Analysis of O6-[4-(3-Pyridyl)-4-oxobut-1-yl]-2′-deoxyguanosine and Other DNA Adducts in Rats Treated with Enantiomeric or Racemic N′-Nitrosonornicotine

Chemical Research in Toxicology

Volumn 29, Issue 1, 2016, Pages 87-95

  Yang, Jing ^a   Villalta, Peter W ^a   Upadhyaya, Pramod ^a   Hecht, Stephen S ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGEN; DEOXYGUANOSINE; NITROSONORNICOTINE; DNA ADDUCT; N'-NITROSONORNICOTINE; NITROSAMINE; O(6)-(4-(3-PYRIDYL)-4-OXOBUT-1-YL)-2'-DEOXYGUANOSINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; COMPARATIVE STUDY; DNA ADDUCT; ENANTIOMER; ESOPHAGUS MUCOSA; LIMIT OF DETECTION; LIMIT OF QUANTITATION; LIQUID CHROMATOGRAPHY; MALE; MOUTH CAVITY; MOUTH MUCOSA; NONHUMAN; NOSE MUCOSA; OLFACTORY EPITHELIUM; RACEMIC MIXTURE; RAT; TANDEM MASS SPECTROMETRY; VALIDATION STUDY; ANALOGS AND DERIVATIVES; ANALYSIS; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; FISCHER 344 RAT; TISSUE DISTRIBUTION;

ANIMALS; DEOXYGUANOSINE; DNA ADDUCTS; MALE; MOLECULAR STRUCTURE; NITROSAMINES; RATS; RATS, INBRED F344; TISSUE DISTRIBUTION;

EID: 84955286043     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/acs.chemrestox.5b00425     Document Type: Article

References (36)

