The secret life of α-catenin: Moonlighting in morphogenesis

Journal of Cell Biology

Volumn 195, Issue 4, 2011, Pages 543-552

  Maiden, Stephanie L ^a   Hardin, Jeff ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; ALPHA CATENIN; BETA CATENIN; CADHERIN; F ACTIN; RHO FACTOR; UVOMORULIN;

BINDING AFFINITY; CELL ADHESION; CELL INTERACTION; CELL STRESS; COMPLEX FORMATION; CYTOPLASM; HUMAN; MECHANOTRANSDUCTION; MOLECULAR MECHANICS; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW;

ALPHA CATENIN; ANIMALS; CELL ADHESION; CYTOPLASM; HUMANS; MORPHOGENESIS;

EID: 81355138558     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201103106     Document Type: Review

References (78)

1. Abe, K., and M. Takeichi. 2008. EPLIN mediates linkage of the cadherin catenin complex to F-actin and stabilizes the circumferential actin belt. Proc. Natl. Acad. Sci. USA. 105:13-19. http://dx.doi.org/10.1073/pnas.0710504105
2. Aberle, H., S. Butz, J. Stappert, H. Weissig, R. Kemler, and H. Hoschuetzky. 1994. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci. 107:3655-3663.
3. Anastasiadis, P.Z. 2007. p120-ctn: A nexus for contextual signaling via Rho GTPases. Biochim. Biophys. Acta. 1773:34-46. http://dx.doi.org/10.1016/j.bbamcr.2006.08.040
4. Barstead, R.J., and R.H. Waterston. 1989. The basal component of the nematode dense-body is vinculin. J. Biol. Chem. 264:10177-10185.
5. Benjamin, J.M., and W.J. Nelson. 2008. Bench to bedside and back again: molecular mechanisms of alpha-catenin function and roles in tumorigenesis. Semin. Cancer Biol. 18:53-64. http://dx.doi.org/10.1016/j.semcancer.2007.08.003
6. Benjamin, J.M., A.V. Kwiatkowski, C. Yang, F. Korobova, S. Pokutta, T. Svitkina, W.I. Weis, and W.J. Nelson. 2010. AlphaE-catenin regulates actin dynamics independently of cadherin-mediated cell-cell adhesion. J. Cell Biol. 189:339-352. http://dx.doi.org/10.1083/jcb.200910041
7. Bershadsky, A.D., N.Q. Balaban, and B. Geiger. 2003. Adhesion-dependent cell mechanosensitivity. Annu. Rev. Cell Dev. Biol. 19:677-695. http://dx.doi.org/10.1146/annurev.cellbio.19.111301.153011
8. Borghi, N., M. Lowndes, V. Maruthamuthu, M.L. Gardel, and W.J. Nelson. 2010. Regulation of cell motile behavior by crosstalk between cadherinand integrin-mediated adhesions. Proc. Natl. Acad. Sci. USA. 107:13324-13329. http://dx.doi.org/10.1073/pnas.1002662107
9. Cadigan, K.M., and M. Peifer. 2009. Wnt signaling from development to disease: insights from model systems. Cold Spring Harb. Perspect. Biol. 1:a002881. http://dx.doi.org/10.1101/cshperspect.a002881
10. Cavey, M., and T. Lecuit. 2009. Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harb. Perspect. Biol. 1:a002998. http://dx.doi.org/10.1101/cshperspect.a002998
11. Cavey, M., M. Rauzi, P.F. Lenne, and T. Lecuit. 2008. A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature. 453:751-756. http://dx.doi.org/10.1038/nature06953
