The structure of the β-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by β-catenin

Cell

Volumn 105, Issue 3, 2001, Pages 391-402

  Huber, Andrew H ^a   Weis, William I ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0035805117     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(01)00330-0     Document Type: Article

References (51)

1. Aberle, H., Schwartz, H., Hoschuetzky, H., and Kemler, R. (1996). Single amino acid substitutions in proteins of the armadillo gene family abolish their binding to α-catenin. J. Biol. Chem. 271, 1520-1526.
2. Aberle, H., Bauer, A., Stappert, J., Kispert, A., and Kemler, R. (1997). β-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16, 3797-3804.
3. Behrens, J., Vakaet, L., Friis, R., Winterhager, E., van Roy, F., Mareel, M.M., and Birchmeier, W. (1993). Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/β-catenin complex in cells transformed with a temperature-sensitive v-src gene. J. Cell Biol. 120, 757-766.
4. Behrens, J., von Kries, J.P., Kühl, M., Bruhn, L., Wedlich, D., Grosschedl, R., and Birchmeier, W. (1996). Functional interaction of β-catenin with the transcription factor LEF-1. Nature 382, 638-642.
5. Behrens, J., Jerchow, B.-A., Würfele, M., Grimm, J., Asbrand, C., Wirtz, R., Kühl, M., Wedlich, D., and Birchmeier, W. (1998). Functional interaction of an Axin homolog, conductin, with β-catenin, APC, and GSK3β. Science 280, 596-599.
6. Brieher, W.M., Yap, A.S., and Gumbiner, B.M. (1996). Lateral dimerization is required for the homophilic binding activity of C-cadherin. J. Cell Biol. 135, 487-496.
7. Brünger, AT., Adams, P.D., Clore, G.M., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N.S., Read, R.J., et al. (1998). Crystallography and NMR System (CNS): a new software system for macromolecular structure determination. Acta Cryst. D54, 905-921.
8. Chitaev, N.A., and Troyanovsky, S.M. (1998). Adhesive but not lateral E-cadherin complexes require calcium and catenins for their formation. J. Cell Biol. 142, 837-846.
9. Chitaev, N.A., Averbakh, A.Z., Troyanovsky, R.B., and Troyanovsky, S.M. (1998). Molecular organization of the desmoglein-plakoglobin complex. J. Cell Sci. 111, 1941-1949.
10. Conti, E., Uy, M., Leighton, L., Blobel, G., and Kuriyan, J. (1998). Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin α. Cell 94, 193-204.
11. Finnemann, S., Mitrik, I., Hess, M., Otto, G., and Wedlich, D. (1997). Uncoupling of XB/U-cadherin-catenin complex formation from its function in cell-cell adhesion. J. Biol. Chem. 272, 11856-11862.
12. Fontes, M.R.M., Teh, T., and Kobe, B. (2000). Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-α. J. Mol. Biol. 297, 1183-1194.
13. Gerstein, M., Lesk, A.M., and Chothia, C. (1994). Structural mechanisms for domain movements in proteins. Biochemistry 33, 6739-6749.
14. Graham, T.A., Weaver, C., Mao, F., Kimmelman, D., and Xu, W. (2000). Crystal structure of a β-catenin/Tcf complex. Cell 103, 885-896.
15. Gumbiner, B.M. (2000). Regulation of cadherin adhesive activity. J. Cell Biol. 148, 399-403.
16. Hamaguchi, M., Matsuyoshi, N., Ohnishi, Y., Gotoh, B., Takeichi, M., and Nagai, Y. (1993). p60v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system. EMBO J. 12, 307-314.
17. Hinck, L., Nathke, I.S., Papkoff, J., and Nelson, W.J. (1994). Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly. J. Cell Biol. 125, 1327-1340.
18. Huber, A.H., Nelson, W.J., and Weis, W.I. (1997). Three-dimensional structure of the armadillo repeat region of β-catenin. Cell 90, 871-882.
19. Huber, A.H., Stewart, D.B., Laurents, D.V., Nelson, W.J., and Weis, W.I. (2001). The cadherin cytoplasmic domain is unstructured in the absence of β-catenin: a possible mechanism for regulating cadherin turnover. J. Biol. Chem. 276, 12301-12309.
20. Hülsken, J., Birchmeier, W., and Behrens, J. (1994). E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton. J. Cell Biol. 127, 2061-2069.
21. Ikeda, S., Kishida, S., Yamamoto, H., Murai, H., Koyama, S., and Kikuchi, A. (1998). Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3β and β-catenin and promotes GSK-3β-depedent phosphorylation of β-catenin. EMBO J. 17, 1371-1384.
22. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G., and Gibson, T.J. (1998). Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23, 403-405.
23. Kelly, L.A., MacCallum, R.M., and Sternberg, M.J.E. (2000). Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299, 501-522.
24. Lickert, H., Bauer, A., Kemler, R., and 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.
25. Matsuyoshi, N., Hamaguchi, M., Taniguchi, S., Nagafuchi, A., Tsukita, S., and Takeichi, M. (1992). Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J. Cell Biol. 118, 703-714.
