELL ADHESION; CYTOSKELETON; HUMAN; MECHANOTRANSDUCTION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

ADHESION; CADHERIN; CATENIN; CYTOSKELETON; FORCE; MECHANOSENSING; STRENGTH; VINCULIN;

ALPHA CATENIN; ANIMALS; CADHERINS; GENE EXPRESSION REGULATION; VINCULIN;

EID: 84883501935     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.25139     Document Type: Review

References (72)

1. Nollet F, Kools P, van Roy F. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 2000; 299:551-72; PMID:10835267; http://dx.doi.org/10.1006/jmbi.2000.3777
2. Hulpiau P, van Roy F. Molecular evolution of the cadherin superfamily. Int J Biochem Cell Biol 2009; 41:349-69; PMID:18848899; http://dx.doi.org/10. 1016/j.biocel.2008.09.027
3. Hulpiau P, van Roy F. New insights into the evolution of metazoan cadherins. Mol Biol Evol 2011; 28:647-57; PMID:20817718; http://dx.doi.org/10. 1093/molbev/msq233
4. Gumbiner BM. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 2005; 6:622-34; PMID:16025097; http://dx.doi.org/10.1038/ nrm1699
5. Redies C, Hertel N, Hübner CA. Cadherins and neuropsychiatric disorders. Brain Res 2012; 1470:130-44; PMID:22765916; http://dx.doi.org/10. 1016/j.brainres.2012.06.020
6. Jeanes A, Gottardi CJ, Yap AS. Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 2008; 27:6920-9; PMID:19029934; http://dx.doi.org/10.1038/onc.2008.343
7. Amagai M, Stanley JR. Desmoglein as a target in skin disease and beyond. J Invest Dermatol 2012; 132:776-84; PMID:22189787; http://dx.doi.org/10.1038/ jid.2011.390
8. Katsamba P, Carroll K, Ahlsen G, Bahna F, Vendome J, Posy S, et al. Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. Proc Natl Acad Sci U S A 2009; 106:11594-9; PMID:19553217; http://dx.doi.org/10.1073/pnas.0905349106
9. Wu Y, Vendome J, Shapiro L, Ben-Shaul A, Honig B. Transforming binding affinities from three dimensions to two with application to cadherin clustering. Nature 2011; 475:510-3; PMID:21796210; http://dx.doi.org/10.1038/nature10183
10. Ladoux B, Anon E, Lambert M, Rabodzey A, Hersen P, Buguin A, et al. Strength dependence of cadherin-mediated adhesions. Biophys J 2010; 98:534-42; PMID:20159149; http://dx.doi.org/10.1016/j.bpj.2009.10.044
11. Adams CL, Chen YT, Smith SJ, Nelson WJ. Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J Cell Biol 1998; 142:1105-19; PMID:9722621; http://dx.doi.org/10.1083/jcb.142.4.1105
12. Vasioukhin V, Bauer C, Yin M, Fuchs E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 2000; 100:209-19; PMID:10660044; http://dx.doi.org/10.1016/S0092-8674(00)81559-7
13. Lambert M, Padilla F, Mege RM. Immobilized dimers of N-cadherin-fc chimera mimic cadherinmediated cell contact formation: contribution of both outiside-in and inside-out signals. J Cell Sci 2000; 113:2207-19; PMID:10825293
14. Lambert M, Thoumine O, Brevier J, Choquet D, Riveline D, Mège RM. Nucleation and growth of cadherin adhesions. Exp Cell Res 2007; 313:4025-40; PMID:17765222; http://dx.doi.org/10.1016/j.yexcr.2007.07.035
15. Braga VM, Machesky LM, Hall A, Hotchin NA. The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J Cell Biol 1997; 137:1421-31; PMID:9182672; http://dx.doi.org/10.1083/jcb.137.6. 1421
16. Shewan AM, Maddugoda M, Kraemer A, Stehbens SJ, Verma S, Kovacs EM, et al. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol Biol Cell 2005; 16:4531-42; PMID:16030252; http://dx.doi.org/10.1091/mbc.E05-04-0330
17. Kovacs EM, Ali RG, McCormack AJ, Yap AS. E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J Biol Chem 2002; 277:6708-18; PMID:11744701; http://dx.doi.org/10.1074/jbc.M109640200
18. Kovacs EM, Goodwin M, Ali RG, Paterson AD, Yap AS. Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr Biol 2002; 12:379-82; PMID:11882288; http://dx.doi.org/10.1016/S0960-9822(02)00661-9
19. Kim NG, Koh E, Chen X, Gumbiner BM. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc Natl Acad Sci U S A 2011; 108:11930-5; PMID:21730131; http://dx.doi.org/10.1073/ pnas.1103345108
