Lack of nrf2 results in progression of proliferative lesions to neoplasms induced by long-term exposure to non-genotoxic hepatocarcinogens involving oxidative stress

Experimental and Toxicologic Pathology

Volumn 66, Issue 1, 2014, Pages 19-26

  Tasaki, Masako ^a   Kuroiwa, Yuichi ^a   Inoue, Tomoki ^a   Hibi, Daisuke ^a   Matsushita, Kohei ^a   Kijima, Aki ^a   Maruyama, Soichi ^b   Nishikawa, Akiyoshi ^a   Umemura, Takashi ^a  

^a NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^b NIHON UNIVERSITY   (Japan)

Author keywords

Cholangiofibrosis; Nrf2 Deficient mice; Pentachlorophenol; Piperonyl butoxide; Regenerative hepatocellular hyperplasia

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; DIETHYLNITROSAMINE; DNA; PENTACHLOROPHENOL; PIPERONYL BUTOXIDE; TRANSCRIPTION FACTOR NRF2;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILE DUCT CARCINOMA; BILE DUCT DISEASE; BODY WEIGHT; CHOLANGIOFIBROSIS; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOSE RESPONSE; EXPOSURE; GENE; GENE FUNCTION; GENOTOXICITY; GENOTYPE; HEPATOCELLULAR ADENOMA; INCIDENCE; LIVER CANCER; LIVER CARCINOGENESIS; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; NRF2 GENE; OXIDATIVE STRESS; REGENERATIVE HEPATOCELLULAR HYPERPLASIA; SHORT TERM EXPOSURE; SURVIVAL RATE; TOXICITY TESTING; WEIGHT GAIN;

MUS;

CHOLANGIOFIBROSIS; NRF2-DEFICIENT MICE; PENTACHLOROPHENOL; PIPERONYL BUTOXIDE; REGENERATIVE HEPATOCELLULAR HYPERPLASIA;

ANIMALS; CARCINOGENS; CARCINOMA, HEPATOCELLULAR; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; LIVER NEOPLASMS; MALE; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PRECANCEROUS CONDITIONS;

EID: 84888821265     PISSN: 09402993     EISSN: 16181433     Source Type: Journal    
DOI: 10.1016/j.etp.2013.07.003     Document Type: Article

References (51)

