A double-negative feedback loop between Wnt-β-catenin signaling and HNF4α regulates epithelial-mesenchymal transition in hepatocellular carcinoma

Journal of Cell Science

Volumn 126, Issue 24, 2013, Pages 5692-5703

  Yang, Meng ^a   Li, Sheng Nan ^a   Anjum, Khalid M ^a   Gui, Long Xin ^a   Zhu, Shan Shan ^a   Liu, Jun ^a   Chen, Jia Kun ^a   Liu, Qing Feng ^a   Ye, Guo Dong ^a   Wang, Wen Jie ^a   Wu, Jia Fa ^a   Cai, Wang Yu ^a   Sun, Guang Bin ^a   Liu, Yun Jia ^a   Liu, Rong Fu ^b   Zhang, Zhi Ming ^b   Li, Bo An ^a  

^a School of Public Health School of Life Science   (China)

^b THE FIRST AFFILIATED HOSPITAL OF XIAMEN UNIVERSITY   (China)

Author keywords

Epithelial mesenchymal transition; Hepatocellular carcinoma; HNF4 ; Wnt catenin signaling

Indexed keywords

BETA CATENIN; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTE NUCLEAR FACTOR 4 ALPHA; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WNT SIGNALING PATHWAY;

EPITHELIAL-MESENCHYMAL TRANSITION; HEPATOCELLULAR CARCINOMA; HNF4Α; WNT-Β-CATENIN SIGNALING;

ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA CATENIN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HEPATOCYTE NUCLEAR FACTOR 4; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; PROTEIN BINDING; RATS; RATS, WISTAR; TRANSCRIPTION FACTORS; WNT SIGNALING PATHWAY;

EID: 84890499677     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.135053     Document Type: Article

References (50)

