Cancer Letters
Volume 234, Issue 2 , Pages 220-231 , 28 March 2006

Bioactivation of 3-aminobenzanthrone, a human metabolite of the environmental pollutant 3-nitrobenzanthrone: evidence for DNA adduct formation mediated by cytochrome P450 enzymes and peroxidases

  • Volker M. Arlt

      Affiliations

    • Section of Molecular Carcinogenesis, Institute of Cancer Research, Brookes Lawley Building, Sutton, Surrey SM2 5NG, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44 208 722 4405; fax: +44 208 722 4052.
    • ,
  • Colin J. Henderson

      Affiliations

    • Cancer Research UK Molecular Pharmacology Unit, Biomedical Research Centre, Dundee DD1 9SY, UK
    • ,
  • C. Roland Wolf

      Affiliations

    • Cancer Research UK Molecular Pharmacology Unit, Biomedical Research Centre, Dundee DD1 9SY, UK
    • ,
  • Heinz H. Schmeiser

      Affiliations

    • Division of Molecular Toxicology, German Cancer Research Center, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany
    • ,
  • David H. Phillips

      Affiliations

    • Section of Molecular Carcinogenesis, Institute of Cancer Research, Brookes Lawley Building, Sutton, Surrey SM2 5NG, UK
    • ,
  • Marie Stiborova

      Affiliations

    • Department of Biochemistry, Faculty of Science, Charles University, Albertov 2030, 128 40 Prague 2, The Czech Republic

Received 2 February 2005 ,Revised 20 March 2005 ,Accepted 24 March 2005.

