Characterization of a cell culture model for clinically aggressive hepatocellular carcinoma induced by chronic hypoxia

Cancer Letters

Volumn 315, Issue 2, 2012, Pages 178-188

  van Malenstein, Hannah ^a   Verslype, Chris ^a   Windmolders, Petra ^a   van Eijsden, Rudy ^b   Nevens, Frederik ^a   van Pelt, Jos ^a  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Hepatocellular carcinoma; Hypoxia; Pathway analysis

Indexed keywords

CYTOCHROME P450; GLUTATHIONE TRANSFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA1;

ADAPTATION; ARTICLE; CELL CULTURE; CELL MOTILITY; CONTROLLED STUDY; DETOXIFICATION; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; LIVER CARCINOMA; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION;

ANOXIA; CARCINOMA, HEPATOCELLULAR; CELL CULTURE TECHNIQUES; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MICROARRAY ANALYSIS; MODELS, BIOLOGICAL; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84355162845     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.09.039     Document Type: Article

References (41)

1. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics, 2002. CA Cancer J. Clin. 2005, 55:74-108.
2. Adler M., De Pauw F., Vereerstraeten P., Fancello A., Lerut J., Starkel P., et al. Outcome of patients with hepatocellular carcinoma listed for liver transplantation within the Eurotransplant allocation system. Liver Transplant. 2008, 14:526-533.
3. Yeh S.H., Chen P.J., Shau W.Y., Chen Y.W., Lee P.H., Chen J.T., et al. Chromosomal allelic imbalance evolving from liver cirrhosis to hepatocellular carcinoma. Gastroenterology 2001, 121:699-709.
4. Chen X., Cheung S.T., So S., Fan S.T., Barry C., Higgins J., et al. Gene expression patterns in human liver cancers. Mol. Biol. Cell 2002, 13:1929-1939.
5. Gort E.H., Groot A.J., van der Wall E., van Diest P.J., Vooijs M.A. Hypoxic regulation of metastasis via hypoxia-inducible factors. Curr. Mol. Med. 2008, 8:60-67.
6. Brown J.M., Giaccia A.J. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 1998, 58:1408-1416.
7. Kim K.R., Moon H.E., Kim K.W. Hypoxia-induced angiogenesis in human hepatocellular carcinoma. J. Mol. Med. 2002, 80:703-714.
8. Brahimi-Horn M.C., Chiche J., Pouyssegur J. Hypoxia and cancer. J. Mol. Med. 2007, 85:1301-1307.
9. Folkman J., Hahnfeldt P., Hlatky L. Cancer: looking outside the genome. Nat. Rev. Mol. Cell. Biol. 2000, 1:76-79.
10. Brown J.M., Wilson W.R. Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 2004, 4:437-447.
11. Semela D., Dufour J.F. Angiogenesis and hepatocellular carcinoma. J. Hepatol. 2004, 41:864-880.
12. van Malenstein H., Gevaert O., Libbrecht L., Daemen A., Allemeersch J., Nevens F., et al. A seven-gene set associated with chronic hypoxia of prognostic importance in hepatocellular carcinoma. Clin. Cancer Res. 2010, 16:4278-4288.
13. R. DevelopmentCoreTeam, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, 2004.
14. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. Ser. B 1995, 57:289-300.
15. Detre S., Saclani Jotti G., Dowsett M. A " quickscore" method for immunohistochemical semiquantitation: validation for oestrogen receptor in breast carcinomas. J. Clin. Pathol. 1995, 48:876-878.
16. Salomonis N., Hanspers K., Zambon A.C., Vranizan K., Lawlor S.C., Dahlquist K.D., et al. GenMAPP 2: new features and resources for pathway analysis. BMC Bioinform. 2007, 8:217.
17. Jensen L.J., Kuhn M., Stark M., Chaffron S., Creevey C., Muller J., et al. STRING 8 - a global view on proteins and their functional interactions in 630 organisms. Nucl. Acids Res. 2009, 37:D412-6.
18. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2002, 2:442-454.
19. Zeisberg M., Neilson E.G. Biomarkers for epithelial-mesenchymal transitions. J. Clin. Invest. 2009, 119:1429-1437.
