Hypoxia activates Wnt/β-catenin signaling by regulating the expression of BCL9 in human hepatocellular carcinoma

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Xu, Wei ^a   Zhou, Wang ^a   Cheng, Mo ^a   Wang, Jing ^a,c   Liu, Zhian ^c   He, Shaohui ^a   Luo, Xiangji ^d   Huang, Wending ^b   Chen, Tianrui ^a   Yan, Wangjun ^a,b   Xiao, Jianru ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^c XUZHOU MEDICAL UNIVERSITY   (China)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BCL9 PROTEIN, HUMAN; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; TUMOR PROTEIN;

ADULT; ANIMAL; BONE TUMOR; CELL HYPOXIA; CELL MOTION; CELL PROLIFERATION; DNA RESPONSIVE ELEMENT; FEMALE; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; HEP-G2 CELL LINE; HUMAN; LIVER CELL CARCINOMA; LIVER TUMOR; MALE; METABOLISM; MIDDLE AGED; NEOVASCULARIZATION (PATHOLOGY); NUCLEOTIDE SEQUENCE; NUDE MOUSE; PATHOLOGY; PROMOTER REGION; SECONDARY; TRANSCRIPTION INITIATION; WNT SIGNALING;

ADULT; ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BONE NEOPLASMS; CARCINOMA, HEPATOCELLULAR; CELL HYPOXIA; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC ENGINEERING; HEP G2 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS; MALE; MICE, NUDE; MIDDLE AGED; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; PROMOTER REGIONS, GENETIC; RESPONSE ELEMENTS; TRANSCRIPTION ACTIVATOR-LIKE EFFECTOR NUCLEASES; TRANSCRIPTIONAL ACTIVATION; WNT SIGNALING PATHWAY;

EID: 85009160067     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep40446     Document Type: Article

References (49)

