3-Aminobenzanthrone, a human metabolite of the carcinogenic environmental pollutant 3-nitrobenzanthrone, induces biotransformation enzymes in rat kidney and lung

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 676, Issue 1, 2009, Pages 93-101

  Stiborová, Marie ^a   Dračínská, Helena ^a   Martínková, Markéta ^a   Mizerovská, Jana ^a   Hudeček, Jiří ^a   Hodek, Petr ^a   Liberda, Jiří ^a   Frei, Eva ^b   Schmeiser, Heinz H ^b   Phillips, David H ^c   Arlt, Volker M ^c  

^a CHARLES UNIVERSITY   (Czech Republic)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

3 Aminobenzanthrone; 3 Nitrobenzanthrone; Cytochrome P450 1A1; DNA adducts; Induction; NAD(P)H:quinone oxidoreductase

Indexed keywords

3 AMINOBENZANTHRONE; 3 NITROBENZANTHRONE; CYTOCHROME P450 1A; CYTOCHROME P450 1A1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); UNCLASSIFIED DRUG;

AIR POLLUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENIC ACTIVITY; CARCINOGENICITY; CHEMICAL STRUCTURE; CONTROLLED STUDY; DNA ADDUCT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME METABOLISM; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT;

ANIMALS; BENZ(A)ANTHRACENES; BIOTRANSFORMATION; CARCINOGENS, ENVIRONMENTAL; CYTOCHROME P-450 CYP1A1; DNA ADDUCTS; HUMANS; KIDNEY; LUNG; MALE; MICROSOMES; NAD(P)H DEHYDROGENASE (QUINONE); RATS; RATS, WISTAR;

ANIMALIA; RATTUS;

EID: 67349090920     PISSN: 13835718     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2009.04.013     Document Type: Article

References (73)