1. Baird L., Dinkova-Kostova A.T. The cytoprotective role of the Keap1-Nrf2 pathway. Archives of Toxicology 2011, 85:241-272.
2. 1 mice. Toxicity Report Series 2011, 82:1-111.
3. Buitrago-Molina L.E., Marhenke S., Longerich T., Sharma A.D., Boukouris A.E., Geffers R., et al. The degree of liver injury determines the role of p21 in liver regeneration and hepatocarcinogenesis. Hepatology 2013, [in press].
4. Bustos M., Sangro B., Alzuguren P., Gil A.G., Ruiz J., Beraza N., et al. Liver damage using suicide genes. A model for oval cell activation. American Journal of Pathology 2000, 157:549-559.
5. Byard J., Needham D. Metabolism and excretion of piperonyl butoxide in the rat. Xenobiotica 2006, 36:1259-1272.
6. Deferme L., Briede J.J., Claessen S.M., Jennen D.G., Cavill R., Kleinjans J.C. Time series analysis of oxidative stress response patterns in HepG2: a toxicogenomics approach. Toxicology 2013, 306 C:24-34.
7. DeNicola G.M., Karreth F.A., Humpton T.J., Gopinathan A., Wei C., Frese K., et al. Oncogenic-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011, 475:106-109.
8. Enomoto A., Itoh K., Nagayoshi E., Haruta J., Kimura T., O'Connor T., et al. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicological Sciences 2001, 59:169-177.
9. Gushima M., Hirahashi M., Matsumoto T., Fujita K., Fujisawa R., Mizumoto K., et al. Altered expression of MUTYH and an increase in 8-hydroxydeoxyguanosine are early events in ulcerative colitis-associated carcinogenesis. Journal of Pathology 2009, 219:77-86.
10. Hartikainen J.M., Tengstrom M., Kosma V.M., Kinnula V.L., Mannermaa A., Soini Y. Genetic polymorphisms and protein expression of NRF2 and sulfiredoxin predict survival outcomes in breast cancer. Cancer Research 2012, 72:5537-5546.
11. Hata M., Iida H., Yamanegi K., Yamada N., Ohyama H., Hirano H., et al. Phenotypic characteristics and proliferative activity of hyperplastic ductile cells in cholangiofibrosis induced by thioacetamide in rats. Experimental and Toxicologic Pathology 2013, 65:351-356.
12. Hickling K.C., Hitchcock J.M., Chipman J.K., Hammond T.G., Evans J.G. Induction of progression of cholangiofibrosis in rat liver injured by oral administration of furan. Toxicologic Pathology 2010, 38:213-229.
13. Hickling K.C., Hitchcock J.M., Oreffo V., Mally A., Hammond T.G., Evans J.G., et al. Evidence of oxidative stress and associated DNA damage, increased proliferative drive, and altered gene expression in rat liver produced by the cholangiocarcinogenic agent furan. Toxicologic Pathology 2010, 38:230-243.
14. Hu X., Roberts J.R., Apopa P.L., Kan Y.W., Ma Q. Accelerated ovarian failure induced by 4-vinyl cyclohexane diepoxide in nrf2 null mice. Molecular and Cellular Biology 2006, 26:940-954.
15. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzymes genes through antioxidant response elements. Biochemical and Biophysical Research Communications 1997, 236:313-322.
16. Jansson K., Jansson V. Induction of mutation in V79 hamsters cells by tetrachrolohydroquinone, a metabolite of pentachlorophenol. Mutation Research 1991, 260:313-322.
17. Jansson K., Jansson V. Induction of micronuclei in V79 hamsters cells by tetrachrolohydroquinone, a metabolite of pentachlorophenol. Mutation Research 1992, 279:205-208.
18. Jin M., Suzuki Y., Hibi D., Inoue T., Ishii Y., Nohmi T., et al. Comprehensive toxicity study of safrole using a medium-term animal model with gpt delta rats. Toxicology 2011, 290:312-321.
19. Kamakura N., Yamamoto J., Brooks P.J., Iwai S., Kuraoka I. Effects of 5',8-cyclodeoxyadenosine triphosphates on DNA synthesis. Chemical Research in Toxicology 2012, 25:2718-2724.
20. Kansanen E., Jyrkkanen H.K., Levonen A.L. Activation of stress signaling pathways by electrophilic oxidized and nitrated lipids. Free Radical Biology and Medicine 2012, 52:973-982.
21. Kawai M., Saegusa Y., Jin M., Dewa Y., Nishimura J., Harada T., et al. Mechanistic study of hepatocarcinogenesis of piperonyl butoxide in mice. Toxicologic Pathology 2009, 37:761-769.
22. Kitamura Y., Umemura T., Kanki K., Kodama Y., Kitamoto S., Saito K., et al. Increased susceptibility to hepatocarcinogenicity of Nrf2-deficient mice exposed to 2-amino-3-methylimidazo[4,5-f]quinolone. Cancer Science 2007, 98:19-24.
23. Klaunigh J.E., Kameddulis L.M. The role of oxidative stress in carcinogenesis. Annual Review of Pharmacology and Toxicology 2004, 44:239-267.
24. Koturbash I., Melnyk S., James S.J., Beland F.A., Pogribny I.P. Role of epigenetic and miR-22 and miR-29b alterations in the downregulation of Mat1a and Mthfr genes in early preneoplastic livers in rats induced by 2-acetylaminofluorene. Molecular Carcinogenesis 2013, 52:318-327.
25. Lee J.C., Son Y.O., Pratheeshkumar P., Shi X. Oxidative stress and metal carcinogenesis. Free Radical Biology & Medicine 2012, 53:742-757.
26. Li H., Wood J., Whitten K., Vadival S., Seng S., Makriyannis A., et al. Inhibition of fatty acid amide hydrolase activates NRF2 signaling and induces heme oxygenase 1 transcription in breast cancer cells. British Journal of Pharmacology 2013, [in press].
