Identification and quantification of DNA adducts in the oral tissues of mice treated with the environmental carcinogen dibenzo[ a,l ]pyrene by HPLC-MS/MS

Chemical Research in Toxicology

Volumn 24, Issue 8, 2011, Pages 1297-1303

  Zhang, Shang Min ^a   Chen, Kun Ming ^a   Aliaga, Cesar ^a   Sun, Yuan Wan ^a   Lin, Jyh Ming ^a   Sharma, Arun K ^a   Amin, Shantu ^a   El Bayoumy, Karam ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGEN; DIBENZO[A,L]PYRENE; DNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALIBRATION; CIRCULAR DICHROISM; DNA ADDUCT; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLIC ACTIVATION; MOUSE; MOUTH; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; STEREOCHEMISTRY; STEREOISOMERISM; TOXICITY TESTING;

ANIMALS; BENZOPYRENES; CARCINOGENS, ENVIRONMENTAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CIRCULAR DICHROISM; DNA; DNA ADDUCTS; EPOXY COMPOUNDS; FEMALE; MICE; MOUTH MUCOSA; STEREOISOMERISM; TANDEM MASS SPECTROMETRY;

ANIMALIA; MUS; NICOTIANA TABACUM;

EID: 80051779963     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx200188j     Document Type: Article

References (42)