1. Hansen T., Seidel A., and Borlak J. The environmental carcinogen 3-nitrobenzanthrone and its main metabolite 3-aminobenzanthrone enhance formation of reactive oxygen intermediates in human A549 lung epithelial cells. Toxicol. Appl. Pharmacol. 221 (2007) 222-234
2. Svobodová M., Šístková J., Dračínská H., Hudeček J., Hodek P., Schmeiser H.H., Arlt V.M., Frei E., and Stiborová M. Reductive activation of environmental pollutants 3-nitrobenzanthrone and 2-nitrobenzanthrone. Chem. Listy 100 (2007) s277-s279
3. Enya T., Suzuki H., Watanabe T., Hirayama T., and Hisamatsu Y. 3-Nitrobenzanthrone, a powerful bacterial mutagen and suspected human carcinogen found in diesel exhausts and airborne particulates. Environ. Sci. Technol. 31 (1997) 2772-2776
4. Seidel A., Dahmann D., Krekeler H., and Jacob J. Biomonitoring of polycyclic aromatic compounds in the urine of mining workers occupationally exposed to diesel exhaust. Int. J. Hyg. Environ. Health 204 (2002) 333-338
5. Arlt V.M. 3-Nitrobenzanthrone, a potential human cancer hazard in diesel exhaust and urban air pollution: a review of the evidence. Mutagenesis 20 (2005) 399-410
6. Nagy E., Zeisig M., Kawamura K., Hisumatsu Y., Sugeta A., Adachi S., and Moller L. DNA-adduct and tumor formations in rats after intratracheal administration of the urban air pollutant 3-nitrobenzanthrone. Carcinogenesis 26 (2005) 1821-1828
7. Borlak J., Hansen T., Yuan Z., Sikka H.C., Kumar S., Schmidbauer S., Frank H., Jacob J., and Seidel A. 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. 21 (2000) 73-86
8. Grabchev I., Moneva I., Betcheva R., and Elyashevich G. Colored microporous polyethylene films: effect of porous structure on dye adsorption. Mater. Res. Innovat. 6 (2002) 34-37
9. Sykora J., Mudago V., Hutterer R., Nepras M., Vanerka J., Kapusta P., Fidler V., and Hof M. ABA-C-15: a new dye for probing solvent relaxation in phospholipid bilayers. Langmuir 18 (2002) 9276-9282
10. 32P-postlabeling. Int. J. Cancer 93 (2001) 450-454
11. Arlt V.M., Sorg B.L., Osborne M., Hewer A., Seidel A., Schmeiser H.H., and Phillips D.H. DNA adduct formation by the ubiquitous environmental pollutant 3-nitrobenzanthrone and its metabolites in rats. Biochem. Biophys. Res. Commun. 300 (2003) 107-114
12. Arlt V.M., Hewer A., Sorg B.L., Schmeiser H.H., Phillips D.H., and Stiborová 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. 17 (2004) 1092-1101
13. Arlt V.M., Stiborová M., Henderson C.J., Osborne M.R., Bieler C.A., Frei E., Martínek V., Sopko B., Wolf C.R., Schmeiser H.H., and Phillips D.H. 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
14. Arlt V.M., Henderson C.J., Wolf C.R., Schmeiser H.H., Phillips D.H., and Stiborová M. 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. Cancer Lett. 234 (2006) 220-231
15. 6 position of adenine. Int. J. Cancer 118 (2006) 2139-2146
16. Bieler C.A., Cornelius M., Klein R., Arlt V.M., Wiessler M., Phillips D.H., and Schmeiser H.H. DNA adduct formation by the environmental contaminant 3-nitrobenzanthrone after intratracheal instillation in rats. Int. J. Cancer 118 (2005) 833-838
17. Bieler C.A., Cornelius M.G., Stiborova M., Arlt V.M., Wiessler M., Phillips D.H., and Schmeiser H.H. Formation and persistence of DNA adducts formed by the carcinogenic air pollutant 3-nitrobenzanthrone in target and non-target organs after intratracheal instillation in rats. Carcinogenesis 28 (2007) 1117-1121
18. Arlt V.M., Zhan L., Schmeiser H.H., Honma M., Hayashi M., Phillips D.H., and Suzuki T. DNA adducts and mutagenic specificity of the ubiquitous environmental pollutant 3-nitrobenzanthrone in Muta Mouse. Environ. Mol. Mutagen. 43 (2004) 186-195
19. Vom Brocke J., Krais A., Whibley C., Hollstein M.C., and Schmeiser H.H. The carcinogenic air pollutant 3-nitrobenzanthrone induces GC to TA transversion mutations in human p53 sequences. Mutagenesis 24 (2009) 17-23
