Identification of carcinogen DNA adducts in human saliva by linear quadrupole ion trap/multistage tandem mass spectrometry

Chemical Research in Toxicology

Volumn 23, Issue 7, 2010, Pages 1234-1244

  Bessette, Erin E ^a   Spivack, Simon D ^b   Goodenough, Angela K ^a,c   Wang, Tao ^b   Pinto, Shailesh ^d   Kadlubar, Fred F ^e   Turesky, Robert J ^a  

^a WADSWORTH CENTER   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

^d MONTEFIORE MEDICAL CENTER   (United States)

^e UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINE; CARCINOGEN; DNA; DNA BASE; TOBACCO SMOKE;

ARTICLE; BODY FLUID; CARCINOGEN DNA INTERACTION; CARCINOGENICITY; DNA ADDUCT; ELECTROSPRAY MASS SPECTROMETRY; HUMAN; HUMAN EXPERIMENT; LIQUID CHROMATOGRAPHY; MASS SPECTROMETER; MEAT; MONITORING; NORMAL HUMAN; SALIVA; SMOKE; TANDEM MASS SPECTROMETRY;

ADULT; AGED; AGED, 80 AND OVER; AMINOBIPHENYL COMPOUNDS; CARCINOGENS; DEOXYGUANOSINE; DNA ADDUCTS; FEMALE; HUMANS; IMIDAZOLES; MALE; MIDDLE AGED; SALIVA; SMOKING; TANDEM MASS SPECTROMETRY;

NICOTIANA TABACUM;

EID: 77955342547     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx100098f     Document Type: Article

References (77)