12. Chausovsky, A., A.D. Bershadsky, and G.G. Borisy. 2000. Cadherin-mediated regulation of microtubule dynamics. Nat. Cell Biol. 2:797-804. http://dx.doi.org/10.1038/35041037
13. Costa, M., W. Raich, C. Agbunag, B. Leung, J. Hardin, and J.R. Priess. 1998. A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 141:297-308. http://dx.doi.org/10.1083/jcb.141.1.297
14. del Rio, A., R. Perez-Jimenez, R. Liu, P. Roca-Cusachs, J.M. Fernandez, and M.P. Sheetz. 2009. Stretching single talin rod molecules activates vinculin binding. Science. 323:638-641. http://dx.doi.org/10.1126/science.1162912
15. Drees, F., S. Pokutta, S. Yamada, W.J. Nelson, and W.I. Weis. 2005. Alphacatenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell. 123:903-915. http://dx.doi.org/10.1016/j.cell.2005.09.021
16. Ehrlich, J.S., M.D. Hansen, and W.J. Nelson. 2002. Spatio-temporal regulation of Rac1 localization and lamellipodia dynamics during epithelial cell-cell adhesion. Dev. Cell. 3:259-270. http://dx.doi.org/10.1016/S1534-5807(02)00216-2
17. Franke, W.W. 2009. Discovering the molecular components of intercellular junctions- a historical view. Cold Spring Harb. Perspect. Biol. 1:a003061. http://dx.doi.org/10.1101/cshperspect.a003061
18. Gates, J., and M. Peifer. 2005. Can 1000 reviews be wrong? Actin, alpha-Catenin, and adherens junctions. Cell. 123:769-772. http://dx.doi.org/10.1016/j.cell.2005.11.009
19. Gottardi, C.J., and B.M. Gumbiner. 2004. Distinct molecular forms of betacatenin are targeted to adhesive or transcriptional complexes. J. Cell Biol. 167:339-349. http://dx.doi.org/10.1083/jcb.200402153
20. Grashoff, C., B.D. Hoffman, M.D. Brenner, R. Zhou, M. Parsons, M.T. Yang, M.A. McLean, S.G. Sligar, C.S. Chen, T. Ha, and M.A. Schwartz. 2010. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature. 466:263-266. http://dx.doi.org/10.1038/nature09198
21. Gumbiner, B.M. 1996. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 84:345-357. http://dx.doi.org/10.1016/S0092-8674(00)81279-9
22. Hanahan, D., and R.A. Weinberg. 2011. Hallmarks of cancer: the next generation. Cell. 144:646-674. http://dx.doi.org/10.1016/j.cell.2011.02.013
23. Herrenknecht, K., M. Ozawa, C. Eckerskorn, F. Lottspeich, M. Lenter, and R. Kemler. 1991. The uvomorulin-anchorage protein alpha catenin is avinculin homologue. Proc. Natl. Acad. Sci. USA. 88:9156-9160. http://dx.doi.org/10.1073/pnas.88.20.9156
24. Heuberger, J., and W. Birchmeier. 2010. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb. Perspect. Biol. 2:a002915. http://dx.doi.org/10.1101/cshperspect.a002915
25. Huber, A.H., W.J. Nelson, and W.I. Weis. 1997a. Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell. 90:871-882. http://dx.doi.org/10.1016/S0092-8674(00)80352-9
26. Huber, O., M. Krohn, and R. Kemler. 1997b. A specific domain in alphacatenin mediates binding to beta-catenin or plakoglobin. J. Cell Sci. 110:1759-1765.
