Epigenetic alterations in liver of C57BL/6J mice after short-term inhalational exposure to 1,3-butadiene

Environmental Health Perspectives

Volumn 119, Issue 5, 2011, Pages 635-640

  Koturbash, Igor ^a   Scherhag, Anne ^a,b   Sorrentino, Jessica ^c   Sexton, Kenneth ^d   Bodnar, Wanda ^d   Tryndyak, Volodymyr ^a   Latendresse, John R ^a   Swenberg, James A ^c,d   Beland, Frederick A ^a   Pogribny, Igor P ^a   Rusyn, Ivan ^c,d  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^c Curriculum in Toxicology   (United States)

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

Author keywords

1,3 butadiene; DNA damage; Epigenetics; Liver; Mouse

Indexed keywords

1,3 BUTADIENE; ALANINE AMINOTRANSFERASE; ARGIPRESSIN RECEPTOR; CALGRANULIN A; CARBONATE DEHYDRATASE III; CASPASE 3; CD36 ANTIGEN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYTOKERATIN 18; DNA METHYLTRANSFERASE 1; FATTY ACID SYNTHASE; HEME OXYGENASE 1; HISTONE DEMETHYLASE; HISTONE DEMETHYLASE 2; HISTONE H3; HISTONE H4; HISTONE LYSINE METHYLTRANSFERASE; LANOSTEROL SYNTHASE; N 7 (2,3,4 TRIHYDROXYBUT 1 YL)GUANINE; PROTEIN DNAJ; RADIXIN; SOMATOMEDIN BINDING PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; THIOREDOXIN REDUCTASE 1; UNCLASSIFIED DRUG;

ACCLIMATIZATION; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CARCINOGENESIS; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENOTOXICITY; GLYCOGEN SYNTHESIS; HISTONE METHYLATION; HISTOPATHOLOGY; IMMUNOPRECIPITATION; LIVER TOXICITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; BODY WEIGHT; BUTADIENES; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA DAMAGE; DNA METHYLATION; EPIGENESIS, GENETIC; HISTONE DEMETHYLASES; INHALATION; LIVER; MALE; METHYLTRANSFERASES; MICE; MICE, INBRED C57BL; POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS;

MUS;

EID: 79955855605     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1002910     Document Type: Article

References (54)