1. International Agency for Research on Cancer (IARC) (2010) Globocan (2008): cancer incidence and mortality worldwide in 2008, http://globocan.iarc. fr/.
2. Warnakulasuriya, S. (2009) Global epidemiology of oral and oropharyngeal cancer Oral Oncol. 45, 309-316
3. Hecht, S. S. (2003) Tobacco carcinogens, their biomarkers and tobacco-induced cancer Nat. Rev. Cancer 3, 733-744 (Pubitemid 37328812)
4. Wogan, G. N., Hecht, S. S., Felton, J. S., Conney, A. H., and Loeb, L. A. (2004) Environmental and chemical carcinogenesis Semin. Cancer Biol. 14, 473-486 (Pubitemid 39360995)
5. Harvey, R. G. (1991) Polycyclic Aromatic Hydrocarbons: Chemistry and Carcinogenicity, Cambridge University Press, Cambridge, England.
6. Krzeminski, J., Lin, J. M., Amin, S., and Hecht, S. S. (1994) Synthesis of Fjord region diol epoxides as potential ultimate carcinogens of dibenzo[ a,l ]pyrene Chem. Res. Toxicol. 7, 125-129 (Pubitemid 24105341)
7. Luch, A. (2009) On the impact of the molecule structure in chemical carcinogenesis EXS 99, 151-179
8. 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 (Pubitemid 28285594)
9. Snook, M. E., Severson, R. F., Arrendale, R. F., Higman, H. C., and Chortyk, O. T. (1977) Identification of high molecular-weight polynuclear aromatic-hydrocarbons in a biologically-active fraction of cigarette-smoke condensate Beitrage Zur Tabakforschung Int. 9, 79-101
10. Guttenplan, J., Kosinska, W., Zhao, Z. L., Chen, K. M., Aliaga, C., DelTondo, J., Cooper, T., Sun, Y. W., Zhang, S. M., Jiang, K., Bruggeman, R., Sharma, A., Shantu, A., Ahn, K., and El-Bayoumy, K. Mutagenesis and carcinogenesis induced by dibenzo[ a,l ]pyrene in the mouse oral cavity: A potential new model for oral cancer. Int. J. Cancer 2011, in press.
11. International Agency for Research on Cancer (2010) Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures, in IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 92, pp 35-818, IARC, Lyon, France.
12. Yoon, 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-11,12-diol-13,14-epoxides in mouse cells Cancer Res. 64, 7321-7328 (Pubitemid 39372070)
13. Prahalad, A. K., Ross, J. A., Nelson, G. B., Roop, B. C., King, L. C., Nesnow, S., and Mass, M. J. (1997) Dibenzo[ a,l ]pyrene-induced DNA adduction, tumorigenicity, and Ki-ras oncogene mutations in strain A/J mouse lung Carcinogenesis 18, 1955-1963 (Pubitemid 28132381)
14. 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, benzo[ g ]chrysene and dibenzo[ a,l ]pyrene Carcinogenesis 16, 1971-1974
15. Buters, J. T., Mahadevan, B., Quintanilla-Martinez, L., Gonzalez, F. J., Greim, H., Baird, W. M., and Luch, A. (2002) Cytochrome P450 1B1 determines susceptibility to dibenzo[ a,l ]pyrene-induced tumor formation Chem. Res. Toxicol. 15, 1127-1135
16. Cai, Y., Wang, L., Ding, S., Schwaid, A., Geacintov, N. E., and Broyde, S. (2010) A bulky DNA lesion derived from a highly potent polycyclic aromatic tumorigen stabilizes nucleosome core particle structure Biochemistry 49, 9943-9945
17. Geacintov, N. E., Cosman, M., Hingerty, B. E., Amin, S., Broyde, S., and Patel, D. J. (1997) NMR solution structures of stereoisometric covalent polycyclic aromatic carcinogen-DNA adduct: principles, patterns, and diversity Chem. Res. Toxicol. 10, 111-146 (Pubitemid 27091881)
18. Mahadevan, B., Luch, A., Bravo, C. F., Atkin, J., Steppan, L. B., Pereira, C., Kerkvliet, N. I., and Baird, W. M. (2005) Dibenzo[ a,l ]pyrene induced DNA adduct formation in lung tissue in vivo Cancer Lett. 227, 25-32 (Pubitemid 41033089)
19. Melendez-Colon, V. J., Luch, A., Seidel, A., and Baird, W. M. (1999) Cancer initiation by polycyclic aromatic hydrocarbons results from formation of stable DNA adducts rather than apurinic sites Carcinogenesis 20, 1885-1891 (Pubitemid 29476112)
20. Sharma, A. K., Kumar, S., and Amin, S. (2004) A highly abbreviated synthesis of dibenzo[ def,p ]chrysene and its 12-methoxy derivative, a key precursor for the synthesis of the proximate and ultimate carcinogens of dibenzo[ def,p ]chrysene J. Org. Chem. 69, 3979-3982 (Pubitemid 38668265)
21. Li, K. M., George, M., Gross, M. L., Seidel, A., Luch, A., Rogan, E. G., and Cavalieri, E. L. (1999) Structure elucidation of the adducts formed by fjord-region dibenzo[ a,l ]pyrene 11,12-dihydrodiol 13,14-epoxides and deoxyadenosine Chem. Res. Toxicol. 12, 758-767 (Pubitemid 29451160)
22. Sundberg, K., Dreij, K., Seidel, A., and Jernstrom, B. (2002) Glutathione conjugation and DNA adduct formation of dibenzo[ a,l ]pyrene and benzo[ a ]pyrene diol epoxides in V79 cells stably expressing different human glutathione transferases Chem. Res. Toxicol. 15, 170-179 (Pubitemid 34163797)