1. Miller, E. C. (1978) Some current perspectives on chemical carcinogenesis in humans and experimental animals: Presidential address Cancer Res. 38, 1479-1496
2. Himmelstein, M. W., Boogaard, P. J., Cadet, J., Farmer, P. B., Kim, J. H., Martin, E. A., Persaud, R., and Shuker, D. E. (2009) Creating context for the use of DNA adduct data in cancer risk assessment: II. Overview of methods of identification and quantitation of DNA damage Crit Rev. Toxicol. 39, 679-694
3. Jarabek, A. M., Pottenger, L. H., Andrews, L. S., Casciano, D., Embry, M. R., Kim, J. H., Preston, R. J., Reddy, M. V., Schoeny, R., Shuker, D., Skare, J., Swenberg, J., Williams, G. M., and Zeiger, E. (2009) Creating context for the use of DNA adduct data in cancer risk assessment: I. Data organization Crit Rev. Toxicol. 39, 659-678
4. Phillips, D. H. (2005) DNA adducts as markers of exposure and risk Mutat. Res. 577, 284-292
5. Hecht, S. S. (2002) Human urinary carcinogen metabolites: biomarkers for investigating tobacco and cancer Carcinogenesis 23, 907-922
6. Talaska, G., Schamer, M., Skipper, P., Tannenbaum, S., Caporaso, N., Unruh, L., Kadlubar, F. F., Bartsch, H., Malaveille, C., and Vineis, P. (1991) Detection of carcinogen-DNA adducts in exfoliated urothelial cells of cigarette smokers: Association with smoking, hemoglobin adducts, and urinary mutagenicity Cancer Epidemiol. Biomarkers Prev. 1, 61-66
7. Thompson, P. A., DeMarini, D. M., Kadlubar, F. F., McClure, G. Y., Brooks, L. R., Green, B. L., Fares, M. Y., Stone, A., Josephy, P. D., and Ambrosone, C. B. (2002) Evidence for the presence of mutagenic arylamines in human breast milk and DNA adducts in exfoliated breast ductal epithelial cells Environ. Mol. Mutagen. 39, 134-142
8. Gorlewska-Roberts, K., Green, B., Fares, M., Ambrosone, C. B., and Kadlubar, F. F. (2002) Carcinogen-DNA adducts in human breast epithelial cells Environ. Mol. Mutagen. 39, 184-192
9. Rundle, A. (2006) Carcinogen-DNA adducts as a biomarker for cancer risk Mutat. Res. 600, 23-36
10. Klinkhamer, J. M. (1963) Human oral leukocytes J. Am. Soc. Periodontists 1, 109-117
11. Osswald, K., Mittas, A., Glei, M., and Pool-Zobel, B. L. (2003) New revival of an old biomarker: characterisation of buccal cells and determination of genetic damage in the isolated fraction of viable leucocytes Mutat. Res. 544, 321-329
12. Prasad, M. P., Mukundan, M. A., and Krishnaswamy, K. (1995) Micronuclei and carcinogen DNA adducts as intermediate end points in nutrient intervention trial of precancerous lesions in the oral cavity Eur. J. Cancer B: Oral Oncol. 31B, 155-159
13. Rojas, E., Valverde, M., Sordo, M., and Ostrosky-Wegman, P. (1996) DNA damage in exfoliated buccal cells of smokers assessed by the single cell gel electrophoresis assay Mutat. Res. 370, 115-120
14. Schwartz, J. L., Muscat, J. E., Baker, V., Larios, E., Stephenson, G. D., Guo, W., Xie, T., Gu, X., and Chung, F. L. (2003) Oral cytology assessment by flow cytometry of DNA adducts, aneuploidy, proliferation and apoptosis shows differences between smokers and non-smokers Oral Oncol. 39, 842-854
15. Schwartz, J. L., Baker, V., Larios, E., and Chung, F. L. (2004) Molecular and cellular effects of green tea on oral cells of smokers: A pilot study Mol. Nutr. Food Res. 49, 43-51
16. Feng, Z., Xia, Y., Tian, D., Wu, K., Schmitt, M., Kwok, R. K., and Mumford, J. L. (2001) DNA damage in buccal epithelial cells from individuals chronically exposed to arsenic via drinking water in Inner Mongolia, China Anticancer Res. 21, 51-57
