Mechanistic insights from structural studies of β-catenin and its binding partners

Journal of Cell Science

Volumn 120, Issue 19, 2007, Pages 3337-3344

  Xu, Wenqing ^a   Kimelman, David ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

catenin structure; Cell adhesion; Protein protein interaction; Wnt signaling

Indexed keywords

ARMADILLO DOMAIN PROTEIN; BETA CATENIN; GLYCOGEN SYNTHASE KINASE; PROTEIN SERINE THREONINE KINASE; UVOMORULIN; WNT PROTEIN;

ACETYLATION; AMINO TERMINAL SEQUENCE; BINDING SITE; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL MEMBRANE; CELL NUCLEUS; CYTOSOL; HUMAN; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; UBIQUITINATION;

ADHERENS JUNCTIONS; BETA CATENIN; BINDING SITES; CADHERINS; CELL NUCLEUS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY;

ARMADILLO;

EID: 35648965654     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.013771     Document Type: Note

References (89)

1. Barker, N., Hurlstone, A., Musisi, H., Miles, A., Bienz, M. and Clevers, H. (2001). The chromatin remodelling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO J. 20, 4935-4943.
2. Bauer, A., Chauvet, S., Huber, O., Usseglio, E, Rothbacher, U., Aragnol, D., Kemler, R. and Pradel, J. (2000). Pondn52 and reptin52 function as antagonistic regulators of β-catenin signalling activity. EMBO J. 19, 6121-6130.
3. Bek, S. and Kemler, R. (2002). Protein kinase CKII regulates the interaction of β-catenin with α-catenin and its protein stability. J. Cell Sci. 115, 4743-4753.
4. Bienz, M. and Clevers, H. (2000). Linking colorectal cancer to Wnt signaling. Cell 103, 311-320.
5. Brembeck, F. H., Schwarz-Romond, T., Bakkers, J., Wilhelm, S., Hammerschmidt, M. and Birchmeier, W. (2004). Essential role of BCL9-2 in the switch between β-catenin's adhesive and transcriptional functions. Genes Dev. 18, 2225-2230.
6. Bustos, V. H., Ferrarese, A., Venerando, A., Marin, O., Allende, J. E. and Pinna, L. A. (2006). The first armadillo repeat is involved in the recognition and regulation of β-catenin phosphorylation by protein kinase CK1. Proc. Natl. Acad. Sci. USA 103, 19725-19730.
7. Castano, J., Raurell, I., Piedra, J. A., Miravet, S., Dunach, M. and Garcai de Herreros, A. (2002). β-catenin N- and C-terminal tails modulate the coordinated binding of adherens junction proteins to β-catenin. J. Biol. Chem. 277, 31541-31550.
8. Choi, H. J., Huber, A. H. and Weis, W. I. (2006). Thermodynamics of β-catenin-ligand interactions: the roles of the N- and C-terminal tails in modulating binding affinity. J. Biol. Chem. 291, 1027-1038.
9. Clevers, H. (2006). Wnt/β-catenin signaling in development and disease. Cell 127, 469-480.
10. Coluccia, A. M., Vacca, A., Dunach, M., Mologni, L., Redaelli, S., Bustos, V. H., Benati, D., Pinna, L. A. and Gambacorti-Passerini, C. (2007). Bcr-Abl stabilizes β-catenin in chronic myeloid leukemia through its tyrosine phosphorylation. EMBO J. 26, 1456-1466.
11. Cox, R. T., Pai, L. M., Kirkpatrick, C., Stein, J. and Peifer, M. (1999). Roles of the C terminus of Armadillo in Wingless signaling in Drosophila. Genetics 153, 319-332.
12. Daniels, D. L. and Weis, W. I. (2002). ICAT inhibits β-catenin binding to Tcf/Lef-family transcription factors and the general coactivator p300 using independent structural modules. Mol. Cell 10, 573-584.
