Exposure and Metabolic Activation Biomarkers of Carcinogenic Tobacco-Specific Nitrosamines

Accounts of Chemical Research

Volumn 49, Issue 1, 2016, Pages 106-114

  Hecht, Stephen S ^a   Stepanov, Irina ^a   Carmella, Steven G ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4-(N-METHYL-N-NITROSAMINO)-1-(3-PYRIDYL)-1-BUTANONE; CARCINOGEN; N'-NITROSONORNICOTINE; NITROSAMINE; TUMOR MARKER;

ANIMAL; CHEMISTRY; HUMAN; LUNG TUMOR; METABOLIC ACTIVATION; METABOLISM; MOUTH TUMOR; RAT; SMOKING; TOBACCO;

ACTIVATION, METABOLIC; ANIMALS; BIOMARKERS, TUMOR; CARCINOGENS; HUMANS; LUNG NEOPLASMS; MOUTH NEOPLASMS; NITROSAMINES; RATS; SMOKING; TOBACCO PRODUCTS;

EID: 84955237948     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/acs.accounts.5b00472     Document Type: Article

References (65)

1. Hecht, S. S. Research Opportunities Related to Establishing Standards for Tobacco Products Under the Family Smoking Prevention and Tobacco Control Act Nicotine Tob. Res. 2012, 14, 18-28 10.1093/ntr/ntq216
2. International Agency for Research on Cancer Smokeless Tobacco and Tobacco-Specific Nitrosamines. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans; IARC: Lyon, FR, 2007; Vol. 89, pp 421-583.
3. International Agency for Research on Cancer Tobacco Smoke and Involuntary Smoking. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans; IARC: Lyon, FR, 2004; Vol. 83, pp 174-176.
4. Hecht, S. S. Tobacco Smoke Carcinogens and Lung Cancer J. Natl. Cancer Inst. 1999, 91, 1194-1210 10.1093/jnci/91.14.1194
5. United States Department of Health and Human Services The Health Consequences of Smoking: 50 Years of Progress. A Report of the Surgeon General; U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health, Atlanta, GA, 2014.
6. Stepanov, I.; Carmella, S. G.; Briggs, A.; Hertsgaard, L.; Lindgren, B.; Hatsukami, D. K.; Hecht, S. S. Presence of the Carcinogen N′-Nitrosonornicotine in the Urine of Some Users of Oral Nicotine Replacement Therapy Products Cancer Res. 2009, 69, 8236-8240 10.1158/0008-5472.CAN-09-1084
7. Hecht, S. S. Biochemistry, Biology, and Carcinogenicity of Tobacco-Specific N-Nitrosamines Chem. Res. Toxicol. 1998, 11, 559-603 10.1021/tx980005y
8. Jalas, J.; Hecht, S. S.; Murphy, S. E. Cytochrome P450 2A Enzymes As Catalysts of Metabolism of 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone(NNK), a Tobacco-Specific Carcinogen Chem. Res. Toxicol. 2005, 18, 95-110 10.1021/tx049847p
9. Breyer-Pfaff, U.; Martin, H. J.; Ernst, M.; Maser, E. Enantioselectivity of Carbonyl Reduction of 4-Methylnitrosamino-1-(3-Pyridyl)-1-Butanone by Tissue Fractions From Human and Rat and by Enzymes Isolated From Human Liver Drug Metab. Dispos. 2004, 32, 915-922
10. Hecht, S. S.; Young, R.; Chen, C. B. Metabolism in the F344 Rat of 4-(N-Methyl-N-Nitrosamino)-1-(3-Pyridyl)-1-Butanone, a Tobacco Specific Carcinogen Cancer Res. 1980, 40, 4144-4150
11. Morse, M. A.; Eklind, K. I.; Toussaint, M.; Amin, S. G.; Chung, F. L. Characterization of a Glucuronide Metabolite of 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone(NNK) and Its Dose-Dependent Excretion in the Urine of Mice and Rats Carcinogenesis 1990, 11, 1819-1823 10.1093/carcin/11.10.1819