17. Proia, N. K., Paszkiewicz, G. M., Nasca, M. A., Franke, G. E., and Pauly, J. L. (2006) Smoking and smokeless tobacco-associated human buccal cell mutations and their association with oral cancerî - ̧A review Cancer Epidemiol. Biomarkers Prev. 15, 1061-1077
18. Vondracek, M., Xi, Z., Larsson, P., Baker, V., Mace, K., Pfeifer, A., Tjalve, H., Donato, M. T., Gomez-Lechon, M. J., and Grafstrom, R. C. (2001) Cytochrome P450 expression and related metabolism in human buccal mucosa Carcinogenesis 22, 481-488
19. Spivack, S. D., Hurteau, G. J., Jain, R., Kumar, S. V., Aldous, K. M., Gierthy, J. F., and Kaminsky, L. S. (2004) Gene-environment interaction signatures by quantitative mRNA profiling in exfoliated buccal mucosal cells Cancer Res. 64, 6805-6813
20. Autrup, H., Seremet, T., Arenholt, D., Dragsted, L., and Jepsen, A. (1985) Metabolism of benzo[a]pyrene by cultured rat and human buccal mucosa cells Carcinogenesis 6, 1761-1765
21. Liu, Y., Sundqvist, K., Belinsky, S. A., Castonguay, A., Tjalve, H., and Grafstrom, R. C. (1993) Metabolism and macromolecular interaction of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in cultured explants and epithelial cells of human buccal mucosa Carcinogenesis 14, 2383-2388
22. Kragelund, C., Hansen, C., Torpet, L. A., Nauntofte, B., Brosen, K., Pedersen, A. M., Buchwald, C., Therkildsen, M. H., and Reibel, J. (2008) Expression of two drug-metabolizing cytochrome P450-enzymes in human salivary glands Oral Dis. 14, 533-540
23. PA (P450IA2), the phenacetin O-deethylase, is primarily responsible for the hepatic 3-demethylation of caffeine and N-oxidation of carcinogenic arylamines Proc. Natl. Acad. Sci. U.S.A. 86, 7696
24. Turesky, R. J., Constable, A., Richoz, J., Varga, N., Markovic, J., Martin, M. V., and Guengerich, F. P. (1998) Activation of heterocyclic aromatic amines by rat and human liver microsomes and by purified rat and human cytochrome P450 1A2 Chem. Res. Toxicol. 11, 925-936
25. Stone, J. G., Jones, N. J., McGregor, A. D., and Waters, R. (1995) Development of a human biomonitoring assay using buccal mucosa: comparison of smoking-related DNA adducts in mucosa versus biopsies Cancer Res. 55, 1267-1270
26. Foiles, P. G., Miglietta, L. M., Quart, A. M., Quart, E., Kabat, G. C., and Hecht, S. S. (1989) Evaluation of 32P-postlabeling analysis of DNA from exfoliated oral mucosa cells as a means of monitoring exposure of the oral cavity to genotoxic agents Carcinogenesis 10, 1429-1434
27. Chacko, M. and Gupta, R. C. (1988) Evaluation of DNA damage in the oral mucosa of tobacco users and non-users by 32P-adduct assay Carcinogenesis 9, 2309-2313
28. Romano, G., Mancini, R., Fedele, P., Curigliano, G., Flamini, G., Giovagnoli, M. R., Malara, N., Boninsegna, A., Vecchione, A., Santella, R. M., and Cittadini, A. (1997) Immunohistochemical analysis of 4-aminobiphenyl-DNA adducts in oral mucosal cells of smokers and nonsmokers Anticancer Res. 17, 2827-2830
29. Besarati, N. A., Van Straaten, H. W., Godschalk, R. W., Van Zandwijk, N., Balm, A. J., Kleinjans, J. C., and Van Schooten, F. J. (2000) Immunoperoxidase detection of polycyclic aromatic hydrocarbon-DNA adducts in mouth floor and buccal mucosa cells of smokers and nonsmokers Environ. Mol. Mutagen. 36, 127-133
30. Santella, R. M. (1999) Immunological methods for detection of carcinogen-DNA damage in humans Cancer Epidemiol. Biomarkers Prev. 8, 733-739
31. Fenn, J. B., Mann, M., Meng, C. K., Wong, S. F., and Whitehouse, C. M. (1989) Electrospray ionization for mass spectrometry of large biomolecules Science 246, 64-71
