Benzo[a]pyrene diol epoxide-deoxyguanosine adducts are accurately bypassed by yeast DNA polymerase ζ in vitro

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 508, Issue 1-2, 2002, Pages 137-145

  Simhadri, Srilatha ^a   Kramata, Pavel ^a   Zajc, Barbara ^b   Sayer, Jane M ^b   Jerina, Donald M ^b   Hinkle, David C ^c   Wei, Caroline S J ^a  

^a RUTGERS UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Benzo a pyrene diol epoxide; BPDE; DNA adduct; Polymerase ; Translesion synthesis

Indexed keywords

DEOXYGUANOSINE DERIVATIVE; DIHYDROXYBENZO[A]PYRENE OXIDE; DNA POLYMERASE; FUNGAL ENZYME; ISOENZYME;

ACCURACY; ARTICLE; CELL LINE; CONTROLLED STUDY; DNA ADDUCT; DNA SEQUENCE; DNA TEMPLATE; ENANTIOMER; GENE AMPLIFICATION; GENE MUTATION; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; DEOXYGUANOSINE; DNA ADDUCTS; DNA-DIRECTED DNA POLYMERASE; FUNGAL PROTEINS; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; TEMPLATES, GENETIC; YEASTS;

CRICETINAE; CRICETULUS GRISEUS;

EID: 0037206593     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0027-5107(02)00211-7     Document Type: Article

References (48)

