Long-term arsenic exposure induces histone H3 Lys9 dimethylation without altering DNA methylation in the promoter region of p16INK4a and down-regulates its expression in the liver of mice

Journal of Applied Toxicology

Volumn 33, Issue 9, 2013, Pages 951-958

  Suzuki, Takehiro ^a   Nohara, Keiko ^a  

^a NATIONAL INSTITUTE FOR ENVIRONMENTAL STUDIES   (Japan)

Author keywords

Arsenic; G9a; Histone H3K9 dimethylation; Liver; P16INK4a

Indexed keywords

ARSENIC; BISULFITE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYTOKERATIN 8; ESTROGEN RECEPTOR ALPHA; HISTONE H3; HISTONE METHYLTRANSFERASE; PROTEIN P16; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; DOWN REGULATION; GENE EXPRESSION; GENE TARGETING; HISTOLOGY; HISTONE METHYLATION; LIVER CARCINOGENESIS; LIVER WEIGHT; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; ONCOGENE H RAS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR GENE;

ARSENIC; G9A; HISTONE H3K9 DIMETHYLATION; LIVER; P16INK4A;

ANIMALS; ARSENIC; CARCINOGENESIS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA METHYLATION; DOWN-REGULATION; EPIGENESIS, GENETIC; ESTROGEN RECEPTOR ALPHA; GENES, RAS; GENETIC LOCI; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LIVER; MALE; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 84880701834     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.2765     Document Type: Article

References (39)

