Novel insight into KLF4 proteolytic regulation in estrogen receptor signaling and breast carcinogenesis

Journal of Biological Chemistry

Volumn 287, Issue 17, 2012, Pages 13584-13597

  Hu, Dong ^a,b   Zhou, Zhuan ^a,b   Davidson, Nancy E ^a,b   Huang, Yi ^a,b   Wan, Yong ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER; BREAST CANCER CELLS; COLORECTAL CANCER; DOWN-REGULATION; ELEVATED LEVEL; ESTROGEN RECEPTOR; IMMUNOHISTOCHEMICAL STAINING; MITOGENIC EFFECTS; ONCOPROTEINS; TRANSACTIVATION; TRANSCRIPTIONAL FACTORS; TUMOR SUPPRESSORS; UNDERLYING MECHANISM;

PATHOLOGY; TISSUE;

DISEASES;

ESTROGEN RECEPTOR; KRUPPEL LIKE FACTOR 4; LYSINE; PROTEASOME; UBIQUITIN PROTEIN LIGASE E3; VON HIPPEL LINDAU PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOACCUMULATION; BREAST CARCINOGENESIS; CANCER GROWTH; CONTROLLED STUDY; DOWN REGULATION; ESTROGEN ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MITOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEADY STATE; TRANSACTIVATION; UPREGULATION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HOMEOSTASIS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MODELS, BIOLOGICAL; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 84859954415     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.343566     Document Type: Article

References (64)

1. Rowland, B. D., and Peeper, D. S. (2006) KLF4, p21, and context-dependent opposing forces in cancer. Nat. Rev. Cancer 6, 11-23 (Pubitemid 43053649)
2. Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (Pubitemid 44233629)
3. Wei, D., Kanai, M., Huang, S., and Xie, K. (2006) Emerging role of KLF4 in human gastrointestinal cancer. Carcinogenesis 27, 23-31 (Pubitemid 43032979)
4. Wang, N., Liu, Z. H., Ding, F., Wang, X. Q., Zhou, C. N., and Wu, M. (2002) Down-regulation of gut-enriched Kruppel-like factor expression inesophageal cancer. World J. Gastroenterol. 8, 966-970 (Pubitemid 35446403)
5. Tetreault, M. P., Yang, Y., Travis, J., Yu, Q. C., Klein-Szanto, A., Tobias, J. W., and Katz, J. P. (2010) Esophageal squamous cell dysplasia and delayed differentiation with deletion of Krüppel-like factor 4 in murine esophagus. Gastroenterology 139, 171-181.e9
6. Ohnishi, S., Ohnami, S., Laub, F., Aoki, K., Suzuki, K., Kanai, Y., Haga, K., Asaka, M., Ramirez, F., and Yoshida, T. (2003) Down-regulation and growth inhibitory effect of epithelial-type Krüppel-like transcription factor KLF4, but not KLF5, in bladder cancer. Biochem. Biophys. Res. Commun. 308, 251-256 (Pubitemid 36937173)
7. Hu, W., Hofstetter, W. L., Li, H., Zhou, Y., He, Y., Pataer, A., Wang, L., Xie, K., Swisher, S. G., and Fang, B. (2009) Putative tumor-suppressive function of Kruppel-like factor 4 in primary lung carcinoma. Clin. Cancer Res. 15, 5688-5695
8. Guan, H., Xie, L., Leithäuser, F., Flossbach, L., Möller, P., Wirth, T., and Ushmorov, A. (2010) KLF4 is a tumor suppressor in B-cell non-Hodgkin lymphoma and in classic Hodgkin lymphoma. Blood 116, 1469-1478