References 

  1. Vineis P, Forastiere F, Hoek G, Lipsett M. Outdoor air pollution and lung cancer: recent epidemiologic evidence. Int. J. Cancer. 2004;111:647–652
  2. Grashick E, Laden F, Hart JE, Rosner B, Smith TJ, Dockery DW, et al. Lung cancer in railroad workers exposed to diesel exhaust. Environ. Health Perspect. 2004;112:1539–1543
  3. IARC . Diesel and gasoline engine exhausts and some nitroarenes. Monographs on the Evaluation of Carcinogenic Risks to Humans, Lyon, No. 46. Lyon: International Agency for Research on Cancer; 1989;
  4. Tokiwa H, Sera N, Horikawa K, Nakanishi Y, Shigematu N. The presence of mutagens/carcinogens in the excised lung and analysis of lung cancer induction. Carcinogenesis. 1993;14:1933–1938
  5. US Environmental Protection Agency, Health Assessment Document for Diesel Engine Exhaust, EPA/600/8–90/057F, 2002.
  6. Enya T, Suzuki H, Watanabe T, Hirayama T, Hisamatsu Y. 3-Nitrobenzanthrone, a powerful bacterial mutagen and suspected human carcinogen found in diesel exhausts and airborne particulates. Environ. Sci. Technol. 1997;31:2772–2776
  7. Adachi S, Kawanura K, Takemoto K, Suzuki H, Hisamatsu Y. Carcinogenicity of 3-nitrobenzanthrone, a potent mutagen in diesel exhaust—preliminary results in F344 rats after intratracheal administration. In:  Heinrich U,  Mohr U editor. Relationships Between Respiratory Disease and Exposure to Air Pollution. Washington, DC: ILSI Press; 2000;p. 315–319
  8. Seidel A, Dahmann D, Krekeler H, Jacob J. Biomonitoring of polycyclic aromatic compounds in the urine of mining workers occupationally exposed to diesel exhaust. Int. J. Hyg. Environ. Health. 2002;204:333–338
  9. Arlt VM, Zhan L, Schmeiser HH, Honma M, Hayashi M, Phillips DH, et al. DNA adducts and mutagenic specificity of the ubiquitous environmental pollutant 3-nitrobenzanthrone in Muta Mouse. Environ. Mol. Mutagen. 2004;43:186–195
  10. Phousongphouang PT, Grosovsky AJ, Eastmond DA, Covarrubias M, Arey J. The genotoxicity of 3-nitrobenzanthrone and the nitropyrene lactones in human lymphoblasts. Mutat. Res. 2000;472:93–103
  11. Lamy E, Kassie F, Gminski R, Schmeiser HH, Mersch-Sundermann V. 3-Nitrobenzanthrone (3-NBA) induced micronucleus formation and DNA damage in human hepatoma (HepG2 cells) cells. Toxicol. Lett. 2003;146:103–109
  12. Arlt VM, Cole KJ, Phillips DH. Activation of 3-nitrobenzanthrone and its metabolites to DNA-damaging species in human B-lymphoblastoid MCL-5 cells. Mutagenesis. 2004;19:149–156
  13. Bieler CA, Wiessler M, Erdinger L, Suzuki H, Enya T, Schmeiser HH. DNA adduct formation from the mutagenic air pollutant 3-nitrobenzanthrone. Mutat. Res. 1999;439:307–311
  14. Bieler CA, Arlt VM, Wiessler M, Schmeiser HH. DNA adduct formation by the environmental contaminant 3-nitrobenzanthrone in V79 cells expressing human cytochrome P450 enzymes. Cancer Lett. 2003;200:9–18
  15. C.A. Bieler, M. Cornelius, R. Klein, V.M. Arlt, M. Wiessler, D.H. Phillips, H.H. Schmeiser, DNA adduct formation by the environmental contaminant 3-nitrobenzanthrone after intratracheal instillation in rats. Int. J. Cancer, in press.
  16. Borlak J, Hansen T, Yuan Z, Sikka HC, Kumar S, Schmidbauer S, et al. Metabolism and DNA-binding of 3-nitrobenzanthrone in primary rat alveolar type II cells, in human fetal bronchial, rat epithelial and mesenchymal cell lines. Polycyclic Aromat. Compd. 2000;21:73–86
  17. Kawanishi M, Enya T, Suzuki H, Takebe H, Matsui S, Yagi T. Postlabelling analysis of DNA adducts formed in human hepatoma cells treated with 3-nitrobenzanthrone. Mutat. Res. 2000;470:133–139
  18. Arlt VM, Bieler CA, Mier W, Wiessler M, Schmeiser HH. DNA adduct formation by the ubiquitous environmental contaminant 3-nitrobenzanthrone in rats determined by 32P-postlabeling. Int. J. Cancer. 2001;93:450–454
  19. Arlt VM, Glatt H, Muckel E, Pabel U, Sorg BL, Schmeiser HH, et al. Metabolic activation of the environmental contaminant 3-nitrobenzanthrone by human acetyltransferases and sulfotransferase. Carcinogenesis. 2002;23:1937–1945
  20. Arlt VM, Sorg BL, Osborne M, Hewer A, Seidel A, Schmeiser HH, et al. DNA adduct formation by the ubiquitous environmental pollutant 3-nitrobenzanthrone and its metabolites in rats. Biochem. Biophys. Res. Commun. 2003;300:107–114
  21. Arlt VM, Glatt H, Muckel E, Pabel U, Sorg BL, Seidel A, et al. Activation of 3-nitrobenzanthrone and its metabolites by human acetyltransferases, sulfotransferases and cytochrome P450 expressed in Chinese hamster V79 cells. Int. J. Cancer. 2003;105:583–592
  22. Arlt VM, Stiborova M, Hewer A, Schmeiser HH, Phillips DH. Human enzymes involved in the metabolic activation of the environmental contaminant 3-nitrobenzanthrone: evidence for reductive activation by human NADPH:cytochrome P450 reductase. Cancer Res. 2003;63:2752–2761