12. Hecht, S. S.; Trushin, N.; Reid-Quinn, C. A.; Burak, E. S.; Jones, A. B.; Southers, J. L.; Gombar, C. T.; Carmella, S. G.; Anderson, L. M.; Rice, J. M. Metabolism of the Tobacco-Specific Nitrosamine 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone in the Patas Monkey: Pharmacokinetics and Characterization of Glucuronide Metabolites Carcinogenesis 1993, 14, 229-236 10.1093/carcin/14.2.229
13. Ren, Q.; Murphy, S. E.; Zheng, Z.; Lazarus, P. O-Glucuronidation of the Lung Carcinogen 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanol(NNAL) by Human UDP-Glucuronosyltransferases 2B7 and 1A9 Drug Metab. Dispos. 2000, 28, 1352-1360
14. Carmella, S. G.; Le, K.; Upadhyaya, P.; Hecht, S. S. Analysis of N- and O-Glucuronides of 4-(Methylnitrosamino)-1-(3- Pyridyl)-1-Butanol(NNAL) in Human Urine Chem. Res. Toxicol. 2002, 15, 545-550 10.1021/tx015584c
15. Carmella, S. G.; Akerkar, S.; Hecht, S. S. Metabolites of the Tobacco-Specific Nitrosamine 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone in Smokers' Urine Cancer Res. 1993, 53, 721-724
16. Shah, K. A.; Karnes, H. T. A Review of the Analysis of Tobacco-Specific Nitrosamines in Biological Matrices Crit. Rev. Toxicol. 2010, 40, 305-327 10.3109/10408440903394435
17. Carmella, S. G.; Ming, X.; Olvera, N.; Brookmeyer, C.; Yoder, A.; Hecht, S. S. High Throughput Liquid and Gas Chromatography-Tandem Mass Spectrometry Assays for Tobacco-Specific Nitrosamine and Polycyclic Aromatic Hydrocarbon Metabolites Associated With Lung Cancer in Smokers Chem. Res. Toxicol. 2013, 26, 1209-1217 10.1021/tx400121n
18. Hecht, S. S.; Carmella, S. G.; Chen, M.; Koch, J. F. D.; Miller, A. T.; Murphy, S. E.; Jensen, J. A.; Zimmerman, C. L.; Hatsukami, D. K. Quantitation of Urinary Metabolites of a Tobacco-Specific Lung Carcinogen After Smoking Cessation Cancer Res. 1999, 59, 590-596
19. Goniewicz, M. L.; Havel, C. M.; Peng, M. W.; Jacob, P., III; Dempsey, D.; Yu, L.; Zielinska-Danch, W.; Koszowski, B.; Czogala, J.; Sobczak, A.; Benowitz, N. L. Elimination Kinetics of the Tobacco-Specific Biomarker and Lung Carcinogen 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanol Cancer Epidemiol., Biomarkers Prev. 2009, 18, 3421-3425 10.1158/1055-9965.EPI-09-0874
20. Hecht, S. S. Human Urinary Carcinogen Metabolites: Biomarkers for Investigating Tobacco and Cancer Carcinogenesis 2002, 23, 907-922 10.1093/carcin/23.6.907
21. Roethig, H. J.; Munjal, S.; Feng, S.; Liang, Q.; Sarkar, M.; Walk, R. A.; Mendes, P. E. Population Estimates for Biomarkers of Exposure to Cigarette Smoke in Adult U.S. Cigarette Smokers Nicotine Tob. Res. 2009, 11, 1216-1225 10.1093/ntr/ntp126
22. Xia, Y.; Bernert, J. T.; Jain, R. B.; Ashley, D. L.; Pirkle, J. L. Tobacco-Specific Nitrosamine 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanol(NNAL) in Smokers in the United States: NHANES 2007-2008 Biomarkers 2011, 16, 112-119 10.3109/1354750X.2010.533288
23. Hecht, S. S.; Carmella, S. G.; Murphy, S. E.; Akerkar, S.; Brunnemann, K. D.; Hoffmann, D. A Tobacco-Specific Lung Carcinogen in the Urine of Men Exposed to Cigarette Smoke N. Engl. J. Med. 1993, 329, 1543-1546 10.1056/NEJM199311183292105
24. International Agency for Research on Cancer Tobacco Smoke and Involuntary Smoking. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans; IARC: Lyon, FR, 2004; Vol. 83, pp 1191-1413.
