Molecular mechanisms of fibrosis-associated promotion of liver carcinogenesis

Toxicological Sciences

Volumn 132, Issue 1, 2013, Pages 53-63

  Uehara, Takeki ^a,f   Ainslie, Garrett R ^a   Kutanzi, Kristi ^b   Pogribny, Igor P ^b   Muskhelishvili, Levan ^b   Izawa, Takeshi ^c   Yamate, Jyoji ^c   Kosyk, Oksana ^a   Shymonyak, Svitlana ^a   Bradford, Blair U ^a   Boorman, Gary A ^d   Bataller, Ramon ^e   Rusyn, Ivan ^a  

^a University of North Carolina at Chapel Hill   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^c Osaka Prefecture University   (Japan)

^d Covance Chantilly ^*  (United States)

^e IL   (United States)

^f SHIONOGI AND CO LTD   (Japan)

Author keywords

Cancer; Fibrosis; Genotoxic; Liver; Mechanisms

Indexed keywords

CARBON TETRACHLORIDE; DIETHYLNITROSAMINE; EPITHELIAL CELL ADHESION MOLECULE; PROTEIN P16;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FIBROGENESIS; GENOTOXICITY; HEPATITIS; LIVER; LIVER CARCINOGENESIS; LIVER FIBROSIS; LIVER TUMOR; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; SENESCENCE; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; CARBON TETRACHLORIDE; CELL TRANSFORMATION, NEOPLASTIC; DIETHYLNITROSAMINE; FEMALE; IMMUNOHISTOCHEMISTRY; LIVER CIRRHOSIS; LIVER NEOPLASMS, EXPERIMENTAL; MICE; PREGNANCY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ANIMALIA; MUS;

EID: 84876471980     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs342     Document Type: Article

References (53)

