Metabolites of the polycyclic aromatic hydrocarbon phenanthrene in the urine of cigarette smokers from five ethnic groups with differing risks for lung cancer

PLoS ONE

Volumn 11, Issue 6, 2016, Pages

  Patel, Yesha M ^a   Park, Sungshim L ^a   Carmella, Steven G ^b   Paiano, Viviana ^b   Olvera, Natalie ^b   Stram, Daniel O ^a   Haiman, Christopher A ^a   Le Marchand, Loic ^c   Hecht, Stephen S ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYPHENANTHRENE; CARCINOGEN; CIGARETTE SMOKE; GLUTATHIONE TRANSFERASE T1; PHENANTHRENE; POLYCYCLIC AROMATIC HYDROCARBON; TETRAOL; UNCLASSIFIED DRUG; GLUTATHIONE S-TRANSFERASE T1; GLUTATHIONE TRANSFERASE; GSTT2 PROTEIN, HUMAN; PHENANTHRENE DERIVATIVE; TUMOR PROTEIN;

ADULT; AFRICAN AMERICAN; AGED; ARTICLE; ASIAN AMERICAN; CANCER RISK; CAUCASIAN; CONTROLLED STUDY; COPY NUMBER VARIATION; FEMALE; GENE; GENETIC ASSOCIATION; GENOME-WIDE ASSOCIATION STUDY; GSTT1 GENE; GSTT2 GENE; HISPANIC; HUMAN; LUNG CANCER; MALE; NATIVE HAWAIIAN; SMOKING; URINALYSIS; CLINICAL TRIAL; ENZYMOLOGY; ETHNOLOGY; GENE DOSAGE; GENETICS; LUNG TUMOR; METABOLISM; MIDDLE AGED; MULTICENTER STUDY; MUTATION; RISK FACTOR; URINE;

AGED; FEMALE; GENE DOSAGE; GLUTATHIONE TRANSFERASE; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; NEOPLASM PROTEINS; PHENANTHRENES; RISK FACTORS; SMOKING;

EID: 84974824548     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0156203     Document Type: Article