20. Stiborová M., Dračínská H., Hájková J., Kadeřábková P., Frei E., Schmeiser H.H., Souček P., Phillips D.H., and Arlt V.M. The environmental pollutant and carcinogen 3-nitrobenzanthrone and its human metabolite 3-aminobenzanthrone are potent inducers of rat hepatic cytochromes P450 1A1 and -1A2 and NAD(P)H:quinone oxidoreductase. Drug Metab. Dispos. 34 (2006) 1398-1405
21. Stiborová M., Dračínská H., Mizerovská J., Frei E., Schmeiser H.H., Hudeček J., Hodek P., Phillips D.H., and Arlt V.M. The environmental pollutant and carcinogen 3-nitrobenzanthrone induces cytochrome P450 1A1 and NAD(P)H:quinone oxidoreductase in rat lung and kidney, thereby enhancing its own genotoxicity. Toxicology 247 (2008) 11-22
22. 32P-postlabelling assay for DNA adducts. Nat. Protoc. 2 (2007) 2772-2781
23. Arlt V.M., Glatt H.R., Muckel E., Pabel U., Sorg B.L., Seidel A., Frank H., Schmeiser H.H., and Phillips D.H. Activation of 3-nitrobenzanthrone and its metabolites by human acetyltransferases, sulfotransferases and cytochrome P450 expressed in Chinese hamster V79 cells. Int. J. Cancer 105 (2003) 583-592
24. Stiborová M., Frei E., Sopko B., Sopková K., Marková V., Laňková M., Kumstýřová T., Wiessler M., and Schmeiser H.H. Human cytosolic enzymes involved in the metabolic activation of carcinogenic aristolochic acid: evidence for reductive activation by human NAD(P)H:quinone oxidoreductase. Carcinogenesis 24 (2003) 1695-1703
25. Stiborová M., Frei E., Hodek P., Wiessler M., and Schmeiser H.H. 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 113 (2005) 189-197
26. Arlt V.M., Stiborová M., Hewer A., Schmeiser H.H., and Phillips D.H. 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. 63 (2003) 2752-2761
27. Stiborová M., Martínek V., Rýdlová H., Hodek P., and Frei E. Sudan I is a potential carcinogen for humans: evidence for its metabolic activation and detoxication by human recombinant cytochrome P450 1A1 and liver microsomes. Cancer Res. 62 (2002) 5678-5684
28. Stiborová M., Martínek V., Rýdlová H., Koblas T., and Hodek P. Expression of cytochrome P450 1A1 and its contribution to oxidation of a potential human carcinogen 1-phenylazo-2-naphthol (Sudan I) in human livers. Cancer Lett. 220 (2005) 145-154
29. Eling T.E., Thompson D.C., Foureman G.L., Curtis J.F., and Hughes M.F. Prostaglandin H synthase and xenobiotic oxidation. Annu. Rev. Pharmacol. Toxicol. 30 (1990) 1-45
30. 32P-postlabeling analysis of DNA adduct formation. Mutat. Res. 493 (2001) 149-160
31. Stiborová M., Poljaková J., Ryšlavá H., Dračínský M., Eckschlager T., and Frei E. Mammalian peroxidases activate anticancer drug ellipticine to intermediates forming deoxyguanosine adducts in DNA identical to those found in vivo and generated from 12-hydroxyellipticine and 13-hydroxyellipticine. Int. J. Cancer 120 (2007) 243-251
32. Drahushuk A.T., McGarrigle B.P., Larsen K.E., Stegeman J.J., and Olson J.R. Detection of CYP1A1 protein in human liver and induction by TCDD in precision-cut liver slices incubated in dynamic organ culture. Carcinogenesis 19 (1998) 1361-1368
33. Rendic S., and DiCarlo F.J. Human cytochrome P450 enzymes: a status report summarizing their reactions, substrates, inducers, and inhibitors. Drug Metab. Rev. 29 (1997) 413-480
34. Hukkanen J., Pelkonen O., Hakkola J., and Raunio H. Expression and regulation of xenobiotic-metabolizing cytochrome P450 (CYP) enzymes in human lung. Crit. Rev. Toxicol. 32 (2002) 391-411
35. Ross D., Kepa J.K., Winski S.L., Beall H.D., Anwar A., and Siegel D. NAD(P)H:quinone oxidoreductase (NQO1): chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem. Biol. Interact. 129 (2000) 77-97
36. Prestera T., Holtzclaw W.D., Zhang Y., and Talalay P. Chemical and molecular regulation of enzymes that detoxify carcinogens. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 2965-2969
