Formation and differential repair of covalent DNA adducts generated by treatment of human cells with (±)-anti-dibenzo[a,l]pyrene-ll,12-diol-13, 14-epoxide

Chemical Research in Toxicology

Volumn 22, Issue 1, 2009, Pages 81-89

  Spencer, Wendy A ^a   Singh, Jaya ^a   Orren, David K ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE 3' PHOSPHATE; CARCINOGEN; CELL DNA; DIBENZO [A,L]PYRENE 11,12 DIOL 13,14 EPOXIDE; DIBENZO(A,L)PYRENE; EPOXIDE; GUANOSINE PHOSPHATE; NUCLEOTIDE; PYRENE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CARCINOGENIC ACTIVITY; CELL LINE; CHROMATOGRAPHY; CULTURE MEDIUM; DNA ADDUCT; DNA REPLICATION; DNA SYNTHESIS; EXCISION REPAIR; HUMAN; HUMAN CELL; METABOLITE;

BENZOPYRENES; CARCINOGENS; CELLS, CULTURED; CHROMATOGRAPHY, THIN LAYER; DNA ADDUCTS; DNA REPAIR; EPOXY COMPOUNDS; HUMANS; TIME FACTORS;

RODENTIA;

EID: 61849169467     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx8001675     Document Type: Article

References (54)

