Sequence specific mutagenesis of the major (+)-anti-benzo[a]pyrene diol epoxide-DNA adduct at a mutational hot spot in vitro and in Escherichia coli cells

Chemical Research in Toxicology

Volumn 10, Issue 4, 1997, Pages 369-377

  Hanrahan, Christopher J ^a   Bacolod, Manny D ^a   Vyas, Rajeev R ^a   Liu, Tongming ^b   Geacintov, Nicholas E ^b   Loechler, Edward L ^c   Basu, Ashis K ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROXYBENZO[A]PYRENE OXIDE; DNA;

ARTICLE; CELL VIABILITY; DNA ADDUCT; DNA REPLICATION; DNA SEQUENCE; DNA SYNTHESIS INHIBITION; ESCHERICHIA COLI; GENETIC TRANSFORMATION; GENOTOXICITY; MUTAGENESIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; BACTERIOPHAGE M13; DNA ADDUCTS; DNA REPLICATION; ESCHERICHIA COLI; GENOME, VIRAL; MUTAGENESIS, SITE-DIRECTED; MUTAGENS;

ESCHERICHIA COLI;

EID: 0030911969     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx9601925     Document Type: Article

References (44)

1. Harvey, R. G. (1991) Polycyclic aromatic hydrocarbons: Chemistry and cancer, Cambridge University Press, Cambridge, U.K.
2. Sims, P., Grover, P. L., Swaisland, A., Pal, K., and Hewer, A. (1974) Metabolic activation of benzo[a]pyrene proceeds by a diolepoxide. Nature 252, 326-328.
3. Yang, S. K., McCourt, D. W., Roller, P. P., and Gelboin, H. V. (1976) Enzymatic conversion of benzo[a]pyrene leading predominantly to the diol-epoxide r-7,t-8-dihydroxy-t-9,10-oxy-7,8,9,10-tetrahydobenzo[a]pyrene through a single enantiomer of r-7,t-8-dihydroxy-7,8-dihydobenzo[a]pyrene. Proc. Natl. Acad. Sci. U.S.A. 73, 2594-2598.
4. Kapitulnik, J., Wislocki, P. G., Levin, W., Yagi, H., Thakker, D. R., Akagi, H., Koreeda, M., Jerina, M., and Conney, A. H. (1978) Marked differences in the carcinogenic activity of optically pure (+)-and (-)-trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene in newborn mice. Cancer Res. 38, 2661-2665.
5. Thakker, D. R., Yagi, H., Lu, A. Y. H., Levin, W., Conney, A. H., and Jerina, D. M. (1976) Metabolism of benzo[a]pyrene. IV. Conversion of (±)-trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene to the highly mutagenic 7,8-diol-9,10-epoxides. Proc. Natl. Acad. Sci. U.S.A. 73, 3381-3385.
6. Buening, M. K., Wislocki, P. G., Levin, W., Yagi, H., Thakker, D. R., Akagi, H., Koreeda, M., Jerina, D. M., and Conney, A. H. (1978) 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, 5358-5361.
7. Slaga, T. J., Bracken, W. J., Gleason, G., Levin, W., Yagi, H., Jerina, D. M., and Conney, A. H. (1979) 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, 67-71.
8. Wood, A. W., Chang, R. L., Levin, W., Yagi, H., Thakker, D. R., Jerina, D. M., and Conney, A. H. (1977) Differences in mutagenicity of the optical enantiomers of the diastereomeric benzo[a]-pyrene 7,8-diol-9,10-epoxides. Biochem. Biophys. Res. Commun. 77, 1389-1396.
9. Brookes, P., and Osborne, M. R. (1982) Mutation in mammalian cells by stereoisomers of anti-benzo[a]pyrene diol epoxide in relation to the extent and nature of the DNA reaction product. Cardnogenesis 3, 1223-1226.
10. Burgess, J. A., Stevens, C. W., and Fahl, W. E. (1985) Mutation at separate gene loci in Salmonella typhimurium TA 100 related to DNA nucleotide modification by stereoisomeric benzo[a]pyrene 7,8-diol-9,10-epoxides. Cancer Res. 45, 4257-4262.
11. Stevens, C. W., Bouck, N., Burgess, J. A., and Fahl, W. E. (1985) Benzo[a]pyrene diol epoxide: different mutagenic efficiency in human and bacterial cells. Mutat. Res. 152, 5.
