Epigenetic mechanisms of mouse interstrain variability in genotoxicity of the environmental toxicant 1,3-butadiene

Toxicological Sciences

Volumn 122, Issue 2, 2011, Pages 448-456

  Koturbash, Igor ^a   Scherhag, Anne ^a,b   Sorrentino, Jessica ^c   Sexton, Kenneth ^d   Bodnar, Wanda ^d   Swenberg, James A ^c,d   Beland, Frederick A ^a   deVillena, Fernando Pardo Manuel ^e   Rusyn, Ivan ^c,d   Pogribny, Igor P ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

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

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

1,3 butadiene; Epigenetics; Liver; Mouse; Systems toxicology

Indexed keywords

1,3 BUTADIENE; GUANINE DERIVATIVE; HISTONE H3; HISTONE H4; LYSINE; N7 (2,3,4 TRIHYDROXYBUT 1 YL) GUANINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; C57BL 6 MOUSE; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA ADDUCT; DNA DAMAGE; DNA METHYLATION; EPIGENETICS; EXPOSURE; GENE EXPRESSION; GENETIC VARIABILITY; GENOTOXICITY; HISTONE METHYLATION; HYPOTHESIS; INHALATION; LIVER TOXICITY; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; STRAIN DIFFERENCE;

ANIMALS; BLOTTING, WESTERN; BUTADIENES; CARCINOGENS, ENVIRONMENTAL; DNA ADDUCTS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION; GENETIC MARKERS; GUANINE; LIVER; MALE; METHYLATION; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MUS;

EID: 80051675851     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr133     Document Type: Article

References (49)