13. Daniels, D. L. and Weis, W. I. (2005). β-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat. Struct. Mol. Biol. 12, 364-371.
14. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J. and Weis, W. I. (2005). α-catenin is a molecular switch that binds E-cadherin-β-catenin and regulates actin-filament assembly. Cell 123, 903-915.
15. Eklof Spink, K., Fridman, S. G. and Weis, W. I. (2001). Molecular mechanisms of β-catenin recognition by adenomatous polyposis coli revealed by the structure of an APC-β-catenin complex. EMBO J. 20, 6203-6212.
16. Fang, D., Hawke, D., Zheng, Y., Xia, Y., Meisenhelder, J., Nika, H., Mills, G. B., Kobayashi, R., Hunter, T. and Lu, Z. (2007). Phosphorylation of β-catenin by AKT promotes β-catenin transcriptional activity. J. Biol. Chem. 282, 11221-11229.
17. Fasolini, M., Wu, X., Flocco, M., Trosset, J. Y., Oppermann, U. and Knapp, S. (2003). Hot spots in Tcf4 for the interaction with β-catenin. J. Biol. Chem. 278, 21092-21098.
18. Gates, J. and Peffer, M. (2005). Can 1000 reviews be wrong? Actin, α-Catenin, and adherens junctions. Cell 123, 769-772.
19. Graham, T. A., Weaver, C., Mao, F., Kimehnan, D. and Xu, W. (2000). Crystal structure of a β-catenin/Tcf complex. Cell 103, 885-896.
20. Graham, T. A., Ferkey, D. M., Mao, F., Kimelman, D. and Xu, W. (2001). Tcf4 can specifically recognize β-catenin using alternative conformations. Nat. Struct. Biol. 8, 1048-1052.
21. Graham, T. A., Clements, W. K., Kimelman, D. and Xu, W. (2002). The crystal structure of the β-catenin/ICAT complex reveals the inhibitory mechanism of ICAT. Mol. Cell 10, 563-571.
22. Ha, N. C., Tonozuka, T., Stamos, J. L., Choi, H. J. and Weis, W. I. (2004). Mechanism of phosphorylation-dependent binding of APC to β-catenin and its role in β-catenin degradation. Mol. Cell 15, 511-521.
23. Hart, M., Concordet, J. P., Lassot, I., Albert, I., del los Santos, R., Durand, H., Perret, C., Rubinfeld, B., Margottin, F., Benarous, R. et al. (1999). The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr Biol. 9, 207-210.
24. Hecht, A., Vleminckx, K., Stemmler, M. P., van Roy, F. and Kemler, R. (2000). The p300/CBP acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates. EMBO J. 19, 1839-1850.
25. Hino, S., Tanji, C., Nakayama, K. I. and Kikuchi, A. (2005). Phosphorylation of β-catenin by cyclic AMP-dependent protein kinase stabilizes β-catenin through inhibition of its ubiquitination. Mol. Cell. Biol. 25, 9063-9072.
26. Hoffmans, R. and Basler, K. (2007). BCL9-2 binds Arm/ β-catenin in a Tyr142-independent manner and requires Pygopus for its function in Wg/Wnt signaling. Mech. Dev. 124, 59-67.
27. Huber, A. H. and Weis, W. I. (2001). The structure of the β-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by β-catenin. Cell 105, 391-402.
28. 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.
29. Hulsken, 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.
30. Jiang, J. and Struhl, G. (1998). Regulation of the Hedgehog and Wingless signalling pathways by the F- box/WD40-repeat protein Slimb. Nature 391, 493-496.
31. Kidd, A. R., 3rd, Miskowski, J. A., Siegfried, K. R., Sawa, H. and Kimble, J. (2005). A β-catenin identified by functional rather than sequence criteria and its role in Wnt/MAPK signaling. Cell 121, 761-772.
32. Kim, S., Xu, X., Hecht, A. and Boyer, T. G. (2006). Mediator is a transducer of Wnt/β-catenin signaling. J. Biol. Chem. 281, 14066-14075.
