Generation of phosphorylated histone H2AX by benzene metabolites

Toxicology in Vitro

Volumn 22, Issue 8, 2008, Pages 1861-1868

  Ishihama, Mio ^a   Toyooka, Tatsushi ^a   Ibuki, Yuko ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

Author keywords

Benzene; Benzene metabolites; DNA double strand breaks; Histone H2AX; Hydroquinone; p Benzoquinone; Reactive oxygen species

Indexed keywords

1,4 BENZOQUINONE; ACETYLCYSTEINE; BENZENE; HISTONE H2AX; HYDROQUINONE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL NUCLEUS; CELL STRAIN HL 60; CELL SURVIVAL; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; GEL ELECTROPHORESIS; GENOMIC INSTABILITY; GENOTOXICITY; HUMAN; HUMAN CELL; MYELOID LEUKEMIA; OXIDATION; PROTEIN PHOSPHORYLATION; SENSITIVITY ANALYSIS;

BENZENE; BENZOQUINONES; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, AGAR GEL; HISTONES; HL-60 CELLS; HUMANS; HYDROQUINONES; LEUKEMIA, PROMYELOCYTIC, ACUTE; MUTAGENS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; TIME FACTORS;

EID: 55149113449     PISSN: 08872333     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tiv.2008.09.005     Document Type: Article

References (46)

