Deletion of an amino-terminal sequence stabilizes β-catenin in vivo and promotes hyperphosphorylation of the adenomatous polyposis coli tumor suppressor protein

Molecular and Cellular Biology

Volumn 16, Issue 8, 1996, Pages 4088-4094

  Munemitsu, Susan ^a   Albert, Iris ^a   Rubinfeld, Bonnee ^a   Polakis, Paul ^a  

^a ONYX PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; MUTANT PROTEIN; NERVE CELL ADHESION MOLECULE; PHOSPHOTRANSFERASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL TRANSFORMATION; COLON POLYPOSIS; CONTROLLED STUDY; GENE DELETION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

EID: 0029898417     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.8.4088     Document Type: Article

References (39)

1. 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.
2. Baker, S. J., S. Markowitz, E. R. Fearon, J. K. Wilson, and B. Vogelstein. 1990. Suppression of human colorectal carcinoma cell growth by wildtype p53. Science 249:912-915.
3. Bradley, R. S., P. Cowin, and A. M. C. Brown. 1993. Expression of Wnt-1 in PC12 cells results in modulation of plakoglohin and E-cadherin and increased cellular adhesion. J Cell Biol. 123:1857-1865.
4. Burt, R. W. 1989. Polyposis syndromes, p. 1674-1696. In T. Yamada, D. H. Alpers, C. Oqyang, D. W. Powell, and F. E. Silverstein (ed.), Textbook of gastroenterology. J. P. Lippincott, Philadelphia.
5. Funayama, N., F. Fagotto, P. McCrea, and B. M. Gumbiner. 1995. Embryonic axis induction by the armadillo repeat domain of β-catenin: evidence for intracellular signaling. J. Cell Biol. 128:959-968.
6. Groden, J., A. Thliveris, W. Samowitz, M. Carlson, L. Gelbert, H. Albertsen, G. Joslyn, J. Stevens, L. Spirio, M. Robertson, L. Sargeant, K. Krapcho, E. Wolff, R. Burt, J. P. Hughes, J. Warrington, J. McPherson, J. Wasmuth, D. LePaslier, H. Abderrahim, D. Cohen, M. Leppert, and R. White. 1991. Identification and characterization of the familial adenomatous polyposis gene. Cell 66:589-600.
7. Grussenmyer, T., K. H. Scheidtmann, M. A. Hutchinson, and G. Walter. 1985. Complexes of polyoma virus medium T antigen and cellular proteins. Proc. Natl. Acad. Sci. USA 82:7952-7954.
8. Heasmen, J., A. Crawford, K. Goldstone, P. Garner-Hamrick, B. Gumbiner, P. McCrea, C. Kitner, C. Y. Noro, and C. Wylie. 1994. Overexpression of cadherins and underexpression of b-catenin inhibit dorsal mesodermal induction in early xenopus embryos. Cell 79:791-803.
9. Hinck, L., W. J. Nelson, and J. Papkoff. 1994. Wnt-1 modulates cell-cell adhesion in mammalian cells by stabilizing β-catenin binding to the cell adhesion protein cadherin. J. Cell Biol. 124:729-741.
10. Hulsken, J., W. Birchmeier, and J. Behrens. 1995. E-cadherin and APC compete for the interaction of β-catenin with the cytoskeleton. J. Cell Biol. 127:2061-2069.
11. Jen, J., S. M. Powell, N. Papadopolous, K. Smith, S. R. Hamilton, B. Vogelstein, and K. Kinzler. 1994. Molecular determinants of dysplasia in colorectal lesions. Cancer Res. 54:5523-5526.
12. Joslyn, G., M. Carlson, A. Thliveris, H. Albertsen, L. Gelbert, W. Samowitz, J. Groden, J. Stevens, L. Spirio, M. Robertson, L. Sargeant, K. Krapcho, E. Wolff, R. Burt, J. P. Hughes, J. Warrington, J. McPherson, J. Wasmuth, D. Le Paslier, H. Abderrahim, D. Cohen, M. Leppert, and R. White. 1991. Identification of deletion mutations and three new genes at the familial polyposis locus. Cell 66:601-613.
13. Kawanishi, J., J. Kato, K. Sasaki, S. Fujii, N. Watanabe, and Y. Niitsu. 1995. Loss of E-cadherin-dependent cell-cell adhesion due to mutation of the β-catenin gene in a human cancer cell line. Mol. Cell. Biol. 15:1175-1181.
14. Kinzler, K. W., M. C. Nilbert, L.-K. Su, B. Vogelstein, T. M. Bryan, D. B. Levy, K. J. Smith, A. C. Preisinger, P. Hedge, D. McKechnie, R. Finniear, A. Markham, J. Groffen, M. S. Boguski, S. F. Altschul, A. Horii, H. Ando, Y. Miyoshi, Y. Miki, I. Nishisho, and Y. Nakamura. 1991. Identification of FAP locus genes from chromosome 5q21. Science 253:661-664.
15. Kowalczyk, A. P., H. L. Palka, H. H. Luu, L. A. Nilles, J. E. Anderson, M. J. Wheelock, and K. J. Green. 1994. Posttranslational regulation of plakoglobin expression. Influence of the desmosomal cadherins on plakoglobin metabolic stability. J. Biol. Chem. 269:31214-31223.
