Wnt/β-catenin signaling enhances hypoxia-induced epithelial-mesenchymal transition in hepatocellular carcinoma via crosstalk with hif-1α signaling

Carcinogenesis

Volumn 34, Issue 5, 2013, Pages 962-973

  Zhang, Qi ^a   Bai, Xueli ^a   Chen, Wei ^a   Ma, Tao ^a   Hu, Qida ^a   Liang, Chao ^a   Xie, Shangzhi ^a   Chen, Conglin ^a   Hu, Liqiang ^a   Xu, Shiguo ^a   Liang, Tingbo ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIN D1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MYC PROTEIN; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR TWIST; UVOMORULIN; VIMENTIN; WNT PROTEIN; WNT3A PROTEIN;

ARTICLE; CELL CYCLE ARREST; CELL HYPOXIA; CELL PROLIFERATION; CELL VIABILITY; COMPLEX FORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR CELL;

BETA CATENIN; CADHERINS; CARCINOMA, HEPATOCELLULAR; CELL CYCLE CHECKPOINTS; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; EPITHELIAL-MESENCHYMAL TRANSITION; HEP G2 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN; TRANSCRIPTION, GENETIC; VIMENTIN; WNT3A PROTEIN;

EID: 84877157115     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgt027     Document Type: Article

References (51)