1. Xue, W., and Warshawsky, D. (2005) Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: 1 review. Toxicol. Appl. Pharmacol. 206, 73-93.
2. Sharma, R. A., and Farmer, R. B. (2004) Biological relevance of adduct detection to the chemoprevention of cancer. Clin. Cancer Res. 10, 4901-4912.
3. Kozin, I. S., Gooijer, C., and Velthorst, N. H. (1995) Direct determination of dibenzo[a,l]pyrene in crude extracts of environmental samples by laser-excited shpol'skii spectroscopy. Anal. Chem. 67, 1623-1626.
4. Cavalieri, E. L., Higginbotham, S., Ramakrishna, N. V., Devanesan, P. D., Todorovic, R., Rogan, E. G., and Salmasi, S. (1991) Comparative dose-response tumorigenicity studies of dibenzo[a,l]pyrene versus 7,12-dimethylbenz[a] anthracene, benzo[a]pyrene and two diben-zo[a,l]pyrene dihydrodiols in mouse skin and rat mammary gland. Carcinogenesis 12, 1939-1944.
5. Higginbotham, S., Ramakrishna, N. V., Johansson, S. L., Rogan, E. G., and Cavalieri, E. L. (1993) Tumor-initiating activity and carcinogenicity of dibenzo[a,l]pyrene versus 7,12-dimethylbenz[a]anthracene and benzo[a]pyrene at low doses in mouse skin. Carcinogenesis 14, 875-878.
6. LaVoie, E. J., He, Z. M., Meegalla, R. L., and Weyand, E. H. (1993) Exceptional tumor-initiating activity of 4-fluorobenzo[j]fluoranthene on mouse skin: Comparison with benzo[j]fluoranthene, 10-fluoro-benzo[j] fluoranthene, benzo[a]pyrene, dibenzo[a,l]pyrene and 7,12dim-ethylbenz[a] anthracene. Cancer Lett. 70, 7-14.
7. Arif, J. M., and Gupta, R. C. (1997) Tissue distribution of DNA adducts in rats treated by intramammillary injection with dibenzo[a,l]pyrene, 7,12 dimethylbenz[a]anthracene and benzo[a]pyrene. Mutat. Res. 378, 31-39.
8. Whitlock, J. P., Jr. (1990) Genetic and molecular aspects of 2,3,7,8-tetrachlorodibenzo-p-dioxin action. Annu. Rev. Pharmacol. Toxicol. 30, 251-277.
9. Whitlock, J. P., Jr., Okino, S. T., Dong, L., Ko, H. P., Clarke-Katzenberg, Q. M., and Li, H. (1996) Cytochromes P450 5: Induction of cytochrome P4501A1: a model for analyzing mammalian gene transcription. FASEB J. 10, 809-818.
10. Shimada, T., Yun, C. H., Yamazaki, H., Gautier, J. C., Beaune, P. H., and Guengerich, F. P. (1992) Characterization of human lung microsomal cytochrome P-450 1A1 and its role in the oxidation of chemical carcinogens. Mol. Pharmacol. 41, 856-864.
11. Shimada, T., Hayes, C. L., Yamazaki, H., Amin, S., Hecht, S. S., Guengerich, F. P., and Sutter, T. R. (1996) Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 56, 2979-2984.
12. Christou, M., Sayas, U., Spink, D. C., Gierthy, J. F., and Jefcoate, C. R. (1994) Co-expression of human CYP1A1 and a human analog of cytochrome P450-EF in response to 2,3,7,8-tetrachloro-dibenzo-p-dioxin in the human mammary carcinoma-derived MCF-7 cells. Carcinogenesis 15, 725-732.
13. Luch, A., Coffing, S. L., Tang, Y. M., Schneider, A., Soballa, V., Greim, H., Jefcoate, C. R., Seidel, A., Greenlee, W. F., Baird, W. M., and Doehmer, J. (1998) Stable expression of human cytochrome P450 1B1 in V79 Chinese hamster cells and metabolically catalyzed DNA adduct formation of dibenzo[a,l]pyrene. Chem. Res. Toxicol. 11, 686-695.
14. Shou, M., Krausz, K. W., Gonzalez, F. J., and Gelboin, H. V. (1996) Metabolic activation of the potent carcinogen dibenzo[a,l]pyrene by human recombinant cytochromes P450, lung and liver microsomes. Carcinogenesis 17, 2429-2433.
15. Ralston, S. L., Lau, H. H., Seidel, A., Luch, A., Plattand, K. L., and Baird, W. M. (1994) The potent carcinogen dibenzo[a,l]pyrene is metabolically activated to fjord-region 11,12-dioI 13,14-epoxides in human mammary carcinoma MCF-7 cell cultures. Cancer Res. 54, 887-890.
16. Ralston, S. L., Seidel, A., Luch, A., Piatt, K. L., and Baird, W. M. (1995) Stereoselective activation of dibenzo[a,l]pyrene to (-)- anti(llR,12S,13S,14R)- and (+)-syn(l1S,12R,13S,14R)-11,12-diol-13,14-epoxides which bind extensively to deoxyadenosine residues of DNA in the human mammary carcinoma cell line MCF-7. Carcinogenesis 16, 2899-2907.