27. 1 mice. Fundamental and Applied Toxicology 1991, 17:519-532.
28. Malhotra D., Portales-Casamar E., Singh A., Srivastava S., Arenillas D., Happel C., et al. Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through ChiP-Seq profiling and network analysis. Nucleic Acids Research 2010, 38:5718-5734.
29. Marczak E.D., Marzec J., Zeldin D.C., Kleeberger S.R., Brown N.J., Pretorius M., et al. Pharmacogenetics and Genomics 2012, 22:620-628.
30. Maronpot R.R., Giles H.D., Dykes D.J., Irwin R.D. Furan-induced hepatic cholangiocarcinomas in Fischer 344 rats. Toxicologic Pathology 1991, 19:561-570.
31. Muguruma M., Nishimura J., Jin M., Kashida Y., Moto M., Takahashi M., et al. Molecular pathological analysis for determining the possible mechanism of piperonyl butoxide-induced hepatocarcinogenesis in mice. Toxicology 2006, 228:178-187.
32. Nilov D.I., Komarov D.Y., Panov M.S., Karabaeva K.E., Mereshchenko A.S., Tarnovsky A.N., et al. Oxidation of adenosine and inosine: the chemistry of 8-oxo-7,8-dihydropurines, purine iminoquinones, and purine quinones as observed by ultrafast spectroscopy. Journal of the American Chemical Society 2013, 135:3423-3438.
33. Oshima H., Matsunaga A., Fujimura T., Tsukamoto T., Taketo M.M., Oshima M. Carcinogenesis in mouse stomach by simultaneous activation of the Wnt signaling and prostaglandin E2 pathway. Gastroenterology 2006, 131:1086-1095.
34. Ooi A., Dykema K., Ansari A., Petillo D., Snider J., Kahnoski R., et al. CUL3 and NRF2 mutations confer an NRF2 activation phenotype in a sporadic form of papillary renal cell carcinoma. Cancer Research 2013, 73:2044-2051.
35. Ramos-Gomez M., Kwak M.-K., Dolan P.M., Itoh K., Yamamoto M., Talalay P., et al. Sensitivity to carcinogenesis is increased and chemopreventive efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:3410-3415.
36. Ramos-Gomez M., Dolan P.M., Itoh K., Yamamoto M., Kensler T.W. Interactive effects of nrf2 genotype and oltipraz on benzo[a]pyrene-DNA adducts and tumor yield in mice. Carcinogenesis 2003, 24:461-467.
37. Satou K., Kasai H., Masutani C., Hanaoka F., Harashima H., Kamiya H. 2-Hydroxy-2'-deoxyadenosine 5'-triphosphate enhances AT-GC mutations caused by 8-hydroxy-2'-deoxyguanosine 5'-triphosphate by suppressing its degradation upon replication in a Hela extract. Biochemistry 2007, 46:6639-6646.
38. Singh B., Ronghe A.M., Chatterjee A., Bhat N.K., Bhat H.K. MicroRNA-93 regulates NRF2 expression and is associated with breast carcinogenesis. Carcinogenesis 2013, [in press].
39. Slocum S.L., Kensler T.W. Nrf2: control of sensitivity to carcinogens. Archives of Toxicology 2011, 85:273-284.
40. Shelton P., Jaiswal A.K. The transcription factor NF-E2-related factor 2 (Nrf2): a protooncogene?. FASEB Journal 2013, 27:414-423.
41. Takahashi O., Oishi S., Fujitani T., Tanaka T., Yoneyama M. Chronic toxicity studies of piperonyl butoxide in CD-1 mice: induction of hepatocellular carcinoma. Toxicology 1997, 124:95-103.
42. Tasaki M., Umemura T., Suzuki Y., Hibi D., Inoue T., Okamura T., et al. Oxidative DNA damage and reporter gene mutation in the livers of gpt delta rats given non-genotoxic hepatocarcinogens with cytochrome P450-inducible potency. Cancer Science 2010, 101:2525-2530.
43. Tasaki M., Kuroiwa Y., Inoue T., Hibi D., Matsushita K., Ishii Y., et al. Oxidative DNA damage and in vivo mutagenicity caused by reactive oxygen species generated in the livers of p53-proficient or deficient gpt delta mice treated with non-genotoxic hepatocarcinogens. Journal of Applied Toxicology 2013, [in press].
44. Thoolen B., Maranpot R.R., Harada T., Nyska A., Rousseaux C., Nolte T., et al. Proliferative and nonproliferative lesions of the rat and mouse hepatobiliary system. Toxicologic Pathology 2010, 38:55-81.
45. Toyokuni S. Novel aspects of oxidative stress-associated carcinogenesis. Antioxidants and Redox Signalling 2006, 8:1373-1377.
46. Tsai C.-H., Lin P.-H., Waidyanatha S., Rappaport S.M. Characterization of metabolic activation of pentachlorophenol to quinones and semiquinones in rodent liver. Chemico-Biological Interactions 2001, 134:55-71.
47. 1 mice exposed to pentachlorophenol in their diet. Fundamental and Applied Toxicology 1996, 30:285-289.
48. 1 mice possibly due to oxidative stress. Toxicologic Pathology 2003, 31:10-13.
49. Umemura T., Kuroiwa Y., Kitamura Y., Ishii Y., Kanki K., Kodama Y., et al. A crucial role of Nrf2 in in vivo defense against oxidative damage by an environmental pollutant, pentachlorophenol. Toxicological Sciences 2006, 90:111-119.
50. Umemura T., Tasaki M., Kijima A., Okamura T., Inoue T., Ishii Y., et al. Possible participation of oxidative stress in causation of cell proliferation and in vivo mutagenicity in kidneys of gpt delta rats treated with potassium bromate. Toxicology 2009, 257:46-52.
51. Wang Y.-J., Lee C.-C., Chang W.-C., Liou H.-B., Ho Y.-S. Oxidative stress and liver toxicity in rats and human hepatoma cell line induced by pentachlorophenol and its major metabolite tetrachlorohydroquinone. Toxicology Letters 2001, 122:157-169.