References (40)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015; 65: 5-29. doi: 10.3322/caac.21254 PMID: 25559415
2. International Agency for Research on Cancer.The Global and Regional Burden of Cancer. In: Stewart BW, Wild CP, editors. World Cancer Report 2014. Lyon, FR: International Agency for Research on Cancer; 2014. pp. 16-53.
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61: 69-90. doi: 10.3322/caac.20107 PMID: 21296855
4. Haiman CA, Stram DO, Wilkens LR, Pike MC, Kolonel LN, Henderson BE, et al. Ethnic and racial differences in the smoking-related risk of lung cancer. N Engl J Med. 2006; 354: 333-342. PMID: 16436765
5. Murphy SE, Park S-SL, Thompson EF, Wilkens LR, Patel Y, Stram DO, et al. Nicotine N-glucurionidation relative to N-oxidation and C-oxidation and UGT2B10 genotype in five ethnic/racial groups. Carcinogenesis. 2014; 35: 2526-2533. doi: 10.1093/carcin/bgu191 PMID: 25233931
6. Patel Y, Stram DO, Wilkens LR, Park SL, Henderson BE, Le Marchand L, et al. The contribution of common genetic variation to nicotine and cotinine glucuronidation in multiple ethnic/racial populations. Cancer Epidemiol Biomarkers Prev. 2015; 24: 119-127. doi: 10.1158/1055-9965.EPI-14-0815 PMID: 25293881
7. Park SL, Carmella SG, Ming X, Stram DO, Le Marchand L, Hecht SS. Variation in levels of the lung carcinogen NNAL and its glucuronides in the urine of cigarette smokers from five ethnic groups with differing risks for lung cancer. Cancer Epidemiol Biomarkers Prev. 2015; 24: 561-569. doi: 10.1158/1055-9965.EPI-14-1054 PMID: 25542827
8. Park SL, Carmella SG, Chen M, Patel Y, Stram DO, Haiman CA, et al. Mercpaturic acids derived from the toxicants acrolein and crotonaldehyde in the urine of cigarettes smokers from five ethnic groups with differing risks for lung cancer. PLoS One. 2015; 10: e0124841. doi: 10.1371/journal.pone.0124841 PMID: 26053186
9. International Agency for Research on Cancer. Some Non-Heterocyclic Polycyclic Aromatic Hydrocarbons and Some Related Exposures. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, v. 92. Lyon, FR: IARC; 2010. pp. 35-818.
10. Dipple A, Moschel RC, Bigger CAH. Polynuclear aromatic hydrocarbons. In: Searle CE, editor. Chemical Carcinogens, Second Edition, ACS Monograph 182 vol. 1. Washington, D.C.: American Chemical Society; 1984. pp. 41-163.
11. Hecht SS. Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst. 1999; 91: 1194-1210. PMID: 10413421
12. Suwan-ampai P, Navas-Acien A, Strickland PT, Agnew J. Involuntary tobacco smoke exposure and urinary levels of polycyclic aromatic hydrocarbons in the United States, 1999 to 2002. Cancer Epidemiol Biomarkers Prev. 2009; 18: 884-893. doi: 10.1158/1055-9965.EPI-08-0939 PMID: 19258471
13. Kolonel LN, Henderson BE, Hankin JH, Nomura AM, Wilkens LR, Pike MC, et al. A multiethnic cohort in Hawaii and Los Angeles: baseline characteristics. Am J Epidemiol. 2000; 151: 346-357. PMID: 10695593
14. Haiman CA, Patel YM, Stram DO, Carmella SG, Chen M, Wilkens L, et al. Benzene uptake and glutathione S-transferase T1 status as determinants of S-phenylmercapturic acid in cigarette smokers in the Multiethnic Cohort. PLoS One. 2015.
15. Carmella SG, Ming X, Olvera N, Brookmeyer C, Yoder A, Hecht SS. 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. doi: 10.1021/tx400121n PMID: 23837805
16. Carmella SG, Chen M, Yagi H, Jerina DM, Hecht SS. Analysis of phenanthrols in human urine by gas chromatography-mass spectrometry: potential use in carcinogen metabolite phenotyping. Cancer Epidemiol Biomarkers Prev. 2004; 13: 2167-2174. PMID: 15598776
17. Delaneau O, Marchini J, Zagury JF. A linear complexity phasing method for thousands of genomes. Nat Methods. 2012; 9: 179-181.
18. Howie BN, Donnelly P, Marchini J. A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 2009; 5: e1000529. doi: 10.1371/journal.pgen.1000529 PMID: 19543373
19. Branstetter SA, Mercincavage M, Muscat JE. Predictors of the nicotine dependence behavior time to the first cigarette in a multiracial cohort. Nicotine Tob Res. 2015; 17: 819-824. doi: 10.1093/ntr/ntu236 PMID: 25431372
20. Park S-L, Tiirikainen M, Patel Y, Wilkens LR, Stram DO, Le Marchand L, et al. Genetic determinants of CYP2A6 activity across racial/ethnic groups with different risk of lung cancer and effect on their smoking behavior. Carcinogenesis. 2016;in press.