20. Wang K., Chen S., Xie W., Wan Y.J. Retinoids induce cytochrome P450 3A4 through RXR/VDR-mediated pathway. Biochem. Pharmacol. 2008, 75:2204-2213.
21. Song K.H., Li T., Owsley E., Strom S., Chiang J.Y. Bile acids activate fibroblast growth factor 19 signaling in human hepatocytes to inhibit cholesterol 7alpha-hydroxylase gene expression. Hepatology 2009, 49:297-305.
22. Yang J.D., Nakamura I., Roberts L.R. The tumor microenvironment in hepatocellular carcinoma: current status and therapeutic targets. Semin. Cancer Biol. 2010, 21:35-43.
23. Joyce J.A., Pollard J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 2009, 9:239-252.
24. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6:392-401.
25. Denko N.C. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat. Rev. Cancer 2008, 8:705-713.
26. Derynck R., Akhurst R.J., Balmain A., F-beta T.G. TGF-beta signaling in tumor suppression and cancer progression. Nat. Genet. 2001, 29:117-129.
27. Coulouarn C., Factor V.M., Thorgeirsson S.S. Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer. Hepatology 2008, 47:2059-2067.
28. Hoshida Y., Nijman S.M., Kobayashi M., Chan J.A., Brunet J.P., Chiang D.Y., et al. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma. Cancer Res. 2009, 69:7385-7392.
29. Tian M., Schiemann W.P. The TGF-beta paradox in human cancer: an update. Future Oncol. 2009, 5:259-271.
30. Lawrence D.A. Latent-TGF-beta: an overview. Mol. Cell. Biochem. 2001, 219:163-170.
31. Liu L., Zhu X.D., Wang W.Q., Shen Y., Qin Y., Ren Z.G., et al. Activation of beta-catenin by hypoxia in hepatocellular carcinoma contributes to enhanced metastatic potential and poor prognosis. Clin. Cancer Res. 2010, 16:2740-2750.
32. Peters J.M., Aoyama T., Cattley R.C., Nobumitsu U., Hashimoto T., Gonzalez F.J. Role of peroxisome proliferator-activated receptor alpha in altered cell cycle regulation in mouse liver. Carcinogenesis 1998, 19:1989-1994.
33. Desvergne B., Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocrinol. Rev. 1999, 20:649-688.
34. Rao M.S., Reddy J.K. Hepatocarcinogenesis of peroxisome proliferators. Ann. NY Acad. Sci. 1996, 804:573-587.
35. Roberts R.A., Soames A.R., Gill J.H., James N.H., Wheeldon E.B. Non-genotoxic hepatocarcinogens stimulate DNA synthesis and their withdrawal induces apoptosis, but in different hepatocyte populations. Carcinogenesis 1995, 16:1693-1698.
36. Zhao W., Iskandar S., Kooshki M., Sharpe J.G., Payne V., Robbins M.E. Knocking out peroxisome proliferator-activated receptor (PPAR) alpha inhibits radiation-induced apoptosis in the mouse kidney through activation of NF-kappaB and increased expression of IAPs. Radiat. Res. 2007, 167:581-591.
37. Morimura K., Cheung C., Ward J.M., Reddy J.K., Gonzalez F.J. Differential susceptibility of mice humanized for peroxisome proliferator-activated receptor alpha to Wy-14,643-induced liver tumorigenesis. Carcinogenesis 2006, 27:1074-1080.
38. Mangelsdorf D.J., Evans R.M. The RXR heterodimers and orphan receptors. Cell 1995, 83:841-850.
39. Shimizu M., Takai K., Moriwaki H. Strategy and mechanism for the prevention of hepatocellular carcinoma: phosphorylated retinoid X receptor alpha is a critical target for hepatocellular carcinoma chemoprevention. Cancer Sci. 2009, 100:369-374.
40. Matsushima-Nishiwaki R., Okuno M., Adachi S., Sano T., Akita K., Moriwaki H., et al. Phosphorylation of retinoid X receptor alpha at serine 260 impairs its metabolism and function in human hepatocellular carcinoma. Cancer Res. 2001, 61:7675-7682.
41. Bressac B., Galvin K.M., Liang T.J., Isselbacher K.J., Wands J.R., Ozturk M. Abnormal structure and expression of p53 gene in human hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 1990, 87:1973-1977.