The p-benzoquinone DNA adducts derived from benzene are highly mutagenic

DNA Repair

Volumn 4, Issue 12, 2005, Pages 1399-1409

  Xie, Zhongwen ^a   Zhang, Yangbin ^a   Guliaev, Anton B ^b   Shen, Huiyun ^a   Hang, Bo ^b   Singer, B ^b   Wang, Zhigang ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Benzene; DNA adducts; Lesion bypass; Mutagenesis; Polymerase ; Translesion synthesis; Y family DNA polymerase

Indexed keywords

1,4 BENZOQUINONE; BENZENE; PLASMID DNA;

CHEMICAL MUTAGENESIS; CONFERENCE PAPER; DNA ADDUCT; DNA DAMAGE; DNA SYNTHESIS; GENE DELETION; GENE INSERTION; GENE MUTATION; GENE REPLICATION; GENE STRUCTURE; GENE SYNTHESIS; GENOTOXICITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN PURIFICATION; YEAST CELL;

BENZENE; BENZOQUINONES; CARCINOGENS; DNA ADDUCTS; DNA DAMAGE; DNA-DIRECTED DNA POLYMERASE; HUMANS; KINETICS; MUTAGENESIS; MUTAGENESIS, INSERTIONAL; MUTAGENS; MUTATION; NUCLEOTIDYLTRANSFERASES; YEASTS;

EID: 27844460203     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2005.08.012     Document Type: Conference Paper

References (58)

