Loss of the SxxSS motif in a human T-cell factor-4 isoform confers hypoxia resistance to liver cancer: An oncogenic switch in Wnt signaling

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Koga, Hironori ^a   Tsedensodnom, Orkhontuya ^a   Tomimaru, Yoshito ^a   Walker, Evan J ^a   Lee, Han Chu ^b   Kim, Kang Mo ^b   Yano, Hirohisa ^c   Wands, Jack R ^a   Kim, Miran ^a  

^a Liver Research Center Brown University Medical School   (United States)

^b University of Ulsan College of Medicine   (South Korea)

^c KURUME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOPROTEIN; MESSENGER RNA; SXXSS PROTEIN; T CELL FACTOR 4 PROTEIN; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL AGGREGATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HUMAN; HYPOXIA; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIVER; LIVER CANCER; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN MOTIF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WNT SIGNALING PATHWAY; XENOGRAFT;

ADULT; AGED; AMINO ACID MOTIFS; ANIMALS; ASIAN CONTINENTAL ANCESTRY GROUP; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS; MALE; MICE; MIDDLE AGED; ONCOGENES; PROTEIN ISOFORMS; PROTEIN STABILITY; REPUBLIC OF KOREA; RNA, MESSENGER; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN; WNT SIGNALING PATHWAY; YOUNG ADULT;

MUS MUSCULUS;

EID: 84863093416     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039981     Document Type: Article

References (45)