1. Andreoli C., Leopardi P., and Crebelli R. Detection of DNA damage in human lymphocytes by alkaline single cell gel electrophoresis after exposure to benzene or benzene metabolites. Mutation Research 377 (1997) 95-104
2. Albino A.P., Huang X., Jorgensen E., Yang J., Gietl D., Traganos F., and Darzynkiewicz Z. Induction of H2AX phosphorylation in pulmonary cells by tobacco smoke: a new assay for carcinogens. Cell Cycle 3 (2004) 1062-1068
3. Bassing C.H., Chua K.F., Sekiguchi J., Suh H., Whitlow S.R., Fleming J.C., Monroe B.C., Ciccone D.N., Yan C., Vlasakova K., Livingston D.M., Ferguson D.O., Scully R., and Alt F.W. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proceedings of the National Academy of Sciences of the United States of America 99 (2002) 8173-8178
4. Bodell W.J., Pathak D.N., Lévay G., Ye Q., and Pongracz K. Investigation of the DNA adducts formed in B6C3F1 mice treated with benzene: implications for molecular dosimetry. Environmental Health Perspectives 104 (1996) 1189-1193
5. Celeste A., Petersen S., Romanienko P.J., Fernandez-Capetillo O., Chen H.T., Sedelnikova O.A., Reina-San-Martin B., Coppola V., Meffre E., Difilippantonio M.J., Redon C., Pilch D.R., Olaru A., Eckhaus M., Camerini-Otero R.D., Tessarollo L., Livak F., Manova K., Bonner W.M., Nussenzweig M.C., and Nussenzweig A. Genomic instability in mice lacking histone H2AX. Science 296 (2002) 922-927
6. Celeste A., Difilippantonio S., Difilippantonio M.J., Fernandez-Capetillo O., Pilch D.R., Sedelnikova O.A., Eckhaus M., Ried T., Bonner W.M., and Nussenzweig A. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114 (2003) 371-383
7. Chenna A., Hang B., Rydberg B., Kim E., Pongracz K., Bodell W.J., and Singer B. The benzene metabolite p-benzoquinone forms adducts with DNA bases that are excised by a repair activity from human cells that differs from an ethenoadenine glycosylase. Proceedings of the National Academy of Sciences of the United States of America 92 (1995) 5890-5894
8. Eastmond D.A., Mondrala S.T., and Hasegawa L. Topoisomerase II inhibition by myeloperoxidase-activated hydroquinone: a potential mechanism underlying the genotoxic and carcinogenic effects of benzene. Chemico-Biological Interactions 153-154 (2005) 207-216
9. Fabiani R., De Bartolomeo A., Rosignoli P., Scamosci M., Lepore L., and Morozzi G. Influence of culture conditions on the DNA-damaging effect of benzene and its metabolites in human peripheral blood mononuclear cells. Environmental and Molecular Mutagenesis 37 (2001) 1-6
10. Frantz C.E., Chen H., and Eastmond D.A. Inhibition of human topoisomerase II in vitro by bioactive benzene metabolites. Environmental Health Perspectives 104 (1996) 1319-1323
11. Gaskell M., McLuckie K.I., and Farmer P.B. Comparison of the mutagenic activity of the benzene metabolites, hydroquinone and para-benzoquinone in the supF forward mutation assay: a role for minor DNA adducts formed from hydroquinone in benzene mutagenicity. Mutation Research 554 (2004) 387-398
12. Gaskell M., McLuckie K.I., and Farmer P.B. Genotoxicity of the benzene metabolites para-benzoquinone and hydroquinone. Chemico-Biological Interactions 153-154 (2005) 267-270
13. Golding, B.T., Watson, W.P., 1999. Possible Mechanisms of Carcinogenesis after Exposure to Benzene. IARC Science Publication 150, 75-88.
14. Greenlee W.F., Sun J.D., and Bus J.S. A proposed mechanism of benzene toxicity: formation of reactive intermediates from polyphenol metabolites. Toxicology and Applied Pharmacology 59 (1981) 187-195
15. Haber J.E. DNA recombination: the replication connection. Trends in Biochemical Sciences 24 (1999) 271-275
16. Hiraku Y., and Kawanishi S. Oxidative DNA damage and apoptosis induced by benzene metabolites. Cancer Research 56 (1996) 5172-5178
17. Huff J. Benzene-induced cancers: abridged history and occupational health impact. International Journal of Occupational and Environmental Health 13 (2007) 213-221
18. Hutt A.M., and Kalf G.F. Inhibition of human DNA topoisomerase II by hydroquinone and p-benzoquinone, reactive metabolites of benzene. Environmental Health Perspectives 104 (1996) 1265-1269
19. Léonce S., Kraus-Berthier L., Golsteyn R.M., David-Cordonnier M.H., Tardy C., Lansiaux A., Poindessous V., Larsen A.K., and Pierré A. Generation of replication-dependent double-strand breaks by the novel N2-G-alkylator S23906-1. Cancer Research 66 (2006) 7203-7210
20. Lewis J.G., Stewart W., and Adams D.O. Role of oxygen radicals in induction of DNA damage by metabolites of benzene. Cancer Research 48 (1988) 4762-4765
21. Li Z., Yang J., and Huang H. Oxidative stress induces H2AX phosphorylation in human spermatozoa. FEBS Letters 580 (2006) 6161-6168
22. Lindsey Jr. R.H., Bromberg K.D., Felix C.A., and Osheroff N. 1, 4-Benzoquinone is a topoisomerase II poison. Biochemistry 43 (2004) 7563-7574