27. Imamura, Y., M. Itoh, Y. Maeno, S. Tsukita, and A. Nagafuchi. 1999. Functional domains of alpha-catenin required for the strong state of cadherin-based cell adhesion. J. Cell Biol. 144:1311-1322. http://dx.doi.org/10.1083/jcb.144.6.1311
28. Itoh, M., A. Nagafuchi, S. Moroi, and S. Tsukita. 1997. Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J. Cell Biol. 138:181-192. http://dx.doi.org/10.1083/jcb.138.1.181
29. Kim, N.G., E. Koh, X. Chen, and B.M. Gumbiner. 2011. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc. Natl. Acad. Sci. USA. 108:11930-11935. http://dx.doi.org/10.1073/pnas.1103345108
30. Knudsen, K.A., A.P. Soler, K.R. Johnson, and M.J. Wheelock. 1995. Interaction of alpha-actinin with the cadherin/catenin cell-cell adhesion complex via alpha-catenin. J. Cell Biol. 130:67-77. http://dx.doi.org/10.1083/jcb.130.1.67
31. Kobielak, A., H.A. Pasolli, and E. Fuchs. 2004. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat. Cell Biol. 6:21-30. http://dx.doi.org/10.1038/ncb1075
32. Koslov, E.R., P. Maupin, D. Pradhan, J.S. Morrow, and D.L. Rimm. 1997. Alpha-catenin can form asymmetric homodimeric complexes and/or heterodimeric complexes with beta-catenin. J. Biol. Chem. 272:27301-27306. http://dx.doi.org/10.1074/jbc.272.43.27301
33. Kostetskii, I., J. Li, Y. Xiong, R. Zhou, V.A. Ferrari, V.V. Patel, J.D. Molkentin, and G.L. Radice. 2005. Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ. Res. 96:346-354. http://dx.doi.org/10.1161/01.RES.0000156274.72390.2c
34. Kwiatkowski, A.V., S.L. Maiden, S. Pokutta, H.J. Choi, J.M. Benjamin, A.M. Lynch, W.J. Nelson, W.I. Weis, and J. Hardin. 2010. In vitro and in vivo reconstitution of the cadherin-catenin-actin complex from Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 107:14591-14596. http://dx.doi.org/10.1073/pnas.1007349107
35. le Duc, Q., Q. Shi, I. Blonk, A. Sonnenberg, N. Wang, D. Leckband, and J. de Rooij. 2010. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin IIdependent manner. J. Cell Biol. 189:1107-1115. http://dx.doi.org/10.1083/jcb.201001149
36. Lien, W.H., O. Klezovitch, T.E. Fernandez, J. Delrow, and V. Vasioukhin. 2006. alphaE-catenin controls cerebral cortical size by regulating the hedgehog signaling pathway. Science. 311:1609-1612. http://dx.doi.org/10.1126/science.1121449
37. Lien, W.H., V.I. Gelfand, and V. Vasioukhin. 2008. Alpha-E-catenin binds to dynamitin and regulates dynactin-mediated intracellular traffic. J. Cell Biol. 183:989-997. http://dx.doi.org/10.1083/jcb.200805041
38. Luo, Y., M. Ferreira-Cornwell, H. Baldwin, I. Kostetskii, J. Lenox, M. Lieberman, and G. Radice. 2001. Rescuing the N-cadherin knockout by cardiacspecific expression of N- or E-cadherin. Development. 128:459-469.
39. Magie, C.R., D. Pinto-Santini, and S.M. Parkhurst. 2002. Rho1 interacts with p120ctn and alpha-catenin, and regulates cadherin-based adherens junction components in Drosophila. Development. 129:3771-3782.
40. Nagafuchi, A., and M. Takeichi. 1988. Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO J. 7:3679-3684.
41. Nagafuchi, A., and M. Takeichi. 1989. Transmembrane control of cadherinmediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell Regul. 1:37-44.
42. Nagafuchi, A., M. Takeichi, and S. Tsukita. 1991. The 102 kd cadherinassociated protein: similarity to vinculin and posttranscriptional regulation of expression. Cell. 65:849-857. http://dx.doi.org/10.1016/0092-8674(91) 90392-C
43. Nagafuchi, A., S. Ishihara, and S. Tsukita. 1994. The roles of catenins in the cadherin-mediated cell adhesion: functional analysis of E-cadherin-alpha catenin fusion molecules. J. Cell Biol. 127:235-245. http://dx.doi.org/10.1083/jcb.127.1.235
44. Nelson, W.J., and R. Nusse. 2004. Convergence of Wnt, beta-catenin, and cadherin pathways. Science. 303:1483-1487. http://dx.doi.org/10.1126/science.1094291
45. Nieset, J.E., A.R. Redfield, F. Jin, K.A. Knudsen, K.R. Johnson, and M.J. Wheelock. 1997. Characterization of the interactions of alpha-catenin with alpha-actinin and beta-catenin/plakoglobin. J. Cell Sci. 110:1013-1022.