1. Hecht, S. S. (1998) Biochemistry, biology, and carcinogenicity of tobacco-specific N-nitrosamines Chem. Res. Toxicol. 11, 559-603 10.1021/tx980005y
2. Smokeless tobacco and some tobacco-specific N-nitrosamines, in IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, IARC, Lyon, France.
3. Balbo, S., James-Yi, S., Johnson, C. S., O'Sullivan, M. G., Stepanov, I., Wang, M. Y., Bandyopadhyay, D., Kassie, F., Carmella, S., Upadhyaya, P., and Hecht, S. S. (2013) (S)-N′-Nitrosonornicotine, a constituent of smokeless tobacco, is a powerful oral cavity carcinogen in rats Carcinogenesis 34, 2178-2183 10.1093/carcin/bgt162
4. Brittebo, E. B., Castonguay, A., Furuya, K., and Hecht, S. S. (1983) Metabolism of tobacco-specific nitrosamines by cultured rat nasal mucosa Cancer Res. 43, 4343-4348
5. Murphy, S. E., Heiblum, R., and Trushin, N. (1990) Comparative metabolism of N′-nitrosonornicotine and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone by cultured F344 rat oral tissue and esophagus Cancer Res. 50, 4685-4691
6. Hecht, S. S., Spratt, T. E., and Trushin, N. (1988) Evidence for 4-(3-pyridyl)-4-oxobutylation of DNA in F344 rats treated with the tobacco specific nitrosamines 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and N′-nitrosonornicotine Carcinogenesis 9, 161-165 10.1093/carcin/9.1.161
7. Trushin, N., Rivenson, A., and Hecht, S. S. (1994) Evidence supporting the role of DNA pyridyloxobutylation in rat nasal carcinogenesis by tobacco-specific nitrosamines Cancer Res. 54, 1205-1211
8. Lao, Y. B., Yu, N. X., Kassie, F., Villalta, P. W., and Hecht, S. S. (2007) Analysis of pyridyloxobutyl DNA adducts in F344 rats chronically treated with (R)- and (S)-N′-nitrosonornicotine Chem. Res. Toxicol. 20, 246-256 10.1021/tx060208j
9. Zhang, S. Y., Wang, M. Y., Villalta, P. W., Lindgren, B. R., Lao, Y. B., and Hecht, S. S. (2009) Quantitation of pyridyloxobutyl DNA adducts in nasal and oral mucosa of rats treated chronically with enantiomers of N′-nitrosonornicotine Chem. Res. Toxicol. 22, 949-956 10.1021/tx900040j
10. McIntee, E. J. and Hecht, S. S. (2000) Metabolism of N′-nitrosonornicotine enantiomers by cultured rat esophagus and in vivo in rats Chem. Res. Toxicol. 13, 192-199 10.1021/tx990171l
11. Zhao, L. J., Balbo, S., Wang, M. Y., Upadhyaya, P., Khariwala, S. S., Villalta, P. W., and Hecht, S. S. (2013) Quantitation of pyridyloxobutyl-DNA adducts in tissues of rats treated chronically with (R)- or (S)-N′-nitrosonornicotine (NNN) in a carcinogenicity study Chem. Res. Toxicol. 26, 1526-1535 10.1021/tx400235x
12. 6-benzylguanine Biochemistry 41, 1027-1038 10.1021/bi011495n
13. 6-alkylguanine-DNA alkyltransferase and mismatch repair Chem. Res. Toxicol. 14, 894-900 10.1021/tx010032f
14. 6-[4-oxo-4-(3-pyridyl)butyl]guanine in Escherichia coli and human cells Chem. Res. Toxicol. 15, 165-169 10.1021/tx0101245
15. 6-[4-oxo-4-(3-pyridyl)butyl]guanine, is detected in tissues from 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-treated A/J mice Chem. Res. Toxicol. 16, 1-6 10.1021/tx025585k
16. 6-[4-oxo-4-(3-pyridyl)butyl]-2′-deoxyguanosine Chem. Res. Toxicol. 17, 1600-1606 10.1021/tx0498298
17. Lao, Y. B., Villalta, P. W., Sturla, S. J., Wang, M. Y., and Hecht, S. S. (2006) Quantitation of pyridyloxobutyl DNA adducts of tobacco-specific nitrosamines in rat tissue DNA by high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry Chem. Res. Toxicol. 19, 674-682 10.1021/tx050351x
18. Zhang, S. Y., Wang, M. Y., Villalta, P. W., Lindgren, B. R., Upadhyaya, P., Lao, Y. B., and Hecht, S. S. (2009) Analysis of pyridyloxobutyl and pyridylhydroxybutyl DNA adducts in extrahepatic tissues of F344 rats treated chronically with 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and enantiomers of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol Chem. Res. Toxicol. 22, 926-936 10.1021/tx900015d
19. Hu, M. W., Bondinell, W. E., and Hoffmann, D. (1974) Chemical studies on tobacco smoke XXIII. Synthesis of carbon-14 labelled myosmine, nornicotine and N′-nitrosonornicotine J. Labelled Compd. 10, 79-88 10.1002/jlcr.2590100110
20. Seeman, J. I., Chavdarian, C. G., and Secor, H. V. (1985) Synthesis of the enantiomers of nornicotine J. Org. Chem. 50, 5419-5421 10.1021/jo00225a094
21. Wang, M. Y., Cheng, G., Sturla, S. J., Shi, Y. L., McIntee, E. J., Villalta, P. W., Upadhyaya, P., and Hecht, S. S. (2003) Identification of adducts formed by pyridyloxobutylation of deoxyguanosine and DNA by 4-(acetoxymethylnitrosamino)-1-(3-pyridyl)-1-butanone, a chemically activated form of tobacco specific carcinogens Chem. Res. Toxicol. 16, 616-626 10.1021/tx034003b
22. 6-alkylguanine-DNA alkyltransferase Chem. Res. Toxicol. 10, 562-567 10.1021/tx9602067
23. Sturla, S. J., Scott, J., Lao, Y. B., Hecht, S. S., and Villalta, P. W. (2005) Mass spectrometric analysis of relative levels of pyridyloxobutylation adducts formed in the reaction of DNA with a chemically activated form of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone Chem. Res. Toxicol. 18, 1048-1055 10.1021/tx050028u
24. 2-ethyldeoxyguanosine Chem. Res. Toxicol. 19, 319-324 10.1021/tx0502948
25. 32P-postlabeling analysis of aromatic carcinogen-DNA adducts Cancer Res. 45, 5656-5662
26. Gorshkov, M. V., Fornelli, L., and Tsybin, Y. O. (2012) Observation of ion coalescence in Orbitrap Fourier transform mass spectrometry Rapid Commun. Mass Spectrom. 26, 1711-1717 10.1002/rcm.6289
27. Smith, R. D., Shen, Y. F., and Tang, K. Q. (2004) Ultrasensitive and quantitative analyses from combined separations-mass spectrometry for the characterization of proteomes Acc. Chem. Res. 37, 269-278 10.1021/ar0301330
28. 6-alkylguanine-DNA alkyltransferase variants Chem. Res. Toxicol. 17, 424-434 10.1021/tx0342417
29. Shrivastav, N., Li, D. Y., and Essigmann, J. M. (2010) Chemical biology of mutagenesis and DNA repair: cellular responses to DNA alkylation Carcinogenesis 31, 59-70 10.1093/carcin/bgp262
30. 2-(3-pyridyl)-4-oxobutylthymine, the most persistent bulky adduct produced by the tobacco specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone by model DNA polymerases Chem. Res. Toxicol. 25, 1195-1202 10.1021/tx200483g
31. 6-methylguanine-DNA methyltransferase by various aldehydes in cultured human bronchial fibroblasts Carcinogenesis 6, 1755-1759 10.1093/carcin/6.12.1755
32. 6-methylguanine repair in human lung cells, in Repair of DNA Lesions Introduced by N-Nitroso Compounds (Myrnes, B. and Krokan, H., Eds.) pp 154-175, Norwegian University Press, Oslo, Norway.
33. 1-DNA adduct Proc. Natl. Acad. Sci. U. S. A. 93, 1535-1539 10.1073/pnas.93.4.1535
34. 1 formamidopyrimidine adduct plays a major role in causing the types of mutations observed in human hepatocellular carcinoma Proc. Natl. Acad. Sci. U. S. A. 99, 6655-6660 10.1073/pnas.102167699
35. Loeb, L. A. and Preston, B. D. (1986) Mutagenesis by apurinic/apyrimidinic sites Annu. Rev. Genet. 20, 201-230 10.1146/annurev.ge.20.120186.001221
36. Boysen, G., Pachkowski, B. F., Nakamura, J., and Swenberg, J. A. (2009) The formation and biological significance of N7-guanine adducts Mutat. Res., Genet. Toxicol. Environ. Mutagen. 678, 76-94 10.1016/j.mrgentox.2009.05.006