  23. V.M. Arlt, M. Stiborova, C.J. Henderson, M.R. Osborne, C.A. Bieler, E. Frei, et al. The environmental pollutant and potent mutagen 3-nitrobenzanthrone forms DNA adducts after reduction by NAD(P)H:quinone oxidoreductase and conjugation by acetyltransferases and sulfotransferases in human hepatic cytosols. Cancer Res. 65 (2005) 2644–2652.
  24. Arlt VM, Hewer A, Sorg BL, Schmeiser HH, Phillips DH, Stiborova M. 3-Aminobenzanthrone, a human metabolite of the environmental pollutant 3-nitrobenzanthrone, forms DNA adducts after metabolic activation by human and rat liver microsomes: evidence for activation by cytochrome P450 1A1 and P450 1A2. Chem. Res. Toxicol. 2004;17:1092–1101
  25. Grabchev I, Moneva I, Betcheva R, Elyashevich G. Colored microporous polyethylene films: effect of porous structure on dye adsorption. Mater. Res. Innovat. 2002;6:34–37
  26. Sykora J, Mudago V, Hutterer R, Nepras M, Vanerka J, Kapusta P, et al. ABA-C-15: a new dye for probing solvent relaxation in phospholipid bilayers. Langmuir. 2002;18:9276–9282
  27. Stiborova M, Frei E, Schmeiser HH, Anzenbacher P. The role of peroxidases in the activation of chemical carcinogens. Drug Metabol. Interact. 1991;9:177–190
  28. Stiborova M, Frei E, Breuer A, Wiessler M, Schmeiser HH. Evidence for reductive activation of carcinogenic aristolochic acids by prostaglandin H synthase—32P-postlabeling analysis of DNA adduct formation. Mutat. Res. 2001;493:149–160
  29. Stiborova M, Miksanova M, Havlicek V, Schmeiser HH, Frei E. Mechanism of peroxidase-mediated oxidation of carcinogenic o-anisidine and its binding to DNA. Mutat. Res. 2002;500:49–66
  30. Schmeiser HH, Frei E, Wiessler M, Stiborova M. Comparison of DNA adduct formation by aristolochic acids in various in vitro activation systems by 32P-post-labelling: evidence for reductive activation by peroxidases. Carcinogenesis. 1997;18:1055–1062
  31. Culp SJ, Roberts DW, Talaska G, Lang NP, Fu PP, Lay JO, et al. Immunochemical, 32P-postlabeling, and GC/MS detection of 4-aminobiphenyl-DNA adducts in human peripheral lung in relation to metabolic activation pathways involving pulmonary N-oxidation, conjugation, and peroxidation. Mutat. Res. 1997;378:97–112
  32. Williams J, Stone EM, Millar BC, Gusterson BA, Grover PL, Phillips DH. Determination of the enzymes responsible for activation of the heterocyclic amine 2-amino-3-methylimidazo[4,5-f]quinoline in the human breast. Pharmacogenetics. 1998;8:519–528
  33. Williams JA, Stone EM, Millar BC, Hewer A, Phillips DH. Pathways of heterocyclic amine activation in the breast: DNA adducts of 2-amino-3-methylimidazo[4,5-f]quinoline (IQ) formed by peroxidases and in human mammary epithelial cells and fibroblasts. Mutagenesis. 2000;15:149–154
  34. Gorlewska-Roberts KM, Teitel CH, Lay JO, Roberts DW, Kadlubar FF. Lactoperoxidase-catalyzed activation of carcinogenic aromatic and heterocyclic amines. Chem. Res. Toxicol. 2004;17:1659–1666
  35. Stiborova M, Frei E, Hodek P, Wiessler M, Schmeiser HH. Human hepatic and renal microsomes, cytochromes P450 1A1/2, NADPH:Cytochrome P450 reductase and prostaglandin H synthase mediate the formation of aristolochic acid-DNA adducts found in patients with urothelial cancer. Int. J. Cancer. 2005;113:189–197
  36. Stiborova M, Frei E, Wiessler M, Schmeiser HH. Human cytochrome P450 enzymes involved in the metabolic activation of carcinogenic aristolochic acids: evidence for reductive activation by CYP1A1 and CYP1A2. Chem. Res. Toxicol. 2001;14:1128–1137
  37. Henderson CJ, Otto DME, Carrie D, Magnuson MA, McLaren AW, Rosewell I, et al. Inactivation of the hepatic cytochrome P450 system by conditional deletion of hepatic cytochrome P450 reductase. J. Biol. Chem. 2003;278:13480–13486
  38. Henderson CJ, Otto DM, McLaren AW, Carrie D, Wolf CR. Knockout mice in xenobiotic metabolism. Drug Metab. Rev. 2003;35:385–392
  39. Williams JA. Single nucleotide polymorphisms, metabolic activation and environmental carcinogenesis: why molecular epidemiologists should think about enzyme expression. Carcinogenesis. 2001;22:209–214
  40. Wiese FW, Thompson PA, Kadlubar FF. Carcinogen substrate specificity of human COX-1 and COX-2. Carcinogenesis. 2001;21:5–10
  41. Williams JA, Phillips DH. Mammary expression of xenobiotic metabolizing enzymes and their potential role in breast cancer. Cancer Res. 2000;60:4667–4677
  42. Noguchi N, Nakano K, Aratani Y, Koyama H, Kodama T, Niki E. Role of myeloperoxidase in the neutrophil-induced oxidation of low density lipoprotein as studied by myeloperoxidase-knockout mouse. J. Biochem. (Tokyo). 2000;127:971–976

PII: S0304-3835(05)00278-8

doi: 10.1016/j.canlet.2005.03.035

Cancer Letters
Volume 234, Issue 2 , Pages 220-231 , 28 March 2006

Article Tools

* Image Usage & Resolution