25. Thomas, J. L.; Guo, H.; Carmella, S. G.; Balbo, S.; Han, S.; Davis, A.; Murphy, S. E.; An, L. C.; Ahluwalia, J. S.; Hecht, S. S. Metabolites of a Tobacco-Specific Lung Carcinogen in Children Exposed to Secondhand or Thirdhand Tobacco Smoke in Their Homes Cancer Epidemiol., Biomarkers Prev. 2011, 20, 1213-1221 10.1158/1055-9965.EPI-10-1027
26. Hecht, S. S.; Ye, M.; Carmella, S. G.; Fredrickson, A.; Adgate, J. L.; Greaves, I. A.; Church, T. R. Metabolites of a Tobacco-Specific Lung Carcinogen in the Urine of Elementary School-Aged Children Cancer Epidemiol. Biomarkers Prev. 2001, 10, 1109-1116
27. Hecht, S. S.; Carmella, S. G.; Le, K.; Murphy, S. E.; Boettcher, A. J.; Le, C.; Koopmeiners, J.; An, L.; Hennrikus, D. J. 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanol and Its Glucuronides in the Urine of Infants Exposed to Environmental Tobacco Smoke Cancer Epidemiol., Biomarkers Prev. 2006, 15, 988-992 10.1158/1055-9965.EPI-05-0596
28. Vogel, R. I.; Carmella, S. G.; Stepanov, I.; Hatsukami, D. K.; Hecht, S. S. The Ratio of a Urinary Tobacco-Specific Lung Carcinogen Metabolite to Cotinine Is Significantly Higher in Passive Than in Active Smokers Biomarkers 2011, 16, 491-497 10.3109/1354750X.2011.598565
29. Wei, B.; Blount, B. C.; Xia, B.; Wang, L. Assessing Exposure to Tobacco-Specific Carcinogen NNK Using Its Urinary Metabolite NNAL Measured in US Population J. Exposure Sci. Environ. Epidemiol. 2015, 10.1038/jes.2014.88
30. Yuan, J. M.; Koh, W. P.; Murphy, S. E.; Fan, Y.; Wang, R.; Carmella, S. G.; Han, S.; Wickham, K.; Gao, Y. T.; Yu, M. C.; Hecht, S. S. Urinary Levels of Tobacco-Specific Nitrosamine Metabolites in Relation to Lung Cancer Development in Two Prospective Cohorts of Cigarette Smokers Cancer Res. 2009, 69, 2990-2995 10.1158/0008-5472.CAN-08-4330
31. Yuan, J.-M.; Gao, Y.-T.; Murphy, S. E.; Carmella, S. G.; Wang, R.; Zhong, Y.; Moy, K. A.; Davis, A. B.; Tao, L.; Chen, M.; Han, S.; Nelson, H. H.; Yu, M. C.; Hecht, S. S. Urinary Levels of Cigarette Smoke Constituent Metabolites Are Prospectively Associated With Lung Cancer Development in Smokers Cancer Res. 2011, 71, 6749-6757 10.1158/0008-5472.CAN-11-0209
32. Pan, J.; Song, Q.; Shi, H.; King, M.; Junga, H.; Zhou, S.; Naidong, W. Development, Validation and Transfer of a Hydrophilic Interaction Liquid Chromatography/Tandem Mass Spectrometric Method for the Analysis of the Tobacco-Specific Nitrosamine Metabolite NNAL in Human Plasma at Low Picogram Per Milliliter Concentrations Rapid Commun. Mass Spectrom. 2004, 18, 2549-2557 10.1002/rcm.1656
33. Carmella, S. G.; Han, S.; Villalta, P. W.; Hecht, S. S. Analysis of Total 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanol(NNAL) in Smokers' Blood Cancer Epidemiol., Biomarkers Prev. 2005, 14, 2669-2672 10.1158/1055-9965.EPI-05-0129