1. R. Snyder Overview of the toxicology of benzene J. Toxicol. Environ. Health A 61 2000 339 346
2. J. Whysner, M.V. Reddy, P.M. Ross, M. Mohan, and E.A. Lax Genotoxicity of benzene and its metabolites Mutat. Res. 566 2004 99 130
3. J.E. Huff, J.K. Haseman, D.M. DeMarini, S. Eustis, R.R. Maronpot, A.C. Peters, R.L. Persing, C.E. Chrisp, and A.C. Jacobs Multiple-site carcinogenicity of benzene in Fischer 344 rats and B6C3F1 mice Environ. Health Perspect. 82 1989 125 163
4. W.F. Greenlee, J.D. Sun, and J.S. Bus A proposed mechanism of benzene toxicity: formation of reactive intermediates from polyphenol metabolites Toxicol. Appl. Pharmacol. 59 1981 187 195
5. 32P- postlabeling of DNA reacted with p-benzoquinone Carcinogenesis 11 1990 1469 1472
6. 32P-postlabeling of DNA reacted with p-benzoquinone Chem. Res. Toxicol. 4 1991 199 202
7. L. Jowa, S. Winkle, G. Kalf, G. Witz, and R. Snyder Deoxyguanosine adducts formed from benzoquinone and hydroquinone Adv. Exp. Med. Biol. 197 1986 825 832
8. L. Jowa, G. Witz, R. Snyder, S. Winkle, and G.F. Kalf Synthesis and characterization of deoxyguanosine-benzoquinone adducts J. Appl. Toxicol. 10 1990 47 54
9. A. Chenna, and B. Singer Large scale synthesis of p-benzoquinone- 2′-deoxycytidine and p-benzoquinone-2′-deoxyadenosine adducts and their site-specific incorporation into DNA oligonucleotides Chem. Res. Toxicol. 8 1995 865 874
10. A. Nakayama, S. Koyoshi, S. Morisawa, and T. Yagi Comparison of the mutations induced by p-benzoquinone, a benzene metabolite, in human and mouse cells Mutat. Res. 470 2000 147 153
11. A. Nakayama, Y. Noguchi, T. Mori, S. Morisawa, and T. Yagi Comparison of mutagenic potentials and mutation spectra of benzene metabolites using supF shuttle vectors in human cells Mutagenesis 19 2004 91 97
12. M. Gaskell, K.I. McLuckie, and P.B. Farmer 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 Mutat. Res. 554 2004 387 398
13. A.H. Mullin, R. Rando, F. Esmundo, and D.A. Mullin Inhalation of benzene leads to an increase in the mutant frequencies of a lacI transgene in lung and spleen tissues of mice Mutat. Res. 327 1995 121 129
14. G.S. Provost, J.C. Mirsalis, B.J. Rogers, and J.M. Short Mutagenic response to benzene and tris(2,3-dibromopropyl)-phosphate in the lambda lacI transgenic mouse mutation assay: a standardized approach to in vivo mutation analysis Environ. Mol. Mutagen. 28 1996 342 347
15. H. Ohmori, E.C. Friedberg, R.P.P. Fuchs, M.F. Goodman, F. Hanaoka, D. Hinkle, T.A. Kunkel, C.W. Lawrence, Z. Livneh, T. Nohmi, L. Prakash, S. Prakash, T. Todo, G.C. Walker, Z. Wang, and R. Woodgate The Y-family of DNA polymerases Mol. Cells 8 2001 7 8
16. Z. Wang Translesion synthesis by the UmuC family of DNA polymerases Mutat. Res. 486 2001 59 70
17. Z. Wang DNA damage-induced mutagenesis: a novel target for cancer prevention Mol. Interv. 1 2001 269 281
18. Z. Livneh DNA damage control by novel DNA polymerases: translesion replication and mutagenesis J. Biol. Chem. 276 2001 25639 25642
19. E.C. Friedberg, P.L. Fischhaber, and C. Kisker Error-prone DNA polymerases: novel structures and the benefits of infidelity Cell 107 2001 9 12
20. P.M. Burgers, E.V. Koonin, E. Bruford, L. Blanco, K.C. Burtis, M.F. Christman, W.C. Copeland, E.C. Friedberg, F. Hanaoka, D.C. Hinkle, C.W. Lawrence, M. Nakanishi, H. Ohmori, L. Prakash, S. Prakash, C.A. Reynaud, A. Sugino, T. Todo, Z. Wang, J.C. Weill, and R. Woodgate Eukaryotic DNA polymerases: proposal for a revised nomenclature J. Biol. Chem. 276 2001 43487 43490
21. R.E. Johnson, S. Prakash, and L. Prakash Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Polη Science 283 1999 1001 1004
22. C. Masutani, M. Araki, A. Yamada, R. Kusumoto, T. Nogimori, T. Maekawa, S. Iwai, and F. Hanaoka Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity EMBO J. 18 1999 3491 3501
23. F. Yuan, Y. Zhang, D.K. Rajpal, X. Wu, D. Guo, M. Wang, J.-S. Taylor, and Z. Wang Specificity of DNA lesion bypass by the yeast DNA polymerase η J. Biol. Chem. 275 2000 8233 8239
24. D. Guo, X. Wu, D.K. Rajpal, J.-S. Taylor, and Z. Wang Translesion synthesis by yeast DNA polymerase ζ from templates containing lesions of ultraviolet radiation and acetylaminofluorene Nucleic Acids Res. 29 2001 2875 2883
25. R.E. Johnson, M.T. Washington, L. Haracska, S. Prakash, and L. Prakash Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions Nature 406 2000 1015 1019
26. Y. Zhang, X. Wu, D. Guo, O. Rechkoblit, and Z. Wang Activities of human DNA polyemrase κ in response to the major benzo[a]pyrene DNA adduct: error-free bypass and extension synthesis from opposite the lesion DNA Repair 1 2002 559 569
27. 2-dG adducts by human DNA polymerases η and κ Mutat. Res. 510 2002 23 35
28. M.T. Washington, R.E. Johnson, L. Prakash, and S. Prakash Human DINB1-encoded DNA polymerase κ is a promiscuous extender of mispaired primer termini Proc. Natl. Acad. Sci. U.S.A. 99 2002 1910 1914
29. B. Zhao, Z. Xie, H. Shen, and Z. Wang Role of DNA polymerase η in the bypass of abasic sites in yeast cells Nucleic Acids Res. 32 2004 3984 3994
30. J.R. Nelson, C.W. Lawrence, and D.C. Hinkle Deoxycytidyl transferase activity of yeast REV1 protein Nature 382 1996 729 731