9. Foster, K. W., Frost, A. R., McKie-Bell, P., Lin, C. Y., Engler, J. A., Grizzle, W. E., and Ruppert, J. M. (2000) Increase of GKLF messenger RNA and protein expression during progression of breast cancer. Cancer Res. 60, 6488-6495
10. Pandya, A. Y., Talley, L. I., Frost, A. R., Fitzgerald, T. J., Trivedi, V., Chakravarthy, M., Chhieng, D. C., Grizzle, W. E., Engler, J. A., Krontiras, H., Bland, K. I., LoBuglio, A. F., Lobo-Ruppert, S. M., and Ruppert, J. M. (2004) Nuclear localization of KLF4 is associated with an aggressive phenotype in early stage breast cancer. Clin. Cancer Res. 10, 2709-2719 (Pubitemid 38509146)
11. Rowland, B. D., Bernards, R., and Peeper, D. S. (2005) The KLF4 tumour suppressor is a transcriptional repressor of p53 that acts as a context-dependent oncogene. Nat. Cell Biol. 7, 1074-1082
12. Foster, K. W., Ren, S., Louro, I. D., Lobo-Ruppert, S. M., McKie-Bell, P., Grizzle, W., Hayes, M. R., Broker, T. R., Chow, L. T., and Ruppert, J. M. (1999) Oncogene expression cloning by retroviral transduction of adenovirus E1A-immortalized rat kidney RK3E cells. Transformation of a host with epithelial features by c-MYC and the zinc finger protein GKLF. Cell Growth Differ. 10, 423-434 (Pubitemid 29284184)
13. Foster, K. W., Liu, Z., Nail, C. D., Li, X., Fitzgerald, T. J., Bailey, S. K., Frost, A. R., Louro, I. D., Townes, T. M., Paterson, A. J., Kudlow, J. E., Lobo-Ruppert, S. M., and Ruppert, J. M. (2005) Induction of KLF4 in basal keratinocytes blocks the proliferation-differentiation switch and initiates squamous epithelial dysplasia. Oncogene 24, 1491-1500 (Pubitemid 40396079)
14. Zhang, W., Geiman, D. E., Shields, J. M., Dang, D. T., Mahatan, C. S., Kaestner, K. H., Biggs, J. R., Kraft, A. S., and Yang, V. W. (2000) The gut-enriched Kruppel-like factor (Kruppel-like factor 4) mediates the transactivating effect of p53 on the p21WAF1/Cip1 promoter. J. Biol. Chem. 275, 18391-18398 (Pubitemid 30414796)
15. Wei, D., Kanai, M., Jia, Z., Le, X., and Xie, K. (2008) Kruppel-like factor 4 induces p27Kip1 expression in and suppresses the growth and metastasis of human pancreatic cancer cells. Cancer Res. 68, 4631-4639
16. Yoon, H. S., and Yang, V. W. (2004) Requirement of Krüppel-like factor 4 in preventing entry into mitosis following DNA damage. J. Biol. Chem. 279, 5035-5041 (Pubitemid 38199100)
17. Shie, J. L., Chen, Z. Y., Fu, M., Pestell, R. G., and Tseng, C. C. (2000) Gut-enriched Krüppel-like factor represses cyclin D1 promoter activity through Sp1 motif. Nucleic Acids Res. 28, 2969-2976 (Pubitemid 30599273)
18. Ghaleb, A. M., Katz, J. P., Kaestner, K. H., Du, J. X., and Yang, V. W. (2007) Krüppel-like factor 4 exhibits antiapoptotic activity following γ-radiation-induced DNA damage. Oncogene 26, 2365-2373 (Pubitemid 46572814)
19. Yu, F., Li, J., Chen, H., Fu, J., Ray, S., Huang, S., Zheng, H., and Ai, W. (2011) Kruppel-like factor 4 (KLF4) is required for maintenance of breast cancer stem cells and for cell migration and invasion. Oncogene 30, 2161-2172