1. A. Dipple, R. Moschel, C.A.H. Bigger, in: C.E. Searle (Ed.), Chemical Carcinogens, second ed., vol. 2, ACS Monograph 182, American Chemical Society, Washington, DC, 1984, pp. 41-163.
2. Sims P., Grover P.L., Swaisland A., Pal K., Hewer A. Metabolic activation of benzo[a]pyrene proceeds by a diol epoxide. Nature. 252:1974;326-328.
3. Koreeda M., Moore P.D., Wislocki P.G., Levin W., Yagi H., Jerina D.M. Binding of benzo[a]pyrene 7,8-diol-9,10-epoxides to DNA, RNA, and protein of mouse skin occurs with high stereoselectivity. Science. 199:1978;778-781.
4. Yagi H., Akagi H., Thakker D.R., Mah H.D., Koreeda M., Jerina D.M. Absolute sterochemistry of the highly mutagenic 7,8-diol-9,10-epoxides derived from the potent carcinogen trans-7,8-dihydroxy-7,8-dihydrobenzol[a]pyrene. J. Am. Chem. Soc. 99:1977;2358-2359.
5. Thakker D.R., Yagi H., Akagi H., Koreeda M., Lu A.H., Levin W., Wood A.W., Conney A.H., Jerina D.M. Metabolism of benzo[a]pyrene. VI. Stereoselective metabolism of benzo[a]pyrene and benzo[a]pyrene 7,8-dihydrodiol to diol epoxides. Chem. Biol. Interact. 16:1977;281-300.
6. Wood A.W., Chang R.L., Levin W., Yagi H., Thakker D.R., Jerina D.M., Conney A.H. Differences in mutagenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides. Biochem. Biophys. Res. Commun. 77:1977;1389-1396.
7. Buening M.K., Wislocki P.G., Levin W., Yagi H., Thakker D.R., Akagi H., Koreeda M., Jerina D.M., Conney A.H. Tumorigenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides in newborn mice: exceptional activity of (+)-7β, 8α-dihydroxy-9α,10α-epoxy-7,8,9,10- tetrahydrobenzo[a]pyrene. Proc. Natl. Acad. Sci. U.S.A. 75:1978;5358-5361.
8. Slaga T.J., Bracken W.J., Gleason G., Levin W., Yagi H., Jerina D.M., Conney A.H. Marked differences in the skin tumor-initiating activities of the optical enantiomers of the diastereomeric benzo[a]pyrene, 7,8-diol-9,10-epoxides. Cancer Res. 39:1979;67-71.
9. Cheng S.C., Hilton B.D., Roman J.M., Dipple A. DNA adducts from carcinogenic and noncarcinogenic enantiomers of benzo[a]pyrene dihydrodiol epoxide. Chem. Res. Toxicol. 2:1989;334-340.
10. Livneh Z. DNA damage control by novel DNA polymerases: replication and mutagenesis. J. Biol. Chem. 276:2001;25639-25642.
11. 2-dG) of the potent environmental carcinogen, benzo[a]pyrene. Mutat. Res. 450:2000;41-59.
12. Morrison A., Christensen R.B., Alley J., Beck A.K., Bernstine E.G., Lemontt J.F., Lawrence C.W. REV3, a Saccharomyces cerevisiae gene whose function is required for induced mutagenesis, is predicted to encode a nonessential DNA polymerase. J. Bacteriol. 171:1989;5659-5667.
13. Torpey L.E., Gibbs P.E., Nelson J., Lawrence C.W. Cloning and sequence of REV7, a gene whose function is required for DNA damage-induced mutagenesis in Saccharomyces cerevisiae. Yeast. 10:1994;1503-1509.
14. Nelson J.R., Lawrence C.W., Hinkle D.C. Thymine-thymine dimer bypass by yeast DNA polymerase ζ Science. 272:1996;1646-1649.
15. Lawrence C.W., Christensen R.B. Ultraviolet-induced reversion of cyc1 alleles in radiation-sensitive strains of yeast. III. rev3 mutant strains. Genetics. 92:1979;397-408.
16. Lawrence C.W., Das G., Christensen R.B. REV7, a new gene concerned with UV mutagenesis in yeast. Mol. Gen. Genet. 200:1985;80-85.
17. Lawrence C.W., Nisson P.E., Christensen R.B. UV and chemical mutagenesis in rev7 mutants of yeast. Mol. Gen. Genet. 200:1985;86-91.
18. Roche H., Gietz R.D., Kunz B.A. Specificity of the yeast rev3 δ antimutator and REV3 dependency of the mutator resulting from a defect (rad1 δ) in nucleotide excision repair. Genetics. 137:1994;637-646.
19. Gibbs P.E., Wang X.D., Li Z., McManus T.P., McGregor W.G., Lawrence C.W., Maher V.M. The function of the human homolog of Saccharomyces cerevisiae REV1 is required for mutagenesis induced by UV light. Proc. Natl. Acad. Sci. U.S.A. 97:2000;4186-4191.
20. Page J.E., Zajc B., Oh-hara T., Lakshman M.K., Sayer J.M., Jerina D.M., Dipple A. Sequence context profoundly influences the mutagenic potency of trans-opened benzo[a]pyrene 7,8-diol-9,10-epoxide-purine nucleoside adducts in site-specific mutation studies. Biochemistry. 37:1998;9127-9137.
21. Wei S.J., Chang R.L., Bhachech N., Cui X.X., Merkler K.A., Wong C.Q., Hennig E., Yagi H., Jerina D.M., Conney A.H. Dose-dependent differences in the profile of mutations induced by (+)-7R,8S-dihydroxy-9S,10R-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene in the coding region of the hypoxanthine (guanine) phosphoribosyltransferase gene in Chinese hamster V-79 cells. Cancer Res. 53:1993;3294-3301.
22. Wei S.J., Chang R.L., Hennig E., Cui X.X., Merkier K.A., Wong C.Q., Yagi H., Jerina D.M., Conney A.H. Mutagenic selectivity at the HPRT locus in V-79 cells: comparison of mutations caused by bay-region benzo[a]pyrene 7,8-diol-9,10-epoxide enantiomers with high and low carcinogenic activity. Carcinogenesis. 15:1994;1729-1735.
23. 2-dG adduct stereoisomers located within the human K-ras codon 12 sequence. Biochemistry. 38:1999;569-581.
24. Sayer J.M., Chadha A., Agarwal S.K., Yeh H.J.C., Yagi H., Jerina D.M. Covalent nucleoside adducts of benzo[a]pyrene 7,8-diol-9,10-epoxides: structural reinvestigation and characterization of a novel adenosine adduct on the ribose moiety. J. Org. Chem. 56:1991;20-29.
