Influence of the metabolic properties of human cells on the kinetic of formation of the major benzo[a]pyrene DNA adducts

Journal of Applied Toxicology

Volumn 28, Issue 5, 2008, Pages 579-590

  Marie, Caroline ^a,b   Maître, Anne ^b   Douki, Thierry ^a   Gateau, Mathilde ^a,c   Tarantini, Adeline ^b   Guiraud, Pascale ^b   Favier, Alain ^a   Ravanat, Jean Luc ^a  

^a CEA GRENOBLE   (France)

^b UNIV GRENOBLE ALPES   (France)

^c Laboratoire de Spectrometrie Physique   (France)

Author keywords

Benzo a pyrene; Benzo a pyrene diol epoxide; DNA adducts; DNA repair; Metabolism; Tandem mass spectrometry

Indexed keywords

BASE; BENZO[A]PYRENE DERIVATIVE; BIOLOGICAL MARKER; CATION; DNA; PYRENE DERIVATIVE;

ARTICLE; CELL LINE; CELL METABOLISM; CONTROLLED STUDY; DNA ADDUCT; DNA DAMAGE; DRUG EXPOSURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; KERATINOCYTE; KINETICS; LIVER CELL; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY;

EID: 47549119258     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1306     Document Type: Article

References (44)