20. Chen, Z. Y., Wang, X., Zhou, Y., Offner, G., and Tseng, C. C. (2005) Destabilization of Krüppel-like factor 4 protein in response to serum stimulation involves the ubiquitin-proteasome pathway. Cancer Res. 65, 10394-10400 (Pubitemid 41743733)
21. Shields, J. M., Christy, R. J., and Yang, V. W. (1996) Identification and characterization of a gene encoding a gut-enriched Krüppel-like factor expressed during growth arrest. J. Biol. Chem. 271, 20009-20017
22. Cullingford, T. E., Butler, M. J., Marshall, A. K., Tham el, L., Sugden, P. H., and Clerk, A. (2008) Differential regulation of Krüppel-like factor family transcription factor expression in neonatal rat cardiac myocytes. Effects of endothelin-1, oxidative stress, and cytokines. Biochim. Biophys. Acta 1783, 1229-1236
23. Shie, J. L., Chen, Z. Y., O'Brien, M. J., Pestell, R. G., Lee, M. E., and Tseng, C. C. (2000) Role of gut-enriched Krüppel-like factor in colonic cell growth and differentiation. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G806-G814
24. Liu, S., Zhang, H., Zhu, L., Zhao, L., and Dong, Y. (2008) Kruppel-like factor 4 is a novel mediator of selenium in growth inhibition. Mol. Cancer Res. 6, 306-313 (Pubitemid 351342418)
25. Chen, Z. Y., Shie, J., and Tseng, C. (2000) Up-regulation of gut-enriched Krüppel-like factor by interferon-γ in human colon carcinoma cells. FEBS Lett. 477, 67-72 (Pubitemid 30438859)
26. Birsoy, K., Chen, Z., and Friedman, J. (2008) Transcriptional regulation of adipogenesis by KLF4. Cell Metab. 7, 339-347 (Pubitemid 351455215)
27. Zhou, Q., Hong, Y., Zhan, Q., Shen, Y., and Liu, Z. (2009) Role for Kruppellike factor 4 in determining the outcome of p53 response toDNAdamage. Cancer Res. 69, 8284-8292
28. Evans, P. M., Zhang, W., Chen, X., Yang, J., Bhakat, K. K., and Liu, C. (2007) Kruppel-like factor 4 is acetylated by p300 and regulates gene transcription via modulation of histone acetylation. J. Biol. Chem. 282, 33994-34002 (Pubitemid 350159428)
29. Du, J. X., McConnell, B. B., and Yang, V. W. (2010) A small ubiquitin-related modifier-interacting motif functions as the transcriptional activation domain of Krüppel-like factor 4. J. Biol. Chem. 285, 28298-28308
30. Chu, P. Y., Hsu, N. C., Liao, A. T., Yeh, K. T., Hou, M. F., and Liu, C. H. (2011) Elevated Krüppel-like factor 4 transcription factor in canine mammary carcinoma. BMC Vet. Res. 7, 58
31. Tyson, J. J., Baumann, W. T., Chen, C., Verdugo, A., Tavassoly, I., Wang, Y., Weiner, L. M., and Clarke, R. (2011) Dynamic modeling of oestrogen signaling and cell fate in breast cancer cells. Nat. Rev. Cancer 11, 523-532
32. Liu, W., Wu, G., Li, W., Lobur, D., and Wan, Y. (2007) Cdh1 anaphasepromoting complex targets Skp2 for destruction in transforming growth factor β-induced growth inhibition. Mol. Cell. Biol. 27, 2967-2979 (Pubitemid 46581310)
33. Fujita, T., Liu, W., Doihara, H., Date, H., and Wan, Y. (2008) Dissection of the APCCdh1-Skp2 cascade in breast cancer. Clin. Cancer Res. 14, 1966-1975 (Pubitemid 351551105)
34. Chen, C. J., Lin, S. E., Lin, Y. M., Lin, S. H., Chen, D. R., and Chen, C. L. (2011) Association of expression of Kruppel-like factor 4 and Kruppel-like factor 5 with the clinical manifestations of breast cancer. Pathol. Oncol. Res., in press