1. Aylor, D. L., Valdar, W., Foulds-Mathes, W., Buus, R. J., Verdugo, R. A., Baric, R. S., Ferris, M. T., Frelinger, J. A., Heise, M., Frieman, M. B., et al. (2011). Genetic analysis of complex traits in the emerging collaborative cross. Genome Res. Advance Access published on March 15, 2011; doi:10.1101/gr.111310.110.
2. Bradford, B. U., Lock, E. F., Kosyk, O., Kim, S., Uehara, T., Harbourt, D., Desimone, M., Threadgill, D. W., Tryndyak, V., Pogribny, I. P., et al. (2011). Inter-strain differences in the liver effects of trichloroethylene in a multi-strain panel of inbred mice. Toxicol. Sci. 120, 206-217.
3. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R. S., and Zhang, Y. (2002). Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science 298, 1039-1043.
4. Chen, R.Z., Pettersson, U., Beard, C., Jackson-Grusby, L., and Jaenisch, R. (1998). DNA hypomethylation leads to elevated mutation rates. Nature 395, 89-93.
5. Chesler, E. J., Miller, D. R., Branstetter, L. R., Galloway, L. D., Jackson, B. L., Philip, V. M., Voy, B. H., Culiat, C. T., Threadgill, D. W., Williams, R. W., et al. (2008). The collaborative cross at Oak Ridge National Laboratory: developing a powerful resource for systems genetics. Mamm. Genome. 19, 382-389.
6. Cochrane, J. E., and Skopek, T. R. (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.
7. Dillon, N. (2004). Heterochromatin structure and function. Biol. Cell. 96, 631-637.
8. Falk, M., Lukasova, E., and Kozubek, S. (2008). Chromatin structure influences the sensitivity of DNA to gamma-radiation. Biochim. Biophys. Acta. 1783, 2398-2414.
9. Fazzari, M. J., and Greally, J. M. (2004). Epigenomics: beyond CpG islands. Nat. Rev. Genet. 5, 446-455.
10. Filser, J. G., Hutzler, C., Meischner, V., Veereshwarayya, V., and Csanady, G. A. (2007). Metabolism of 1,3-butadiene to toxicologically relevant metabolites in single-exposed mice and rats. Chem. Biol. Interact. 166, 93-103.
11. Gao, W., Mizukawa, Y., Nakatsu, N., Minowa, Y., Yamada, H., Ohno, Y., and Urushidani, T. (2010). Mechanism-based biomarker gene sets for glutathione depletion-related hepatotoxicity in rats. Toxicol. Appl. Pharmacol. 247, 211-221.
12. Harrill, A. H., Ross, P. K., Gatti, D. M., Threadgill, D. W., and Rusyn, I. (2009a). Population-based discovery of toxicogenomics biomarkers for hepatotoxicity using a laboratory strain diversity panel. Toxicol. Sci. 110, 235-243.
13. Harrill, A. H., Watkins, P. B., Su, S., Ross, P. K., Harbourt, D. E., Stylianou, I. M., Boorman, G. A., Russo, M. W., Sackler, R. S., Harris, S. C., et al. (2009b). Mouse population-guided resequencing reveals that variants in CD44 contribute to acetaminophen-induced liver injury in humans. Genome Res. 19, 1507-1515.
14. Himmelstein, M. W., Turner, M. J., Asgharian, B., and Bond, J. A. (1996). Metabolism of 1,3-butadiene: inhalation pharmacokinetics and tissue dosimetry of butadiene epoxides in rats and mice. Toxicology 113, 306-309.
15. IARC. (2009). 1,3-Butadiene, Ethylene Oxide and Vinyl Halides (Vinyl Fluoride and Vinyl Bromide). WHO, Lyon, France.
16. Jenuwein, T. (2006). The epigenetic magic of histone lysine methylation. FEBS J. 273, 3121-3135.
17. Jones, P. A., and Baylin, S. B. (2007). The epigenomics of cancer. Cell 128, 683-692.
18. Judson, R., Richard, A., Dix, D. J., Houck, K., Martin, M., Kavlock, R., Dellarco, V., Henry, T., Holderman, T., Sayre, P., et al. (2009). The toxicity data landscape for environmental chemicals. Environ. Health Perspect. 117, 685-695.
19. Kavlock, R. J., Austin, C. P., and Tice, R. R. (2009). Toxicity testing in the 21st century: implications for human health risk assessment. Risk Anal. 29, 485-487.
20. Kemper, R. A., Krause, R. J., and Elfarra, A. A. (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.
21. Kinner, A., Wu, W., Staudt, C., and Iliakis, G. (2008). Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36, 5678-5694.
22. Kladde, M. P., and Simpson, R. T. (1994). Positioned nucleosomes inhibit Dam methylation in vivo. Proc. Natl. Acad. Sci. U.S.A. 91, 1361-1365.
23. Koc, H., Tretyakova, N. Y.,Walker, V. E., Henderson, R. F., and Swenberg, J. A. (1999). Molecular dosimetry of N-7 guanine adduct formation in mice and rats exposed to 1,3-butadiene. Chem. Res. Toxicol. 12, 566-574.
24. Kongruttanachok, N., Phuangphairoj, C., Thongnak, A., Ponyeam, W., Rattanatanyong, P., Pornthanakasem, W., and Mutirangura, A. (2010). Replication independent DNA double-strand break retention may prevent genomic instability. Mol. Cancer. 9, 70.