37. Li Y., and Jaiswal A.K. Human antioxidant-response-element-mediated regulation of type 1 NAD(P)H:quinone oxidoreductase gene expression. Effect of sulfhydryl modifying agents. Eur. J. Biochem. 226 (1994) 31-39
38. Jaiswal A.K. Antioxidant response element. Biochem. Pharmacol. 48 (1994) 439-444
39. Schulz W.A., Krummeck A., Rosinger I., Eickelman P., Neuhaus C., Ebert T., Schmitz-Drager B.J., and Sies H. Increased frequency of a null-allele for NAD(P)H-quinone oxidoreductase in patients with urological malignancies. Pharmacogenetics 7 (1997) 235-239
40. Chen R.M., Chou M.W., and Ueng T.H. Induction of cytochrome P450 1A in hamster liver and lung by 6-nitrochrysene. Arch. Toxicol. 72 (1998) 395-401
41. Wiemels J., Pagnamenta A., Taylor G.M., Eden O.B., Alexander F.E., and Greaves M.F. A lack of functional NAD(P)H:quinone oxidoreductase allele is selectively associated with pediatric leukemias that have MLL fusions. United Kingdom Childhood Cancer Study Investigators. Cancer Res. 59 (1999) 4095-4099
42. Dickins M. Induction of cytochromes P450. Curr. Top. Med. Chem. 4 (2004) 1745-1766
43. D'Alo A., Voso M., Guidy F., Kaseiny G., Sica S., Pagano L., Hohaus S., and Leone G. Polymorphisms of CYP1A1 and glutathione S-transferase and susceptibility to adult acute myeloid leukaemia. Haematologica 89 (2004) 664-670
44. Yang C.-X., Matsuo K., Wang Z., and Tajima K. Phase I/II enzyme gene polymorphisms and esophageal cancer risk: a meta-analysis of the literature. World J. Gastroenterol. 11 (2005) 2534-2538
45. Li Y., Millikan R., Bell D., Cui L., Tse C., Newman B., and Conway K. Cigarette smoking, cytochrome P450 1A1 polymorphisms, and breast cancer among African-American and white women. Breast Cancer Res. 6 (2004) R460-R473
46. Li Y., Millikan R., Bell D., Cui L., Tse C., Newman B., and Conway K. Polychlorinated biphenyls, cytochrome P450 1A1 (CYP1A1) polymorphisms, and breast cancer risk among African American women and white women in North Carolina: a population-based case-control study. Breast Cancer Res. 7 (2005) R12-R18
47. Lubet R.A., Connolly G., Kouri R.E., Nebert D.W., and Bigelow S.W. Biological effects of the Sudan dyes. Role of the Ah cytosolic receptor. Biochem. Pharmacol. 15 (1983) 3053-3058
48. Fujita S., Suzuki M., Peisach J., and Suzukii T. Induction of hepatic microsomal drug metabolism by azo compounds: a structure-activity relationship. Chem. Biol. Interact. 52 (1984) 15-37
49. De Long M.J., Prochaska H.J., and Talalay P. Induction of NAD(P)H:quinone reductase in murine hepatoma cells by phenolic antioxidants, azo dyes, and other chemoprotectors: a model system for the study of anticarcinogens. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 787-791
50. De Long M.J., Santamaria A.B., Prochaska H.J., and Talalay P. Role of cytochrome P1-450 in the induction of NAD(P)H:quinone reductase in a murine hepatoma cell line and its mutants. Carcinogenesis 8 (1987) 1549-1553
51. Stiborová M., Asfaw B., Anzenbacher P., Lešetický L., and Hodek P. The first identification of the benzenediazonium ion formation from a non-aminoazo dye, 1-phenylazo-2-hydroxynaphthalene (Sudan I) by microsomes of rat livers. Cancer Lett. 40 (1988) 319-326
52. Refat N.A., Ibrahim Z.S., Moustafa G.G., Sakamoto K.Q., Ishizuka M., and Fujita S. The induction of cytochrome P450 1A1 by Sudan dyes. J. Biochem. Mol. Toxicol. 22 (2008) 77-84
53. Cresteil T., Le Provost E., Leroux J.P., and Lesca P. Enzymatic and immunological characterization of cytochromes P 450 from ellipticine-treated rat liver. Biochem. Biophys. Res. Commun. 107 (1982) 1037-1045
54. Cresteil T., and Lesca P. Enhancement of DNA binding, mutagenicity and carcinogenicity of polycyclic aromatic hydrocarbons after induction of cytochrome P-450 by ellipticines in rats and mice. Chem. Biol. Interact. 47 (1983) 145-156
