A colon cancer-derived mutant of Krüppel-like factor 5 (KLF5) is resistant to degradation by glycogen synthase kinase 3β (GSK3β) and the E3 ubiquitin ligase F-box and WD repeat domain-containing 7α(FBW7α)

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 5997-6005

  Bialkowska, Agnieszka B ^a   Liu, Yang ^a   Nandan, Mandayam O ^a   Yang, Vincent W ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; COLORECTAL CANCER CELL; GLYCOGEN SYNTHASE KINASE-3; INTESTINAL EPITHELIAL CELLS; LUCIFERASE ASSAYS; PROTEASOMAL DEGRADATION; TRANSCRIPTIONAL ACTIVITY; ZINC FINGER TRANSCRIPTION FACTOR;

AMINO ACIDS; CELLS; PHOSPHORYLATION;

DISEASES;

CYCLIN D1; F BOX AND WD REPEAT DOMAIN CONTAINING 7 ALPHA PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; KRUPPEL LIKE FACTOR 5; PROLINE; SERINE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIGEN EXPRESSION; ARTICLE; CELL PROLIFERATION; COLORECTAL CANCER; CONTROLLED STUDY; EMBRYO; ENZYME PHOSPHORYLATION; HALF LIFE TIME; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY;

CELL BIOLOGY; CYCLIN D1; MUTANT; PROMOTERS; PROTEIN STABILITY; TRANSCRIPTION FACTORS;

AMINO ACID SUBSTITUTION; CELL CYCLE PROTEINS; CELL LINE, TUMOR; COLONIC NEOPLASMS; F-BOX PROTEINS; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MUTATION, MISSENSE; NEOPLASM PROTEINS; PHOSPHORYLATION; PROTEOLYSIS; UBIQUITIN-PROTEIN LIGASES;

EID: 84896891027     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.508549     Document Type: Article

References (35)