25. Koturbash, I., Scherhag, A., Sorrentino, J., Sexton, K., Bodnar, W., Tryndyak, V., Latendresse, J. R., Swenberg, J. A., Beland, F. A., Pogribny, I. P., et al. (2011). Epigenetic alterations in liver of C57BL/6J mice after short-term inhalational exposure to 1,3-butadiene. Environ. Health Perspect. 119, 635-640.
26. LeBaron, M. J., Rasoulpour, R. J., Klapacz, J., Ellis-Hutchings, R. G., Hollnagel, H. M., and Gollapudi, B. B. (2010). Epigenetics and chemical safety assessment. Mutat. Res. 705, 83-95.
27. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
28. Loeb, L. A., and Harris, C. C. (2008). Advances in chemical carcinogenesis: a historical review and prospective. Cancer Res. 68, 6863-6872.
29. Lucier, G. W., and Schecter, A. (1998). Human exposure assessment and the National Toxicology Program. Environ. Health Perspect. 106, 623-627.
30. Marlowe, J., Teo, S. S., Chibout, S. D., Pognan, F., and Moggs, J. (2009). Mapping the epigenome-impact for toxicology. EXS 99, 259-288.
31. Martens, J. H., O'Sullivan, R. J., Braunschweig, U., Opravil, S., Radolf, M., Steinlein, P., and Jenuwein, T. (2005). The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800-812.
32. Martin, C., and Zhang, Y. (2005). The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6, 838-849.
33. Miranda, T. B., Kelly, T. K., Bouazoune, K., and Jones, P. A. Methylationsensitive single-molecule analysis of chromatin structure. Curr. Protoc. Mol. Biol. Chapter 21, Unit 21.17.1-21.17.16.
34. National Research Council. (2008). Science and Decisions: Advancing Risk Assessment. The National Academies Press, Washington, DC.
35. National Toxicology Program. (1984). NTP toxicology and carcinogenesis studies of 1,3-butadiene (CAS No. 106-99-0) in B6C3F1 mice (inhalation studies). Natl. Toxicol. Program Tech. Rep. Ser. 288, 1-111.
36. National Toxicology Program. (1993). NTP toxicology and carcinogenesis studies of 1,3-butadiene (CAS No. 106-99-0) in B6C3F1 mice (inhalation studies). Natl. Toxicol. Program Tech. Rep. Ser. 434, 1-389.
37. Neumann, H. G. (2009). Risk assessment of chemical carcinogens and thresholds. Crit. Rev. Toxicol. 39, 449-461.
38. Pogribny, I., Yi, P., and James, S. J. (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.
39. Pogribny, I. P., Rusyn, I., and Beland, F. A. (2008). Epigenetic aspects of genotoxic and non-genotoxic hepatocarcinogenesis: studies in rodents. Environ. Mol. Mutagen. 49, 9-15.
40. Poirier, M. C. (2004). Chemical-induced DNA damage and human cancer risk. Nat. Rev. Cancer. 4, 630-637.
41. Rappaport, S. M., and Smith, M. T. (2010). Epidemiology. Environment and disease risks. Science 330, 460-461.
42. Rusyn, I., Gatti, D. M., Wiltshire, T., Kleeberger, S. R., and Threadgill, D. W. (2010). Toxicogenetics: population-based testing of drug and chemical safety in mouse models. Pharmacogenomics 11, 1127-1136.
43. Strauss, W. M. (1989). Preparation of genomic DNA from mammalian tissue. In Current Protocols in Molecular Biology (F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. A. Seidman, J. A. Smith, and K. Struhl, Eds.), pp. 2.2.1-2.2.3. Wiley-Interscience, New York, NY.
44. Swenberg, J. A., Bordeerat, N. K., Boysen, G., Carro, S., Georgieva, N. I., Nakamura, J., Troutman, J. M., Upton, P. B., Albertini, R. J., Vacek, P. M., et al. (2010). 1,3-Butadiene: biomarkers and application to risk assessment. Chem. Biol. Interact. Advance Access published on October 23, 2010; doi:10.1016/j.cbi.2010.10.010.
45. Swenberg, J. A., Ham, A. J., Koc, H., Morinello, E., Ranasinghe, A., Tretyakova, N., Upton, P. B., and Wu, K. Y. (2000). DNA adducts: effects of low exposure to ethylene oxide, vinyl chloride and butadiene. Mutat. Res. 464, 77-86.
46. Tryndyak, V. P., Muskhelishvili, L., Kovalchuk, O., Rodriguez-Juarez, R., Montgomery, B., Churchwell, M. I., Ross, S. A., Beland, F. A., and Pogribny, I. P. (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. Wild, C. P. (2009). Environmental exposure measurement in cancer epidemiology. Mutagenesis 24, 117-125.
48. Yang, H., Wang, J. R., Didion, J. P., Buus, R. J., Bell, T. A., Welsh, C. E., Bonhomme, F., Boursot, P., Harr, B., Yu, A. H. T., et al. (2011). Genomewide maps of subspecific origin and identity by descent in the laboratory mouse. Nat. Genet. Advance Access published on May 29, 2011; doi:10.1038/ng.847.
49. Ziegler, J. (1993). Health risk assessment research: the OTA report. Environ. Health Perspect. 101, 402-406.