1. Alkofer, B., Lepennec, V., Chiche, L. (2011). Hepatocellular cancer in the non-cirrhotic liver. J. Visc. Surg. 148, 3-11.
2. Aoyama, T., Inokuchi, S., Brenner, D. A., Seki, E. (2010). CX3CL1-CX3CR1 interaction prevents carbon tetrachloride-induced liver inflammation and fibrosis in mice. Hepatology 52, 1390-1400.
3. Becker, F. F. (1983). Thioacetamide hepatocarcinogenesis. J. Natl. Cancer Inst. 71, 553-558.
4. Braeuning, A., Jaworski, M., Schwarz, M., Köhle, C. (2006). Rex3 (reduced in expression 3) as a new tumor marker in mouse hepatocarcinogenesis. Toxicology 227, 127-135.
5. Bucher, J. R. (1998). Update on national toxicology program (NTP) assays with genetically altered or "transgenic" mice. Environ. Health Perspect. 106, 619-621.
6. Cabré, M., Camps, J., Paternáin, J. L., Ferré, N., Joven, J. (2000). Timecourse of changes in hepatic lipid peroxidation and glutathione metabolism in rats with carbon tetrachloride-induced cirrhosis. Clin. Exp. Pharmacol. Physiol. 27, 694-699.
7. Center, M. M., Jemal, A. (2011). International trends in liver cancer incidence rates. Cancer Epidemiol. Biomarkers Prev. 20, 2362-2368.
8. Chazal, M., Marionnet, C., Michel, L., Mollier, K., Dazard, J. E., Della Valle, V., Larsen, C. J., Gras, M. P., Basset-Séguin, N. (2002). P16(INK4A) is implicated in both the immediate and adaptative response of human keratinocytes to UVB irradiation. Oncogene 21, 2652-2661.
9. Della Corte, C., Colombo, M. (2012). Surveillance for hepatocellular carcinoma. Semin. Oncol. 39, 384-398.
10. Dragani, T. A., Manenti, G., Della Porta, G. (1986). Enhancing effects of carbon tetrachloride in mouse hepatocarcinogenesis. Cancer Lett. 31, 171-179.
11. Druckrey, H., Steinhoff, D., Preussmann, R., Ivankovic, S. (1964). [Induction of cancer by a single dose of methylnitroso-urea and various dialkylnitrosamines in rats]. Z. Krebsforsch. 66, 1-10.
12. Eastmond, D. A. (2008). Evaluating genotoxicity data to identify a mode of action and its application in estimating cancer risk at low doses: A case study involving carbon tetrachloride. Environ. Mol. Mutagen. 49, 132-141.
13. El-Serag, H. B., Rudolph, K. L. (2007). Hepatocellular carcinoma: Epidemiology and molecular carcinogenesis. Gastroenterology 132, 2557-2576.
14. Farazi, P. A., DePinho, R. A. (2006). Hepatocellular carcinoma pathogenesis: From genes to environment. Nat. Rev. Cancer 6, 674-687.
15. Fausto, N., Campbell, J. S. (2010). Mouse models of hepatocellular carcinoma. Semin. Liver Dis. 30, 87-98.
16. Fujii, T., Fuchs, B. C., Yamada, S., Lauwers, G. Y., Kulu, Y., Goodwin, J. M., Lanuti, M., Tanabe, K. K. (2010). Mouse model of carbon tetrachloride induced liver fibrosis: Histopathological changes and expression of CD133 and epidermal growth factor. BMC Gastroenterol. 10, 79.
17. Graveel, C. R., Jatkoe, T., Madore, S. J., Holt, A. L., Farnham, P. J. (2001). Expression profiling and identification of novel genes in hepatocellular carcinomas. Oncogene 20, 2704-2712.
18. Greenbaum, L. E., Wells, R. G. (2011). The role of stem cells in liver repair and fibrosis. Int. J. Biochem. Cell Biol. 43, 222-229.
19. Guzman, G., Chennuri, R., Voros, A., Boumendjel, R., Locante, A., Patel, R., Valyi-Nagy, T. (2011). Nucleometric study of anisonucleosis, diabetes and oxidative damage in liver biopsies of orthotopic liver transplant recipients with chronic hepatitis C virus infection. Pathol. Oncol. Res. 17, 191-199.
20. Hanahan, D., Weinberg, R. A. (2011). Hallmarks of cancer: The next generation. Cell 144, 646-674.
21. Heindryckx, F., Colle, I., Van Vlierberghe, H. (2009). Experimental mouse models for hepatocellular carcinoma research. Int. J. Exp. Pathol. 90, 367-386.
22. Hoenerhoff, M. J., Pandiri, A. R., Lahousse, S. A., Hong, H. H., Ton, T. V., Masinde, T., Auerbach, S. S., Gerrish, K., Bushel, P. R., Shockley, K. R., et al. (2011). Global gene profiling of spontaneous hepatocellular carcinoma in B6C3F1 mice: Similarities in the molecular landscape with human liver cancer. Toxicol. Pathol. 39, 678-699.
23. Huff, J., Cirvello, J., Haseman, J., Bucher, J. (1991). Chemicals associated with site-specific neoplasia in 1394 long-term carcinogenesis experiments in laboratory rodents. Environ. Health Perspect. 93, 247-270.
24. Inokuchi, S., Aoyama, T., Miura, K., Osterreicher, C. H., Kodama, Y., Miyai, K., Akira, S., Brenner, D. A., Seki, E. (2010). Disruption of TAK1 in hepatocytes causes hepatic injury, inflammation, fibrosis, and carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 107, 844-849.
25. Jacobson-Kram, D. (2010). Cancer risk assessment approaches at the FDA/ CDER: Is the era of the 2-year bioassay drawing to a close? Toxicol. Pathol. 38, 169-170.
26. Jepsen, P., Vilstrup, H., Tarone, R. E., Friis, S., Sørensen, H. T. (2007). Incidence rates of hepatocellular carcinoma in the U.S. and Denmark: Recent trends. Int. J. Cancer 121, 1624-1626.
27. Ji, J., Wang, X. W. (2012). Clinical implications of cancer stem cell biology in hepatocellular carcinoma. Semin. Oncol. 39, 461-472.
28. Katoonizadeh, A., Nevens, F., Verslype, C., Pirenne, J., Roskams, T. (2006). Liver regeneration in acute severe liver impairment: A clinicopathological correlation study. Liver Int. 26, 1225-1233.