1. McConnell, B. B., Ghaleb, A. M., Nandan, M. O., and Yang, V. W. (2007) The diverse functions of Kruppel-like factors 4 and 5 in epithelial biology and pathobiology. BioEssays 29, 549-557 (Pubitemid 46903942)
2. McConnell, B. B., and Yang, V. W. (2010) Mammalian Kruppel-like factors in health and diseases. Physiol. Rev. 90, 1337-1381
3. Min mutation in the intestine. Cancer Res. 69, 4125-4133
4. V12 mutations. Mol. Cancer 9, 63
5. Nandan, M. O., Yoon, H. S., Zhao, W., Ouko, L. A., Chanchevalap, S., and Yang, V. W. (2004) Kruppel-like factor 5 mediates the transforming activity of oncogenic H-Ras. Oncogene 23, 3404-3413 (Pubitemid 38669830)
6. Nandan, M. O., Chanchevalap, S., Dalton, W. B., and Yang, V. W. (2005) Kruppel-like factor 5 promotes mitosis by activating the cyclin B1/Cdc2 complex during oncogenic Ras-mediated transformation. FEBS Lett. 579, 4757-4762 (Pubitemid 41218659)
7. Yang, Y., Tetreault, M. P., Yermolina, Y. A., Goldstein, B. G., and Katz, J. P. (2008) Kruppel-like factor 5 controls keratinocyte migration via the integrin-linked kinase. J. Biol. Chem. 283, 18812-18820
8. Chen, C., Zhou, Y., Zhou, Z., Sun, X., Otto, K. B., Uht, R. M., and Dong, J. T. (2004) Regulation of KLF5 involves the Sp1 transcription factor in human epithelial cells. Gene 330, 133-142 (Pubitemid 38490426)
9. Mori, D., Okuro, N., Fujii-Kuriyama, Y., and Sogawa, K. (2003) Gene structure and promoter analysis of the rat BTEB2 gene. Gene 304, 163-170 (Pubitemid 36140140)
10. Chen, C., Sun, X., Ran, Q., Wilkinson, K. D., Murphy, T. J., Simons, J. W., and Dong, J. T. (2005) Ubiquitin-proteasome degradation of KLF5 transcription factor in cancer and untransformed epithelial cells. Oncogene 24, 3319-3327 (Pubitemid 40695113)
11. Dong, J. T., and Chen, C. (2009) Essential role of KLF5 transcription factor in cell proliferation and differentiation and its implications for human diseases. Cell. Mol. Life Sci. 66, 2691-2706
12. Du, J. X., Bialkowska, A. B., McConnell, B. B., and Yang, V. W. (2008) SUMOylation regulates nuclear localization of Kruppel-like factor 5. J. Biol. Chem. 283, 31991-32002
13. Du, J. X., Yun, C. C., Bialkowska, A., and Yang, V. W. (2007) Protein inhibitor of activated STAT1 interacts with and up-regulates activities of the pro-proliferative transcription factor Kruppel-like factor 5. J. Biol. Chem. 282, 4782-4793 (Pubitemid 47100934)
14. Guo, P., Dong, X. Y., Zhang, X., Zhao, K. W., Sun, X., Li, Q., and Dong, J. T. (2009) Pro-proliferative factor KLF5 becomes anti-proliferative in epithelial homeostasis upon signaling-mediated modification. J. Biol. Chem. 284, 6071-6078
15. Guo, P., Zhao, K. W., Dong, X. Y., Sun, X., and Dong, J. T. (2009) Acetylation of KLF5 alters the assembly of p15 transcription factors in transforming growth factor-β-mediated induction in epithelial cells. J. Biol. Chem. 284, 18184-18193
16. Miyamoto, S., Suzuki, T., Muto, S., Aizawa, K., Kimura, A., Mizuno, Y., Nagino, T., Imai, Y., Adachi, N., Horikoshi, M., and Nagai, R. (2003) Positive and negative regulation of the cardiovascular transcription factor KLF5 by p300 and the oncogenic regulator SET through interaction and acetylation on the DNA-binding domain. Mol. Cell. Biol. 23, 8528-8541 (Pubitemid 37433360)
17. Zhang, Z., and Teng, C. T. (2003) Phosphorylation of Kruppel-like factor 5 (KLF5/IKLF) at the CBP interaction region enhances its transactivation function. Nucleic Acids Res. 31, 2196-2208 (Pubitemid 37442086)
18. Zhao, D., Zhi, X., Zhou, Z., and Chen, C. (2012) TAZ antagonizes the WWP1-mediated KLF5 degradation and promotes breast cell proliferation and tumorigenesis. Carcinogenesis 33, 59-67
19. Zhao, D., Zheng, H. Q., Zhou, Z., and Chen, C. (2010) The Fbw7 tumor suppressor targets KLF5 for ubiquitin-mediated degradation and suppresses breast cell proliferation. Cancer Res. 70, 4728-4738