1. El-Serag, H. B., & Rudolph, K. L. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132(7), 2557-2576 (2007
2. Miyoshi, Y., et al. Activation of the beta-catenin gene in primary hepatocellular carcinomas by somatic alterations involving exon 3. Cancer Res 58(12), 2524-2527 (1998
3. Wands, J. R., & Kim, M. WNT/beta-catenin signaling and hepatocellular carcinoma. Hepatology 60(2), 452-454 (2014
4. Clevers, H. Wnt/beta-catenin signaling in development and disease. Cell 127(3), 469-480 (2006
5. Klaus, A., & Birchmeier, W.: Wnt signalling and its impact on development and cancer. Nat Rev Cancer 8(5), 387-398 (2008
6. He, T. C., et al. Identification of c-MYC as a target of the APC pathway. Science 281(5382), 1509-1512 (1998
7. Tetsu, O., & McCormick, F.: Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398(6726), 422-426 (1999
8. Kramps, T., et al. Wnt/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex. Cell 109(1), 47-60 (2002
9. Townsley, F. M., Cliffe, A., & Bienz, M.: Pygopus and Legless target Armadillo/beta-catenin to the nucleus to enable its transcriptional co-Activator function. Nat Cell Biol 6(7), 626-633 (2004
10. Sustmann C., Flach, H., Ebert, H., Eastman, Q., & Grosschedl, R.: Cell-Type-specific function of BCL9 involves a transcriptional activation domain that synergizes with beta-catenin. Mol Cell Biol 28(10), 3526-3537 (2008
11. De la Roche, M., Worm, J., & Bienz, M.: The function of BCL9 in Wnt/beta-catenin signaling and colorectal cancer cells. BMC Cancer 8, 199 (2008
12. Mani, M., et al. BCL9 promotes tumor progression by conferring enhanced proliferative, metastatic, and angiogenic properties to cancer cells. Cancer Res 69(19), 7577-7586 (2009
13. Hyeon, J., Ahn, S., Lee, J. J., Song, D. H., & Park, C. K. Prognostic Significance of BCL9 Expression in Hepatocellular Carcinoma. Korean J Pathol 47(2), 130-6 (2013
14. Takada, K., et al. Targeted disruption of the BCL9/beta-catenin complex inhibits oncogenic Wnt signaling. Sci Transl Med 4(148), 148ra117 (2012
15. Zhao, J. J., et al. miR-30-5p functions as a tumor suppressor and novel therapeutic tool by targeting the oncogenic Wnt/beta-catenin/BCL9 pathway. Cancer Res 74(6), 1801-1813 (2014
16. Harris, A. L. Hypoxia-A key regulatory factor in tumour growth. Nat Rev Cancer 2(1), 38-47 (2002
17. Menrad, H., et al. Roles of hypoxia-inducible factor-1alpha (HIF-1alpha) versus HIF-2alpha in the survival of hepatocellular tumor spheroids. Hepatology 51(6), 2183-2192 (2010
18. Sun, H. X., et al. Hypoxia inducible factor 2 alpha inhibits hepatocellular carcinoma growth through the transcription factor dimerization partner 3/ E2F transcription factor 1-dependent apoptotic pathway. Hepatology 57(3), 1088-1097 (2013
19. Keith, B., Johnson, R. S., & Simon, M. C. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 12(1), 9-22 (2012
20. Mazumdar, J., et al. HIF-2alpha deletion promotes Kras-driven lung tumor development. Proc Natl Acad Sci USA 107(32), 14182-14187 (2010
21. Semenza, G. L. HIF-1 and mechanisms of hypoxia sensing. Curr Opin Cell Biol 13(2), 167-71 (2001
22. Rankin, E. B., & Giaccia, A. J. The role of hypoxia-inducible factors in tumorigenesis. Cell Death Differ 15(4), 678-685 (2008
23. Skuli, N., & Simon, M. C. HIF-1alpha versus HIF-2alpha in endothelial cells and vascular functions: is there a master in angiogenesis regulation. Cell Cycle 8(20), 3252-3253 (2009
24. Skuli, N., et al. Endothelial deletion of hypoxia-inducible factor-2alpha (HIF-2alpha) alters vascular function and tumor angiogenesis. Blood 114(2), 469-477 (2009
25. Bogaerts, E., Heindryckx, F., Vandewynckel, Y. P., Van Grunsven, L. A., & Van Vlierberghe, H. The roles of transforming growth factor-β , Wnt, Notch and hypoxia on liver progenitor cells in primary liver tumours. Int J Oncol 44(4), 1015-1022 (2014
26. Zhang, Q., et al. Wnt/beta-catenin signaling enhances hypoxia-induced epithelial-mesenchymal transition in hepatocellular carcinoma via crosstalk with hif-1alpha signaling. Carcinogenesis 34(5), 962-973 (2013
27. Giles, R. H., et al. Interplay between VHL/HIF1alpha and Wnt/beta-catenin pathways during colorectal tumorigenesis. Oncogene 25(21), 3065-3070 (2006
28. Wu, M. Z., et al. Hypoxia Drives Breast Tumor Malignancy through a TET-TNFalpha-p38-MAPK Signaling Axis. Cancer Res 75(18), 3912-3924 (2015
29. Hu, C. J., Wang, L. Y., Chodosh, L. A., Keith, B., & Simon, M. C. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 23(24), 9361-9374 (2003
30. Covello, K. L., et al. HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 20(5), 557-570 (2006
31. Edmondson, H. A., & Steiner, P. E. Primary carcinoma of the liver: a study of 100 cases among 48, 900 necropsies. Cancer 7(3), 462-503 (1954
32. Tetreault, M. P., Weinblatt, D., Shaverdashvili, K., Yang, Y., & Katz, J. P. KLF4 transcriptionally activates non-canonical WNT5A to control epithelial stratification. Sci Rep 6, 26130 (2016
33. Lee, S. H., et al. Identification of a novel role of ZMIZ2 protein in regulating the activity of the Wnt/β -catenin signaling pathway. J Biol Chem 288(50), 35913-35924 (2013
34. Zhang, T., et al. Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res 61(24), 8664-8667 (2001
35. Huang, S. M., et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461, 614-620 (2009
36. Jia, W., Eneh, J. O., Ratnaparkhe, S., Altman, M. K., & Murph, M. M. MicroRNA-30c-2 expressed in ovarian cancer cells suppresses growth factor-induced cellular proliferation and downregulates the oncogene BCL9. Mol Cancer Res 9(12), 1732-1745 (2011
37. Wu, L., et al. HIF-2alpha mediates hypoxia-induced LIF expression in human colorectal cancer cells. Oncotarget 6(6), 4406-4417 (2015
38. Cuninghame, S., Jackson, R., & Zehbe, I. Hypoxia-inducible factor 1 and its role in viral carcinogenesis. Virology 456-457, 370-383 (2014
39. Dang, C. V. Links between metabolism and cancer. Genes Dev 26(9), 877-890 (2012
40. Loboda, A., Jozkowicz, A., & Dulak, J. HIF-1 versus HIF-2-is one more important than the other. Vascul Pharmacol 56(5-6), 245-251 (2012
41. Hu, C. J., Sataur, A., Wang, L., Chen, H., & Simon, M. C. The N-Terminal transactivation domain confers target gene specificity of hypoxia-inducible factors HIF-1alpha and HIF-2alpha. Mol Biol Cell 18(11), 4528-4542 (2007
42. Masoud, G. N., & Li, W. HIF-1alpha pathway: role, regulation and intervention for cancer therapy. Acta Pharm Sin B 5(5), 378-389 (2015
43. Bishop, T., & Ratcliffe, P. J. HIF hydroxylase pathways in cardiovascular physiology and medicine. Circ Res 117(1), 65-79 (2015
44. Ema, M., et al. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA 94(9), 4273-4278 (1997
45. Yoo, Y. G., Christensen, J., & Huang, L. E. HIF-1alpha confers aggressive malignant traits on human tumor cells independent of its canonical transcriptional function. Cancer Res 71(4), 1244-1252 (2011
46. Vaupel, P., & Mayer, A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 26(2), 225-239 (2007
47. Wu, X. Z., Xie, G. R., & Chen, D. Hypoxia and hepatocellular carcinoma: The therapeutic target for hepatocellular carcinoma. J Gastroenterol Hepatol 22(8), 1178-1182 (2007
48. Bengochea, A., et al. Common dysregulation of Wnt/Frizzled receptor elements in human hepatocellular carcinoma. Br J Cancer 99(1), 143-150 (2008
49. Mazumdar, J., et al. O2 regulates stem cells through Wnt/beta-catenin signalling. Nat Cell Biol 12(10), 1007-1013 (2010