1. Bonzo, J. A., Ferry, C. H., Matsubara, T., Kim, J. H. and Gonzalez, F. J. (2012). Suppression of hepatocyte proliferation by hepatocyte nuclear factor 4a in adult mice. J. Biol. Chem. 287, 7345-7356.
2. Bruix, J., Boix, L., Sala, M. and Llovet, J. M. (2004). Focus on hepatocellular carcinoma. Cancer Cell 5, 215-219.
3. Cattin, A. L., Le Beyec, J., Barreau, F., Saint-Just, S., Houllier, A., Gonzalez, F. J., Robine, S., Pinçon-Raymond, M., Cardot, P., Lacasa, M. et al. (2009). Hepatocyte nuclear factor 4alpha, a key factor for homeostasis, cell architecture, and barrier function of the adult intestinal epithelium. Mol. Cell. Biol. 29, 6294-6308.
4. Cereghini, S. (1996). Liver-enriched transcription factors and hepatocyte differentiation. FASEB J. 10, 267-282.
5. Chaffer, C. L., Brennan, J. P., Slavin, J. L., Blick, T., Thompson, E. W. and Williams, E. D. (2006). Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res. 66, 11271- 11278.
6. Chen, X., Halberg, R. B., Burch, R. P. and Dove, W. F. (2008). Intestinal adenomagenesis involves core molecular signatures of the epithelial-mesenchymal transition. J. Mol. Histol. 39, 283-294.
7. Chung, M. T., Lai, H. C., Sytwu, H. K., Yan, M. D., Shih, Y. L., Chang, C. C., Yu, M. H., Liu, H. S., Chu, D. W. and Lin, Y. W. (2009). SFRP1 and SFRP2 suppress the transformation and invasion abilities of cervical cancer cells through Wnt signal pathway. Gynecol. Oncol. 112, 646-653.
8. Cicchini, C., Filippini, D., Coen, S., Marchetti, A., Cavallari, C., Laudadio, I., Spagnoli, F. M., Alonzi, T. and Tripodi, M. (2006). Snail controls differentiation of hepatocytes by repressing HNF4alpha expression. J. Cell. Physiol. 209, 230-238.
9. Colletti, M., Cicchini, C., Conigliaro, A., Santangelo, L., Alonzi, T., Pasquini, E., Tripodi, M. and Amicone, L. (2009). Convergence of Wnt signaling on the HNF4alpha-driven transcription in controlling liver zonation. Gastroenterology 137, 660-672.
10. Daniels, D. L. and Weis, W. I. (2005). Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat. Struct. Mol. Biol. 12, 364-371.
11. DiMeo, T. A., Anderson, K., Phadke, P., Fan, C., Perou, C. M., Naber, S. and Kuperwasser, C. (2009). A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 69, 5364-5373.
12. El-Serag, H. B. and Rudolph, K. L. (2007). Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132, 2557-2576.
13. Guo, Y., Zi, X., Koontz, Z., Kim, A., Xie, J., Gorlick, R., Holcombe, R. F. and Hoang, B. H. (2007). Blocking Wnt/LRP5 signaling by a soluble receptor modulates the epithelial to mesenchymal transition and suppresses met and metalloproteinases in osteosarcoma Saos-2 cells. J. Orthop. Res. 25, 964-971.
14. Hanse, E. A., Mashek, D. G., Becker, J. R., Solmonson, A. D., Mullany, L. K., Mashek, M. T., Towle, H. C., Chau, A. T. and Albrecht, J. H. (2012). Cyclin D1 inhibits hepatic lipogenesis via repression of carbohydrate response element binding protein and hepatocyte nuclear factor 4a. Cell Cycle 11, 2681-2690.
15. Hayhurst, G. P., Lee, Y. H., Lambert, G., Ward, J. M. and Gonzalez, F. J. (2001). Hepatocyte nuclear factor 4alpha (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell. Biol. 21, 1393-1403.
16. Howe, L. R., Watanabe, O., Leonard, J. and Brown, A. M. (2003). Twist is upregulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res. 63, 1906-1913.
17. Huber, M. A., Kraut, N. and Beug, H. (2005). Molecular requirements for epithelialmesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 17, 548-558.
18. Jiang, Y. G., Luo, Y., He, D. L., Li, X., Zhang, L. L., Peng, T., Li, M. C. and Lin, Y. H. (2007). Role of Wnt/beta-catenin signaling pathway in epithelial-mesenchymal transition of human prostate cancer induced by hypoxia-inducible factor-1alpha. Int. J. Urol. 14, 1034-1039.
19. Krieghoff, E., Behrens, J. and Mayr, B. (2006). Nucleo-cytoplasmic distribution of beta-catenin is regulated by retention. J. Cell Sci. 119, 1453-1463.
20. Lazarevich, N. L. and Fleishman, D. I. (2008). Tissue-specific transcription factors in progression of epithelial tumors. Biochemistry (Mosc) 73, 573-591.
21. Lazarevich, N. L., Shavochkina, D. A., Fleishman, D. I., Kustova, I. F., Morozova, O. V., Chuchuev, E. S. and Patyutko, Y. I. (2010). Deregulation of hepatocyte nuclear factor 4 (HNF4) as a marker of epithelial tumors progression. Exp. Oncol. 32, 167-171.
22. Li, J., Ning, G. and Duncan, S. A. (2000). Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev. 14, 464-474.
23. Liotta, L. A. (1985). Mechanisms of cancer invasion and metastasis. Important Adv. Oncol. 1985, 28-41.
24. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X. and He, X. (2002). Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837-847.