20. Liu, N., Li, H., Li, S., Shen, M., Xiao, N., Chen, Y., Wang, Y., Wang, W., Wang, R., Wang, Q., Sun, J., and Wang, P. (2010) The Fbw7/human CDC4 tumor suppressor targets proproliferative factor KLF5 for ubiquitination and degradation through multiple phosphodegron motifs. J. Biol. Chem. 285, 18858-18867
21. Sjöblom, T., Jones, S., Wood, L. D., Parsons, D. W., Lin, J., Barber, T. D., Mandelker, D., Leary, R. J., Ptak, J., Silliman, N., Szabo, S., Buckhaults, P., Farrell, C., Meeh, P., Markowitz, S. D., Willis, J., Dawson, D., Willson, J. K., Gazdar, A. F., Hartigan, J., Wu, L., Liu, C., Parmigiani, G., Park, B. H., Bachman, K. E., Papadopoulos, N., Vogelstein, B., Kinzler, K. W., and Velculescu, V. E. (2006) The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274 (Pubitemid 44571966)
22. Ekstrand, A. I., Jönsson, M., Lindblom, A., Borg, A., and Nilbert, M. (2010) Frequent alterations of the PI3K/AKT/mTOR pathways in hereditary nonpolyposis colorectal cancer. Fam. Cancer 9, 125-129
23. Fearon, E. R. (2011) Molecular genetics of colorectal cancer. Annu. Rev. Pathol. 6, 479-507
24. Goel, A., Arnold, C. N., Niedzwiecki, D., Carethers, J. M., Dowell, J. M., Wasserman, L., Compton, C., Mayer, R. J., Bertagnolli, M. M., and Boland, C. R. (2004) Frequent inactivation of PTEN by promoter hypermethylation in microsatellite instability-high sporadic colorectal cancers. Cancer Res. 64, 3014-3021 (Pubitemid 38581399)
25. Simi, L., Pratesi, N., Vignoli, M., Sestini, R., Cianchi, F., Valanzano, R., Nobili, S., Mini, E., Pazzagli, M., and Orlando, C. (2008) High-resolution melting analysis for rapid detection of KRAS, BRAF, and PIK3CA gene mutations in colorectal cancer. Am. J. Clin. Pathol. 130, 247-253
26. Zhang, J., Roberts, T. M., and Shivdasani, R. A. (2011) Targeting PI3K signaling as a therapeutic approach for colorectal cancer. Gastroenterology 141, 50-61
27. Korinek, V., Barker, N., Morin, P. J., van Wichen, D., de Weger, R., Kinzler, K. W., Vogelstein, B., and Clevers, H. (1997) Constitutive transcriptional activation by a β-catenin-Tcf complex in APC-/- colon carcinoma. Science 275, 1784-1787 (Pubitemid 27136714)
28. Morin, P. J., Sparks, A. B., Korinek, V., Barker, N., Clevers, H., Vogelstein, B., and Kinzler, K. W. (1997) Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science 275, 1787-1790 (Pubitemid 27136715)
29. 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 (Pubitemid 34327534)
30. Van der Flier, L. G., Sabates-Bellver, J., Oving, I., Haegebarth, A., De Palo, M., Anti, M., Van Gijn, M. E., Suijkerbuijk, S., Van de Wetering, M., Marra, G., and Clevers, H. (2007) The intestinal Wnt/TCF signature. Gastroenterology 132, 628-632
31. Burgess, A. W., Faux, M. C., Layton, M. J., and Ramsay, R. G. (2011) Wnt signaling and colon tumorigenesis-a view from the periphery. Exp. Cell Res. 317, 2748-2758
32. Bamford, S., Dawson, E., Forbes, S., Clements, J., Pettett, R., Dogan, A., Flanagan, A., Teague, J., Futreal, P. A., Stratton, M. R., and Wooster, R. (2004) The COSMIC (Catalogue of Somatic Mutations in Cancer) database and website. Br. J. Cancer 91, 355-358 (Pubitemid 39037083)
33. Davis, H., Lewis, A., Behrens, A., and Tomlinson, I. (2013) Investigation of the atypical FBXW7 mutation spectrum in human tumours by conditional expression of a heterozygous propellor tip missense allele in the mouse intestines. Gut 10.1136/gutjnl-2013-304719
34. Rajagopalan, H., Jallepalli, P. V., Rago, C., Velculescu, V. E., Kinzler, K. W., Vogelstein, B., and Lengauer, C. (2004) Inactivation of hCDC4 can cause chromosomal instability. Nature 428, 77-81 (Pubitemid 38332360)
35. Kemp, Z., Rowan, A., Chambers, W., Wortham, N., Halford, S., Sieber, O., Mortensen, N., von Herbay, A., Gunther, T., Ilyas, M., and Tomlinson, I. (2005) CDC4 mutations occur in a subset of colorectal cancers but are not predicted to cause loss of function and are not associated with chromosomal instability. Cancer Res. 65, 11361-11366 (Pubitemid 41821693)