PAX2 protein induces expression of cyclin D1 through activating AP-1 protein and promotes proliferation of colon cancer cells

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44164-44172

  Zhang, Hai Sheng ^a   Yan, Bing ^a   Li, Xue Bing ^a   Fan, Li ^a   Zhang, Yun Fang ^a   Wu, Guo Hao ^b   Li, Min ^c   Fang, Jing ^a  

^a Chinese Academy of Sciences   (China)

^b FUDAN UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLON CANCER CELLS; CYCLIND1; HUMAN COLON CANCER; MALIGNANT TUMORS; UNDERLYING MECHANISM;

PHOSPHORYLATION; TISSUE; TRANSCRIPTION FACTORS;

CELLS;

CYCLIN D1; MESSENGER RNA; PROTEIN C FOS; PROTEIN C JUN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR JUNB; TRANSCRIPTION FACTOR PAX2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; CYCLIN D1 GENE; DISEASE ASSOCIATION; EMBRYO; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION FACTOR AP 1 GENE; TRANSCRIPTION FACTOR PAX2 GENE; TUMOR GENE; TUMOR PROMOTION; TUMOR XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; CYCLIN D1; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; PAX2 TRANSCRIPTION FACTOR; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; TRANSCRIPTION FACTOR AP-1; UP-REGULATION;

EID: 84871757427     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.401521     Document Type: Article

References (41)