20. Cavallaro U, Christofori G. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer 2004; 4:118-32; PMID:14964308; http://dx.doi.org/10.1038/nrc1276
21. Mège RM, Gavard J, Lambert M. Regulation of cell-cell junctions by the cytoskeleton. Curr Opin Cell Biol 2006; 18:541-8; PMID:16905303; http://dx.doi.org/10.1016/j.ceb.2006.08.004
22. Chu YS, Thomas WA, Eder O, Pincet F, Perez E, Thiery JP, et al. Force measurements in E-cadherinmediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J Cell Biol 2004; 167:1183-94; PMID:15596540; http://dx.doi.org/10.1083/jcb.200403043
23. Friedl P, Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 2009; 10:445-57; PMID:19546857; http://dx.doi.org/10.1038/nrm2720
24. Cavey M, Rauzi M, Lenne PF, Lecuit T. A twotiered mechanism for stabilization and immobilization of E-cadherin. Nature 2008; 453:751-6; PMID:18480755; http://dx.doi.org/10.1038/nature06953
25. Ozawa M, Baribault H, Kemler R. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 1989; 8:1711-7; PMID:2788574
26. Imamura Y, Itoh M, Maeno Y, Tsukita S, Nagafuchi A. Functional domains of α-catenin required for the strong state of cadherin-based cell adhesion. J Cell Biol 1999; 144:1311-22; PMID:10087272; http://dx.doi.org/10.1083/jcb.144. 6.1311
27. Chen YT, Stewart DB, Nelson WJ. Coupling assembly of the E-cadherin/beta-catenin complex to efficient endoplasmic reticulum exit and basallateral membrane targeting of E-cadherin in polarized MDCK cells. J Cell Biol 1999; 144:687-99; PMID:10037790; http://dx.doi.org/10.1083/jcb.144.4.687
28. Desai R, Sarpal R, Ishiyama N, Pellikka M, Ikura M, Tepass U. Monomeric α-catenin links cadherin to the actin cytoskeleton. Nat Cell Biol 2013; 15:261-73; PMID:23417122; http://dx.doi.org/10.1038/ncb2685
29. Kobielak A, Fuchs E. Alpha-catenin: at the junction of intercellular adhesion and actin dynamics. Nat Rev Mol Cell Biol 2004; 5:614-25; PMID:15366705; http://dx.doi.org/10.1038/nrm1433
30. Geiger B, Tokuyasu KT, Dutton AH, Singer SJ. Vinculin, an intracellular protein localized at specialized sites where microfilament bundles terminate at cell membranes. Proc Natl Acad Sci U S A 1980; 77:4127-31; PMID:6776523; http://dx.doi.org/10.1073/pnas.77.7.4127
31. Geiger B, Bershadsky A. Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol 2001; 13:584-92; PMID:11544027; http://dx.doi.org/10.1016/S0955-0674(00)00255-6
32. Leerberg JM, Yap AS. Vinculin, cadherin mechanotransduction and homeostasis of cell-cell junctions. Protoplasma 2012; 250:817-29; PMID:23274283; http://dx.doi.org/10.1007/s00709-012-0475-6
33. Peng X, Nelson ES, Maiers JL, DeMali KA. New insights into vinculin function and regulation. Int Rev Cell Mol Biol 2011; 287:191-231; PMID:21414589; http://dx.doi.org/10.1016/B978-0-12-386043-9.00005-0
34. Bakolitsa C, Cohen DM, Bankston LA, Bobkov AA, Cadwell GW, Jennings L, et al. Structural basis for vinculin activation at sites of cell adhesion. Nature 2004; 430:583-6; PMID:15195105; http://dx.doi.org/10.1038/nature02610
35. Chen H, Choudhury DM, Craig SW. Coincidence of actin filaments and talin is required to activate vinculin. J Biol Chem 2006; 281:40389-98; PMID:17074767; http://dx.doi.org/10.1074/jbc. M607324200
36. Choi HJ, Pokutta S, Cadwell GW, Bobkov AA, Bankston LA, Liddington RC, et al. αE-catenin is an autoinhibited molecule that coactivates vinculin. Proc Natl Acad Sci U S A 2012; 109:8576-81; PMID:22586082; http://dx.doi.org/10. 1073/pnas.1203906109
37. Hazan RB, Kang L, Roe S, Borgen PI, Rimm DL. Vinculin is associated with the E-cadherin adhesion complex. J Biol Chem 1997; 272:32448-53; PMID:9405455; http://dx.doi.org/10.1074/jbc.272.51.32448
38. Sarpal R, Pellikka M, Patel RR, Hui FY, Godt D, Tepass U. Mutational analysis supports a core role for Drosophila α-catenin in adherens junction function. J Cell Sci 2012; 125:233-45; PMID:22266901; http://dx.doi.org/10.1242/jcs.096644
39. Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI. α-catenin is a molecular switch that binds E-cadherin-β-catenin and regulates actin-filament assembly. Cell 2005; 123:903-15; PMID:16325583; http://dx.doi.org/10.1016/j.cell.2005.09.021
40. Koslov ER, Maupin P, Pradhan D, Morrow JS, Rimm DL. Alpha-catenin can form asymmetric homodimeric complexes and/or heterodimeric complexes with beta-catenin. J Biol Chem 1997; 272:27301-6; PMID:9341178; http://dx.doi.org/10. 1074/jbc.272.43.27301
41. Rimm DL, Koslov ER, Kebriaei P, Cianci CD, Morrow JS. Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc Natl Acad Sci U S A 1995; 92:8813-7; PMID:7568023; http://dx.doi.org/10.1073/pnas.92.19.8813
42. Rangarajan ES, Izard T. Dimer asymmetry defines α-catenin interactions. Nat Struct Mol Biol 2013; 20:188-93; PMID:23292143; http://dx.doi.org/10.1038/nsmb.2479
43. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ. Deconstructing the cadherin-catenin-actin complex. Cell 2005; 123:889-901; PMID:16325582; http://dx.doi.org/10.1016/j.cell.2005.09.020
44. Abe K, Takeichi M. EPLIN mediates linkage of the cadherin catenin complex to F-actin and stabilizes the circumferential actin belt. Proc Natl Acad Sci U S A 2008; 105:13-9; PMID:18093941; http://dx.doi.org/10.1073/pnas.0710504105
45. Weiss EE, Kroemker M, Rüdiger AH, Jockusch BM, Rüdiger M. Vinculin is part of the cadherincatenin junctional complex: complex formation between alpha-catenin and vinculin. J Cell Biol 1998; 141:755-64; PMID:9566974; http://dx.doi.org/10.1083/jcb.141.3.755
46. Thomas WA, Boscher C, Chu YS, Cuvelier D, Martinez-Rico C, Seddiki R, et al. α-Catenin and vinculin cooperate to promote high E-cadherin-based adhesion strength. J Biol Chem 2013; 288:4957-69; PMID:23266828; http://dx.doi.org/10.1074/jbc. M112.403774
47. Dawes AT. A mathematical model of α-catenin dimerization at adherens junctions in polarized epithelial cells. J Theor Biol 2009; 257:480-8; PMID:19135061; http://dx.doi.org/10.1016/j.jtbi.2008.11.028
48. Kwiatkowski AV, Maiden SL, Pokutta S, Choi HJ, Benjamin JM, Lynch AM, et al. In vitro and in vivo reconstitution of the cadherin-catenin-actin complex from Caenorhabditis elegans. Proc Natl Acad Sci U S A 2010; 107:14591-6; PMID:20689042; http://dx.doi.org/10.1073/pnas.1007349107
49. Rangarajan ES, Izard T. The cytoskeletal protein α-catenin unfurls upon binding to vinculin. J Biol Chem 2012; 287:18492-9; PMID:22493458; http://dx.doi.org/10.1074/jbc.M112.351023
50. Peng X, Maiers JL, Choudhury D, Craig SW, DeMali KA. α-Catenin uses a novel mechanism to activate vinculin. J Biol Chem 2012; 287:7728-37; PMID:22235119; http://dx.doi.org/10.1074/jbc. M111.297481
51. Gavard J, Lambert M, Grosheva I, Marthiens V, Irinopoulou T, Riou JF, et al. Lamellipodium extension and cadherin adhesion: two cell responses to cadherin activation relying on distinct signalling pathways. J Cell Sci 2004; 117:257-70; PMID:14657280; http://dx.doi.org/10.1242/jcs.00857
52. Ganz A, Lambert M, Saez A, Silberzan P, Buguin A, Mège RM, et al. Traction forces exerted through N-cadherin contacts. Biol Cell 2006; 98:721-30; PMID:16895521; http://dx.doi.org/10.1042/BC20060039
53. Shewan AM, Maddugoda M, Kraemer A, Stehbens SJ, Verma S, Kovacs EM, et al. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol Biol Cell 2005; 16:4531-42; PMID:16030252; http://dx.doi.org/10.1091/mbc.E05-04-0330
54. Bershadsky A, Kozlov M, Geiger B. Adhesionmediated mechanosensitivity: a time to experiment, and a time to theorize. Curr Opin Cell Biol 2006; 18:472-81; PMID:16930976; http://dx.doi.org/10.1016/j.ceb.2006.08.012
55. Borghi N, Sorokina M, Shcherbakova OG, Weis WI, Pruitt BL, Nelson WJ, et al. E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. Proc Natl Acad Sci U S A 2012; 109:12568-73; PMID:22802638; http://dx.doi.org/10.1073/pnas. 1204390109
56. Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M. α-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 2010; 12:533-42; PMID:20453849; http://dx.doi.org/10.1038/ncb2055
57. Yang J, Dokurno P, Tonks NK, Barford D. Crystal structure of the M-fragment of alpha-catenin: implications for modulation of cell adhesion. EMBO J 2001; 20:3645-56; PMID:11447106; http://dx.doi.org/10.1093/emboj/20.14.3645
58. Pokutta S, Drees F, Takai Y, Nelson WJ, Weis WI. Biochemical and structural definition of the l-afadin-and actin-binding sites of alpha-catenin. J Biol Chem 2002; 277:18868-74; PMID:11907041; http://dx.doi.org/10.1074/jbc. M201463200
59. Sumida GM, Tomita TM, Shih W, Yamada S. Myosin II activity dependent and independent vinculin recruitment to the sites of E-cadherin-mediated cell-cell adhesion. BMC Cell Biol 2011; 12:48; PMID:22054176; http://dx.doi.org/10.1186/ 1471-2121-12-48
60. Huveneers S, Oldenburg J, Spanjaard E, van der Krogt G, Grigoriev I, Akhmanova A, et al. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J Cell Biol 2012; 196:641-52; PMID:22391038; http://dx.doi.org/10.1083/jcb.201108120
61. Twiss F, Le Duc Q, Van Der Horst S, Tabdili H, Van Der Krogt G, Wang N, et al. Vinculin-dependent Cadherin mechanosensing regulates efficient epithelial barrier formation. Biol Open 2012; 1:1128-40; PMID:23213393; http://dx.doi.org/10.1242/bio.20122428
62. le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N, Leckband D, et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J Cell Biol 2010; 189:1107-15; PMID:20584916; http://dx.doi.org/10.1083/jcb. 201001149
63. Thomas WA, Boscher C, Chu YS, Cuvelier D, Martinez-Rico C, Seddiki R, et al. α-Catenin and vinculin cooperate to promote high E-cadherin-based adhesion strength. J Biol Chem 2013; 288:4957-69; PMID:23266828; http://dx.doi.org/10.1074/jbc. M112.403774
64. Chu YS, Dufour S, Thiery JP, Perez E, Pincet F. Johnson-Kendall-Roberts theory applied to living cells. Phys Rev Lett 2005; 94:028102; PMID:15698233; http://dx.doi.org/10.1103/PhysRevLett.94.028102
65. Chu YS, Eder O, Thomas WA, Simcha I, Pincet F, Ben-Ze'ev A, et al. Prototypical type I E-cadherin and type II cadherin-7 mediate very distinct adhesiveness through their extracellular domains. J Biol Chem 2006; 281:2901-10; PMID:16253998; http://dx.doi.org/10.1074/jbc.M506185200
66. Capaldo CT, Macara IG. Depletion of E-cadherin disrupts establishment but not maintenance of cell junctions in Madin-Darby canine kidney epithelial cells. Mol Biol Cell 2007; 18:189-200; PMID:17093058; http://dx.doi.org/10.1091/ mbc.E06-05-0471
67. Bajpai S, Correia J, Feng Y, Figueiredo J, Sun SX, Longmore GD, et al. alpha-Catenin mediates initial E-cadherin-dependent cell-cell recognition and subsequent bond strengthening. Proc Natl Acad Sci U S A 2008; 105:18331-6; PMID:19017792; http://dx.doi.org/10.1073/pnas.0806783105
68. Vermeulen SJ, Bruyneel EA, Bracke ME, De Bruyne GK, Vennekens KM, Vleminckx KL, et al. Transition from the noninvasive to the invasive phenotype and loss of alpha-catenin in human colon cancer cells. Cancer Res 1995; 55:4722-8; PMID:7553655
69. Shimoyama Y, Nagafuchi A, Fujita S, Gotoh M, Takeichi M, Tsukita S, et al. Cadherin dysfunction in a human cancer cell line: possible involvement of loss of alpha-catenin expression in reduced cellcell adhesiveness. Cancer Res 1992; 52:5770-4; PMID:1394201
70. Tozeren A, Wu S, Hoxter B, Xu W, Adamson ED, Byers SW. Vinculin and cell-cell adhesion. Cell Adhes Commun 1998; 5:49-59; PMID:9638341; http://dx.doi.org/10.3109/15419069809005598
71. Zaidel-Bar R. Cadherin adhesome at a glance. J Cell Sci 2013; 126:373-8; PMID:23547085; http://dx.doi.org/10.1242/jcs.111559
72. Taguchi K, Ishiuchi T, Takeichi M. Mechanosensitive EPLIN-dependent remodeling of adherens junctions regulates epithelial reshaping. J Cell Biol 2011; 194:643-56; PMID:21844208; http://dx.doi.org/10.1083/jcb.201104124