1. Aden DP, Fogel A, Plotkin S, Damjanov I, Knowles BB. 1979. Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature 282(5739): 615-616.
2. Bacon JR, Williamson G, Garner RC, Lappin G, Langouet S, Bao Y. 2003. Sulforaphane and quercetin modulate PhIP-DNA adduct formation in human HepG2 cells and hepatocytes. Carcinogenesis 24: 1903-1911.
3. Baird WM, Hooven LA, Mahadevan B. 2005. Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ. Mol. Mutagen. 45: 106-114.
4. Balu N, Padgett WT, Lambert GR, Swank AE, Richard AM, Nesnow S. 2004. Identification and characterization of novel stable deoxyguanosine and deoxyadenosine adducts of benzo[a]pyrene-7,8-quinone from reactions at physiological pH. Chem. Res. Toxicol. 17: 827-838.
5. Banasiewicz M, Nelson G, Swank A, Grubor N, Ross J, Nesnow S, Kofeler H, Small GJ, Jankowiak R. 2004. Identification and quantitation of benzo[a]pyrene-derived DNA adducts formed at low adduction level in mice lung tissue. Anal. Biochem. 334: 390-400.
6. Barry JP, Norwood C, Vouros P. 1996. Detection and identification of benzo[a]pyrene diol epoxide adducts to DNA utilizing capillary electrophoresis-electrospray mass spectrometry. Anal. Chem. 68: 1432-1438.
7. Binkova B, Sram RJ. 2004. The genotoxic effect of carcinogenic PAHs, their artificial and environmental mixtures (EOM) on human diploid lung fibroblasts. Mutat. Res. 547: 109-121.
8. Boffetta P, Jourenkova N, Gustavsson P. 1997. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control 8: 444-472.
9. Bouchard M, Viau C. 1997. Urinary excretion of benzo[a]pyrene metabolites following intravenous, oral, and cutaneous benzo[a]pyrene administration. Can. J. Physiol. Pharmacol. 75: 185-192.
10. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell. Biol. 106: 761-771.
11. Boysen G, Hecht SS. 2003. Analysis of DNA and protein adducts of benzo[a]pyrene in human tissues using structure-specific methods. Mutat. Res. 543: 17-30.
12. Briede JJ, Godschalk RW, Emans MT, De Kok TM, Van Agen E, Van Maanen J, Van Schooten FJ, Kleinjans JC. 2004. In vitro and in vivo studies on oxygen free radical and DNA adduct formation in rat lung and liver during benzo[a]pyrene metabolism. Free Radic. Res. 38: 995-1002.
13. Buening MK, Wislocki PG, Levin W, Yagi H, Thakker DR, Akagi H, Koreeda M, Jerina DM, Conney AH. 1978. Tumorigenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides in newborn mice: exceptional activity of (+)-7 beta,8 alpha-dihydroxy-9 alpha,10 alpha-epoxy-7,8,9,10-tetrahydrobenzo-[a]pyrene. Proc. Natl Acad. Sci. USA 75: 5358-5361.
14. Chen L, Devanesan PD, Higginbotham S, Ariese F, Jankowiak R, Small GJ, Rogan EG, Cavalieri EL. 1996. Expanded analysis of benzo[a]pyrene-DNA adducts formed in vitro
15. and in mouse skin: their significance in tumor initiation. Chem. Res. Toxicol. 9: 897-903.
16. de Kok TM, Moonen HJ, van Delft J, van Schooten FJ. 2002. Methodologies for bulky DNA adduct analysis and biomonitoring of environmental and occupational exposures. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 778: 345-355.
17. Dreij K, Seidel A, 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.
18. Farmer PB. 2004. DNA and protein adducts as markers of genotoxicity. Toxicol. Lett. 149: 3-9.
19. Godschalk RW, Moonen EJ, Schilderman PA, Broekmans WM, Kleinjans JC, Van Schooten FJ. 2000. Exposure-route-dependent DNA adduct formation by polycyclic aromatic hydrocarbons. Carcinogenesis 21: 87-92.
20. Guetens G, De Boeck G, Highley MS, Wood M, Maes RA, Eggermont AA, Hanauske A, de Bruijn EA, Tjaden UR. 2002. Hyphenated techniques in anticancer drug monitoring. II. Liquid chromatography-mass spectrometry and capillary electrophoresis-mass spectrometry. J. Chromatogr. A 976: 239-247.
21. Kaneko M, Cerutti PA. 1982. Excision of benzo[a]pyrene diol epoxide I adducts from nucleosomal DNA of confluent normal human fibroblasts. Chem. Biol. Interact. 38: 261-274.
22. Kapitulnik J, Wislocki PG, Levin W, Yagi H, Jerina DM, Conney AH. 1978. Tumorigenicity studies with diol-epoxides of benzo(a)pyrene which indicate that (+/-)-trans-7 beta,8 alpha-dihydroxy-9 alpha,10 alpha-epoxy-7,8,9,10- tetrahydrobenzo(a)pyrene is an ultimate carcinogen in newborn mice. Cancer Res. 38: 354-358.