26. Navaza, J., and Saludjian, P. (1997). AMoRe: an automated molecular replacement program package. Methods Enzymol. 276, 581-594.
27. Nollet, F., Kools, P., and van Roy, F. (2000). Phylogenetic analysis of the cadherin super-family allows identification of six major subfamilies besides several solitary members. J. Mol. Biol. 299, 551-572.
28. Norvell, S.M., and Green, K.J. (1998). Contributions of extracellular and intracellular domains of full length and chimeric cadherin molecules to junction assembly in epithelial cells. J. Cell Sci. 111, 1305-1318.
29. Orford, K., Crockett, C., Jensen, J.P., Weissman, A.M., and Byers, S.W. (1997). Serine phosphorylation-regulated ubiquitination and degradation of β-catenin. J. Biol. Chem. 272, 24735-24738.
30. Pai, L.-M., Kirkpatrick, C., Blanton, J., Oda, H., Takeichi, M., and Peifer, M. (1996). Drosophila α-catenin and E-cadherin bind to distinct regions of Drosophila Armadillo. J. Biol. Chem. 271, 32411-32420.
31. Pokutta, S., and Weis, W.I. (2000). Structure of the dimerization and β-catenin binding region of α-catenin. Mol. Cell 5, 533-543.
32. Polakis, P. (2000). Wnt signaling and cancer. Genes Dev. 14, 1837-1851.
33. Rechsteiner, M., and Rogers, S.W. (1996). PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21, 267-271.
34. Rosin-Arbesfeld, R., Townsley, F., and Bienz, M. (2000). The APC tumour suppressor has a nuclear export function. Nature 406, 1009-1012.
35. Roura, S., Miravet, S., Piedra, J., García de Herreros, A., and Dunach, M. (1999). Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J. Biol. Chem. 274, 36734-36740.
36. Rubinfeld, B., Souza, B., Albert, I., Müller, O., Chamberlain, S.H., Masiarz, F.R., Munemitsu, S., and Polakis, P. (1993). Association of the APC gene product with β-catenin. Science 262, 1731-1734.
37. Rubinfeld, B., Souza, B., Albert, I., Munemitsu, S., and Polakis, P. (1995). The APC protein and E-cadherin form similar but independent complexes with α-catenin, β-catenin, and plakoglobin. J. Biol. Chem. 270, 5549-5555.
38. Rubinfeld, B., Albert, I., Porfiri, E., Fiol, C., Munemitsu, S., and Polakis, P. (1996). Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science 272, 1023-1026.
39. Ruiz, P., Brinkmann, V., Ledermann, B., Behrend, M., Grund, C., Thalhammer, C., Vogel, F., Birchmeir, C., Günthert, U., Franke, W.W., and Birchmeier, W. (1996). Targeted mutation of plakoglobin in mice reveals essential functions of desmosomes in the embryonic heart. J. Cell Biol. 135, 215-225.
40. Stappert, J., and Kemler, R. (1994). A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated. Cell Adhesion Commun. 2, 319-327.
41. Su, L.-K., Vogelstein, B., and Kinzler, K.W. (1993). Association of the APC tumor suppressor protein with catenins. Science 262, 1734-1737.
42. Takeda, H., Nagafuchi, A., Yonemura, S., Tsukita, S., Behrens, J., Birchmeier, W., and Tsukita, S. (1995). V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and β catenin is not required for the shift. J. Cell Biol. 131, 1839-1847.
43. Takeda, H., Shimoyama, Y., Nagafuchi, A., and Hirohashi, S. (1999). E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo. Nat. Struct. Biol. 6, 310-312.
44. Troyanovsky, R.B., Chitaev, N.A., and Troyanovsky, S.M. (1996). Cadherin binding sites of plakoglobin: localization, specificity and role in targeting to adhering junctions. J. Cell Sci. 109, 3069-3078.
45. van de Wetering, M., Cavallo, R., Booijes, D., van Beest, M., van Es, J., Loureiro, J., Ypma, A., Hursh, D., Jones, T., Bejsovec, A., et al. (1997). Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789-799.
46. von Kries, J.P., Winbeck, G., Asbrand, C., Schwarz-Romond, T., Sochnikova, N., Dell'Oro, A., Behrens, J., and Birchmeier, W. (2000). Hot spots in β-catenin for interactions with LEF-1, conductin, and APC. Nat. Struct. Biol. 7, 800-807.
47. Wahl, J.K.I., Nieset, J.E., Sacco-Bubulya, P.A., Sadler, T.M., Johnson, K.R., and Wheelock, M.J. (2000). The amino- and carboxylterminal tails of β-catenin reduce its affinity for desmoglein 2. J. Cell Sci. 113, 1737-1745.
48. Witcher, L.L., Collins, R., Puttagunta, S., Mechanic, S.E., Munson, M., Gumbiner, B., and Cowin, P. (1996). Desmosomal cadherin binding domains of plakoglobin. J. Biol. Chem. 271, 10904-10909.
49. Yap, A.S., Brieher, W.M., and Gumbiner, B.M. (1997a). Molecular and functional analysis of cadherin-based adherens junctions. Annu. Rev. Cell Dev. Biol. 13, 119-146.
50. Yap, A.S., Brieher, W.M., Pruschy, M., and Gumbiner, B.M. (1997b). Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function. Curr. Biol. 7, 308-315.
51. ctn. J. Cell Biol. 141, 779-789.