33. Kimelman, D. and Xu, W. (2006). β-catenin destruction complex: insights and questions from a structural perspective. Oncogene 25, 7482-7491.
34. Kinzler, K. W. and Vogelstein, B. (1996). Lessons from hereditary colorectal cancer. Cell 87, 159-170.
35. Kitagawa, M., Hatakeyama, S., Shirane, M., Matsumoto, M., Ishida, N., Hattori, K., Nakamichi, I., Kikuchi, A. and Nakayama, K. (1999). An F-box protein, FWD1, mediates ubiquitin-dependent proteolysis of β-catenin. EMBO J. 18, 2401-2410.
36. Korswagen, H. C., Herman, M. A. and Clevers, H. C. (2000). Distinct β-catenins mediate adhesion and signalling functions in C. elegans. Nature 406, 527-532.
37. Kramps, T., Peter, O., Brunner, E., Nellen, D., Froesch, B., Chatterjee, S., Murone, M., Zullig, S. and Basler, K. (2002). Wnt/ wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear β-catenin-TCF complex. Cell 109, 47-60.
38. Kuramochi, J., Arai, T., Ikeda, S., Kumagai, J., Uetake, H. and Sugihara, K. (2006). High Pinl expression is associated with tumor progression in colorectal cancer. J. Surg. Oncol. 94, 155-160.
39. Latres, E., Chiaur, D. S. and Pagano, M. (1999). The human F box protein β-Trcp associates with the Cull/Skpl complex and regulates the stability of β-catenin. Oncogene 18, 849-854.
40. Levy, L., Wei, Y., Labalette, C., Wu, Y., Renard, C. A., Buendia, M. A. and Neuveut, C. (2004). Acetylation of β-catenin by p300 regulates β-catenin-Tcf4 interaction. Mol. Cell. Biol. 24, 3404-3414.
41. Liu, C., Kato, Y., Zhang, Z., Do, V. M., Yankner, B. A. and He, X. (1999). β-Trcp couples β-catenin phosphorylation-degradation and regulates Xenopus axis formation. Proc. Natl. Acad. Sci. USA 96, 6273-6278.
42. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X. and He, X. (2002). Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837-847.
43. Liu, J., Xing, Y., Hinds, T. R., Zheng, J. and Xu, W. (2006). The third 20 amino acid repeat is the tightest binding site of APC for β-catenin. J. Mol. Biol. 360, 133-144.
44. Megy, S., Bertho, G., Gharbi-Benarous, J., Baleux, F., Benarous, R. and Girault, J. P. (2005a). Solution structure of a peptide derived from the oncogenic protein β-Catenin in its phosphorylated and nonphosphorylated states. Peptides 26, 227-241.
45. Megy, S., Bertho, G., Gharbi-Benarous, J., Evrard-Todeschi, N., Coadou, G., Segeral, E., Iehle, C., Quemeneur, E., Benarous, R. and Girault, J. P. (2005b). STD and TRNOESY NMR studies on the conformation of the oncogenic protein β-catenin containing the phosphorylated motif DpSGXXpS bound to the β-TrCP protein. J. Biol. Chem. 280, 29107-29116.
46. Miyagishi, M., Fujii, R., Hatta, M., Yoshida, E., Araya, N., Nagafuchi, A., Ishihara, S., Nakajima, T. and Fukamizu, A. (2000). Regulation of Lef-mediated transcription and p53-dependent pathway by associating β-catenin with CBP/p300. J. Biol. Chem. 275, 35170-35175.
47. Moon, R. T., Bowerman, B., Boutros, M. and Perrimon, N. (2002). The promise and perils of Wnt signaling through β-catenin. Science 296, 1644-1646.
48. Morin, P. J. (1999). β-catenin signaling and cancer. BioEssays 21, 1021-1030.
49. Mosimann, C., Hausmann, G. and Basler, K. (2006). Paraftbromin/ Hyrax activates Wnt/Wg target gene transcription by direct association with β-catenin/Armadillo. Cell 125, 327-341.
50. Munoz, J. P., Huichalaf, C. H., Orellana, D. and Maccioni, R. B. (2007). cdk5 modulates β- and σ-catenin/Pin1 interactions in neuronal cells. J. Cell. Biochem. 100, 738-749.
