Hepatocyte nuclear factor 6 suppresses the migration and invasive growth of lung cancer cells through p53 and the inhibition of epithelial-mesenchymal transition

Journal of Biological Chemistry

Volumn 288, Issue 43, 2013, Pages 31206-31216

  Yuan, Xin Wang ^a   Wang, Dong Mei ^a   Hu, Ying ^a   Tang, Yun Neng ^a   Shi, Wei Wei ^a   Guo, Xiao Jie ^a   Song, Jian Guo ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIAL-MESENCHYMAL TRANSITION; HEPATOCYTE NUCLEAR FACTORS; HUMAN LUNG CANCER CELLS; PATHOLOGICAL FUNCTIONS; POSITIVE CORRELATIONS; PROMOTER ACTIVITIES; TRANSCRIPTIONAL ACTIVATIONS; TUMOR SUPPRESSORS;

BIOLOGICAL ORGANS; DISEASES; RESPIRATORY SYSTEM; TUMORS;

CELLS;

HEPATOCYTE NUCLEAR FACTOR 6; PROTEIN P53; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL MIGRATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION; TUMOR INVASION; TUMOR XENOGRAFT;

CELL MIGRATION; EMT; EPITHELIAL CELL; HNF6; INVASION; P53; TRANSFORMING GROWTH FACTOR BETA (TGFBETA);

ADENOCARCINOMA; ANIMALS; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HEPATOCYTE NUCLEAR FACTOR 6; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; MICE; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA1; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84886652512     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.480285     Document Type: Article

References (36)