1. Baccarelli A, Bollati V. 2009. Epigenetics and environmental chemicals. Curr Opin Pediatr 21:243-251.
2. Bachman AN, Phillips JM, Goodman JI. 2006. Phenobarbital induces progressive patterns of GC-rich and gene-specific altered DNA methylation in the liver of tumor-prone B6C3F1 mice. Toxicol Sci 91:393-405.
3. Bagnyukova TV, Tryndyak VP, Montgomery B, Churchwell MI, Karpf AR, James SR, et al. 2008. Genetic and epigenetic changes in rat preneoplastic liver tissue induced by 2-acetylaminofluorene. Carcinogenesis 29:638-646.
4. Barreto G, Schafer A, Marhold J, Stach D, Swaminathan SK, Handa V, et al. 2007. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445:671-675.
5. Benetti R, Gonzalo S, Jaco I, Schotta G, Klatt P, Jenuwein T, et al. 2007. Suv4-20h deficiency results in telomere elongation and derepression of telomere recombination. J Cell Biol 178:925-936.
6. Choi BM, Pae HO, Kim YM, Chung HT. 2003. Nitric oxide-mediated cytoprotection of hepatocytes from glucose deprivation-induced cytotoxicity: involvement of heme oxygenase-1. Hepatology 37:810-823.
7. Cochrane JE, Skopek TR. 1994. Mutagenicity of butadiene and its epoxide metabolites: I. Mutagenic potential of 1,2-epoxybutene, 1,2,3,4-diepoxybutane and 3,4-epoxy-1,2-butanediol in cultured human lymphoblasts. Carcinogenesis 15:713-717.
8. Couture JF, Collazo E, Ortiz-Tello PA, Brunzelle JS, Trievel RC. 2007. Specificity and mechanism of JMJD2A, a trimethyllysine-specific histone demethylase. Nat Struct Mol Biol 14:689-695.
9. Dion V, Lin Y, Hubert L Jr, Waterland RA, Wilson JH. 2008. Dnmt1 deficiency promotes CAG repeat expansion in the mouse germline. Hum Mol Genet 17:1306-1317.
10. Esteve PO, Chin HG, Smallwood A, Feehery GR, Gangisetty O, Karpf AR, et al. 2006. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 20:3089-3103.
11. Filser JG, Hutzler C, Meischner V, Veereshwarayya V, Csanady GA. 2007. Metabolism of 1,3-butadiene to toxicologically relevant metabolites in single-exposed mice and rats. Chem Biol Interact 166:93-103.
12. Fodor BD, Kubicek S, Yonezawa M, O'Sullivan RJ, Sengupta R, Perez-Burgos L, et al. 2006. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev 20:1557-1562.
13. Fuks F, Hurd PJ, Deplus R, Kouzarides T. 2003. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res 31:2305-2312.
14. Garzon R, Liu S, Fabbri M, Liu Z, Heaphy CE, Callegari E, et al. 2009. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood 113:6411-6418.
15. Goggin M, Swenberg JA, Walker VE, Tretyakova N. 2009. Molecular dosimetry of 1,2,3,4-diepoxybutane-induced DNA-DNA cross-links in B6C3F1 mice and F344 rats exposed to 1,3-butadiene by inhalation. Cancer Res 69:2479-2486.
16. Goll MG, Bestor TH. 2005. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481-514.
17. Greeson NT, Sengupta R, Arida AR, Jenuwein T, Sanders SL. 2008. Di-methyl H4 lysine 20 targets the checkpoint protein Crb2 to sites of DNA damage. J Biol Chem 283:33168-33174.
18. Himmelstein MW, Acquavella JF, Recio L, Medinsky MA, Bond JA. 1997. Toxicology and epidemiology of 1,3-butadiene. Crit Rev Toxicol 27:1-108.
19. Hsieh HC, Chen YT, Li JM, Chou TY, Chang MF, Huang SC, et al. 2009. Protein profilings in mouse liver regeneration after partial hepatectomy using iTRAQ technology. J Proteome Res 8:1004-1013.
20. Huang J, Wang Y, Guo Y, Sun S. 2010. Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology 52:60-70.
21. IARC (International Agency for Research on Cancer). 2008. 1,3-Butadiene, Ethylene Oxide and Vinyl Halides (Vinyl Fluoride, Vinyl Chloride and Vinyl Bromide). IARC Monogr Eval Carcinog Risks Hum 97:3-471.
22. Jacinto FV, Esteller M. 2007. MGMT hypermethylation: a prognostic foe, a predictive friend. DNA Repair (Amst) 6:1155-1160.
23. Kemper RA, Krause RJ, Elfarra AA. 2001. Metabolism of butadiene monoxide by freshly isolated hepatocytes from mice and rats: different partitioning between oxidative, hydrolytic, and conjugation pathways. Drug Metab Dispos 29:830-836.
24. Koc H, Tretyakova NY, Walker VE, Henderson RF, Swenberg JA. 1999. Molecular dosimetry of N-7 guanine adduct formation in mice and rats exposed to 1,3-butadiene. Chem Res Toxicol 12:566-574.
25. Kojima M, Nemoto K, Murai U, Yoshimura N, Ayabe Y, Degawa M. 2002. Altered gene expression of hepatic lanosterol 14α-demethylase (CYP51) in lead nitrate-treated rats. Arch Toxicol 76:398-403.