51. Natarajan, L., Witwer, N. E. and Eisenmann, D. M. (2001). The divergent Caenorhabditis elegans β-catenin proteins BAR-1, WRM-1 and HMP-2 make distinct protein interactions but retain functional redundancy in vivo. Genetics 159, 159-172.
52. Nathke, I. S. (2004). The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu. Rev. Cell Dev. Biol. 20, 337-366.
53. Nelson, W. J. and Nusse, R. (2004). Convergence of Wnt, β-catenin, and cadherin pathways. Science 303, 1483-1487.
54. Nusse, R. (1999). WNT targets. Repression and activation. Trends Genet. 15, 1-3.
55. Pang, R., Yuen, J., Yuen, M. F., Lai, C. L., Lee, T. K., Man, K., Poon, R. T., Fan, S. T., Wong, C. M., Ng, I. O. et al. (2004). PIN1 overexpression and β-catenin gene mutations are distinct oncogenic events in human hepatocellular carcinoma. Oncogene 23, 4182-4186.
56. Piedra, J., Martinez, D., Castano, J., Miravet, S., Dunach, M. and de Herreros, A. G. (2001). Regulation of β-catenin structure and activity by tyrosine phosphorylation. J. Biol. Chem. 276, 20436-20443.
57. Pokutta, S. and Weis, W. I. (2000). Structure of the dimerization and β-catenin-binding region of α-calenin. Mol. Cell 5, 533-543.
58. Polakis, P. (1995). Mutations in the APC gene and their implications for protein structure and function. Curr Opin. Genet. Dev. 5, 66-71.
59. Polakis, P. (2000). Wnt signaling and cancer. Genes Dev. 14, 1837-1851.
60. Poy, F., Lepourcelet, M., Shivdasani, R. A. and Eck, M. J. (2001). Structure of a human Tcf4-β-catenin complex. Nat. Struct. Biol. 8, 1053-1057.
61. Reya, T. and Clevers, H. (2005). Wnt signalling in stem cells and cancer. Nature 434, 843-850.
62. Rimm, D. L., Koslov, E. R., Kebriaei, P., Cianci, C. D. and Morrow, J. S. (1995). α1(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.
63. Roose, J. and Clevers, H. (1999). TCF transcription factors: molecular switches in carcinogenesis. Biochim. Biophys. Acta 1424, M23-M37.
64. Roura, S., Miravet, S., Piedra, J., Garcia de Herreros, A. and Dunach, M. (1999). Regulation of E-cadherin/Catenin association by tyrosine phosphorylation. J. Biol. Chem. 274, 36734-36740.
65. Rubinfeld, B., Tice, D. A. and Polakis, F. (2001). Axin-dependent phosphorylation of the adenornatous polyposis coli protein mediated by casein kinase lepsilon. J. Biol. Chem. 276, 39037-39045.
66. Ryo, A., Nakamura, M., Wulf, G., Liou, Y. C. and Lu, K. P. (2001). Pin1 regulates turnover and subcellular localization of β-catenin by inhibiting its interaction with APC. Nat Cell Biol. 3, 793-801.
67. Sampietro, J., Dahlberg, C. L., Cho, U. S., Hinds, T. R., Kimelman, D. and Xu, W. (2006). Crystal structure of a β-catenin/BCL9/Tcf4 complex. Mol. Cell 24, 293-300.
68. Solanas, G., Miravet, S., Casagolda, D., Castano, J., Raurell, I., Corrionero, A., de Herreros, A. G. and Dunach, M. (2004). β-Catenin and plakoglobin N- and C-tails determine ligand specificity. J. Biol. Chem. 279, 49849-49856.
69. Song, D. H., Dominguez, I., Mzuno, J., Kaut, M., Mohr, S. C. and Seldin, D. C. (2003). CK2 phosphorylation of the armadillo repeat region of β-catenin potentiates Wnt signaling. J. Biol. Chem. 278, 24018-24025.
70. Stadeli, R., Hoffmans, R. and Basler, K. (2006). Transcription under the control of nuclear Arm/β-catenin. Curr. Biol. 16, R378-R385.