31. W. Lin, H. Xin, Y. Zhang, X. Wu, F. Yuan, and Z. Wang The human REV1 gene codes for a DNA template-dependent dCMP transferase Nucleic Acids Res. 27 1999 4468 4475
32. Y. Zhang, X. Wu, O. Rechkoblit, N.E. Geacintov, J.-S. Taylor, and Z. Wang Response of human REV1 to different DNA damage: preferential dCMP insertion opposite the lesion Nucleic Acids Res. 30 2002 1630 1638
33. J.R. Nelson, P.E. Gibbs, A.M. Nowicka, D.C. Hinkle, and C.W. Lawrence Evidence for a second function for Saccharomyces cerevisiae Rev1p Mol. Microbiol. 37 2000 549 554
34. D.K. Rajpal, X. Wu, and Z. Wang Alteration of ultraviolet-induced mutagenesis in yeast though molecular modulation of the REV3 and REV7 gene expression Mutat. Res. 461 2000 133 143
35. Y. Zhang, F. Yuan, X. Wu, O. Rechkoblit, J.-S. Taylor, N.E. Geacintov, and Z. Wang Error-prone lesion bypass by human DNA polymerase η Nucleic Acids Res. 28 2000 4717 4724
36. Y. Zhang, F. Yuan, H. Xin, X. Wu, D. Rajpal, D. Yang, and Z. Wang Human DNA polymerase κ synthesizes DNA with extraordinarily low fidelity Nucleic Acids Res. 28 2000 4147 4156
37. Y. Zhang, F. Yuan, X. Wu, and Z. Wang Preferential incorporation of G opposite template T by the low fidelity human DNA polymerase ι Mol. Cell. Biol. 20 2000 7099 7108
38. D. Guo, Z. Xie, H. Shen, Z. Bo, and Z. Wang Translesion synthesis of acetylaminofluorene-dG adducts by DNA polymerase ζ is stimulated by yeast Rev1 protein Nucleic Acids Res. 32 2004 1122 1130
39. 2-benzetheno-2′-deoxyguanosine, and its site-specific incorporation into DNA oligonucleotides Chem. Res. Toxicol. 10 1997 165 171
40. Z. Xie, E. Braithwaite, D. Guo, Z. Bo, N.E. Geacintov, and Z. Wang Mutagenesis of benzo[a]pyrene diol epoxide in yeast: requirement for DNA polymerase ζ and involvement of DNA polymerase η Biochemistry 42 2003 11253 11262
41. A.B. Guliaev, J. Sagi, and B. Singer Sequence-dependent conformational perturbation in DNA duplexes containing an εA.T mismatch using molecular dynamics simulation Carcinogenesis 21 2000 1727 1736
42. A.B. Guliaev, B. Hang, and B. Singer Structural insights by molecular dynamics simulations into differential repair efficiency for ethano-A versus etheno-A adducts by the human alkylpurine-DNA N-glycosylase Nucleic Acids Res. 30 2002 3778 3787
43. P. Cieplak, J. Caldwell, and P. Kollman Molecular mechanical models for organic and biological systems going beyond the atom centered two body additive approximation: aqueous solution free energies of methanol and N-methyl acetamide, nucleic acid base, and amide hydrogen bonding and chloroform/water partition coefficients of the nucleic acid bases J. Comput. Chem. 22 2001 1048 1057
44. S. Creighton, L.B. Bloom, and M.F. Goodman Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading, and lesion bypass efficiencies Methods Enzymol. 262 1995 232 256
45. D.M. Becker, and L. Guarente High-efficiency transformation of yeast by electroporation Methods Enzymol. 194 1991 182 187
46. J.N. Strathern, and D.R. Higgins Recovery of plasmids from yeast into Escherichia coli: shuttle vectors Methods Enzymol. 194 1991 319 329
47. A.B. Guliaev, B. Hang, and B. Singer Structural insights by molecular dynamics simulations into specificity of the major human AP endonuclease toward the benzene-derived DNA adduct, pBQ-C Nucleic Acids Res. 32 2004 2844 2852
48. R.P. Fuchs, N. Schwartz, and M.P. Daune Hot spots of frameshift mutations induced by the ultimate carcinogen N-acetoxy-N-2-acetylaminofluorene Nature 294 1981 657 659
49. R.S. Tebbs, and L.J. Romano Mutagenesis at a site-specifically modified NarI sequence by acetylated and deacetylated aminofluorene adducts Biochemistry 33 1994 8998 9006
50. I.B. Lambert, R.L. Napolitano, and R.P. Fuchs Carcinogen-induced frameshift mutagenesis in repetitive sequences Proc. Natl. Acad. Sci. U.S.A. 89 1992 1310 1314
51. K. Baynton, A. Bresson-Roy, and R.P. Fuchs Distinct roles for Rev1p and Rev7p during translesion synthesis in Saccharomyces cerevisiae Mol. Microbiol. 34 1999 124 133
52. Y. Zhang, X. Wu, D. Guo, O. Rechkoblit, J.S. Taylor, N.E. Geacintov, and Z. Wang Lesion bypass activities of human DNA polymerase μ J. Biol. Chem. 277 2002 44582 44587
53. J.M. Havener, S.A. McElhinny, E. Bassett, M. Gauger, D.A. Ramsden, and S.G. Chaney Translesion synthesis past platinum DNA adducts by human DNA polymerase μ Biochemistry 42 2003 1777 1788
54. B. Hang, A. Chenna, H. Fraenkel-Conrat, and B. Singer An unusual mechanism for the major human apurinic/apyrimidinic (AP) endonuclease involving 5′ cleavage of DNA containing a benzene-derived exocyclic adduct in the absence of an AP site Proc. Natl. Acad. Sci. U.S.A. 93 1996 13737 13741
55. 6- benzetheno-dA, by the major human AP endonuclease HAP1 and Escherichia coli exonuclease III and endonuclease IV Carcinogenesis 19 1998 1339 1343
56. Y. Zhang, F. Yuan, X. Wu, J.-S. Taylor, and Z. Wang Response of human DNA polymerase ι to DNA lesions Nucleic Acids Res. 29 2001 928 935
57. 4-benzetheno-dC, in the major human AP endonuclease Biochemistry 36 1997 15411 15418
58. Y. Hiraku, and S. Kawanishi Oxidative DNA damage and apoptosis induced by benzene metabolites Cancer Res. 56 1996 5172 5178