Novel self-association of the APC molecule affects APC clusters and cell migration

Journal of Cell Science

Volumn 121, Issue 11, 2008, Pages 1916-1925

  Li, Zhuoyu ^a   Kroboth, Karin ^a   Newton, Ian P ^a   Näthke, Inke S ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Adenomatous; Cell migration; Polyposis coli

Indexed keywords

APC PROTEIN; PROTEIN 14 3 3;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LINE; CELL MIGRATION; CELL STRAIN; COLON POLYPOSIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; WESTERN BLOTTING; WILD TYPE;

14-3-3 PROTEINS; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; CARCINOMA; CELL LINE; CELL MOVEMENT; CELL SURFACE EXTENSIONS; COLONIC NEOPLASMS; DOGS; HUMANS; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS;

EID: 46749094255     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.029470     Document Type: Article

References (42)

1. Bienz, M. and Clevers, H. (2000). Linking colorectal cancer to Wnt signaling. Cell 103, 311-320.
2. Day, C. L. and Alber, T. (2000). Crystal structure of the amino-terminal coiled-coil domain of the APC tumor suppressor. J. Mol. Biol. 301, 147-156.
3. Dikovskaya, D., Newton, I. P. and Näthke, I. S. (2004). The Adenomatous Polyposis Coli protein is required for the formation of robust spindles formed in CSF Xenopus extracts. Mol, Biol. Cell 15, 2978-2991.
4. Dikovskaya, D., Schiffmann, D., Newton, I. P., Oakley, A., Kroboth, K., Sansom, O., Jamieson, T. J., Meniel, V., Clarke, A. and Näthke, I. S. (2007). Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J. Cell Biol. 176, 183-195.
5. Etienne-Manneville, S. and Hall, A. (2003). Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421, 753-756.
6. Faux, M. C., Ross, J. L., Meeker, C., Johns, T., Ji, H., Simpson, R. J., Layton, M. J. and Burgess, A. W. (2004). Restoration of full-length adenomatous polyposis coli (APC) protein in a colon cancer cell line enhances cell adhesion. J. Cell Sci. 117, 427-439.
7. Fodde, R. (2002). The APC gene in colorectal cancer. Eur. J. Cancer 38, 867-871.
8. Green, R. A. and Kaplan, K. B. (2003). Chromosome instability in colorectal tumor cells is associated with defects in microtubule plus-end attachments caused by a dominant mutation in APC. J. Cell Biol. 163, 949-961.
9. Green, R. A., Wollman, R. and Kaplan, K. B. (2005). A-PC and EB1 function together in mitosis to regulate spindle dynamics and chromosome alignment. Mol. Biol. Cell 16, 4609-4622.
10. Hall, A. (2005). Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33, 891-895.
11. Hanson, C. A. and Miller, J. R. (2005). Non-traditional roles for the Adenomatous Polyposis Coli (APC) tumor suppressor protein. Gene 361, 1-12.
12. Honnappa, S., John, C. M., Kostrewa, D., Winkler, F. K. and Steinmetz, M. O. (2005). Structural insights into the EB1-APC interaction. EMBO J 24, 261-269.
13. Iizuka-Kogo, A., Shimomura, A. and Senda, T. (2005). Colocalization of APC and DLG at the tips of cellular protrusions in cultured epithelial cells and its dependency on cytoskeletons. Histochem. Cell Biol. 123, 67-73.
14. Jimbo, T., Kawasaki, Y., Koyama, R., Sato, R., Takada, S., Haraguchi, K. and Akiyama, T. (2002). Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat. Cell Biol. 4, 323-327.
15. Joslyn, G., Richardson, D. S., White, R. and Alber, T. (1993). Dimer formation by an N-terminal coiled coil in the APC protein. Proc. Natl. Acad. Sci. USA 90, 11109-11113.
16. Kawasaki, Y., Senda, T., Ishidate, T., Koyama, R., Morishita, T., Iwayama, Y., Higuchi, O. and Akiyama, T. (2000). Asef, a link between the tumor suppressor APC and G-protein signaling. Science 289, 1194-1197.
17. Kinzler, W. K. and Vogelstein, B. (1996). Lessons from hereditary colorectal cancer. Cell 87, 159-170.
18. Kita, K., Wittmann, T., Näthke, I. S. and Waterman-Storer, C. M. (2006). APC on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol. Biol. Cell 17, 2331-2345.
19. Kroboth, K., Newton, I. P., Kita, K., Dikovskaya, D., Zumbrunn, J., Waterman-Storer, C. M. and Näthke, I. S. (2007). Lack of adenomatous polyposis coli protein correlates with a decrease in cell migration and overall changes in microtubule stability. Mol. Biol. Cell 18, 910-918.
20. Li, Z. and Näthke, I. S. (2005). Tumor-associated NH2-terminal fragments are the most stable part of the adenomatous polyposis coli protein and can be regulated by interactions with COOH-terminal domains. Cancer Res. 65, 5195-5204.