25. Lustig, B. and Behrens, J. (2003). The Wnt signaling pathway and its role in tumor development. J. Cancer Res. Clin. Oncol. 129, 199-221.
26. MacDonald, B. T., Semenov, M. V. and He, X. (2007). SnapShot: Wnt/beta-catenin signaling. Cell 131, 1204.e1-1204.e2.
27. Moon, R. T. and Miller, J. R. (1997). The APC tumor suppressor protein in development and cancer. Trends Genet. 13, 256-258.
28. Naiki, T., Nagaki, M., Shidoji, Y., Kojima, H., Imose, M., Kato, T., Ohishi, N., Yagi, K. and Moriwaki, H. (2002). Analysis of gene expression profile induced by hepatocyte nuclear factor 4alpha in hepatoma cells using an oligonucleotide microarray. J. Biol. Chem. 277, 14011-14019.
29. Nieto, M. A. (2011). The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu. Rev. Cell Dev. Biol. 27, 347-376.
30. Ning, B. F., Ding, J., Yin, C., Zhong, W., Wu, K., Zeng, X., Yang, W., Chen, Y. X., Zhang, J. P., Zhang, X. et al. (2010). Hepatocyte nuclear factor 4 alpha suppresses the development of hepatocellular carcinoma. Cancer Res. 70, 7640-7651.
31. Parviz, F., Matullo, C., Garrison, W. D., Savatski, L., Adamson, J. W., Ning, G., Kaestner, K. H., Rossi, J. M., Zaret, K. S. and Duncan, S. A. (2003). Hepatocyte nuclear factor 4alpha controls the development of a hepatic epithelium and liver morphogenesis. Nat. Genet. 34, 292-296.
32. Polakis, P. (2000). Wnt signaling and cancer. Genes Dev. 14, 1837-1851.
33. Portolani, N., Coniglio, A., Ghidoni, S., Giovanelli, M., Benetti, A., Tiberio, G. A. and Giulini, S. M. (2006). Early and late recurrence after liver resection for hepatocellular carcinoma: prognostic and therapeutic implications. Ann. Surg. 243, 229-235.
34. Ruse, M. D., Jr, Privalsky, M. L. and Sladek, F. M. (2002). Competitive cofactor recruitment by orphan receptor hepatocyte nuclear factor 4alpha1: modulation by the F domain. Mol. Cell. Biol. 22, 1626-1638.
35. Sakai, D., Tanaka, Y., Endo, Y., Osumi, N., Okamoto, H. and Wakamatsu, Y. (2005). Regulation of Slug transcription in embryonic ectoderm by beta-catenin- Lef/Tcf and BMP-Smad signaling. Dev. Growth Differ. 47, 471-482.
36. Sekiya, T. and Zaret, K. S. (2007). Repression by Groucho/TLE/Grg proteins: genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Mol. Cell 28, 291-303.
37. Sladek, F. M., Zhong, W. M., Lai, E. and Darnell, J. E., Jr (1990). Liver-enriched transcription factor HNF-4 is a novel member of the steroid hormone receptor superfamily. Genes Dev. 4 12B, 2353-2365.
38. Späth, G. F. and Weiss, M. C. (1998). Hepatocyte nuclear factor 4 provokes expression of epithelial marker genes, acting as a morphogen in dedifferentiated hepatoma cells. J. Cell Biol. 140, 935-946.
39. Stracke, M. L. and Liotta, L. A. (1992). Multi-step cascade of tumor cell metastasis. In Vivo 6, 309-316.
40. Takeichi, M. (1995). Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627.
41. Tanaka, T., Jiang, S., Hotta, H., Takano, K., Iwanari, H., Sumi, K., Daigo, K., Ohashi, R., Sugai, M., Ikegame, C. et al. (2006). Dysregulated expression of P1 and P2 promoter-driven hepatocyte nuclear factor-4alpha in the pathogenesis of human cancer. J. Pathol. 208, 662-672.
42. Thiery, J. P. (2002). Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2, 442-454.
43. Thiery, J. P., Acloque, H., Huang, R. Y. and Nieto, M. A. (2009). Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890.
44. Thompson, M. D. and Monga, S. P. (2007). WNT/beta-catenin signaling in liver health and disease. Hepatology 45, 1298-1305.
45. Ungaro, P., Teperino, R., Mirra, P., Longo, M., Ciccarelli, M., Raciti, G. A., Nigro, C., Miele, C., Formisano, P. and Beguinot, F. (2010). Hepatocyte nuclear factor (HNF)-4alpha-driven epigenetic silencing of the human PED gene. Diabetologia 53, 1482-1492.
46. Walesky, C., Edwards, G., Borude, P., Gunewardena, S., O'Neil, M., Yoo, B. and Apte, U. (2013). Hepatocyte nuclear factor 4 alpha deletion promotes diethylnitrosamineinduced hepatocellular carcinoma in rodents. Hepatology 57, 2480-2490.
47. Wodarz, A. and Nusse, R. (1998). Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14, 59-88.
48. Yang, J. and Weinberg, R. A. (2008). Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829.
49. Yin, C., Lin, Y., Zhang, X., Chen, Y. X., Zeng, X., Yue, H. Y., Hou, J. L., Deng, X., Zhang, J. P., Han, Z. G. et al. (2008). Differentiation therapy of hepatocellular carcinoma in mice with recombinant adenovirus carrying hepatocyte nuclear factor- 4alpha gene. Hepatology 48, 1528-1539.
50. Yook, J. I., Li, X. Y., Ota, I., Hu, C., Kim, H. S., Kim, N. H., Cha, S. Y., Ryu, J. K., Choi, Y. J., Kim, J. et al. (2006). A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat. Cell Biol. 8, 1398-1406.