32. Turesky, R. J. and Vouros, P. (2004) Formation and analysis of heterocyclic aromatic amine-DNA adducts in vitro and in vivo J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 802, 155-166
33. Singh, R. and Farmer, P. B. (2006) Liquid chromatography-electrospray ionization-mass spectrometry: The future of DNA adduct detection Carcinogenesis 27, 178-196
34. Bessette, E. E., Goodenough, A. K., Langouet, S., Yasa, I., Kozekov, I. D., Spivack, S. D., and Turesky, R. J. (2009) Screening for DNA adducts by data-dependent constant neutral loss-triple stage mass spectrometry with a linear quadrupole ion trap mass spectrometer Anal. Chem. 81, 809-819
35. Hecht, S. S. (2003) Tobacco carcinogens, their biomarkers and tobacco-induced cancer Nat. Rev. Cancer 3, 733-744
36. Lin, D., Kaderlik, K. R., Turesky, R. J., Miller, D. W., Lay, J. O., Jr., and Kadlubar, F. F. (1992) Identification of N -(deoxyguanosin-8-yl)-2-amino-1- methyl-6-phenylimidazo[4,5-b]pyridine as the major adduct formed by the food-borne carcinogen, 2-amino-1-methyl-6-phenylimidazo[4,5- b[pyridine, with DNA Chem. Res. Toxicol. 5, 691-697
37. n method for the characterization and quantification of 2'-deoxyguanosine adducts of the dietary carcinogen 2-amino-1-methyl-6- phenylimidazo[4,5- b[pyridine by 2-D linear quadrupole ion trap mass spectrometry Chem. Res. Toxicol. 20, 263-276
38. 2 atoms of guanine Chem. Res. Toxicol. 5, 479-490
39. Paehler, A., Richoz, J., Soglia, J., Vouros, P., and Turesky, R. J. (2002) Analysis and quantification of DNA adducts of 2-amino-3,8- dimethylimidazo[4,5- f[quinoxaline in liver of rats by liquid chromatography/electrospray tandem mass spectrometry Chem. Res. Toxicol. 15, 551-561
40. Frederiksen, H., Frandsen, H., and Pfau, W. (2004) Syntheses of DNA-adducts of two heterocyclic amines, 2-amino-3-methyl-9H-pyrido[2,3 b[indole (MeA{alpha}C) and 2-amino-9H-pyrido[2,3- b[indole (A{alpha}C) and identification of DNA-adducts in organs from rats dosed with MeA{alpha}C Carcinogenesis 25, 1525-1533
41. Jones, C. R. and Sabbioni, G. (2003) Identification of DNA adducts using HPLC/MS/MS following in vitro and in vivo experiments with arylamines and nitroarenes Chem. Res. Toxicol. 16, 1251-1263
42. Ruan, Q., Kim, H. Y., Jiang, H., Penning, T. M., Harvey, R. G., and Blair, I. A. (2006) Quantification of benzo[a]pyrene diol epoxide DNA-adducts by stable isotope dilution liquid chromatography/tandem mass spectrometry Rapid Commun. Mass Spectrom. 20, 1369-1380
43. Beland, F. A., Doerge, D. R., Churchwell, M. I., Poirier, M. C., Schoket, B., and Marques, M. M. (1999) Synthesis, characterization, and quantitation of a 4-aminobiphenyl-DNA adduct standard Chem. Res. Toxicol. 12, 68-77
44. Beland, F. A., Churchwell, M. I., Von Tungeln, L. S., Chen, S., Fu, P. P., Culp, S. J., Schoket, B., Gyorffy, E., Minarovits, J., Poirier, M. C., Bowman, E. D., Weston, A., and Doerge, D. R. (2005) High-performance liquid chromatography electrospray ionization tandem mass spectrometry for the detection and quantitation of benzo[ a[pyrene-DNA adducts Chem. Res. Toxicol. 18, 1306-1315
45. Lum, A. and Le, M. L. (1998) A simple mouthwash method for obtaining genomic DNA in molecular epidemiological studies Cancer Epidemiol. Biomarkers Prev. 7, 719-724
46. Patrianakos, C. and Hoffmann, D. (1979) Chemical studies on tobacco smoke LXIV. On the analysis of aromatic amines in cigarette smoke J. Assoc. Off Anal. Chem. 3, 150-154
47. Manabe, S., Tohyama, K., Wada, O., and Aramaki, T. (1991) Detection of a carcinogen, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine, in cigarette smoke condensate Carcinogenesis 12, 1945-1947