21. Mackintosh, C. (2004). Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem. J. 381, 329-342.
22. Mahmoud, N. N., Boolbol, S. K., Bilinski, R. T., Martucci, C., Chadburn, A. and Bertagnolli, M. M. (1997). Apc gene mutation is associated with a dominant-negative effect upon intestinal cell migration. Cancer Res. 57, 5045-5050.
23. Marfatia, S. M., Byron, O., Campbell, G., Liu, S. C. and Chishti, A. H. (2000). Human homologue of the Drosophila discs large tumor suppressor protein forms an oligomer in solution. Identification of the self-association site. J. Biol. Chem. 275, 13759-13770.
24. Midgley, C. A., White, S., Howitt, R., Save, V., Dunlop, M. G., Hall, P. A., Lane, D. P., Wyllie, A. H. and Bubb, V. J. (1997). APC expression in normal human tissue. J. Pathol. 181, 426-433.
25. Moorhead, G., Douglas, P., Cotelle, V., Harthill, J., Morrice, N., Meek, S., Deiting, U., Stitt, M., Scarabel, M., Aitken, A. et al. (1999). Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. Plant J. 18, 1-12.
26. Morin, P. J., Vogelstein, B. and Kinzier, K. W. (1996). Apoptosis and APC in colorectal tumorigenesis. Proc. Natl. Acad. Sci. USA 93, 7950-7954.
27. Näthke, I. S., Adams, C. L., Polakis, P., Sellin, J. H. and Nelson, W. J. (1996a). The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J. Cell Biol. 134, 165-179.
28. Näthke, I. S., Barth, A. I. M. and Nelson, W. J. (1996b). Role for the tumor suppressor adenomatous polyposis coli porotein in epithelial migration and adhesion: a hypothesis. In Cytoskeletal-Membrane Interactions and Signal Transduction (ed. P. Cowin and M. W. Klymkowsky), pp. 103-110. New York: Chapman & Hall.
29. Oshima, H., Oshima, M., Kobayashi, M., Tsutsumi, M. and Taketo, M. M. (1997). Morphological and molecular processes of polyp formation in Apc(delta716). Cancer Res. 57, 1644-1649.
30. Polakis, P. (2000). Wnt signaling and cancer. Genes Dev. 14, 1837-1851.
31. Pozuelo Rubio, M., Peggie, M., Wong, B. H., Morrice, N. and MacKintosh, C. (2003). 14-3-3s regulate fructose-2,6-bisphosphate levels by binding to PKB-phosphorylated cardiac fructose-2,6-bisphosphate kinase/phosphatase. EMBO J. 22, 3514-3523.
32. Rubinfeld, B., Albert, I., Porfiri, E., Fiol, C., Munemitsu, S. and Polakis, P. (1996). Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272, 1023-1026.
33. Sansom, O. J., Reed, K. R., Hayes, A. J., Ireland, H., Brinkmann, H., Newton, I. P., Battle, E., Simon-Assmann, P., Clevers, H., Näthke, I. S. et al. (2004). Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev. 18, 1385-1390.
34. Schneikert, J. and Behrens, J. (2007). The canonical Wnt signalling pathway and its APC partner in colon cancer development. Gut 56, 417-425.
35. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E. and Tsien, R. Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572.
36. Su, L.-K., Johnson, K. A., Smith, K. J., Hill, D. E., Vogelstein, B. and Kinzler, K. W. (1993). Association between wildtype and mutant APC gene products. Cancer Res. 53, 2728-2731.
37. Su, L.-K., Burrell, M., Hill, D. E., Gyuris, J., Brent, R., Wiltshire, R., Trent, J., Vogelstein, B. and Kinzler, K. W. (1995). APC binds to the novel protein EB1. Cancer Res. 55, 2972-2977.
38. Tighe, A., Johnson, V. L. and Taylor, S. S. (2004). Truncating APC mutations have dominant effects on proliferation, spindle checkpoint control, survival and chromosome stability. J. Cell Sci. 117, 6339-6353.
39. van de Wetering, M., Sancho, E., Verweij, C., de Lau, W., Oving, I., Hurlstone, A., van der Horn, K., Battle, E., Coudreuse, D., Haramis, A. P. et al. (2002). The betacatenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241-250.
40. Watanabe, T., Wang, S., Noritake, J., Sato, K., Fukata, M., Takefuji, M., Nakagawa, M., Izumi, N., Akiyama, T. and Kaibuchi, K. (2004). Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev. Cell 7, 871-883.
41. Wilker, E. and Yaffe, M. B. (2004). 14-3-3 Proteins-a focus on cancer and human disease. J. Mol. Cell. Cardiol. 37, 633-642.
42. Zumbrunn, J., Inoshita, K., Hyman, A. A. and Näthke, I. S. (2001). Binding of the Adenomatous Polyposis Coli protein to microtubules increases microtubule stability and is regulated by GSK3b phosphorylation. Curr. Biol. 11, 44-49.