34. Church, T. R.; Anderson, K. E.; Caporaso, N. E.; Geisser, M. S.; Le, C.; Zhang, Y.; Benoit, A. R.; Carmella, S. G.; Hecht, S. S. A Prospectively Measured Serum Biomarker for a Tobacco-Specific Carcinogen and Lung Cancer in Smokers Cancer Epidemiol., Biomarkers Prev. 2009, 18, 260-266 10.1158/1055-9965.EPI-08-0718
35. Stepanov, I.; Jensen, J.; Hatsukami, D.; Hecht, S. S. Mass Spectrometric Quantitation of Nicotine, Cotinine, and 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanol, in Human Toenails Cancer Epidemiol., Biomarkers Prev. 2006, 15, 2378-2383 10.1158/1055-9965.EPI-06-0265
36. Stepanov, I.; Hecht, S. S.; Lindgren, B.; Jacob, P., III; Wilson, M.; Benowitz, N. L. Relationship of Human Toenail Nicotine, Cotinine, and 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanol to Levels of These Biomarkers in Plasma and Urine Cancer Epidemiol., Biomarkers Prev. 2007, 16, 1382-1386 10.1158/1055-9965.EPI-07-0145
37. Upadhyaya, P.; Zimmerman, C. L.; Hecht, S. S. Metabolism and Pharmacokinetics of N′-Nitrosonornicotine in the Patas Monkey Drug Metab. Dispos. 2002, 30, 1115-1122 10.1124/dmd.30.10.1115
38. Stepanov, I.; Hecht, S. S. Tobacco-Specific Nitrosamines and Their N-Glucuronides in the Urine of Smokers and Smokeless Tobacco Users Cancer Epidemiol., Biomarkers Prev. 2005, 14, 885-891 10.1158/1055-9965.EPI-04-0753
39. Urban, M.; Scherer, G.; Kavvadias, D.; Hagedorn, H. W.; Feng, S.; Serafin, R.; Kapur, S.; Muhammad, R.; Jin, Y.; Mendes, P.; Roethig, H. Quantitation of N′-Nitrosonornicotine(NNN) in Smokers' Urine by Liquid Chromatography-Tandem Mass Spectrometry J. Anal. Toxicol. 2009, 33, 260-265 10.1093/jat/33.5.260
40. Sarkar, M.; Liu, J.; Koval, T.; Wang, J.; Feng, S.; Serafin, R.; Jin, Y.; Xie, Y.; Newland, K.; Roethig, H. J. Evaluation of Biomarkers of Exposure in Adult Cigarette Smokers Using Marlboro Snus Nicotine Tob. Res. 2010, 12, 105-116 10.1093/ntr/ntp183
41. Xia, B.; Xia, Y.; Wong, J.; Nicodemus, K. J.; Xu, M.; Lee, J.; Guillot, T.; Li, J. Quantitative Analysis of Five Tobacco-Specific N-Nitrosamines in Urine by Liquid Chromatography-Atmospheric Pressure Ionization Tandem Mass Spectrometry Biomed. Chromatogr. 2014, 28, 375-384 10.1002/bmc.3031
42. Stepanov, I.; Jensen, J.; Hatsukami, D.; Hecht, S. S. New and Traditional Smokeless Tobacco: Comparison of Toxicant and Carcinogen Levels Nicotine Tob. Res. 2008, 10, 1773-1782 10.1080/14622200802443544
43. Stepanov, I.; Biener, L.; Knezevich, A.; Nyman, A. L.; Bliss, R.; Jensen, J.; Hecht, S. S.; Hatsukami, D. K. Monitoring Tobacco-Specific N-Nitrosamines and Nicotine in Novel Marlboro and Camel Smokeless Tobacco Products: Findings From Round 1 of the New Product Watch Nicotine Tob. Res. 2012, 14, 274-281 10.1093/ntr/ntr209