48. Yoshida, D. and Matsumoto, T. (1980) Amino-alpha-carbolines as mutagenic agents in cigarette smoke condensate Cancer Lett. 10, 141-149
49. Felton, J. S., Jagerstad, M., Knize, M. G., Skog, K., and Wakabayashi, K. (2000) Contents in Foods, Beverages and Tobacco. In Food Borne Carcinogens Heterocyclic Amines (Nagao, M. and Sugimura, T., Eds.) pp 31 - 71, John Wiley & Sons Ltd., Chichester, England.
50. Spink, B. C., Bennett, J. A., Pentecost, B. T., Lostritto, N., Englert, N. A., Benn, G. K., Goodenough, A. K., Turesky, R. J., and Spink, D. C. (2009) Long-term estrogen exposure promotes carcinogen bioactivation, induces persistent changes in gene expression, and enhances the tumorigenicity of MCF-7 human breast cancer cells Toxicol. Appl. Pharmacol. 240, 355-366
51. MacDougall, D., Amore, F. J., Cox, G. V., Crosby, D. G., Estes, F. L., Freeman, D. H., Gibbs, W. E., Gordon, G. E., Keith, L. H., Lal, J., Langner, R. R., McClelland, N. I., Phillips, W. F., Pojasek, R. B., and Sievers, R. E. (1980) Guidelines for data acquistion and data quality evaluation in environmental chemistry Anal. Chem. 52, 2242-2249
52. Turesky, R. J., Bendaly, J., Yasa, I., Doll, M. A., and Hein, D. W. (2009) The impact of NAT2 acetylator genotype on mutagenesis and DNA adducts from 2-amino-9 H -pyrido[2,3- b[indole Chem. Res. Toxicol. 22, 726-733
53. Walsh, D. J., Corey, A. C., Cotton, R. W., Forman, L., Herrin, G. L., Jr., Word, C. J., and Garner, D. D. (1992) Isolation of deoxyribonucleic acid (DNA) from saliva and forensic science samples containing saliva J. Forensic Sci. 37, 387-395
54. Grollman, A. P., Shibutani, S., Moriya, M., Miller, F., Wu, L., Moll, U., Suzuki, N., Fernandes, A., Rosenquist, T., Medverec, Z., Jakovina, K., Brdar, B., Slade, N., Turesky, R. J., Goodenough, A. K., Rieger, R., Vukelic, M., and Jelakovic, B. (2007) Aristolochic acid and the etiology of endemic (Balkan) nephropathy Proc. Natl. Acad. Sci. U.S.A. 104, 12129-12134
55. Rindgen, D., Turesky, R. J., and Vouros, P. (1995) Determination of in vitro formed DNA adducts of 2-amino-1-methyl-6-phenylimidazo[4,5- b[pyridine using capillary liquid chromatography/electrospray ionization/tandem mass spectrometry Chem. Res. Toxicol. 8, 1005-1013
56. Volmer, D. A. and Sleno, L. (2005) Mass analyzers, Part I: An overview over several designs and their applications Spectroscopy 20, 20-26 (Pubitemid 41687792)
57. Ni, W., McNaughton, L., LeMaster, D. M., Sinha, R., and Turesky, R. J. (2008) Quantitation of 13 heterocyclic aromatic amines in cooked beef, pork, and chicken by liquid chromatography-electrospray ionization/tandem mass spectrometry J. Agric. Food Chem. 56, 68-78
58. Sinha, R., Rothman, N., Brown, E. D., Mark, S. D., Hoover, R. N., Caporaso, N. E., Levander, O. A., Knize, M. G., Lang, N. P., and Kadlubar, F. F. (1994) Pan-fried meat containing high levels of heterocyclic aromatic amines but low levels of polycyclic aromatic hydrocarbons induces cytochrome P4501A2 activity in humans Cancer Res. 54, 6154-6159
59. Vistisen, K., Poulsen, H. E., and Loft, S. (1992) Foreign compound metabolism capacity in man measured from metabolites of dietary caffeine Carcinogenesis 13, 1561-1568
60. Turesky, R. J., Lang, N. P., Butler, M. A., Teitel, C. H., and Kadlubar, F. F. (1991) Metabolic activation of carcinogenic heterocyclic aromatic amines by human liver and colon Carcinogenesis 12, 1839-1845
61. Sinha, R., Rothman, N., Brown, E. D., Salmon, C. P., Knize, M. G., Swanson, C. S., Rossi, S. C., Mark, S. D., Levander, O. A., and Felton, J. S. (1995) High concentrations of the carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine (PhIP) occur in chicken but are dependent on the cooking method Cancer Res. 55, 4516-4519