46. Ozawa, M., H. Baribault, and R. Kemler. 1989. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J. 8:1711-1717.
47. Ozawa, M., M. Ringwald, and R. Kemler. 1990. Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule. Proc. Natl. Acad. Sci. USA. 87:4246-4250. http://dx.doi.org/10.1073/pnas.87.11.4246
48. Pacquelet, A., and P. Rørth. 2005. Regulatory mechanisms required for DE-cadherin function in cell migration and other types of adhesion. J. Cell Biol. 170:803-812. http://dx.doi.org/10.1083/jcb.200506131
49. Pappas, D.J., and D.L. Rimm. 2006. Direct interaction of the C-terminal domain of alpha-catenin and F-actin is necessary for stabilized cell-cell adhesion. Cell Commun. Adhes. 13:151-170. http://dx.doi.org/10.1080/15419060600726142
50. Peifer, M., P.D. McCrea, K.J. Green, E. Wieschaus, and B.M. Gumbiner. 1992. The vertebrate adhesive junction proteins beta-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J. Cell Biol. 118:681-691. http://dx.doi.org/10.1083/jcb.118.3.681
51. Pettitt, J., E.A. Cox, I.D. Broadbent, A. Flett, and J. Hardin. 2003. The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis. J. Cell Biol. 162:15-22. http://dx.doi.org/10.1083/jcb.200212136
52. Pokutta, S., and W.I. Weis. 2000. Structure of the dimerization and beta-cateninbinding region of alpha-catenin. Mol. Cell. 5:533-543. http://dx.doi.org/10.1016/S1097-2765(00)80447-5
53. Pokutta, S., F. Drees, Y. Takai, W.J. Nelson, and W.I. Weis. 2002. Biochemical and structural definition of the l-afadin- and actin-binding sites of alphacatenin. J. Biol. Chem. 277:18868-18874. http://dx.doi.org/10.1074/jbc.M201463200
54. Pokutta, S., F. Drees, S. Yamada, W.J. Nelson, and W.I. Weis. 2008. Biochemical and structural analysis of alpha-catenin in cell-cell contacts. Biochem. Soc. Trans. 36:141-147. http://dx.doi.org/10.1042/BST0360141
55. Priess, J.R., and D.I. Hirsh. 1986. Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev. Biol. 117:156-173. http://dx.doi.org/10.1016/0012-1606(86)90358-1
56. Radice, G.L., H. Rayburn, H. Matsunami, K.A. Knudsen, M. Takeichi, and R.O. Hynes. 1997. Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 181:64-78. http://dx.doi.org/10.1006/dbio.1996.8443
57. Raich, W.B., C. Agbunag, and J. Hardin. 1999. Rapid epithelial-sheet sealing in the Caenorhabditis elegans embryo requires cadherin-dependent filopodial priming. Curr. Biol. 9:1139-1146. http://dx.doi.org/10.1016/S0960-9822(00)80015-9
58. Rauzi, M., P.F. Lenne, and T. Lecuit. 2010. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature. 468:1110-1114. http://dx.doi.org/10.1038/nature09566
59. Reynolds, A.B., J. Daniel, P.D. McCrea, M.J. Wheelock, J. Wu, and Z. Zhang. 1994. Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol. Cell. Biol. 14:8333-8342.
60. Rimm, D.L., E.R. Koslov, P. Kebriaei, C.D. Cianci, and J.S. Morrow. 1995. 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. USA. 92:8813-8817. http://dx.doi.org/10.1073/pnas.92.19.8813
61. Schlegelmilch, K., M. Mohseni, O. Kirak, J. Pruszak, J.R. Rodriguez, D. Zhou, B.T. Kreger, V. Vasioukhin, J. Avruch, T.R. Brummelkamp, and F.D. Camargo. 2011. Yap1 acts downstream of α-catenin to control epidermal proliferation. Cell. 144:782-795. http://dx.doi.org/10.1016/j.cell.2011.02.031
62. Schneider, S., K. Herrenknecht, S. Butz, R. Kemler, and P. Hausen. 1993. Catenins in Xenopus embryogenesis and their relation to the cadherinmediated cell-cell adhesion system. Development. 118:629-640.