21. Hecht SS. Human urinary carcinogen metabolites: biomarkers for investigating tobacco and cancer. Carcinogenesis. 2002; 23: 907-922. PMID: 12082012
22. Chu I, Ng KM, Benoit FM, Moir D. Comparative metabolism of phenanthrene in the rat and guinea pig. J Environ Sci Health, Part B. 1992; 27: 729-749.
23. Hecht SS, Chen M, Yagi H, Jerina DM, Carmella SG. r-1,t-2,3,c-4-Tetrahydroxy-1,2,3,4-tetrahydrophenanthrene in human urine: a potential biomarker for assessing polycyclic aromatic hydrocarbon metabolic activation. Cancer Epidemiol Biomarkers Prev. 2003; 12: 1501-1508. PMID: 14693744
24. Cooper CS, Grover PL, Sims P. The metabolism and activation of benzo[a]pyrene. Prog Drug Metab. 1983; 7: 295-396.
25. Conney AH. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G.H.A. Clowes Memorial Lecture. Cancer Res. 1982; 42: 4875-4917. PMID: 6814745
26. Hochalter JB, Zhong Y, Han S, Carmella SG, Hecht SS. Quantitation of a minor enantiomer of phenanthrene tetraol in human urine: correlations with levels of overall phenanthrene tetraol, benzo[a]pyrene tetraol, and 1-hydroxypyrene. Chem Res Toxicol. 2011; 24: 262-268. doi: 10.1021/tx100391z PMID: 21229973
27. Hecht SS. Tobacco smoke carcinogens and lung cancer. In: Penning TM, editor. Chemical Carcinogenesis. Springer; 2011. pp. 53-74.
28. Hoffmann D, Schmeltz I, Hecht SS, Wynder EL. Tobacco carcinogenesis. In: Gelboin H, Ts'o POP, editors. Polycyclic Hydrocarbons and Cancer. New York: Academic Press; 1978. pp. 85-117.
29. Rodgman A, Perfetti T. The Chemical Components of Tobacco and Tobacco Smoke. Boca Raton, FL: CRC Press; 2009.
30. Denissenko MF, Pao A, Tang M, Pfeifer GP. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hot spots in P53. Science. 1996; 274: 430-432. PMID: 8832894
31. Smith LE, Denissenko MF, Bennett WP, Li H, Amin S, Tang M, et al. Targeting of lung cancer mutational hotspots by polycyclic aromatic hydrocarbons. J Natl Cancer Inst. 2000; 92: 803-811. PMID: 10814675
32. Tretyakova N, Matter B, Jones R, Shallop A. Formation of benzo[a]pyrene diol epoxide-DNA adducts at specific guanines within K-ras and p53 gene sequences: stable isotope-labeling mass spectrometry approach. Biochemistry. 2002; 41: 9535-9544. PMID: 12135376
33. Feng Z, Hu W, Hu Y, Tang M-S. Acrolein is a major cigarette-related lung cancer agent. Preferential binding at p53 mutational hotspots and inhibition of DNA repair. Proc Natl Acad Sci USA. 2006; 103:15404-15409. PMID: 17030796
34. Upadhyaya P, Hochalter JB, Balbo S, McIntee EJ, Hecht SS. Preferential glutathione conjugation of a reverse diol epoxide compared with a bay region diol epoxide of benzo[a]pyrene in human hepatocytes. Drug Metab Dispos. 2010; 38: 1397-1402. doi: 10.1124/dmd.110.034181 PMID: 20547966
35. Hecht SS, Berg JZ, Hochalter JB. Preferential glutathione conjugation of a reverse diol epoxide compared to a bay region diol epoxide of phenanthrene in human hepatocytes: Relevance to molecular epidemiology studies of glutathione-S-transferase polymorphisms and cancer. Chem Res Toxicol. 2009; 22: 426-432. doi: 10.1021/tx800315m PMID: 19187038
36. Rojas M, Cascorbi I, Alexandrov K, Kriek E, Auburtin G, Mayer L, et al. Modulation of benzo[a]pyrene diolepoxide-DNA adduct levels in human white blood cells by CYP1A1, GSTM1, and GSTT1 polymorphims. Carcinogenesis. 2000; 21: 35-41. PMID: 10607731
37. Sundberg K, Dreij K, Seidel A, Jernström B. 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. 2002; 15: 170-179. PMID: 11849043
38. Fields WR, Morrow CS, Doss AJ, Sundberg K, Jernstrom B, Townsend AJ. Overexpression of stably transfected human glutathione S-transferase P1-1 protects against DNA damage by benzo[a]pyrene diol-epoxide in human T47D cells. Mol Pharmacol. 1998; 54: 298-304. PMID: 9687571
39. Landi S. Mammalian class theta GST and differential susceptibility to carcinogens: a review. Mutat Res. 2000; 463: 247-283. PMID: 11018744
40. Garte S, Taioli E, Popov T, Kalina I, Sram R, Farmer P. Role of GSTT1 deletion in DNA oxidative damage by exposure to polycyclic aromatic hydrocarbons in humans. Int J Cancer. 2007; 120: 2499-2503. PMID: 17330842