29. Kossatz, U., Breuhahn, K., Wolf, B., Hardtke-Wolenski, M., Wilkens, L., Steinemann, D., Singer, S., Brass, F., Kubicka, S., Schlegelberger, B., et al. (2010). The cyclin E regulator cullin 3 prevents mouse hepatic progenitor cells from becoming tumor-initiating cells. J. Clin. Invest. 120, 3820-3833.
30. Krishnamurthy, J., Torrice, C., Ramsey, M. R., Kovalev, G. I., Al-Regaiey, K., Su, L., Sharpless, N. E. (2004). Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 114, 1299-1307.
31. Lee, J. S., Chu, I. S., Mikaelyan, A., Calvisi, D. F., Heo, J., Reddy, J. K., Thorgeirsson, S. S. (2004). Application of comparative functional genomics to identify best-fit mouse models to study human cancer. Nat. Genet. 36, 1306-1311.
32. Lee, T. K., Cheung, V. C., Ng, I. O. (2012). Liver tumor-initiating cells as a therapeutic target for hepatocellular carcinoma. Cancer Lett. (forthcoming).
33. Li, J., Poi, M. J., and Tsai, M. D. (2011). Regulatory mechanisms of tumor suppressor P16(INK4A) and their relevance to cancer. Biochemistry 50, 5566-5582.
34. Loeb, L. A. (2001). A mutator phenotype in cancer. Cancer Res. 61, 3230-3239.
35. Ma, S., Chan, K. W., Hu, L., Lee, T. K., Wo, J. Y., Ng, I. O., Zheng, B. J., Guan, X. Y. (2007). Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 132, 2542-2556.
36. Majumdar, A., Curley, S. A., Wu, X., Brown, P., Hwang, J. P., Shetty, K., Yao, Z. X., He, A. R., Li, S., Katz, L., et al. (2012). Hepatic stem cells and transforming growth factor β in hepatocellular carcinoma. Nat. Rev. Gastroenterol. Hepatol. 9, 530-538.
37. Marquardt, J. U., Thorgeirsson, S. S. (2010). Stem cells in hepatocarcinogenesis: Evidence from genomic data. Semin. Liver Dis. 30, 26-34.
38. Nagano, K., Sasaki, T., Umeda, Y., Nishizawa, T., Ikawa, N., Ohbayashi, H., Arito, H., Yamamoto, S., Fukushima, S. (2007). Inhalation carcinogenicity and chronic toxicity of carbon tetrachloride in rats and mice. Inhal. Toxicol. 19, 1089-1103.
39. Nault, J. C., Zucman-Rossi, J. (2011). Genetics of hepatobiliary carcinogenesis. Semin. Liver Dis. 31, 173-187.
40. Oh, J. Y., Jeong, J. S., Kim, Y. J., Nam, K. J., Park, B. H., Kwon, E. Y., Kim, Y. H., Hwang, T. H. (2002). Ultrasonographic evidence of phenotypic instability during hepatocarcinogenesis in N-nitrosomorpholine-treated rats. Exp. Mol. Pathol. 73, 67-73.
41. Oishi, N., Wang, X. W. (2011). Novel therapeutic strategies for targeting liver cancer stem cells. Int. J. Biol. Sci. 7, 517-535.
42. Pitot, H. C. (1977). The natural history of neoplasia. Newer insights into an old problem. Am. J. Pathol. 89, 402-411.
43. Powell, C. L., Kosyk, O., Ross, P. K., Schoonhoven, R., Boysen, G., Swenberg, J. A., Heinloth, A. N., Boorman, G. A., Cunningham, M. L., Paules, R. S., et al. (2006). Phenotypic anchoring of acetaminophen-induced oxidative stress with gene expression profiles in rat liver. Toxicol. Sci. 93, 213-222.
44. Rusyn, I., Asakura, S., Pachkowski, B., Bradford, B. U., Denissenko, M. F., Peters, J. M., Holland, S. M., Reddy, J. K., Cunningham, M. L., Swenberg, J. A. (2004). Expression of base excision DNA repair genes is a sensitive biomarker for in vivo detection of chemical-induced chronic oxidative stress: Identification of the molecular source of radicals responsible for DNA damage by peroxisome proliferators. Cancer Res. 64, 1050-1057.
45. Sancho-Bru, P., Altamirano, J., Rodrigo-Torres, D., Coll, M., Millán, C., José Lozano, J., Miquel, R., Arroyo, V., Caballería, J., Ginès, P., et al. (2012). Liver progenitor cell markers correlate with liver damage and predict short-term mortality in patients with alcoholic hepatitis. Hepatology 55, 1931-1941.
46. Seki, E., De Minicis, S., Gwak, G. Y., Kluwe, J., Inokuchi, S., Bursill, C. A., Llovet, J. M., Brenner, D. A., Schwabe, R. F. (2009). CCR1 and CCR5 promote hepatic fibrosis in mice. J. Clin. Invest. 119, 1858-1870.
47. Stowell, R. E., Lee, C. S., Tsuboi, K. K., Villasana, A. (1951). Histochemical and microchemical changes in experimental cirrhosis and hepatoma formation in mice by carbon tetrachloride. Cancer Res. 11, 345-354.
48. Vesselinovitch, S. D., Mihailovich, N. (1983). Kinetics of diethylnitrosamine hepatocarcinogenesis in the infant mouse. Cancer Res. 43, 4253-4259.
49. Vucur, M., Roderburg, C., Bettermann, K., Tacke, F., Heikenwalder, M., Trautwein, C., Luedde, T. (2010). Mouse models of hepatocarcinogenesis: What can we learn for the prevention of human hepatocellular carcinoma? Oncotarget 1, 373-378.
50. Wang, B., Jacob, S. T. (2011). Role of cancer stem cells in hepatocarcinogenesis. Genome Med. 3, 11.
51. Wells, M. Y., Williams, E. S. (2009). The transgenic mouse assay as an alternative test method for regulatory carcinogenicity studies-implications for REACH. Regul. Toxicol. Pharmacol. 53, 150-155.
52. Yamashita, T., Ji, J., Budhu, A., Forgues, M., Yang, W., Wang, H. Y., Jia, H., Ye, Q., Qin, L. X., Wauthier, E., et al. (2009). EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 136, 1012-1024.
53. Yang, S., Koteish, A., Lin, H., Huang, J., Roskams, T., Dawson, V., Diehl, A. M. (2004). Oval cells compensate for damage and replicative senescence of mature hepatocytes in mice with fatty liver disease. Hepatology 39, 403-411.