62. Luceri, F., Pieraccini, G., Moneti, G., and Dolara, P. (1993) Primary aromatic amines from side-stream cigarette smoke are common contaminants of indoor air Toxicol. Ind. Health 9, 405-413
63. Grimmer, G., Schneider, D., Naujack, K. W., Dettbarn, G., and Jacob, J. (1996) Intercept-reactant method for the determination of aromatic amines in mainstream tobacco smoke Polycylic Aromat. Compd. 9, 85-92
64. Jagerstad, M., Skog, K., Grivas, S., and Olsson, K. (1991) Formation of heterocyclic amines using model systems Mutat. Res. 259, 219-233
65. Manabe, S., Kurihara, N., Wada, O., Izumikawa, S., Asakuno, K., and Morita, M. (1993) Detection of a carcinogen, 2-amino-1-methyl-6-phenylimidazo [4,5-b]pyridine, in airborne particles and diesel-exhaust particles Environ. Pollut. 80, 281-286
66. Alexander, J., Reistad, R., Hegstad, S., Frandsen, H., Ingebrigtsen, K., Paulsen, J. E., and Becher, G. (2002) Biomarkers of exposure to heterocyclic amines: approaches to improve the exposure assessment Food Chem. Toxicol. 40, 1131-1137
67. Kobayashi, M., Hanaoka, T., Hashimoto, H., and Tsugane, S. (2005) 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) level in human hair as biomarkers for dietary grilled/stir-fried meat and fish intake Mutat. Res. 588, 136-142
68. Bessette, E. E., Yasa, I., Dunbar, D., Wilkens, L. R., Marchand, L. L., and Turesky, R. J. (2009) Biomonitoring of carcinogenic heterocyclic aromatic amines in hair: A validation study Chem. Res. Toxicol. 22, 1454-1463
69. Zhu, J., Chang, P., Bondy, M. L., Sahin, A. A., Singletary, S. E., Takahashi, S., Shirai, T., and Li, D. (2003) Detection of 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine-DNA adducts in normal breast tissues and risk of breast cancer Cancer Epidemiol. Biomarkers Prev. 12, 830-837
70. Tang, D., Liu, J. J., Rundle, A., Neslund-Dudas, C., Savera, A. T., Bock, C. H., Nock, N. L., Yang, J. J., and Rybicki, B. A. (2007) Grilled meat consumption and PhIP-DNA adducts in prostate carcinogenesis Cancer Epidemiol. Biomarkers Prev. 16, 803-808
71. Kaderlik, K. R., Minchin, R. F., Mulder, G. J., Ilett, K. F., Daugaard-Jenson, M., Teitel, C. H., and Kadlubar, F. F. (1994) Metabolic activation pathway for the formation of DNA adducts of the carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5- b[pyridine (PhIP) in rat extrahepatic tissues Carcinogenesis 15, 1703-1709
72. Crofts, F. G., Sutter, T. R., and Strickland, P. T. (1998) Metabolism of 2-amino-1-methyl-6-phenylimidazo[4,5- b[pyridine by human cytochrome P4501A1, P4501A2 and P4501B1 Carcinogenesis 19, 1969-1973
73. Crofts, F. G., Strickland, P. T., Hayes, C. L., and Sutter, T. R. (1997) Metabolism of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) by human cytochrome P4501B1 Carcinogenesis 18, 1793-1798
74. Ihalin, R., Loimaranta, V., and Tenovuo, J. (2006) Origin, structure, and biological activities of peroxidases in human saliva Arch. Biochem. Biophys. 445, 261-268
75. Gorlewska-Roberts, K. M., Teitel, C. H., Lay, J. O., Jr., Roberts, D. W., and Kadlubar, F. F. (2004) Lactoperoxidase-catalyzed activation of carcinogenic aromatic and heterocyclic amines Chem. Res. Toxicol. 17, 1659-1666
76. Squier, C. A., Johnson, N. W., and Hopps, R. M. (1976) Human Oral Mucosa: Development, Structure and Function, pp 3 - 42, Blackwell, Oxford, United Kingdom.
77. Ashkenazi, M. and Dennison, D. K. (1989) A new method for isolation of salivary neutrophils and determination of their functional activity J. Dent. Res. 68, 1256-1261