63. Sehgal, R.N., B.M. Gumbiner, and L.F. Reichardt. 1997. Antagonism of cell adhesion by an alpha-catenin mutant, and of the Wnt-signaling pathway by alpha-catenin in Xenopus embryos. J. Cell Biol. 139:1033-1046. http://dx.doi.org/10.1083/jcb.139.4.1033
64. Sheffield, M., T. Loveless, J. Hardin, and J. Pettitt. 2007. C. elegans Enabled exhibits novel interactions with N-WASP, Abl, and cell-cell junctions. Curr. Biol. 17:1791-1796. http://dx.doi.org/10.1016/j.cub.2007.09.033
65. Sheikh, F., Y. Chen, X. Liang, A. Hirschy, A.E. Stenbit, Y. Gu, N.D. Dalton, T. Yajima, Y. Lu, K.U. Knowlton, et al. 2006. alpha-E-catenin inactivation disrupts the cardiomyocyte adherens junction, resulting in cardiomyopathy and susceptibility to wall rupture. Circulation. 114:1046-1055. http://dx.doi.org/10.1161/CIRCULATIONAHA.106.634469
66. Shtutman, M., A. Chausovsky, M. Prager-Khoutorsky, N. Schiefermeier, S. Boguslavsky, Z. Kam, E. Fuchs, B. Geiger, G.G. Borisy, and A.D. Bershadsky. 2008. Signaling function of alpha-catenin in microtubule regulation. Cell Cycle. 7:2377-2383.
67. Silvis, M.R., B.T. Kreger, W.H. Lien, O. Klezovitch, G.M. Rudakova, F.D. Camargo, D.M. Lantz, J.T. Seykora, and V. Vasioukhin. 2011. α-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci. Signal. 4:ra33. http://dx.doi.org/10.1126/scisignal.2001823
68. Stappert, J., and R. Kemler. 1994. A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated. Cell Adhes. Commun. 2:319-327. http://dx.doi.org/10.3109/15419069409014207
69. Stehbens, S.J., A. Akhmanova, and A.S. Yap. 2009. Microtubules and cadherins: a neglected partnership. Front. Biosci. 14:3159-3167. http://dx.doi.org/10.2741/3442
70. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1451-1455. http://dx.doi.org/10.1126/science.2006419
71. Vasioukhin, V., C. Bauer, M. Yin, and E. Fuchs. 2000. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell. 100:209-219. http://dx.doi.org/10.1016/S0092-8674(00)81559-7
72. Vasioukhin, V., C. Bauer, L. Degenstein, B. Wise, and E. Fuchs. 2001. Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin. Cell. 104:605-617. http://dx.doi.org/10.1016/S0092-8674(01)00246-X
73. Watabe-Uchida, M., N. Uchida, Y. Imamura, A. Nagafuchi, K. Fujimoto, T. Uemura, S. Vermeulen, F. van Roy, E.D. Adamson, and M. Takeichi. 1998. alpha-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells. J. Cell Biol. 142:847-857. http://dx.doi.org/10.1083/jcb.142.3.847
74. Weis, W.I., and W.J. Nelson. 2006. Re-solving the cadherin-catenin-actin conundrum. J. Biol. Chem. 281:35593-35597. http://dx.doi.org/10.1074/jbc.R600027200
75. Weiss, E.E., M. Kroemker, A.H. Rüdiger, B.M. Jockusch, and M. Rüdiger. 1998. Vinculin is part of the cadherin-catenin junctional complex: complex formation between alpha-catenin and vinculin. J. Cell Biol. 141:755-764. http://dx.doi.org/10.1083/jcb.141.3.755
76. Yamada, S., S. Pokutta, F. Drees, W.I. Weis, and W.J. Nelson. 2005. Deconstructing the cadherin-catenin-actin complex. Cell. 123:889-901. http://dx.doi.org/10.1016/j.cell.2005.09.020
77. Yonemura, S., Y. Wada, T. Watanabe, A. Nagafuchi, and M. Shibata. 2010. alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12:533-542. http://dx.doi.org/10.1038/ncb2055
78. Zhang, H., F. Landmann, H. Zahreddine, D. Rodriguez, M. Koch, and M. Labouesse. 2011. A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature. 471:99-103. http://dx.doi.org/10.1038/nature09765