71. Sun, Y., Kolligs, F. T., Hottiger, M. O., Mosavin, R., Fearon, E. R. and Nabel, G. J. (2000). Regulation of β-catenin transformation by the p300 transcriptional coactivator. Proc. Natl. Acad. Sci. USA 97, 12613-12618.
72. Tago, K., Nakamura, T., Nishita, M., Hyodo, J., Nagai, S., Murata, Y., Adachi, S., Ohwada, S., Morishita, Y., Shibuya, H. et al. (2000). Inhibition of Wnt signaling by ICAT, a novel β-catenin-interacting protein. Genes Dev. 14, 1741-1749.
73. Takemaru, K. I. and Moon, R. T. (2000). The transcriptional coactivator CBP interacts with β-catenin to activate gene expression. J. Cell Biol. 149, 249-254.
74. Takemaru, K., Yamaguchi, S., Lee, Y. S., Zhang, Y., Carthew, R. W. and Moon, R. T. (2003). Cbibby, a nuclear β-catenin-associated antagonist of the Wnt/Wingless pathway. Nature 422, 905-909.
75. Taurin, S., Sandbo, N., Qin, Y., Browning, D. and Dulin, N. O. (2006). Phosphorylation of β-catenin by cyclic AMP-dependent protein kinase. J. Biol. Chem. 281, 9971-9976.
76. Thompson, B., Townsley, F., Rosin-Arbesfeld, R., Musisi, H. and Bienz, M. (2002). A new nuclear component of the Wnt signalling pathway. Nat. Cell Biol. 4, 367-373.
77. van Noort, M., van de Wetering, M. and Clevers, H. (2002). Identification of two novel regulated serines in the N terminus of β-catenin. Exp. Cell Res. 276, 264-272.
78. von Kries, J. F., 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.
79. Weis, W. I. and Nelson, W. J. (2006). Re-solving the cadherin-catenin-actin conundrum. J. Biol. Chem. 281, 35593-35597.
80. Willert, K. and Jones, K. A. (2006). Wnt signaling: is the party in the nucleus? Genes Dev. 20, 1394-1404.
81. Winston, J. T., Strack, P., Beer-Romero, P., Chu, C. Y., Elledge, S. J. and Harper, J. W. (1999). The SCF β-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IκBα and β-catenin and stimulates IΒα ubiquitination in vitro. Genes Dev. 13, 270-283.
82. Wolf, D., Rodova, M., Miska, E. A., Calvet, J. P. and Kouzarides, T. (2002). Acetylation of β-catenin by CREB-binding protein (CBP). J. Biol. Chem. 277, 25562-25567.
83. Wu, G. and He, X. (2006). Threonine 41 in β-catenin serves as a key phosphorylation relay residue in β-catenin degradation. Biochemistry 45, 5319-5323.
84. Wu, G., Xu, G., Schulman, B. A., Jeffrey, P. D., Harper, J. W. and Pavletich, N. P. (2003). Structure of a β-TrCP1-Skp1-β-catenin complex: destruction motif binding and lysine specificity of the SCF(β-TrCP1) ubiquidn ligase. Mol. Cell 11, 1445-1456.
85. Wulf, G. M., Ryo, A., Wulf, G. G., Lee, S. W., Niu, T., Petkova, V. and Lu, K. P. (2001). Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J. 20, 3459-3472.
86. Xing, Y., Clements, W. K., Kimelman, D. and Xu, W. (2003). Crystal structure of a β-catenin/axin complex suggests a mechanism for the β-catenin destruction complex. Genes Dev. 17, 2753-2764.
87. Xing, Y., Clements, W. K., Le Trong, I., Hinds, T. R., Stenkamp, R., Kimelman, D. and Xu, W. (2004). Crystal structure of a β-catenin/APC complex reveals a critical role for APC phosphorylation in APC function. Mol. Cell 15, 523-533.
88. Yamada, S., Pokutta, S., Drees, F., Weis, W. I. and Nelson, W. J. (2005). Deconstructing the cadherin-catenin-actin complex. Cell 123, 889-901.
89. Zeng, G., Apte, U., Micsenyi, A., Bell, A. and Monga, S. P. (2006). Tyrosine residues 654 and 670 in β-catenin are crucial in regulation of Met-β-catenin interactions. Exp. Cell Res. 312, 3620-3630.