23. Mitra S., Boldogh I., Izumi T., and Hazra T.K. Complexities of the DNA base excision repair pathway for repair of oxidative DNA damage. Environmental and Molecular Mutagenesis 38 (2001) 180-190
24. Niedernhofer L.J., Odijk H., Budzowska M., van Drunen E., Maas A., Theil A.F., de Wit J., Jaspers N.G., Beverloo H.B., Hoeijmakers J.H., and Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Molecular and Cellular Biology 24 (2004) 5776-5787
25. Oikawa S., Hirosawa I., Hirakawa K., and Kawanishi S. Site specificity and mechanism of oxidative DNA damage induced by carcinogenic catechol. Carcinogenesis 22 (2001) 1239-1245
26. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., and Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Current Biology 10 (2000) 886-895
27. Rassool F.V., Gaymes T.J., Omidvar N., Brady N., Beurlet S., Pla M., Reboul M., Lea N., Chomienne C., Thomas N.S., Mufti G.J., and Padua R.A. Reactive oxygen species, DNA damage, and error-prone repair: a model for genomic instability with progression in myeloid leukemia?. Cancer Research 67 (2007) 8762-8771
28. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. Journal of Biological Chemistry 273 (1998) 5858-5868
29. Rogakou E.P., Boon C., Redon C., and Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. Journal of Cell Biology 146 (1999) 905-916
30. Rothkamm K., and Löbrich M. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low X-ray doses. Proceedings of the National Academy of Sciences of the United States of America 100 (2003) 5057-5062
31. Sallmyr A., Fan J., and Rassool F.V. Genomic instability in myeloid malignancies: increased reactive oxygen species (ROS), DNA double strand breaks (DSBs) and error-prone repair. Cancer Letters 270 (2008) 1-9
32. Smart D.J., Halicka H.D., Schmuck G., Traganos F., Darzynkiewicz Z., and Williams G.M. Assessment of DNA double-strand breaks and gammaH2AX induced by the topoisomerase II poisons etoposide and mitoxantrone. Mutation Research 641 (2008) 43-47
33. Snyder R., and Hedli C.C. An overview of benzene metabolism. Environmental Health Perspectives 104 (1996) 1165-1171
34. Soares D.G., Escargueil A.E., Poindessous V., Sarasin A., de Gramont A., Bonatto D., Henriques J.A., and Larsen A.K. Replication and homologous recombination repair regulate DNA double-strand break formation by the antitumor alkylator ecteinascidin 743. Proceedings of the National Academy of Sciences of the United States of America 104 (2007) 13062-13067
35. Tanaka T., Huang X., Halicka H.D., Zhao H., Traganos F., Albino A.P., Dai W., and Darzynkiewicz Z. Cytometry of ATM activation and histone H2AX phosphorylation to estimate extent of DNA damage induced by exogenous agents. Cytometry A. 71 (2007) 648-661
36. Toyooka T., and Ibuki Y. Co-exposure to benzo[a]pyrene and UVA induces phosphorylation of histone H2AX. FEBS Letters 579 (2005) 6338-6342
37. Toyooka T., and Ibuki Y. New method for testing phototoxicity of polycyclic aromatic hydrocarbons. Environmental Science and Technology 40 (2006) 3603-3608
38. Toyooka T., Ohnuki G., and Ibuki Y. Solar-simulated light-exposed benzo[a]pyrene induces phosphorylation of histone H2AX. Mutation Research 650 (2008) 132-139
39. Whysner J., Reddy M.V., Ross P.M., Mohan M., and Lax E.A. Genotoxicity of benzene and its metabolites. Mutation Research 566 (2004) 99-130
40. Winn L.M. Homologous recombination initiated by benzene metabolites: a potential role of oxidative stress. Toxicological Sciences 72 (2003) 143-149
41. Yang N., Galick H., and Wallace S.S. Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks. DNA Repair 3 (2004) 1323-1334
42. Yang N., Chaudhry M.A., and Wallace S.S. Base excision repair by hNTH1 and hOGG1: a two edged sword in the processing of DNA damage in gamma-irradiated human cells. DNA Repair 5 (2006) 43-51
43. Yih L.H., Hsueh S.W., Luu W.S., Chiu T.H., and Lee T.C. Arsenite induces prominent mitotic arrest via inhibition of G2 checkpoint activation in CGL-2 cells. Carcinogenesis 26 (2005) 53-63
44. Yu Y., Zhu W., Diao H., Zhou C., Chen F.F., and Yang J. A comparative study of using comet assay and gammaH2AX foci formation in the detection of N-methyl-N′-nitro-N-nitrosoguanidine-induced DNA damage. Toxicology In Vitro 20 (2006) 959-965
45. Zhou C., Li Z., Diao H., Yu Y., Zhu W., Dai Y., Chen F.F., and Yang J. DNA damage evaluated by gammaH2AX foci formation by a selective group of chemical/physical stressors. Mutation Research 604 (2006) 8-18
46. Zykova T.A., Zhu F., Lu C., Higgins L., Tatsumi Y., Abe Y., Bode A.M., and Dong Z. Lymphokine-activated killer T-cell-originated protein kinase phosphorylation of histone H2AX prevents arsenite-induced apoptosis in RPMI7951 melanoma cells. Clinical Cancer Research 12 (2006) 6884-6893