17. Luch, A., Glatt, H., Piatt, K. L., Oesch, F., and Seidel, A. (1994) Synthesis and mutagenicity of the diastereomeric fjord-region 11,12-dihydrodiol 13,14-epoxides of dibenzo[a,l]pyrene. Carcinogenesis 11, 2507-2516.
18. Amin, S., Krzeminski, J., Rivenson, A., Kurtzke, C., Hecht, S. S., and el-Bayoumy, K. (1995) Mammary carcinogenicity in female CD rats of fjord region diol epoxides of benzo[c]phenanthrene, ben-zo[g]chrysene and dibenzo[a,l]pyrene. Carcinogenesis 8, 1971-1974.
19. Amin, S., Desai, D., Dai, W., Harvey, R. G., and Hecht, S. S. (1995) Tumorigenicity in newborn mice of fjord region and other sterically hindered diol epoxides of benzo[g]chrysene, dibenzo[a,l]pyrene (diben-zo[def,p]chrysene), 4H-cyclopenta[def]chrysene and fluoranthene. Carcinogenesis 11, 2813-2817.
20. Sancar, A. (1996) DNA excision repair. Annu. Rev. Biochem. 65, 43-81.
21. Wood, R. D. (1999) DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie 81, 39-44.
22. Sancar, A. (1995) DNA repair in humans. Annu. Rev. Genet. 29, 69-105.
23. Friedberg, E. C., Bardwell, A. J., Bardwell, L., Feaver, W. J., Romberg, R. D., Svejstrup, J. Q., Tomkinson, A. E., and Wang, Z. (1995) Nucleotide excision repair in the yeast Saccharomyces cerevisiae: Its relationship to specialized mitotic recombination and RNA polymerase II basal transcription. Philos. Trans. R. Soc. London B. Biol. Sci. 347, 63-68.
24. Batty, D. P., and Wood, R. D. (2000) Damage recognition in nucleotide excision repair of DNA. Gene 241, 193-204.
25. Hess, M. T., Gunz, D., Luneva, N., Geacintov, N. E., and Naegeli, H. (1997) Base pair conformation-dependent excision of benzo[a]pyrene diol epoxide-guanine adducts by human nucleotide excision repair enzymes. Mol. Cell. Biol. 17, 7069-7076.
26. Buterin, T., Hess, M. T., Luneva, N., Geacintov, N. E., Amin, S., Kroth, H., Seidel, A., and Naegeli, H. (2000) Unrepaired fjord region polycyclic aromatic hydrocarbon-DNA adducts in ras codon 61 mutational hot spots. Cancer Res. 60, 1849-1856.
27. 32P-postlabeling assay. Carcinogenesis 13, 1053-1074.
28. 32P-Postlabelling for detection of DNA adducts. In Technologies for Detection of DNA Damage and Mutations (Pfeifer, G. P., Eds.) pp 45-61, Plenum Press, New York.
29. Porter, P. C., Mellon, I., and States, J. C. (2005) XP-A cells complemented with Arg228Gln and Val234Leu polymorphic XPA alleles repair BPDE-induced DNA damage better than cells complemented with the wild type allele. DNA Repair 4, 341-349.
30. States, J. C., Quan, T., Hines, R. N., Novak, R. F., and Runge-Morris, M. (1993) Expression of human cytochrome P450 1A1 in DNA repair deficient and proficient human fibroblasts stably transformed with an inducible expression vector. Carcinogenesis 14, 1643-1649.
31. 32P- postlabeling. Carcinogenesis 18, 1999-2007.
32. Pfeifer, G. P., Denissenko, M. F., Olivier, M., Tretyakova, N., Hecht, S. S., and Hainaut, P. (2002) Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene 21, 7435-7451.
33. Peltonen, K., and Dipple, A. (1995) Polycyclic aromatic hydrocarbons: Chemistry of DNA adduct formation. J. Occup. Environ. Med. 37, 52-58.
34. Durant, J. L., Busby, W. F., Lafleur, A. L., Jr., Penman, B. W., and Crespi, C. L. (1996) Human cell mutagenicity of oxygenated, nitrated and unsubstituted polycyclic aromatic hydrocarbons associated with urban aerosols. Mutat. Res. 371, 123-157.
35. Costa, R. M., Chigancas, V., Galhardo, R. S., Carvalho, H., and Menck, C. F. (2003) The eukaryotic nucleotide excision repair pathway. Biochimie 85, 1083-1099.
36. Bergvall, C., and Westerholm, R. (2007) Identification and determination of highly carcinogenic dibenzopyrene isomers in air particulate samples from a street canyon, a rooftop, and a subway station in Stockholm. Environ. Sci. Technol. 41, 731-737.