25. P.D. Moore, M. Koreeda, P.G. Wislocki, W. Levin, A.H. Conney, H. Yagi, D.M. Jerina, In vitro reactions of the diastereomeric 9,10-epoxides of (+)- and (-)-trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene with polyguanylic acid and evidence for formation of an enantiomer of each diastereomeric 9,10-epoxide from benzo[a]pyrene in mouse skin, in: D.M. Jerina (Ed.), Drug Metabolism Concepts, ACS Symposium Series No. 44, American Chemical Society, Washington, DC, 1977, pp. 127-154.
26. Lawrence C.W., Maher V.M. Mutagenesis in eukaryotes dependent on DNA polymerase ζ and Rev1p. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 356:2000;41-46.
27. Baynton K., Bresson-Roy A., Fuchs R.P. Analysis of damage tolerance pathways in Saccharomyces cerevisiae: a requirement for Rev3 DNA polymerase in translesion synthesis. Mol. Cell. Biol. 18:1998;960-966.
28. Gibbs P.E., Lawrence C.W. Novel mutagenic properties of abasic sites in Saccharomyces cerevisiae. J. Mol. Biol. 251:1995;229-236.
29. Gibbs P.E., McGregor W.G., Maher V.M., Nisson P., Lawrence C.W. A human homolog of the Saccharomyces cerevisiae REV3 gene, which encodes the catalytic subunit of DNA polymerase ζ Proc. Natl. Acad. Sci. U.S.A. 95:1998;6876-6880.
30. Shibutani S., Margulis L.A., Geacintov N.E., Grollman A.P. Translesional synthesis on a DNA template containing a single stereoisomer of dG-(+)- or dG-(-)-anti-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene). Biochemistry. 32:1993;7531-7541.
31. Lipinski L.J., Ross H.L., Zajc B., Sayer J.M., Jerina D.M., Dipple A. Effect of single benzo[a]pyrene diol epoxide-deoxyguanosine adducts on the action of DNA polymerases in vitro. Int. J. Oncol. 13:1998;269-273.
32. Hruszkewycz A.M., Canella K.A., Peltonen K., Kotrappa L., Dipple A. DNA polymerase action on benzo[a]pyrene-DNA adducts. Carcinogenesis. 13:1992;2347-2352.
33. Zhang Y., Yuan F., Wu X., Wang M., Rechkoblit O., Taylor J.S., Geacintov N.E., Wang Z. Error-free and error-prone lesion bypass by human DNA polymerase κ in vitro. Nucleic Acids Res. 28:2000;4138-4146.
34. 2-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tertrahydrobenzo[a]pyrene. Biochemistry. 41:2002;6100-6106.
35. Zhang Y., Yuan F., Wu X., Rechkoblit O., Taylor J.S., Geacintov N.E., Wang Z. Error-prone lesion bypass by human DNA polymerase η Nucleic Acids Res. 28:2000;4717-4724.
36. Chiapperino D., Kroth H., Kramarczuk I.H., Sayer J.M., Masutani C., Hanaoka F., Jerina D.M., Cheh A.M. Preferential misincorporation of purine nucleotides by human DNA polymerase η opposite benzo[a]pyrene 7,8-diol-9,10-epoxide-deoxyguanosine adducts. J. Biol. Chem. 277:2002;11765-11771.
37. Guo D., Wu X., Rajpal D.K., Taylor J.S., Wang Z. Translesion synthesis by yeast DNA polymerase ζ from templates containing lesions of ultraviolet radiation and acetylaminofluorene. Nucleic Acids Res. 29:2001;2875-2883.
38. Masutani C., Kusumoto R., Iwai S., Hanaoka F. Mechanisms of accurate translesion synthesis by human DNA polymerase η EMBO J. 19:2000;3100-3109.
39. Ohashi E., Ogi T., Kusumoto R., Iwai S., Masutani C., Hanaoka F., Ohmori H. Error-prone bypass of certain DNA lesions by the human DNA polymerase κ Genes Dev. 14:2000;1589-1594.
40. Zhang Y., Yuan F., Wu X., Taylor J.S., Wang Z. Response of human DNA polymerase ι to DNA lesions. Nucleic Acids Res. 29:2001;928-935.
41. Johnson R.E., Kondratick C.M., Prakash S., Prakash L. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science. 285:1999;263-265.
42. Murakumo Y., Roth T., Ishii H., Rasio D., Numata S., Croce C.M., Fishel R. A human REV7 homolog that interacts with the polymerase ζ catalytic subunit hREV3 and the spindle assembly checkpoint protein hMAD2. J. Biol. Chem. 275:2000;4391-4397.
43. Watanabe M., Maher V.M., McCormick J.J. Excision repair of UV- or benzo[a]pyrene diol epoxide-induced lesions in xeroderma pigmentosum variant cells is 'error free'. Mutat. Res. 146:1985;285-294.
44. Cordeiro-Stone M., Boyer J.C., Smith B.A., Kaufmann W.K. Xeroderma pigmentosum variant and normal fibroblasts show the same response to the inhibition of DNA replication by benzo[a]pyrene diol epoxide-I. Carcinogenesis. 7:1986;1783-1786.
45. Lin W., Wu X., Wang Z. A full-length cDNA of hREV3 is predicted to encode DNA polymerase ζ for damage-induced mutagenesis in humans. Mutat. Res. 433:1999;89-98.
46. Xiao W., Lechcer T., Chow B.L., Fontanie T., Agustus M., Carter K.C., Wei Y.F. Identification, chromosomal mapping and tissue-specific expression of hREV3 encoding a putative human DNA polymerase ζ Carcinogenesis. 19:1998;945-949.
47. McDonald J.P., Rapic-Otrin V., Epstein J.A., Broughton B.C., Wang X., Lehmann A.R., Wolgemuth D.J., Woodgate R. Novel human and mouse homologs of Saccharomyces cerevisiae DNA polymerase η Genomics. 60:1999;20-30.
48. Gerlach V.L., Aravind L., Gotway G., Schultz R.A., Koonin E.V., Friedberg E.C. Human and mouse homologs of Escherichia coli DinB (DNA polymerase IV), members of the UmuC/DinB superfamily. Proc. Natl. Acad. Sci. U.S.A. 96:1999;11922-11927.