1. Robson, E. J., He, S. J., and Eccles, M. R. (2006) A PANorama of PAX genes in cancer and development. Nat. Rev. Cancer 6, 52-62
2. Lang, D., Powell, S. K., Plummer, R. S., Young, K. P., and Ruggeri, B. A. (2007) PAX genes: roles in development, pathophysiology, and cancer. Biochem. Pharmacol. 73, 1-14
3. Muratovska, A., Zhou, C., He, S., Goodyer, P., and Eccles, M. R. (2003) Paired-box genes are frequently expressed in cancer and often required for cancer cell survival. Oncogene 22, 7989-7997
4. Luu, V. D., Boysen, G., Struckmann, K., Casagrande, S., von Teichman, A., Wild, P. J., Sulser, T., Schraml, P., and Moch, H. (2009) Loss of VHL and hypoxia provokes PAX2 up-regulation in clear cell renal cell carcinoma. Clin. Cancer Res. 15, 3297-3304
5. Torban, E., Eccles, M. R., Favor, J., and Goodyer, P. R. (2000) PAX2 suppresses apoptosis in renal collecting duct cells. Am. J. Pathol. 157, 833-842
6. Hueber, P. A., Waters, P., Clark, P., Eccles, M., and Goodyer, P. (2006) PAX2 inactivation enhances cisplatin-induced apoptosis in renal carcinoma cells. Kidney Int. 69, 1139-1145
7. Hueber, P. A., Iglesias, D., Chu, L. L., Eccles, M., and Goodyer, P. (2008) In vivo validation of PAX2 as a target for renal cancer therapy. Cancer Lett. 265, 148-155
8. Gnarra, J. R., and Dressler, G. R. (1995) Expression of Pax2 in human renal cell carcinoma and growth inhibition by antisense oligonucleotides. Cancer Res. 55, 4092-4098
9. Buttiglieri, S., Deregibus, M. C., Bravo, S., Cassoni, P., Chiarle, R., Bussolati, B., and Camussi, G. (2004) Role of PAX2 in apoptosis resistance and proinvasive phenotype of Kaposi's sarcoma cells. J. Biol. Chem. 279, 4136-4143
10. Gibson, W., Green, A., Bullard, R. S., Eaddy, A. C., and Donald, C. D. (2007) Inhibition of PAX2 expression results in alternate cell death pathways in prostate cancer cells differing in p53 status. Cancer Lett. 248, 251-261
11. Davies, R. J., Miller, R., and Coleman, N. (2005) Colorectal cancer screening: prospects for molecular stool analysis. Nat. Rev. Cancer 5, 199-209
12. Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J. Q., Murray, T., and Thun, M. J. (2008) Cancer statistics, 2008. CA Cancer J. Clin. 58, 71-96
13. Yan, B., Jiao, S., Zhang, H. S., Lv, D. D., Xue, J., Fan, L., Wu, G. H., and Fang, J. (2011) Prolyl hydroxylase domain protein 3 targets Pax2 for destruction. Biochem. Biophys. Res. Commun. 409, 315-320
14. Albanese, C., Johnson, J., Watanabe, G., Eklund, N., Vu, D., Arnold, A., and Pestell, R. G. (1995) Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J. Biol. Chem. 270, 23589-23597
15. Xue, J., Li, X., Jiao, S., Wei, Y., Wu, G., and Fang, J. (2010) Prolyl hydroxylase-3 is downregulated in colorectal cancer cells and inhibits IKKβ, independent of hydroxylase activity. Gastroenterology 138, 606-615
16. Fang, J., Zhou, Q., Shi, X. L., and Jiang, B. H. (2007) Luteolin inhibits insulin-like growth factor 1 receptor signaling in prostate cancer cells. Carcinogenesis 28, 713-723
17. Li, Z., Zhang, H., Chen, Y., Fan, L., and Fang, J. (2012) Forkhead transcription factor FOXO3a protein activates nuclear factor κB through B-cell lymphoma/leukemia 10 (BCL10) protein and promotes tumor cell survival in serum deprivation. J. Biol. Chem. 287, 17737-17745
18. Tetsu, O., and McCormick, F. (1999) β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426
19. 1-to-S-phase transition. Mol. Cell. Biol. 19, 2690-2698
20. Bakiri, L., Lallemand, D., Bossy-Wetzel, E., and Yaniv, M. (2000) Cell cycle-dependent variations in c-Jun and JunB phosphorylation: a role in the control of cyclin D1 expression. EMBO J. 19, 2056-2068
21. Deng, T., and Karin, M. (1993) JunB differs from c-Jun in its DNA-binding and dimerization domains, and represses c-Jun by formation of inactive heterodimers. Genes Dev. 7, 479-490
22. Schütte, J., Viallet, J., Nau, M., Segal, S., Fedorko, J., and Minna, J. (1989) jun-B inhibits and c-fos stimulates the transforming and trans-activating activities of c-jun. Cell 59, 987-997
23. Chiu, R., Angel, P., and Karin, M. (1989) Jun-B differs in its biological properties from, and is a negative regulator of, c-Jun. Cell 59, 979-986
24. Reddy, S. P., and Mossman, B. T. (2002) Role and regulation of activator protein-1 in toxicant-induced responses of the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 283, L1161-L1178
25. Eferl, R., and Wagner, E. F. (2003) AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer 3, 859-868
26. Pulverer, B. J., Kyriakis, J. M., Avruch, J., Nikolakaki, E., and Woodgett, J. R. (1991) Phosphorylation of c-jun mediated by MAP kinases. Nature 353, 670-674
27. Palmqvist, R., Stenling, R., Oberg, A., and Landberg, G. (1998) Expression of cyclin D1 and retinoblastoma protein in colorectal cancer. Eur. J. Cancer 34, 1575-1581
28. Arber, N., Hibshoosh, H., Moss, S. F., Sutter, T., Zhang, Y., Begg, M., Wang, S., Weinstein, I. B., and Holt, P. R. (1996) Increased expression of cyclin D1 is an early event in multistage colorectal carcinogenesis. Gastroenterology 110, 669-674
29. Palmqvist, R., Rutegârd, J. N., Bozoky, B., Landberg, G., and Stenling, R. (2000) Human colorectal cancers with an intact p16/cyclin D1/pRb pathway have up-regulated p16 expression and decreased proliferation in small invasive tumor clusters. Am. J. Pathol 157, 1947-1953
30. Shtutman, M., Zhurinsky, J., Simcha, I., Albanese, C., D'Amico, M., Pestell, R., and Ben-Ze'ev, A. (1999) The cyclin D1 gene is a target of the β-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 5522-5527
31. Shaulian, E., and Karin, M. (2002) AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4, E131-E136
32. Nagata, D., Suzuki, E., Nishimatsu, H., Satonaka, H., Goto, A., Omata, M., Hirata, Y. (2001) Transcriptional activation of the cyclin D1 gene is mediated by multiple cis-elements, including SP1 sites and a cAMP-responsive element in vascular endothelial cells. J. Biol. Chem. 276, 662-669
33. Maeda, S., and Karin, M. (2003) Oncogene at last-c-Jun promotes liver cancer in mice. Cancer Cell 3, 102-104
34. Jochum, W., Passegué, E., Wagner, E. F. (2001) AP-1 in mouse development and tumorigenesis. Oncogene 20, 2401-2412
35. Matthews, C. P., Colburn, N. H., and Young, M. R. (2007) AP-1 a target for cancer prevention. Curr. Cancer Drug Targets 7, 317-324
36. Wang, H. L., Wang, J., Xiao, S. Y., Haydon, R., Stoiber, D., He, T. C., Bissonnette, M., and Hart, J. (2002) Elevated protein expression of cyclin D1 and Fra-1 but decreased expression of c-Myc in human colorectal adenocarcinomas overexpressing β-catenin. Int. J. Cancer 101, 301-310
37. Suto, R., Tominaga, K., Mizuguchi, H., Sasaki, E., Higuchi, K., Kim, S., Iwao, H., and Arakawa, T. (2004) Dominant-negative mutant of c-Jun gene transfer: a novel therapeutic strategy for colorectal cancer. Gene. Ther. 11, 187-193
38. Xu, Y. M., Zhu, F., Cho, Y. Y., Carper, A., Peng, C., Zheng, D., Yao, K., Lau, A. T., Zykova, T. A., Kim, H. G., Bode, A. M., and Dong, Z. (2010) Extracellular signal-regulated kinase 8-mediated c-Jun phosphorylation increases tumorigenesis of human colon cancer. Cancer Res. 70, 3218-3227
39. Nateri, A. S., Spencer-Dene, B., and Behrens, A. (2005) Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437, 281-285
40. Sancho, R., Nateri, A. S., de Vinuesa, A. G., Aguilera, C., Nye, E., Spencer-Dene, B., and Behrens, A. (2009) JNK signalling modulates intestinal homeostasis and tumourigenesis in mice. EMBO J. 28, 1843-1854
41. Ashida, R., Tominaga, K., Sasaki, E., Watanabe, T., Fujiwara, Y., Oshitani, N., Higuchi, K., Mitsuyama, S., Iwao, H., and Arakawa, T. (2005) AP-1 and colorectal cancer. Inflammopharmacology 13, 113-125