26. Kovalenko VM, Bagnyukova TV, Sergienko OV, Bondarenko LB, Shayakhmetova GM, Matvienko AV, et al. 2007. Epigenetic changes in the rat livers induced by pyrazinamide treatment. Toxicol Appl Pharmacol 225:293-299.
27. Lu K, Boysen G, Gao L, Collins LB, Swenberg JA. 2008. Formaldehyde-induced histone modifications in vitro. Chem Res Toxicol 21:1586-1593.
28. Marlowe J, Teo SS, Chibout SD, Pognan F, Moggs J. 2009. Mapping the epigenome-impact for toxicology. EXS 99:259-288.
29. Martens JH, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, et al. 2005. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 24:800-812.
30. Melnick RL, Sills RC. 2001. Comparative carcinogenicity of 1,3-butadiene, isoprene, and chloroprene in rats and mice. Chem Biol Interact 135-136:27-42.
31. Moggs JG, Orphanides G. 2004. The role of chromatin in molecular mechanisms of toxicity. Toxicol Sci 80:218-224.
32. Morio LA, Leone A, Sawant SP, Nie AY, Parker JB, Taggart P, et al. 2006. Hepatic expression of heme oxygenase-1 and antioxidant response element-mediated genes following administration of ethinyl estradiol to rats. Toxicol Appl Pharmacol 216:416-425.
33. Peng JC, Karpen GH. 2009. Heterochromatic genome stability requires regulators of histone H3 K9 methylation. PLoS Genet 5:e1000435; doi:10.1371/journal.pgen.1000435 [Online 27 March 2009].
34. Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, et al. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323-337.
35. Pogribny IP, Rusyn I, Beland FA. 2008. Epigenetic aspects of genotoxic and non-genotoxic hepatocarcinogenesis: studies in rodents. Environ Mol Mutagen 49:9-15.
36. Pogribny IP, Tryndyak VP, Woods CG, Witt SE, Rusyn I. 2007. Epigenetic effects of the continuous exposure to peroxisome proliferator WY-14,643 in mouse liver are dependent upon peroxisome proliferator activated receptor alpha. Mutat Res 625:62-71.
37. Pogribny I, Yi P, James SJ. 1999. A sensitive new method for rapid detection of abnormal methylation patterns in global DNA and within CpG islands. Biochem Biophys Res Commun 262:624-628.
38. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, et al. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593-599.
39. Reamon-Buettner SM, Mutschler V, Borlak J. 2008. The next innovation cycle in toxicogenomics: environmental epigenetics. Mutat Res 659:158-165.
40. Sanders SL, Portoso M, Mata J, Bahler J, Allshire RC, Kouzarides T. 2004. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603-614.
41. Sawan C, Vaissiere T, Murr R, Herceg Z. 2008. Epigenetic drivers and genetic passengers on the road to cancer. Mutat Res 642:1-13.
42. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101-1108.
43. Shivapurkar N, Wilson MJ, Poirier LA. 1984. Hypomethylation of DNA in ethionine-fed rats. Carcinogenesis 5:989-992.
44. Shuker DE. 2002. The enemy at the gates? DNA adducts as biomarkers of exposure to exogenous and endogenous genotoxic agents. Toxicol Lett 134:51-56.
45. Swenberg JA, Ham AJ, Koc H, Morinello E, Ranasinghe A, Tretyakova N, et al. 2000. DNA adducts: effects of low exposure to ethylene oxide, vinyl chloride and butadiene. Mutat Res 464:77-86.
46. Tryndyak VP, Muskhelishvili L, Kovalchuk O, Rodriguez-Juarez R, Montgomery B, Churchwell MI, et al. 2006. Effect of long-term tamoxifen exposure on genotoxic and epigenetic changes in rat liver: implications for tamoxifen-induced hepatocarcinogenesis. Carcinogenesis 27:1713-1720.
47. Valinluck V, Sowers LC. 2007. Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res 67:946-950.
48. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, et al. 2006. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439:871-874.
49. Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J, et al. 2009. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet 41:125-129.
50. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, et al. 2005. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 37:853-862.
51. White WC. 2007. Butadiene production process overview. Chem Biol Interact 166:10-14.
52. Yamane K, Toumazou C, Tsukada Y, Erdjument-Bromage H, Tempst P, Wong J, et al. 2006. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125:483-495.
53. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. 2004. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res 32:e38.
54. Yang H, Mizzen CA. 2009. The multiple facets of histone H4-lysine 20 methylation. Biochem Cell Biol 87:151-161.