12. Weinstein, I. B., Jeffrey, A. M., Jennette, K. W., Blobstein, S. H., Harvey, R. G., Harris, C., Autrup, H., Kasai, H., and Nakanishi, K. (1976) Benzo[a]pyrene diol epoxides as intermediates in nucleic acid binding in vitro and in vivo. Science 193, 592-594.
13. Jeffrey, A. M., Jennette, K. W., Blobstein, S. H., Weinstein, I. B., Beland, F. A., Harvey, R. G., Kasai, H., Miura, I., and Nakanishi, K. (1976) Benzo[a]pyrene-nucleic acid derivative found in vivo: Structure of a benzo[a]pyrenetetrahydrodiol epoxide-guanosine adduct. J. Am. Chem. Soc. 98, 5714-5715.
14. Osborne, M. R., Beland, F. A., Harvey, R. G., and Brookes, P. (1976) The reaction of (±)-7α,8β-dihydroxy-9β,10β-epoxy-7,8,9,10- tetrahydrobenzo[a]pyrene with DNA. Int. J. Cancer 18, 362-368.
15. Osborne, M. R., Harvey, R. G., and Brookes, P. (1978) The reaction of trans-7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo-[a]pyrene with DNA involves attack at the N7-position of guanine moeities. Chem.-Biol. Interact. 20, 123-130.
16. Cheng, S. C., Hilton, B. D., Roman, J. M., and Dipple, A. (1989) DNA adducts from carcinogenic and noncarcinogenic enantiomers of benzo[a]pyrene dihydrodiol epoxide. Chem. Res. Toxicol. 2, 334-340.
17. Sayer, J. M., Chadha, A., Agarwal, H. S. K., Yeh, H. J. C., Yagi, H., and Jerina, D. M. (1991) 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, 20-29.
18. Eisenstadt, E., Warren, J., Porter, J., Atkins, D., and Miller, J. H. (1982) Carcinogenic epoxides of benzo[a]pyrene and cyclopenta[cd]pyrene induce base substitutions via specific transversions. Proc. Natl. Acad. Sci. U.S.A. 79, 1945-1949.
19. Yang, J.-L., Mahar, V. M., and McCormick, J. J. (1987) Kinds of mutations formed when a shuttle vector containing adducts of (±)-7β,8α-dihydroxy-9α,10α-epoxy-7,8,9,10- tetrahydrobezo[a]pyrene replicates in human cells. Proc. Natl. Acad. Sci. U.S.A. 84, 3787-3791.
20. Chen, R.-H., Mahar, V. M., and McCormick, J. J. (1990) Effects of excision repair by diploid human fibroblasts on the kinds and locations of mutations induced by (+/-)-7β,8α-dihydroxy-9α,10α-epoxy-7,8,9,10- tetrahydrobenzo[a]pyrene in the coding region of HPRT gene. Proc. Natl. Acad. Sci., U.S.A. 87, 8680-8684.
21. Wei, S.-J. C., Chang, R. L., Wong, C.-Q., Bhachech, N., Cui, X. X., Hennig, E., Yagi, H., Sayer, S. M., Jerina, D. M., Preston, B. D., and Conney, A. H. (1991) Dose-dependent differences in the profile of mutations induced by an ultimate carcinogen from benzo[a]pyrene. Proc. Natl. Acad. Sci. U.S.A. 88, 11227-11230.
22. Wei, S.-J. C., Chang, R. L., Bhachech, N., Cui, X. X., Merkler, K. A., Wong, C.-Q., Hennig, E., Yagi, H., Sayer, S. M., Jerina, D. M., and Conney, A. H. (1993) Dose-dependent differences in the profile of mutations induced by (+)-7R,8S-dihydroxy-9S,10R-epoxy-7,8,9,10-tetrahydrobezo[a]pyrene in the coding region of the hypoxanthine (guanine) phosphoribosyltransferase gene in Chinese hamster V79 cells. Cancer Res. 53, 3294-3301.
23. Rodriguez, H., and Loechler, E. L. (1993) Mutational specificity of the (+)-anti-diol epoxide of benzo[a]pyrene in a supF gene of an Escherichia coli plasmid: DNA sequence context influences hot spots, mutagenic specificity and the extent of SOS enhancement of mutagenesis. Carcinogenesis 14, 373-383.
24. Rodriguez, H., and Loechler, E. L. (1993) Mutagenesis by the (+)-anti-dial epoxide of benzo[a]pyrene: What controls mutagenic specifity? Biochemistry 32, 1759-1769.
25. Basu, A. K., and Essigmann, J. M. (1988) Site-specifically modified oligodeoxynucleotides as probes for the structural and biological effects of DNA damaging agents. Chem. Res. Toxicol. 1, 1-18.