1. Reya T, Clevers H, (2005) Wnt signalling in stem cells and cancer. Nature 434: 843-850.
2. Clevers H, (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
3. Ying Y, Tao Q, (2009) Epigenetic disruption of the WNT/beta-catenin signaling pathway in human cancers. Epigenetics 4: 307-312.
4. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, et al. (1998) Identification of c-MYC as a target of the APC pathway. Science 281: 1509-1512.
5. Tetsu O, McCormick F, (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426.
6. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, et al. (2009) EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 136: 1012-1024.
7. El-Serag HB, Rudolph KL, (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132: 2557-2576.
8. Merle P, de la Monte S, Kim M, Herrmann M, Tanaka S, et al. (2004) Functional consequences of frizzled-7 receptor overexpression in human hepatocellular carcinoma. Gastroenterology 127: 1110-1122.
9. Kim M, Lee HC, Tsedensodnom O, Hartley R, Lim YS, et al. (2008) Functional interaction between Wnt3 and Frizzled-7 leads to activation of the Wnt/beta-catenin signaling pathway in hepatocellular carcinoma cells. J Hepatol 48: 780-791.
10. Bengochea A, de Souza MM, Lefrancois L, Le Roux E, Galy O, et al. (2008) Common dysregulation of Wnt/Frizzled receptor elements in human hepatocellular carcinoma. Br J Cancer 99: 143-150.
11. Duval A, Rolland S, Tubacher E, Bui H, Thomas G, et al. (2000) The human T-cell transcription factor-4 gene: structure, extensive characterization of alternative splicings, and mutational analysis in colorectal cancer cell lines. Cancer Res 60: 3872-3879.
12. Pukrop T, Gradl D, Henningfeld KA, Knochel W, Wedlich D, et al. (2001) Identification of two regulatory elements within the high mobility group box transcription factor XTCF-4. J Biol Chem 276: 8968-8978.
13. Tsedensodnom O, Koga H, Rosenberg SA, Nambotin SB, Carroll JJ, et al. (2011) Identification of T-cell factor-4 isoforms that contribute to the malignant phenotype of hepatocellular carcinoma cells. Exp Cell Res 317: 920-931.
14. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
15. Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A, (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7: 150-161.
16. Kaidi A, Williams AC, Paraskeva C, (2007) Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat Cell Biol 9: 210-217.
17. Choi H, Chun YS, Kim TY, Park JW, (2010) HIF-2alpha enhances beta-catenin/TCF-driven transcription by interacting with beta-catenin. Cancer Res 70: 10101-10111.
18. Franovic A, Gunaratnam L, Smith K, Robert I, Patten D, et al. (2007) Translational up-regulation of the EGFR by tumor hypoxia provides a nonmutational explanation for its overexpression in human cancer. Proc Natl Acad Sci U S A 104: 13092-13097.
19. Nakamura K, Zen Y, Sato Y, Kozaka K, Matsui O, et al. (2007) Vascular endothelial growth factor, its receptor Flk-1, and hypoxia inducible factor-1alpha are involved in malignant transformation in dysplastic nodules of the liver. Hum Pathol 38: 1532-1546.
20. Knowles BB, Howe CC, Aden DP, (1980) Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science 209: 497-499.
21. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J, (1982) Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42: 3858-3863.
22. Graham FL, Smiley J, Russell WC, Nairn R, (1977) Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 36: 59-74.
23. He L, Isselbacher KJ, Wands JR, Goodman HM, Shih C, et al. (1984) Establishment and characterization of a new human hepatocellular carcinoma cell line. In Vitro 20: 493-504.
24. Yano H, Iemura A, Fukuda K, Mizoguchi A, Haramaki M, et al. (1993) Establishment of two distinct human hepatocellular carcinoma cell lines from a single nodule showing clonal dedifferentiation of cancer cells. Hepatology 18: 320-327.
25. Wang GL, Semenza GL, (1993) General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci U S A 90: 4304-4308.
26. Maeyama M, Koga H, Selvendiran K, Yanagimoto C, Hanada S, et al. (2008) Switching in discoid domain receptor expressions in SLUG-induced epithelial-mesenchymal transition. Cancer 113: 2823-2831.
27. Hecht A, Stemmler MP, (2003) Identification of a promoter-specific transcriptional activation domain at the C terminus of the Wnt effector protein T-cell factor 4. J Biol Chem 278: 3776-3785.
28. Kojiro M, (2004) 'Nodule-in-nodule' appearance in hepatocellular carcinoma: its significance as a morphologic marker of dedifferentiation. Intervirology 47: 179-183.
29. Brown JM, Wilson WR, (2004) Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer 4: 437-447.
30. Franovic A, Holterman CE, Payette J, Lee S, (2009) Human cancers converge at the HIF-2alpha oncogenic axis. Proc Natl Acad Sci U S A 106: 21306-21311.
31. Semenza GL, (2010) Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29: 625-634.
32. Liebner S, Cattelino A, Gallini R, Rudini N, Iurlaro M, et al. (2004) Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J Cell Biol 166: 359-367.
33. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
34. Yang XR, Xu Y, Shi GM, Fan J, Zhou J, et al. (2008) Cytokeratin 10 and cytokeratin 19: predictive markers for poor prognosis in hepatocellular carcinoma patients after curative resection. Clin Cancer Res 14: 3850-3859.
35. Borovski T, De Sousa EMF, Vermeulen L, Medema JP, (2011) Cancer stem cell niche: the place to be. Cancer Res 71: 634-639.
36. Heddleston JM, Li Z, Lathia JD, Bao S, Hjelmeland AB, et al. (2010) Hypoxia inducible factors in cancer stem cells. Br J Cancer 102: 789-795.
37. Li Z, Bao S, Wu Q, Wang H, Eyler C, et al. (2009) Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15: 501-513.
38. Yoneda N, Sato Y, Kitao A, Ikeda H, Sawada-Kitamura S, et al. (2011) Epidermal growth factor induces cytokeratin 19 expression accompanied by increased growth abilities in human hepatocellular carcinoma. Lab Invest 91: 262-272.
39. Satoh S, Daigo Y, Furukawa Y, Kato T, Miwa N, et al. (2000) AXIN1 mutations in hepatocellular carcinomas, and growth suppression in cancer cells by virus-mediated transfer of AXIN1. Nat Genet 24: 245-250.
40. Segditsas S, Tomlinson I, (2006) Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 25: 7531-7537.
41. Deng Y, Yu B, Cheng Q, Jin J, You H, et al. (2011) Epigenetic silencing of WTF-1 in hepatocellular carcinomas. J Cancer Res Clin Oncol 136: 1161-1167.
42. Weise A, Bruser K, Elfert S, Wallmen B, Wittel Y, et al. (2010) Alternative splicing of Tcf7l2 transcripts generates protein variants with differential promoter-binding and transcriptional activation properties at Wnt/beta-catenin targets. Nucleic Acids Res 38: 1964-1981.
43. Kaelin WG Jr, Ratcliffe PJ, (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30: 393-402.
44. Gordan JD, Bertout JA, Hu CJ, Diehl JA, Simon MC, (2007) HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 11: 335-347.
45. Patel SA, Simon MC, (2008) Biology of hypoxia-inducible factor-2alpha in development and disease. Cell Death Differ 15: 628-634.