1. Kalluri,R. et al. (2009) The basics of epithelial-mesenchymal transition. J. Clin. Invest., 119, 1420-1428.
2. Weinberg,R.A. (2008) Mechanisms of malignant progression. Carcinogenesis, 29, 1092-1095.
3. Michael Zeisberg,E.G.N. (2009) Biomarkers for epithelial-mesenchymal transitions. J. Clin. Invest., 119, 1429-1437.
4. Singh,A. et al. (2010) EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene, 29, 4741-4751.
5. Wilson,W.R. et al. (2011) Targeting hypoxia in cancer therapy. Nat. Rev. Cancer, 11, 393-410.
6. Vaupel,P. (2004) The role of hypoxia-induced factors in tumor progression. Oncologist, 9 (suppl. 5), 10-17.
7. Moen,I. et al. (2009) Hyperoxic treatment induces mesenchymal-to-epithelial transition in a rat adenocarcinoma model. PLoS ONE, 4, e6381.
8. Lu,X. et al. (2010) Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin. Cancer Res., 16, 5928-5935.
9. Martin,A. et al. (2010) Tumorigenesis: Twist1 links EMT to self-renewal. Nat. Cell Biol., 12, 924-925.
10. Sahlgren,C. et al. (2008) Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc. Natl Acad. Sci. USA, 105, 6392-6397.
11. Liu,L. et al. (2010) Activation of beta-catenin by hypoxia in hepatocellular carcinoma contributes to enhanced metastatic potential and poor prognosis. Clin. Cancer Res., 16, 2740-2750.
12. Haase,V.H. (2009) Oxygen regulates epithelial-to-mesenchymal transition: insights into molecular mechanisms and relevance to disease. Kidney Int., 76, 492-499.
13. MacDonald,B.T. et al. (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell, 17, 9-26.
14. Reya,T. et al. (2005) Wnt signalling in stem cells and cancer. Nature, 434, 843-850.
15. Fatima,S. et al. (2011) Dickkopfs and Wnt/β-catenin signalling in liver cancer. World J. Clin. Oncol., 2, 31-325.
16. Calvisi,D.F. et al. (2004) Activation of beta-catenin provides proliferative and invasive advantages in c-myc/TGF-alpha hepatocarcinogenesis promoted by phenobarbital. Carcinogenesis, 25, 901-908.
17. Trevisani,F. et al. (2008) Recent advances in the natural history of hepatocellular carcinoma. Carcinogenesis, 29, 1299-1305.
18. Sanchez-Tillo,E. et al. (2011) β-catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness. Proc. Natl Acad. Sci. USA, 108, 19204-19209.
19. Schmalhofer,O. et al. (2009) E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev., 28, 151-166.
20. Wincewicz,A. et al. (2010) Comparison of beta-catenin with TGF-beta1, HIF-1alpha and patients' disease-free survival in human colorectal cancer. Pathol. Oncol. Res., 16, 31-318.
21. Lim,J.H. et al. (2008) Hypoxia-inducible factor-1alpha obstructs a Wnt signaling pathway by inhibiting the hARD1-mediated activation of betacatenin. Cancer Res., 68, 5177-5184.
22. Verras,M. et al. (2008) Tumor hypoxia blocks Wnt processing and secretion through the induction of endoplasmic reticulum stress. Mol. Cell. Biol., 28, 7212-7224.
23. Wang,D. et al. (2011) Hypoxia-induced β-catenin downregulation involves p53-dependent activation of Siah-1. Cancer Sci., 102, 1322-1328.
24. Kaidi,A. et al. (2007) Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat. Cell Biol., 9, 210-217.
25. Zhao,J.H. et al. (2011) Knockdown of β-Catenin through shRNA cause a reversal of EMT and metastatic phenotypes induced by HIF-1α. Cancer Invest., 29, 377-382.
26. Zhu,X.D. et al. (2008) High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J. Clin. Oncol., 26, 2707-2716.
27. Jiao,M. et al. (2012) Activation of PI3 kinase/Akt/HIF-1α pathway contributes to hypoxia-induced epithelial-mesenchymal transition and chemoresistance in hepatocellular carcinoma. Int. J. Oncol., 40, 461-468.
28. Lester,R.D. et al. (2007) uPAR induces epithelial-mesenchymal transition in hypoxic breast cancer cells. J. Cell Biol., 178, 425-436.
29. Wu,M.Z. et al. (2011) Interplay between HDAC3 and WDR5 is essential for hypoxia-induced epithelial-mesenchymal transition. Mol. Cell, 43, 811-822.
30. Zhou,J. et al. (2011) Transcriptional up-regulation of RhoE by hypoxiainducible factor (HIF)-1 promotes epithelial to mesenchymal transition of gastric cancer cells during hypoxia. Biochem. Biophys. Res. Commun., 415, 348-354.
31. Zhou,G. et al. (2009) Hypoxia-induced alveolar epithelial-mesenchymal transition requires mitochondrial ROS and hypoxia-inducible factor 1. Am. J. Physiol. Lung Cell Mol. Physiol., 297, L1120-L1130.
32. Cannito,S. et al. (2008) Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells. Carcinogenesis, 29, 2267-2278.
33. Jiang,Y.G. et al. (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.
34. Lundgren,K. et al. (2009) Hypoxia, Snail and incomplete epithelial-mesenchymal transition in breast cancer. Br. J. Cancer, 101, 1769-1781.
35. Carmeliet,P. et al. (1998) Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature, 394, 485-490.
36. Yang,M.H. et al. (2008) Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol., 10, 295-305.
37. Luo,D. et al. (2011) Mouse snail is a target gene for HIF. Mol. Cancer Res., 9, 234-245.
38. Thiery,J.P. et al. (2009) Epithelial-mesenchymal transitions in development and disease. Cell, 139, 871-890.
39. Choi,S.S. et al. (2009) Epithelial-to-mesenchymal transitions in the liver. Hepatology, 50, 2007-2013.
40. Jou,J. et al. (2010) Epithelial-mesenchymal transitions and hepatocarcinogenesis. J. Clin. Invest., 120, 1031-1034.
41. Yan,W. et al. (2009) PI3 kinase/Akt signaling mediates epithelial-mesenchymal transition in hypoxic hepatocellular carcinoma cells. Biochem. Biophys. Res. Commun., 382, 631-636.
42. Li,J. et al. (2011) Activation of β-catenin and Akt pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC Cancer, 11, 49.
43. Ameri,K. et al. (2004) Anoxic induction of ATF-4 through HIF-1-independent pathways of protein stabilization in human cancer cells. Blood, 103, 1876-1882.
44. Mizukami,Y. et al. (2007) Hypoxia inducible factor-1 independent pathways in tumor angiogenesis. Clin. Cancer Res., 13, 5670-5674.
45. Giles,R.H. et al. (2006) Interplay between VHL/HIF1alpha and Wnt/ beta-catenin pathways during colorectal tumorigenesis. Oncogene, 25, 3065-3070.
46. Vakkila,J. et al. (2004) Inflammation and necrosis promote tumour growth. Nat. Rev. Immunol., 4, 641-648.
47. Klaus,A. et al. (2008) Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer, 8, 387-398.
48. Zhang,Y. et al. (2012) Regulation of cell cycle progression by forkhead transcription factor FOXO3 through its binding partner DNA replication factor Cdt1. Proc. Natl Acad. Sci. USA, 109, 5717-5722.
49. Semenza,G.L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer, 3, 721-732.
50. Wang,R. et al. (2011) Cancer therapeutic agents targeting hypoxia-inducible factor-1. Curr. Med. Chem., 18, 3168-3189.
51. Lepourcelet,M. et al. (2004) Small-molecule antagonists of the oncogenic Tcf/beta-catenin protein complex. Cancer Cell, 5, 91-102