35. Gluck, S., Ross, J. S., Royce, M., McKenna, E. F., Jr., Perou, C. M., Avisar, E., and Wu, L. (2011) TP53 genomics predict higher clinical and pathologic tumor response in operable early stage breast cancer treated with docetaxel-capecitabine ± trastuzumab. Breast Cancer Res. Treat., in press
36. Evans, P. M., and Liu, C. (2008) Roles of Krüpel-like factor 4 in normal homeostasis, cancer, and stem cells. Acta Biochim. Biophys. Sin. 40, 554-564 (Pubitemid 352009081)
37. McConnell, B. B., Ghaleb, A. M., Nandan, M. O., and Yang, V. W. (2007) The diverse functions of Krüppel-like factors 4 and 5 in epithelial biology and pathobiology. BioEssays 29, 549-557 (Pubitemid 46903942)
38. Musgrove, E. A., and Sutherland, R. L. (2009) Biological determinants of endocrine resistance in breast cancer. Nat. Rev. Cancer 9, 631-643
39. Kudo, Y., Guardavaccaro, D., Santamaria, P. G., Koyama-Nasu, R., Latres, E., Bronson, R., Yamasaki, L., and Pagano, M. (2004) Role of F-box protein βTrcp1 in mammary gland development and tumorigenesis. Mol. Cell. Biol. 24, 8184-8194 (Pubitemid 39167466)
40. Zia, M. K., Rmali, K. A., Watkins, G., Mansel, R. E., and Jiang, W. G. (2007) The expression of the von Hippel-Lindau gene product and its impact on invasiveness of human breast cancer cells. Int. J. Mol. Med. 20, 605-611
41. Signoretti, S., Di Marcotullio, L., Richardson, A., Ramaswamy, S., Isaac, B., Rue, M., Monti, F., Loda, M., and Pagano, M. (2002) Oncogenic role of the ubiquitin ligase subunit Skp2 in human breast cancer. J. Clin. Invest. 110, 633-641 (Pubitemid 34988787)
42. Schuetz, A., Nana, D., Rose, C., Zocher, G., Milanovic, M., Koenigsmann, J., Blasig, R., Heinemann, U., and Carstanjen, D. (2011) The structure of the Klf4 DNA-binding domain links to self-renewal and macrophage differentiation. Cell. Mol. Life Sci. 68, 3121-3131
43. Brown, R. J., and Davidson, N. E. (2006) Adjuvant hormonal therapy for premenopausal women with breast cancer. Semin. Oncol. 33, 657-663 (Pubitemid 44828125)
44. Kaelin, W. G. (2007) Von Hippel-Lindau disease. Annu. Rev. Pathol. 2, 145-173
45. Hu, D., and Wan, Y. (2011) Regulation of Krüppel-like factor 4 by the anaphase-promoting complex pathway is involved in TGF-β signaling. J. Biol. Chem. 286, 6890-6901
46. Thomas, C., and Gustafsson, J. Å. (2011) The different roles of ER subtypes in cancer biology and therapy. Nat. Rev. Cancer 11, 597-608
47. Geiman, D. E., Ton-That, H., Johnson, J. M., and Yang, V. W. (2000) Transactivation and growth suppression by the gut-enriched Krüppel-like factor (Krüppel-like factor 4) are dependent on acidic amino acid residues and protein-protein interaction. Nucleic Acids Res. 28, 1106-1113 (Pubitemid 30107678)
48. Feinberg, M. W., Cao, Z., Wara, A. K., Lebedeva, M. A., Senbanerjee, S., and Jain, M. K. (2005) Kruppel-like factor 4 is a mediator of proinflammatory signaling in macrophages. J. Biol. Chem. 280, 38247-38258 (Pubitemid 43853721)