23. Knasmuller S, Parzefall W, Sanyal R, Ecker S, Schwab C, Uhl M, Mersch-Sundermann V, Williamson G, Hietsch G, Langer T, Darroudi F, Natarajan AT. 1998. Use of metabolically competent human hepatoma cells for the detection of mutagens and anti-mutagens. Mutat. Res. 402: 185-202.
24. Koc H, Swenberg JA. 2002. Applications of mass spectrometry for quantitation of DNA adducts. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 778: 323-343.
25. Mastrangelo G, Fadda E, Marzia V. 1996. Polycyclic aromatic hydrocarbons and cancer in man. Environ. Health Perspect. 104: 1166-1170.
26. McCoull KD, Rindgen D, Blair LA, Penning TM. 1999. Synthesis and characterization of polycyclic aromatic hydrocarbon o-quinone depurinating N7-guanine adducts. Chem. Res. Toxicol. 12: 237-246.
27. Misaki K, Matsui S, Matsuda T. 2007. Metabolic enzyme induction by HepG2 cells exposed to oxygenated and nonoxygenated polycyclic aromatic hydrocarbons. Chem. Res. Toxicol. 20: 277-283.
28. Osborne MR, Harvey RG, Brookes P. 1978. The reaction of trans-7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo(a)pyrene with DNA involves attack at the N7-position of guanine moieties. Chem. Biol. Interact. 20: 123-130.
29. Park JH, Troxel AB, Harvey RG, Penning TM. 2006. Polycyclic aromatic hydrocarbon (PAH) o-quinones produced by the aldoketo-reductases (AKRs) generate abasic sites, oxidized pyrimidines, and 8-oxo-dGuo via reactive oxygen species. Chem. Res. Toxicol. 19: 719-728.
30. Perera FP, Weinstein IB. 2000. Molecular epidemiology: recent advances and future directions. Carcinogenesis 21: 517-524.
31. RamaKrishna NV, Gao F, Padmavathi NS, CavaUeri EL, Rogan EG, Cemy RL, Gross ML. 1992. Model adducts of benzo[a]pyrene and nucleosides formed from its radical cation and diol epoxide. Chem. Res. Toxicol. 5: 293-302.
32. Ravanat JL, Douki T, Duez P, Gremaud E, Herbert K, Hofer T, Lasserre L, Saint-Pierre C, Favier A, Cadet J. 2002. Cellular background level of 8-oxo-7,8-dihydro-2′-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up. Carcinogenesis 23: 1911-1918.
33. Rogan EG, CavaUeri EL, Tibbels SR, Cremonesi P, Warner CD, Nagel DL, Tomer KB, Cerny RL, Gross ML. 1988. Synthesis and identification of benzo[a]pyrene-guanine nucleoside adducts formed by electrochemical oxidation and by horseradish peroxidase catalysed reaction of benzo[a]pyrene with DNA. J. Am. Chem. Soc. 110: 4023-4029.
34. Ruan Q, Kim HY, Jiang H, Penning TM, Harvey RG, Blair IA. 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.
35. Sayer J, Chadha A, Agarwal S, Yeh H, Yagi H, Jerina D. 1990. 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.
36. Shen YM, Troxel AB, Vedantam S, Penning TM, Field J. 2006. Comparison of p53 mutations induced by PAH o-quinones with those caused by anti-benzo[a]pyrene diol epoxide in vitro: role of reactive oxygen and biological selection. Chem. Res. Toxicol. 19: 1441-1450.
37. Singh R, Farmer PB. 2006. Liquid chromatography-electrospray ionization-mass spectrometry: the future of DNA adduct detection. Carcinogenesis 27: 178-196.
38. Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, Cogliano V. 2005. Carcinogenicity of polycyclic aromatic hydrocarbons. Lancet Oncol. 6: 931-932.
39. Tang D, Phillips DH, Stampfer M, Mooney LA, Hsu Y, Cho S, Tsai W, Ma J, Cole KJ, Ni Shé M, Perera FP. 2001. Association between carcinogen-DNA adducts in white blood cells and lung cancer risk in the physicians health study. Cancer Res. 61: 6708-6712.
40. Veglia F, Matullo G, Vineis P. 2003. Bulky DNA adducts and risk of cancer: a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 12: 157-160.
41. Wang JJ, Marshall WD, Frazer DG, Law B, Lewis DM. 2003a. Characterization of DNA adducts from lung tissue of asphalt fume-exposed mice by nanoflow liquid chromatography quadrupole time-of-flight mass spectrometry. Anal. Biochem. 322: 79-88.
42. Wang JJ, Marshall WD, Law B, Lewis DM. 2003b. Fragmentation patterns of DNA-benzo(a)pyrene diol epoxide adducts characterized by nanoflow LC/quadrupole time-of-flight mass spectrometry. Int. J. Mass Spectrom. 230: 45-55.
43. Xue W, Warshawsky D. 2005. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol. Appl. Pharmacol. 206: 73-93.
44. Yang SC, Jenq SN, Kang ZC, Lee H. 2000. Identification of benzo[a]pyrene 7,8-diol 9,10-epoxide N2-deoxyguanosine in human lung adenocarcinoma cells exposed to cooking oil fumes from frying fish under domestic conditions. Chem. Res. Toxicol. 13: 1046-1050.