37. Li, K. M., Todorovic, R., Rogan, E. G., Cavalieri, E. L., Ariese, F., Suh, M., Jankowiak, R., and Small, G. J. (1995) Identification and quantitation of dibenzo[a,l]pyrene-DNA adducts formed by rat liver microsomes in vitro: Preponderance of depurinating adducts. Biochemistry 34, 8043-8049.
38. Mahadevan, B., Luch, A., Bravo, C. F., Atkin, J., Steppan, L. B., Pereira, C., Kerkvliet, N. I., and Baird, W. M. (2005) Diben-zo[a,l] pyrene induced DNA adduct formation in lung tissue in vivo. Cancer Lett. 227, 25-32.
39. Dipple, A., Pigott, M. A., Agarwal, S. K., Yagi, H., Sayer, J. M., and Jerina, D. M. (1987) Optically active benzo[c]phenanthrene diol epoxides bind extensively to adenine in DNA. Nature 327, 535-536.
40. Jerina, D. M., Chadha, A. M., Schurdak, M. E., Wood, A. W., and Sayer, J. M. (1991) pp 533-553, Plenum Press, New York. Dipple, A., Ed. (1994) Vol. 125, pp 107-129, IARC Scientific Publishers, Lyon.
41. Li, K. M., Todorovic, R., Devanesan, P., Higginbotham, S., Köfeler, H., Ramanathan, R., Gross, M. L., Rogan, E. G., and Cavalieri, E. L. (2004) Metabolism and DNA binding studies of 4-hydroxyestradiol and estradiol-3,4-quinone in vitro and in female ACI rat mammary gland in vivo. Carcinogenesis 25, 289-297.
42. Todorovic, R., Devanesan, P., Rogan, E., and Cavalieri, E. (2005) Identification and quantification of stable DNA adducts formed from dibenzo[a,l]pyrene or its metabolites in vitro and in mouse skin and rat mammary gland. Chem. Res. Toxicol. 18, 984-990.
43. Dreij, K., Seidel, A., and Jerngtstrom, B. (2005) Differential removal of DNA adducts derived from anti-diol epoxides of dibenzo[a,l]pyrene and benzo[a]pyrene in human cell. Chem. Res. Toxicol. 18, 655-664.
44. Mahadevan, B., Dashwood, W.-M., Luch, A., Pecaj, A., Doehmer, J., Seidel, A., Pereira, C., and Baird, W. M. (2003) Mutations induced by (-)-anri-ll/U2S-dihydrodiol-13S,14R-epoxide of diben-zo[a,l]pyrene in the coding region of the hypoxanthine phosphoribo-syltransferase (Hprt) gene in Chinese hamster V79 cells. Environ. Mol. Mutagen. 41, 131-139.
45. Joon, J.-H., Besaratinia, A., Feng, Z., Tang, M.-S., Amin, S., Luch, A., and Pfeifer, G. P. (2004) DNA damage, repair, and mutation induction by (+)-syn and (-)-anti-dibenzo[a,l]pyrene-l l,12diol-13,14-epoxides in mouse cells. Cancer Res. 64, 7321-7328.
46. Suh, M., Ariese, F., Small, G. J., Jankowiak, R., Hewer, A., and Phillips, D. H. (1995) Formation and persistence of benzo[a]pyrene-DNA adducts in mouse epidermis in vivo: importance of adduct conformation. Carcinogenesis 16, 2561-2569.
47. 32P-postlabeling and fluorescence studies. Chem. Res. Toxicol. 11, 674-685.
48. Zhang, N., Lin, C., Huang, X., Kolbanovskiy, A., Hingerty, B. E., Amin, S., Broyde, S., Geacintov, N. E., and Patel, D. J. (2005) Methylation of cytosine at C5 in a CpG sequence context causes a conformational switch of a benzo[a]pyrene diol epoxide-N2-guanine adduct in DNA from a minor groove alignment to intercalation with base displacement. J. Mol. Biol. 346, 951-965.
49. Moyer, R., Marien, K., van Holde, K., and Bailey, G. (1989) Site-specific aflatoxin B adduction of sequence-positioned nucleosome core particles. J. Biol. Chem. 264, 12226-12231.
50. Seidman, M., Slor, H., and Bustin, M. (1983) The binding of a carcinogen to the nucleosomal and non-nucleosomal regions of the simian virus 40 chromosome in vivo. J. Biol. Chem. 258, 5215-5220.
51. Thrall, B. D., Mann, D. B., Smerdon, M. J., and Springer, D. L. (1994) Nucleosome structure modulates benzo[a]pyrenediol epoxide adduct formation. Biochemistry 33, 2210-2216.
52. Quan, T., and States, C. (1996) Preferential DNA damage in the p53 gene by benzo[a]pyrene metabolites in cytochrome P4501A1-expressing xeroderma pigmentosum group A cells. Mol. Carcinogen. 16, 32-43.
53. Obi, F. O., Ryan, A. J., and Billett, M. A. (1986) Preferential binding of the carcinogen benzo[a]pyrene to DNA in active chromatin and the nuclear matrix. Carcinogenesis 7, 907-913.
54. Goodman, M. F., and Tippin, B. (2000) The expanding polymerase universe. Nat. Rev. Mol. Cell. Biol. 1, 101-109.+