49. Ai, W., Zheng, H., Yang, X., Liu, Y., and Wang, T. C. (2007) Tip60 functions as a potential corepressor of KLF4 in regulation of HDC promoter activity. Nucleic Acids Res. 35, 6137-6149 (Pubitemid 350018576)
50. Hanstein, B., Eckner, R., DiRenzo, J., Halachmi, S., Liu, H., Searcy, B., Kurokawa, R., and Brown, M. (1996) p300 is a component of an estrogen receptor coactivator complex. Proc. Natl. Acad. Sci. U.S.A. 93, 11540-11545 (Pubitemid 26347157)
51. Gaughan, L., Brady, M. E., Cook, S., Neal, D. E., and Robson, C. N. (2001) Tip60 is a co-activator specific for class I nuclear hormone receptors. J. Biol. Chem. 276, 46841-46848
52. Williamson, L. M., and Lees-Miller, S. P. (2011) Estrogen receptor α-mediated transcription induces cell cycle-dependent DNA double strand breaks. Carcinogenesis 32, 279-285
53. Pedram, A., Razandi, M., Evinger, A. J., Lee, E., and Levin, E. R. (2009) Estrogen inhibits ATR signaling to cell cycle checkpoints andDNArepair. Mol. Biol. Cell 20, 3374-3389
54. 1/S cell cycle arrest in response to DNA damage. J. Biol. Chem. 278, 2101-2105
55. Yoon, H. S., Ghaleb, A. M., Nandan, M. O., Hisamuddin, I. M., Dalton, W. B., and Yang, V. W. (2005) Krüppel-like factor 4 prevents centrosome amplification following γ-irradiation-induced DNA damage. Oncogene 24, 4017-4025 (Pubitemid 40897049)
56. Hoeller, D., and Dikic, I. (2009) Targeting the ubiquitin system in cancer therapy. Nature 458, 438-444
57. Sun, Y. (2006) E3 ubiquitin ligases as cancer targets and biomarkers. Neoplasia 8, 645-654
58. Kaelin, W. G., Jr. (2008) The von Hippel-Lindau tumor suppressor protein. O2 sensing and cancer. Nat. Rev. Cancer 8, 865-873
59. Hoffman, M. A., Ohh, M., Yang, H., Klco, J. M., Ivan, M., and Kaelin, W. G., Jr. (2001) von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to down-regulate HIF. Hum. Mol. Genet. 10, 1019-1027 (Pubitemid 32447779)
60. Elson, D. A., Thurston, G., Huang, L. E., Ginzinger, D. G., McDonald, D. M., Johnson, R. S., and Arbeit, J. M. (2001) Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1α. Genes Dev. 15, 2520-2532 (Pubitemid 32937863)
61. Sourvinos, G., Miyakis, S., Liloglou, T. L., Field, J. K., and Spandidos, D. A. (2001) Von Hippel-Lindau tumour suppressor gene is not involved in sporadic human breast cancer. Tumour Biol. 22, 131-136 (Pubitemid 32245408)
62. Seagroves, T. N., Peacock, D. L., Liao, D., Schwab, L. P., Krueger, R., Handorf, C. R., Haase, V. H., and Johnson, R. S. (2010) VHL deletion impairs mammary alveologenesis but is not sufficient for mammary tumorigenesis. Am. J. Pathol. 176, 2269-2282
63. Asselin-Labat, M. L., Vaillant, F., Sheridan, J. M., Pal, B., Wu, D., Simpson, E. R., Yasuda, H., Smyth, G. K., Martin, T. J., Lindeman, G. J., and Visvader, J. E. (2010) Control of mammary stem cell function by steroid hormone signaling. Nature 465, 798-802
64. Joshi, P. A., Jackson, H. W., Beristain, A. G., Di Grappa, M. A., Mote, P. A., Clarke, C. L., Stingl, J., Waterhouse, P. D., and Khokha, R. (2010) Progesterone induces adult mammary stem cell expansion. Nature 465, 803-807