44. Yuan, J. M.; Knezevich, A. D.; Wang, R.; Gao, Y. T.; Hecht, S. S.; Stepanov, I. Urinary Levels of the Tobacco-Specific Carcinogen N′-Nitrosonornicotine and Its Glucuronide Are Strongly Associated With Esophageal Cancer Risk in Smokers Carcinogenesis 2011, 32, 1366-1371 10.1093/carcin/bgr125
45. Stepanov, I.; Sebero, E.; Wang, R.; Gao, Y. T.; Hecht, S. S.; Yuan, J. M. Tobacco-Specific N-Nitrosamine Exposures and Cancer Risk in the Shanghai Cohort Study: Remarkable Coherence With Rat Tumor Sites Int. J. Cancer 2014, 134, 2278-2283 10.1002/ijc.28575
46. Knezevich, A.; Muzic, J.; Hatsukami, D. K.; Hecht, S. S.; Stepanov, I. Nornicotine Nitrosation in Saliva and Its Relation to Endogenous Synthesis of N′-Nitrosonornicotine in Humans Nicotine Tob. Res. 2013, 15, 591-595 10.1093/ntr/nts172
47. Stepanov, I.; Hecht, S. S. Detection and Quantitation of N′-Nitrosonornicotine in Human Toenails by Liquid Chromatography-Electrospray Ionization-Tandem Mass Spectrometry Cancer Epidemiol., Biomarkers Prev. 2008, 17, 945-948 10.1158/1055-9965.EPI-07-2711
48. Hecht, S. S.; Yuan, J.-M.; Hatsukami, D. K. Applying Tobacco Carcinogen and Toxicant Biomarkers in Product Regulation and Cancer Prevention Chem. Res. Toxicol. 2010, 23, 1001-1008 10.1021/tx100056m
49. Wang, H.; Tan, W.; Hao, B.; Miao, X.; Zhou, G.; He, F.; Lin, D. Substantial Reduction in Risk of Lung Adenocarcinoma Associated With Genetic Polymorphism in CYP2A13, the Most Active Cytochrome P450 for the Metabolic Activation of Tobacco-Specific Carcinogen NNK Cancer Res. 2003, 63, 8057-8061
50. Yuan, J.-Y.; Nelson, H. H.; Butler, L. M.; Carmella, S. G.; Wang, R.; Kuriger-Laber, J.; Adams-Haduch, J.; Hecht, S. S.; Gao, Y.-T.; Murphy, S. E. Genetic Determinants of Cytochrome P450 2A6 and Biomarkers of Tobacco Smoke Exposure in Relation to Risk of Lung Cancer Development in the Shanghai Cohort Study. Int. J. Cancer 2015, DOI: 10.1002/ijc.29963
51. 4]4-Hydroxy-4-(3-Pyridyl)Butanoic Acid, a Biomarker of 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone Metabolic Activation in Smokers Chem. Res. Toxicol. 2014, 27, 1547-1555 10.1021/tx5001915
52. Ehrenberg, L.; Osterman-Golkar, S. Alkylation of Macromolecules for Detecting Mutagenic Agents Teratog., Carcinog., Mutagen. 1981, 1, 105-127 10.1002/tcm.1770010111
53. Tornqvist, M.; Osterman-Golkar, S.; Kautiainen, A.; Jensen, S.; Farmer, P. B.; Ehrenberg, L. Tissue Doses of Ethylene Oxide in Cigarette Smokers Determined From Adduct Levels in Hemoglobin Carcinogenesis 1986, 7, 1519-1521 10.1093/carcin/7.9.1519
54. Bryant, M. S.; Skipper, P. L.; Tannenbaum, S. R.; Maclure, M. Hemoglobin Adducts of 4-Aminobiphenyl in Smokers and Nonsmokers Cancer Res. 1987, 47, 602-608