23. Delclos, K. B., Miller, D. W., Lay, J. O., Jr., Casciano, D. A., Walker, R. P., Fu, P. P., and Kadlubar, F. F. (1987) Identification of C8-modified deoxyinosine and N2- and C8-modified deoxyguanosine as major products of the in vitro reaction of N-hydroxy-6-aminochrysene with DNA and the formation of these adducts in isolated rat hepatocytes treated with 6-nitrochrysene and 6-aminochrysene Carcinogenesis 8, 1703-1709
24. Singh, R., Gaskell, M., Le Pla, R. C., Kaur, B., zim-Araghi, A., Roach, J., Koukouves, G., Souliotis, V. L., Kyrtopoulos, S. A., and Farmer, P. B. (2006) Detection and quantitation of benzo[ a ]pyrene-derived DNA adducts in mouse liver by liquid chromatography-tandem mass spectrometry: comparison with 32P-postlabeling Chem. Res. Toxicol. 19, 868-878 (Pubitemid 43939066)
25. Yagi, H., Frank, H., Seidel, A., and Jerina, D. M. (2008) Revised assignment of absolute configuration of the cis- and trans-N6-deoxyadenosine adducts at C14 of (±)-11beta,12alpha-dihydroxy-13alpha,14alpha-epoxy-11, 12,13,14-tetrahydr -odibenzo[ a,l ]pyrene by stereoselective synthesis Chem. Res. Toxicol. 21, 2379-2392
26. Szeliga, J. and Dipple, A. (1998) DNA adduct formation by polycyclic aromatic hydrocarbon dihydrodiol epoxides Chem. Res. Toxicol. 11, 1-11 (Pubitemid 28065267)
27. Sayer, J. M., Chadha, A., Agarwal, 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
28. Agarwal, S. K., Sayer, J. M., Yeh, H. J. C., Pannell, L. K., Hilton, B. D., Pigott, M. A., Dipple, A., Yagi, H., and Jerina, D. M. (1987) Chemical characterization of DNA adducts derived from the configurationally isomeric benzo[ c ]phenanthrene-3,4-diol 1,2-epoxides J. Am. Chem. Soc. 109, 2497-2504
29. Ruan, Q., Kolbanovskiy, A., Zhuang, P., Chen, J., Krzeminski, J., Amin, S., and Geacintov, N. E. (2002) Synthesis and characterization of site-specific and stereoisomeric fjord dibenzo[ a,l ]pyrene diol epoxide-N(6)-adenine adducts: unusual thermal stabilization of modified DNA duplexes Chem. Res. Toxicol. 15, 249-261 (Pubitemid 34163806)
30. Ralston, S. L., Seidel, A., Luch, A., Platt, K. L., and Baird, W. M. (1995) Stereoselective activation of dibenzo[ a,l ]pyrene to (-)-anti (11R,12S,13S,14R)- and (+)-syn(11S,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
31. Melendez-Colon, V. J., Luch, A., Seidel, A., and Baird, W. M. (2000) Formation of stable DNA adducts and apurinic sites upon metabolic activation of bay and fjord region polycyclic aromatic hydrocarbons in human cell cultures Chem. Res. Toxicol. 13, 10-17 (Pubitemid 30055953)
32. Mahadevan, B., Marston, C. P., Luch, A., Dashwood, W. M., Brooks, E., Pereira, C., Doehmer, J., and Baird, W. M. (2007) Competitive inhibition of carcinogen-activating CYP1A1 and CYP1B1 enzymes by a standardized complex mixture of PAH extracted from coal tar Int. J. Cancer 120, 1161-1168
33. Nesnow, S., Davis, C., Nelson, G., Ross, J. A., Allison, J., Adams, L., and King, L. C. (1997) Comparison of the morphological transforming activities of dibenzo[ a,l ]pyrene and benzo[ a ]pyrene in C3H10T1/2CL8 cells and characterization of the dibenzo[ a,l ]pyrene-DNA adducts Carcinogenesis 18, 1973-1978 (Pubitemid 28132383)
34. Shimada, T. and Fujii-Kuriyama, Y. (2004) Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1 Cancer Sci. 95, 1-6 (Pubitemid 38208399)
35. Courter, L. A., Musafia-Jeknic, T., Fischer, K., Bildfell, R., Giovanini, J., Pereira, C., and Baird, W. M. (2007) Urban dust particulate matter alters PAH-induced carcinogenesis by inhibition of CYP1A1 and CYP1B1 Toxicol. Sci. 95, 63-73 (Pubitemid 44942777)
36. Sancar, A. (1996) DNA excision repair Annu. Rev. Biochem. 65, 43-81 (Pubitemid 26250604)
37. Wood, R. D. (1999) DNA damage recognition during nucleotide excision repair in mammalian cells Biochimie 81, 39-44
38. 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 (Pubitemid 30207643)
39. Cai, Y., Ding, S., Geacintov, N. E., and Broyde, S. (2011) Intercalative Conformations of the 14R (+)- and 14S (-)-trans-anti-DB[ a,l ]P-N(6)-dA Adducts: Molecular Modeling and MD Simulations Chem. Res. Toxicol. 24, 522-531
40. Kropachev, K., Kolbanovskiy, M., Rodriguez, F. A., Cai, Y., Ding, S., Zhang, L., Amin, S., Broyde, S., and Geacintov, N. E. (2009) Dibenzo[ a,l ]pyrene diol epoxide-adenine but not -guanine adducts are resistant to nucleotide excision repair in human cell extracts. From Abstracts of Papers, 238th ACS National Meeting, Washington, DC Chem. Res. Toxicol. 23, 282
41. Roth, R. B., Amin, S., Geacintov, N. E., and Scicchitano, D. A. (2001) Bacteriophage T7 RNA polymerase transcription elongation is inhibited by site-specific, stereospecific benzo[ c ]phenanthrene diol epoxide DNA lesions Biochemistry 40, 5200-5207 (Pubitemid 32374002)
42. Dreij, K., Seidel, A., and Jernstrom, B. (2005) Differential removal of DNA adducts derived from anti-diol epoxides of dibenzo[ a,l ]pyrene and benzo[ a ]pyrene in human cells Chem. Res. Toxicol. 18, 655-664 (Pubitemid 40563279)