1. Yang, J., Mani, S. A., Donaher, J. L., Ramaswamy, S., Itzykson, R. A., Come, C., Savagner, P., Gitelman, I., Richardson, A., and Weinberg, R. A. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939
2. Thiery, J. P. (2002) Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2, 442-454
3. Hugo, H., Ackland, M. L., Blick, T., Lawrence, M. G., Clements, J. A., Williams, E. D., and Thompson, E. W. (2007) Epithelial-mesenchymal and mesenchymal-epithelial transitionsin carcinoma progression. J. Cell. Physiol. 213, 374-383
4. Tang, Y., Shu, G., Yuan, X., Jing, N., and Song, J. (2011) FOXA2 functions as a suppressor of tumor metastasis by inhibition of epithelial-to-mesenchymal transition in human lung cancers.. Cell Res. 21, 316-326
5. Song, Y., Washington, M. K., and Crawford, H. C. (2010) Loss of FOXA1/2 is essential for the epithelial-to-mesenchymal transition in pancreatic cancer. Cancer Res. 70, 2115-2125
6. Yue, H. Y., Yin, C, Hou, J. L., Zeng, X., Chen, Y. X., Zhong, W., Hu, P. F., Deng, X., Tan, Y. X., Zhang, J. P., Ning, B. F., Shi, J., Zhang, X., Wang, H. Y., Lin, Y., and Xie, W. F. (2010) Hepatocyte nuclear factor 4a attenuates hepatic fibrosis in rats. Gut 59, 236-246
7. Wang, K., and Holterman, A. X. (2012) Pathophysiologic role of hepatocyte nuclear factor 6. Cell. Signal. 24, 9-16
8. Vanhorenbeeck, V., Jenny, M., Cornut, J. F., Gradwohl, G., Lemaigre, F. P., Rousseau, G. G., and Jacquemin, P. (2007) Role of the Onecut transcription factors in pancreas morphogenesis and in pancreatic and enteric endocrine differentiation.. Dev. Biol. 305, 685-694
9. Clotman, F., Lannoy, V. J., Reber, M., Cereghini, S., Cassiman, D., Jacquemin, P., Roskams, T., Rousseau, G. G., and Lemaigre, F. P. (2002) The onecut transcription factor HNF6 is required for normal development of the biliary tract. Development 129, 1819-1828
10. Holterman, A. X., Tan, Y., Kim, W., Yoo, K. W., and Costa, R. H. (2002) Diminished hepatic expression of the HNF-6 transcription factor during bile duct obstruction. Hepatology 35, 1392-1399
11. Tan, Y., Yoshida, Y., Hughes, D. E., and Costa, R. H. (2006) Increased expression of hepatocyte nuclear factor 6 stimulates hepatocyte proliferation during mouse liver regeneration.. Gastroenterology 130, 1283-1300
12. Lehner, F., Kulik, U., Klempnauer, J., and Borlak, J. (2007) The hepatocyte nuclear factor 6 (HNF6) and FOXA2 are key regulators in colorectal liver metastases.. FASEBJ. 21, 1445-1462
13. Samadani, U., and Costa, R. H. (1996) The transcriptional activator hepatocyte nuclear factor 6 regulates liver gene expression. Mol. Cell Biol. 16, 6273-6284
14. Rausa, F. M., Tan, Y., and Costa, R. H. (2003) Association between hepatocyte nuclear factor 6 (HNF-6) and FoxA2 DNA binding domains stimulates FOXA2 transcriptional activity but inhibits HNF-6 DNA binding.. Mol. Cell Biol. 23, 437-449
15. Clotman, F., Jacquemin, P., Plumb-Rudewiez, N, Pierreux, C. E., Van Der Smissen, P., Dietz, H. C, Courtoy, P. J., Rousseau, G. G., and Lemaigre, F. P. (2005) Control of liver cell fate decision by a gradient of TGF/3 signaling modulated by Onecut transcription factors.. Genes Dev. 19, 1849-1854
16. Gould Rothberg, B. E., and Bracken, M. B. (2006) E-cadherin immunohistochemical expression as a prognostic factor in infiltrating ductal carcinoma of the breast: a systematic review and meta-analysis.. Breast Cancer Res. Treat. 100, 139-148
17. Jiang, X., Zhang, W., Kayed, H., Zheng, P., Giese, N. A., Friess, H., and Kleeff, J. (2008) Loss of ONECUT1 expression in human pancreatic cancer cells. Oncol. Rep. 19, 157-163
18. Levine, A. J. (1997) p53, the cellular gatekeeper for growth and division. Cell 88, 323-331
19. Wade, M., Li, Y. C, and Wahl, G. M. (2013) MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat. Rev. Cancer 13, 83-96
20. Teodoro, J. G., Parker, A. E., Zhu, X., and Green, M. R. (2006) p53-mediated inhibition of angiogenesis through up-regulation of a collagen prolyl hydroxylase. Science 313, 968-971
21. Kim, T., Veronese, A., Pichiorri, F., Lee, T. J., Jeon, Y. J., Volinia, S., Pineau, P., Marchio, A., Palatini, J., Suh, S. S., Alder, H., Liu, C. G., Dejean, A., and Croce, C. M. (2011) p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J. Exp. Med. 208, 875-883
22. Chang, C. J., Chao, C. H., Xia, W., Yang, J. Y., Xiong, Y., Li, C. W., Yu, W. H., Rehman, S. K., Hsu, J. L., Lee, H. H., Liu, M., Chen, C. T., Yu, D., and Hung, M. C. (2011) p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs.. Nat. Cell Biol. 13, 317-323
23. Dong, P., Karaayvaz, M., Jia, N, Kaneuchi, M., Hamada, J., Watari, H, Sudo, S., Ju, J., and Sakuragi, N (2013) Mutant p53 gain-of-function induces epithelial-mesenchymal transition through modulation of the miR-130b-ZEB1 axis.. Oncogene 32, 3286-3295
24. Zhang, K. H., Tian, H. Y., Gao, X., Lei, W. W., Hu, Y., Wang, D. M., Pan, X. C, Yu, M. L., Xu, G. J., Zhao, F. K., and Song, J. G. (2009) Ferritin heavy chain-mediated iron homeostasis and subsequent increased reactive oxygen species production are essential for epithelial-mesenchymal transition.. Cancer Res. 69, 5340-5348
25. Tiscornia, G., Singer, O., and Verma, I. M. (2006) Production and purification of lentiviral vectors. Nat. Protoc. 1, 241-245
26. Prudkin, L., Liu, D. D., Ozburn, N. C, Sun, M., Behrens, C, Tang, X., Brown, K. C, Bekele, B. N, Moran, C, and Wistuba, I. I. (2009) Epithelialto-mesenchymal transition in the development and progression of adenocarcinoma and squamous cell carcinoma of the lung.. Mod. Pathol. 22, 668-678
27. Shi, J., Wang, D. M., Wang, C. M., Hu, Y., Liu, A. H, Zhang, Y. L., Sun, B., and Song, J. G. (2009) Insulin receptor substrate-1 suppresses transforming growth factor-beta1-mediated epithelial-mesenchymal transition.. Cancer Res. 69, 7180-7187
28. Kim, N. H, Kim, H. S., Li, X. Y., Lee, I., Choi, H. S., Kang, S. E., Cha, S. Y., Ryu, J. K., Yoon, D., Fearon, E. R., Rowe, R. G., Lee, S., Maher, C. A., Weiss, S. J., and Yook, J. I. (2011) A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J. Cell Biol. 195, 417-433
29. Rosenau, J., Bahr, M. J., Von Wasielewski, R., Mengel, M., Schmidt, H. H, Nashan, B., Lang, H., Klempnauer, J., Manns, M. P., and Boeker, K. H. (2002) Ki67, E-cadherin, and p53 as prognostic indicators of long-term outcome after liver transplantation for metastatic neuroendocrine tumors.. Transplantation 73, 386-394
30. Lannoy, V. J., Bürglin, T. R., Rousseau, G. G., and Lemaigre, F. P. (1998) Isoforms of hepatocyte nuclear factor-6 differ in DNA-binding properties, contain a bifunctional homeodomain, and define the new ONECUT class of homeodomain proteins. J. Biol. Chem. 273, 13552-13562
31. Peinado, H, Olmeda, D., and Cano, A. (2007) Snail, Zeb andbHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer 7, 415-428
32. Harris, S. L., and Levine, A. J. (2005) The p53 pathway: positive and negative feedback loops. Oncogene 24, 2899-2908
33. Vousden, K. H., and Lane, D. P. (2007) p53 in health and disease. Nat. Rev. Mol. Cell Biol. 8, 275-283
34. Marión, R. M., Strati, K., Li, H., Murga, M., Blanco, R., Ortega, S., Fernandez-Capetillo, O., Serrano, M., and Blasco, M. A. (2009) A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460, 1149-1153
35. Takenaka, C, Nishishita, N, Takada, N, Jakt, L. M., and Kawamata, S. (2010) Effective generation of iPS cells from CD34+ cord blood cells by inhibition of p53. Exp. Hematol. 38, 154-162
36. Schubert, J., and Brabletz, T. (2011) p53 Spreads out further: suppression of EMT and stemness by activating miR-200c expression. Cell Res. 21, 705-707