55. Carmella, S. G.; Hecht, S. S. Formation of Hemoglobin Adducts Upon Treatment of F344 Rats With the Tobacco-Specific Nitrosamines 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone and N′-Nitrosonornicotine Cancer Res. 1987, 47, 2626-2630
56. Carmella, S. G.; Kagan, S. S.; Hecht, S. S. Evidence That a Hemoglobin Adduct of 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone Is a 4-(3-Pyridyl)-4-Oxobutyl Carboxylic Acid Ester Chem. Res. Toxicol. 1992, 5, 76-80 10.1021/tx00025a013
57. Murphy, S. E.; Palomino, A.; Hecht, S. S.; Hoffmann, D. Dose-Response Study of DNA and Hemoglobin Adduct Formation by 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone in F344 Rats Cancer Res. 1990, 50, 5446-5452
58. Hecht, S. S.; Carmella, S. G.; Foiles, P. G.; Murphy, S. E. Biomarkers for Human Uptake and Metabolic Activation of Tobacco-Specific Nitrosamines Cancer Res. [Suppl.] 1994, 54, 1912s-1917s
59. Hecht, S. S. Progress and Challenges in Selected Areas of Tobacco Carcinogenesis Chem. Res. Toxicol. 2008, 21, 160-171 10.1021/tx7002068
60. Ma, B.; Villalta, P. W.; Zarth, A.; Kotandeniya, D.; Upadhyaya, P.; Stepanov, I. S.; Hecht, S. S. Comprehensive High Resolution Mass Spectrometric Analysis of DNA Phosphate Adducts Formed by the Tobacco-Specific Lung Carcinogen 4-(Methylnitrosamino)-1-(3-Pyridyl)-1-Butanone(NNK) Chem. Res. Toxicol. 2015, 28, 2151-2159 10.1021/acs.chemrestox.5b00318
61. Foiles, P. G.; Akerkar, S. A.; Carmella, S. G.; Kagan, M.; Stoner, G. D.; Resau, J. H.; Hecht, S. S. Mass Spectrometric Analysis of Tobacco-Specific Nitrosamine-DNA Adducts in Smokers and Nonsmokers Chem. Res. Toxicol. 1991, 4, 364-368 10.1021/tx00021a017
62. Hölzle, D.; Schlöbe, D.; Tricker, A. R.; Richter, E. Mass Spectrometric Analysis of 4-Hydroxy-1-(3-Pyridyl)-1-Butanone-Releasing DNA Adducts in Human Lung Toxicology 2007, 232, 277-285 10.1016/j.tox.2007.01.016
63. Schlöbe, D.; Holzle, D.; Hatz, D.; Von Meyer, L.; Tricker, A. R.; Richter, E. 4-Hydroxy-1-(3-Pyridyl)-1-Butanone-Releasing DNA Adducts in Lung, Lower Esophagus and Cardia of Sudden Death Victims Toxicology 2008, 245, 154-161 10.1016/j.tox.2007.12.021
64. Stepanov, I.; Muzic, J.; Le, C. T.; Sebero, E.; Villalta, P.; Jensen, J.; Hatsukami, D.; Hecht, S. S. Analysis of 4-Hydroxy-1-(3-Pyridyl)-1-Butanone(HPB)-Releasing DNA Adducts in Human Exfoliated Oral Mucosa Cells by Liquid Chromatography-Electrospray Ionization-Tandem Mass Spectrometry Chem. Res. Toxicol. 2013, 26, 37-45 10.1021/tx300282k
65. Zhao, L.; Balbo, S.; Wang, M.; Upadhyaya, P.; Khariwala, S. S.; Villalta, P. W.; Hecht, S. S. 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. 2013, 26, 1526-1535 10.1021/tx400235x