26. Singer, B., and Essigmann, J. M. (1991) Site-specific mutagenesis: retrospective and prospective. Carcinogenesis 12, 949-955.
27. Loechler, E. L. (1996) The role of adduct site-specific mutagenesis in understanding how carcinogen-DNA adducts cause mutations: perspective, prospects and problems. Carcinogenesis 17, 895-902.
28. 2-Gua, the major adduct of activated benzo[a]pyrene, when studied in an Escherichia coli plasmid using site-directed methods. Carcinogenesis 13, 1415-1425.
29. Hruszkewycz, A. M., Canella, K. A., Peltonen, K., Kotrappa, L., and Dipple, A. (1992) DNA polymerase action on benzo[a]pyrene-DNA adducts. Carcinogenesis 13, 2347-2352.
30. Shibutani, S., Margulis, L. A., Geacintov, N. E., and Grollman, A. P. (1993) Translesional synthesis on a DNA template containing a single stereoisomer of dG-(+)-and dG-(-)-anti-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene). Biochemistry 32, 7531-7541.
31. 2-Gua adduct of the (+)-anti-benzo[a]pyrene diol epoxide is capable of inducing G → A and G → C, in addition to G → T, mutations. Biochemistry 34, 13545-13553.
32. 3 sequence: Effects of SOS, proofreading, and mismatch repair. Biochemistry 35, 4568-4577.
33. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) In Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Basu, A. K., Hanrahan, C. J., Malia, S. A., Kumar, S., Bizanek, R., and Tomasz, M. (1993) Effect of site-specifically located mitomycin C-DNA monoadducts on in vitro DNA synthesis by DNA polymerases. Biochemistry 32, 4708-4718.
35. Boosalis, M. S., Petruska, J., and Goodman, M. F. (1987) DNA polymerase insertion fidelity: Gel assay for site-specific kinetics. J. Biol. Chem. 262, 14689-14696.
36. Clark, J. M. (1988) Novel non-templated nucleotide addition reactions catalyzed by procaryotic and eucaryotic DNA polymerases. Nucleic Acids Res. 16, 9677-9686.
37. Moore, P. D., Bose, K. K., Rabkin, S. D., and Strauss, B. S. (1981) Sites of termination of in vitro DNA synthesis on ultraviolet-and N-acetylaminofluorene-treated φx 174 templates by prokaryotic and eukaryotic DNA polymerases. Proc. Natl. Acad. Sci. U.S.A. 78, 110-114.
38. Strauss, B. S., Rabkin, S., Sagher, D., and Moore, P. (1982) The role of DNA polymerase in base substitution mutagenesis on non-instructional templates Biochimie 64, 829-838.
39. Strauss, B. S. (1985) Translesion DNA synthesis: polymerase response to altered nucleotides. Cancer Surv. 4, 493-516.
40. Banerjee, S. K., Christensen, R. B., Lawrence, C. W., and LeClerc, J. E. (1988) Frequency and spectrum of mutations produced by a single cis-syn thymine-thymine cylobutane dimer in a single-stranded vector. Proc. Natl. Acad. Sci. U.S.A. 85, 8141-8145.
41. Lawrence, C. W., Borden, A., Banerjee, S. K., and LeClerc, J. E. (1990) Mutation frequency and spectrum resulting from a single abasic site in a single-stranded vector. Nucleic Acids Res. 18, 2153-2157.
42. Cosman, M., de los Santos, C., Fiala, R., Hingerty, B. E., Singh, S., Ibanez, V., Margulis, L., Live, D., Geacintov, N. E., Broyde, S., and Patel, D. J. (1992) Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[a]pyrene diol epoxide and DNA. Proc. Natl. Acad. Sci. U.S.A. 89, 1914-1918.
43. 6 at the second position of N-ras codon 61. J. Biol. Chem. 270, 4990-5000.
44. Moriya, M., Spiegel, S., Farnandes, A., Amin, S., Liu, T., Geacintov, N., and Grollman, A. P. (1995) Fidelity of translesional synthesis past benzo[a]pyrene diol epoxide-2′-deoxyguanosine DNA adducts: marked effects of host cell, sequence context and chirality. Biochemistry 35, 16646-16651.