1. Bachman KE, Park BH, Rhee I, Rajagopalan H, Herman JG, Baylin SB, Kinzler KW, Vogelstein B. 2003. Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell 3: 89-95.
2. Brenner C, Fuks F. 2007. A methylation rendezvous: reader meets writers. Dev. Cell 12: 843-844.
3. Bursch W, Grasl-Kraupp B, Wastl U, Hufnagl K, Chabicovsky M, Taper H, Schulte-Hermann R. 2004. Role of apoptosis for mouse liver growth regulation and tumor promotion: comparative analysis of mice with high (C3H/He) and low (C57Bl/6J) cancer susceptibility. Toxicol. Lett. 149: 25-35.
4. Chen H, Li S, Liu J, Diwan BA, Barrett JC, Waalkes MP. 2004. Chronic inorganic arsenic exposure induces hepatic global and individual gene hypomethylation: implications for arsenic hepatocarcinogenesis. Carcinogenesis 25: 1779-1786.
5. INK4a and RASSF1A and induces lung cancer in A/J mice. Toxicol. Sci. 91: 372-381.
6. Dammann R, Li C, Yoon JH, Chin PL, Bates S, Pfeifer GP. 2000. Epigenetic inactivation of a RAS association domain family protein from the lung tumour suppressor locus 3p21.3. Nat. Genet. 25: 315-319.
7. Fang S, Miao J, Xiang L, Ponugoti B, Treuter E, Kemper JK. 2007. Coordinated recruitment of histone methyltransferase G9a and other chromatin-modifying enzymes in SHP-mediated regulation of hepatic bile acid metabolism. Mol. Cell. Biol. 27: 1407-1424.
8. Gil J, Peters G. 2006. Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat. Rev. Mol. Cell Biol. 7: 667-677.
9. Gopalakrishnan S, Van Emburgh BO, Robertson KD. 2008. DNA methylation in development and human disease. Mutat. Res. 647: 30-38.
10. Hughes MF, Beck BD, Chen Y, Lewis AS, Thomas DJ. 2011. Arsenic exposure and toxicology: a historical perspective. Toxicol. Sci. 123: 305-332.
11. IARC (International Agency for Research on Cancer). 2004. Monographs on evaluation of carcinogenic risk to humans. In Some Drinking Water Disinfectants and Contaminants, including Arsenic, vol. 84. IARC Press: Lyon; 269-477.
12. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. 1999. The oncogene and Polycomb-group gene Bmi1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168.
13. Jensen TJ, Wozniak RJ, Eblin KE, Wnek SM, Gandolfi AJ, Futscher BW. 2009. Epigenetic mediated transcriptional activation of WNT5A participates in arsenical-associated malignant transformation. Toxicol. Appl. Pharmacol. 235: 39-46.
14. Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, Rhodes CJ, Valko M. 2011. Arsenic: toxicity, oxidative stress and human disease. J. Appl. Toxicol. 31: 95-107.
15. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
16. Kakehashi A, Kato A, Inoue M, Ishii N, Okazaki E, Wei M, Tachibana T, Wanibuchi H. 2010.Cytokeratin 8/18 as a new marker of mouse liver preneoplastic lesions. Toxicol. Appl. Pharmacol. 242: 47-55.
17. Kikuchi R, Kusuhara H, Hattori N, Kim I, Shiota K, Gonzalez FJ, Sugiyama Y. 2007. Regulation of tissue-specific expression of the human and mouse urate transporter 1 gene by hepatocyte nuclear factor 1 alpha/beta and DNA methylation. Mol. Pharmacol. 72: 1619-1625.
18. Kim JK, Estève PO, Jacobsen SE, Pradhan S. 2009. UHRF1 binds G9a and participates in p21 transcriptional regulation in mammalian cells. Nucleic Acids Res. 37: 493-505.
19. Kondo Y, Shen L, Suzuki S, Kurokawa T, Masuko K, Tanaka Y, Kato H, Mizuno Y, Yokoe M, Sugauchi F, Hirashima N, Orito E, Osada H, Ueda R, Guo Y, Chen X, Issa JP, Sekido Y. 2007. Alterations of DNA methylation and histone modifications contribute to gene silencing in hepatocellular carcinomas. Hepatol. Res. 37: 974-983.
20. INK4a tumor suppressor gene. Genes Dev. 21: 49-54.
21. Liu J, Waalkes MP. 2008. Liver is a target of arsenic carcinogenesis. Toxicol. Sci. 105: 24-32.
22. Maronpot RR, Fox T, Malarkey DE, Goldsworthy TL. 1995. Mutations in the ras proto-oncogene: clues to etiology and molecular pathogenesis of mouse liver tumors. Toxicology 101: 125-156.
23. Merlo A, Herman JG, Mao L, Lee DJ, Gabrielson E, Burger PC, Baylin SB, Sidransky D. 1995. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat. Med. 1: 686-692.
24. Nohara K, Pan X, Tsukum S, Hida A, Ito T, Nagai H, Inouye K, Motohashi H, Yamamoto M, Fujii-Kuriyama Y, Tohyama C. 2005. Constitutively active aryl hydrocarbon receptor expressed specifically in T-lineage cells causes thymus involution and suppresses the immunization-induced increase in splenocytes. J. Immunol. 174: 2770-2777.
25. Nohara K, Ao K, Miyamoto Y, Ito T, Suzuki T, Toyoshiba H, Tohyama C. 2006. Comparison of the 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD)-induced CYP1A1 gene expression profile in lymphocytes from mice, rats, and humans: most potent induction in humans. Toxicology 225: 204-213.
26. Nohara K, Baba T, Murai H, Kobayashi Y, Suzuki T, Tateishi Y, Matsumoto M, Nishimura N, Sano T. 2011. Global DNA methylation in the mouse liver is affected by methyl deficiency and arsenic in a sex-dependent manner. Arch. Toxicol. 85: 653-661.
27. Okoji RS, Yu RC, Maronpot RR, Froines JR. 2002. Sodium arsenite administration via drinking water increases genome-wide and Ha-ras DNA hypomethylation in methyl-deficient C57BL/6J mice. Carcinogenesis 23: 777-785.
28. Reichard JF, Puga A. 2010. Effects of arsenic exposure on DNA methylation and epigenetic gene regulation. Epigenomics 2: 87-104.
29. Ren X, McHale CM, Skibola CF, Smith AH, Smith MT, Zhang L. 2011. An emerging role for epigenetic dysregulation in arsenic toxicity and carcinogenesis. Environ. Health Perspect. 119: 11-19.
30. Rossman TG. 2003. Mechanism of arsenic carcinogenesis: an integrated approach. Mutat. Res. 533: 37-65.
31. Smith AH, Goycolea M, Haque R, Biggs ML. 1998. Marked increase in bladder and lung cancer mortality in a region of Northern Chile due to arsenic in drinking water. Am. J. Epidemiol. 147: 660-669.
32. Smallwood A, Estève PO, Pradhan S, Carey M. 2007. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev. 21: 1169-1178.
33. Sugimoto K, Kage H, Aki N, Sano A, Kitagawa H, Nagase T, Yatomi Y, Ohishi N, Takai D. 2007. The induction of H3K9 methylation by PIWIL4 at the p16Ink4a locus. Biochem. Biophys. Res. Commun. 359: 497-502.
34. Suzuki T, Nohara K. 2007. Regulatory factors involved in species-specific modulation of arylhydrocarbon receptor (AhR)-dependent gene expression in humans and mice. J. Biochem. (Tokyo) 142: 443-452.
35. Ushijima T, Okochi-Takada E. 2005. Aberrant methylations in cancer cells: where do they come from? Cancer Sci. 96: 206-211.
36. Wu H, Zhang Y. 2011. Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev. 25: 2436-2452.
37. Wu LP, Wang X, Li L, Zhao Y, Lu S, Yu Y, Zhou W, Liu X, Yang J, Zheng Z, Zhang H, Feng J, Yang Y, Wang H, Zhu WG. 2008. Histone deacetylase inhibitor depsipeptide activates silenced genes through decreasing both CpG and H3K9 methylation on the promoter. Mol. Cell. Biol. 28: 3219-3235.
38. Yoshida T, Yamauchi H, Fan Sun G. 2004. Chronic health effects in people exposed to arsenic via the drinking water: dose-response relationships in review. Toxicol. Appl. Pharmacol. 198: 243-252.
39. Zhou X, Sun H, Ellen TP, Chen H, Costa M. 2008. Arsenite alters global histone H3 methylation. Carcinogenesis 29: 1831-1836.