16. McCrea, P. D., W. M. Brieher, and B. M. Gumbiner. 1993. Induction of secondary axis in Xenopus by antibodies to β-catenin. J. Cell Biol. 123:477-484.
17. McCrea, P. D., C. W. Turck, and B. Gumbiner. 1991. A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 254:1359-1361.
18. Miyoshi, Y., H. Nagase, H. Ando, S. Ichii, S. Nakatsura, T. Aoki, Y. Miki, T. Mori, and Y. Nakamura. 1992. Somatic mutations of the APC gene in colorectal tumors: mutation cluster region in the APC gene. Hum. Mol. Genet. 1:229-223.
19. Munemitsu, S., I. Albert, B. Souza, B. Rubinfeld, and P. Polakis. 1995. Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. USA 92:3046-3050.
20. Munemitsu, S., and P. Polakis. Unpublished data.
21. Munemitsu, S., B. Souza, O. Muller, I. Albert, B. Rubinfeld, and P. Polakis. 1994. The APC gene product associates with microtubules in vivo and promotes their assembly in vitro. Cancer Res. 54:3676-3681.
22. Nagafuchi, A., and M. Takeichi. 1988. Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO J. 7:3679-3684.
23. Nishisho, I., Y. Nakamura, Y. Miyoshi, Y. Miki, H. Ando, A. Horii, K. Koyama, J. Utsunomiya, S. Baba, P. Hedge, A. Markham, A. J. Krush, G. Petersen, S. R. Hamilton, M. C. Nilbert, D. B. Levy, T. M. Bryan, A. C. Preisinger, K. J. Smith, L. K. Su, K. W. Kinzler, and B. Vogelstein. 1991. Mutations of chromosome 5q21 genes in FAP and colorectal patients. Science 253:665-669.
24. Oyama, T., Y. Kanai, A. Ochiai, S. Akimoto, T. Oda, K. Yanagihara, A. Nagafuchi, S. Tsukita, S. Shibamaoto, F. Ito, M. Takeichi, H. Malsuda, and S. Hirohashi. 1994. A truncated β-catenin disrupts the interaction between E-cadherin and α-catenin: a cause of loss of intracellular adhesiveness in human cancer cell lines. Cancer Res. 54:6282-6287.
25. 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.
26. Papkoff, J. (Megabios Corp., Burlingame, Calif.). Personal communication.
27. Papkoff, J., B. Rubinfeld, B. Schryver, and P. Polakis. 1996. Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes. Mol. Cell. Biol. 16:2128-2134.
28. Peifer, M. 1995. Cell adhesion and signal transduction: the armadillo connection. Trends Cell Biol. 5:224-229.
29. Peifer, M., D. Sweeton, M. Casey, and E. Wieschaus. 1994. wingless and zeste-white 3 kinase trigger opposing changes in the intracellular distribution of armadillo. Development 120:369-380.
30. Polakis, P. 1995. Mutations in the APC gene and their implications lor protein structure and function. Curr. Opin. Genet. Dev. 5:65-71.
31. Powell, S. M., N. Zilz, Y. Beazer-Barclay, T. M. Bryan, S. R. Hamilton, S. N. Thihodeau, B. Vogelstein, and K. W. Kinzler. 1992. APC mutations occur early during colorectal tumorigenesis. Nature (London) 359:235-237.
32. Rubinfeld, B., I. Albert, E. Porfiri, C. Fiol, S. Munemitsu, and P. Polakis. 1996. Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science 272:1023-1026.
33. Rubinfeld, B., B. Souza, I. Albert, O. Muller, S. C. Chamberlain, F. Masiarz, S. Munemitsu, and P. Polakis. 1993. Association of the APC gene product with β-catenin. Science 262:1731-1734.
34. Rubinfeld, B. R., B. Souza, I. Albert, S. Munemitsu, and P. Polakis. 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.
35. Siegfried, E., E. L. Wilder, and N. Perrimon. 1994. Components of the wingless signalling pathway. Nature (London) 367:76-80.
36. Smith, A. J., H. S. Stern, M. Penner, H. Kazy, A. Mitri, B. V. Bapat, and S. Gallinger. 1994. Somatic APC and K-ras codon 12 mutations in aberrant crypt foci from human colons. Cancer Res. 54:5527-5530.
37. Smith, K. J., D. B. Levy, P. Maupin, T. D. Pollard, B. Vogelstein, and K. W. Kinzler. 1994. Wild-type but not mutant APC associates with the microtubule cytoskeleton. Cancer Res. 54:3672-3675.
38. Tsukamoto, A. S., R. Grosschedl, R. C. Guzman, T. Parslow, and H. E. Varmus. 1988. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell 55:619-625.
39. Whitehead, I., H. Kirk, and R. Kay. 1995. Expression cloning of oncogenes by retroviral transfer of cDNA libraries. Mol. Cell. Biol. 15:704-710.