55. Fernandez N., Roy M., and Lesca P. Binding characteristics of Ah receptors from rats and mice before and after separation from hepatic cytosols. 7-Hydroxyellipticine as a competitive antagonist of cytochrome P-450 induction. Eur. J. Biochem. 172 (1988) 585-592
56. Gasiewicz T.A., Kende R.S., Rucci G., Whitney B., and Willey J.J. Analysis of structural requirements for Ah receptor antagonist activity: ellipticines, flavones, and related compounds. Biochem. Pharmacol. 52 (1996) 1787-1830
57. Chang C.-Y., and Puga A. Constitutive activation of the aromatic hydrocarbon receptor. Mol. Cell. Biol. 18 (1998) 525-535
58. Wei Y.D., Bergander L., Rannug U., and Rannug A. Regulation of CYP1A1 transcription via the metabolism of the tryptophan-derived 6-formylindolo[3,2-b]carbazole. Arch. Biochem. Biophys. 383 (2000) 99-107
59. Aimová D., Svobodová L., Kotrbová V., Mrázová B., Hodek P., Hudeček J., Václavíková R., Frei E., and Stiborová M. The anticancer drug ellipticine is a potent inducer of rat cytochromes P450 1A1 and 1A2, thereby modulating its own metabolism. Drug Metab. Dispos. 35 (2007) 1926-1934
60. Stiborová M., Dračínská H., Aimová D., Hodek P., Hudeček J., Ryšlavá H., Schmeiser H.H., and Frei E. The anticancer drug ellipticine is an inducer of rat NAD(P)H:quinone oxidoreductase. Collect. Czech Chem. Commun. 72 (2007) 1350-1364
61. Dagawa M., Nakayama M., Konno Y., Masobuchi K., and Yamazou Y. 2-Methoxy-4-nitroaniline and its isomers induce cytochrome P450 1A (CYP1A) enzymes with different selectivities in the rat livers. Biochim. Biophys. Acta 1379 (1998) 391-398
62. Pan J., Hong J.-Y., Li D., Schuetz E.G., Guzelian P.S., Huang W., and Yang C.S. Regulation of cytochrome P450 2B1/2 genes by diallyl sulfone, disufiram, and other organosulfur compounds in primary cultures of rat hepatocytes. Biochem. Pharmacol. 45 (1993) 2323-2329
63. Iba M.M., Fung J., Pak Y.M., Thomas P.E., Fisher H., Sekowski A., Halladay A.K., and Wagner G.C. Dose-dependent up-regulation of rat pulmonary, renal, and hepatic cytochrome P-450 (CYP) 1A expression by nicotine feeding. Drug Metab. Dispos. 27 (1999) 977-982
64. Iba M.M., Fung J., Giannone J.V., and Okey A.B. Comparative induction of CYP1A1 expression by pyridine and its metabolites. Arch. Biochem. Biophys. 378 (2000) 299-310
65. Kitamura R., Matsuoka K., Nagayama S., and Otagiri M. Time-dependent induction of rat hepatic CYP1A1 and CYP1A2 expression after single-dose administration of the anti-angiogenic agent TSU-68. Drug Metab. Pharmacokinet. 23 (2008) 421-427
66. Zhang Q.Y., Wikoff J., Dunbar D., Fasco M., and Kaminsky L. Regulation of cytochrome P4501A1 expression in rat small intestine. Drug Metab. Dispos. 25 (1997) 21-26
67. Meredith C., Scott M.P., Renwick A.B., Price R.J., and Lake B.G. Studies on the induction of rat hepatic CYP1A, CYP2B, CYP3A and CYP4A subfamily form mRNAs in vivo and in vitro using precision-cut rat liver slices. Xenobiotica 33 (2003) 511-527
68. Shih H., Pickwell G.V., Guenette D.K., Bilir B., and Quattrochi L.C. Species differences in hepatocyte induction of CYP1A1 and CYP1A2 by omeprazole. Hum. Exp. Toxicol. 18 (1999) 95-105
69. Zhang Z.Y., Pelletier R.D., Wong Y.N., Sugawara M., Zhao N., and Littlefield B.A. Preferential inducibility of CYP1A1 and CYP1A2 by TCDD: differential regulation in primary human hepatocytes versus transformed human cells. Biochem. Biophys. Res. Commun. 10 (2006) 399-407
70. Yamazoe Y., Zenser T.V., Miller D.W., and Kadlubar F.F. Mechanism of formation and structural characterization of DNA adducts derived from peroxidative activation of benzidine. Carcinogenesis 9 (1988) 1635-1641
71. Krauss R.S., Angerman-Stewart J., Eling T.E., Dooley K.L., and Kadlubar F.F. The formation of 2-aminofluorene-DNA adducts in vivo: evidence for peroxidase-mediated activation. J. Biochem. Toxicol. 4 (1989) 111-117
72. 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. 378 (1997) 97-112
73. Stiborová M., Mikšanová M., Havlíček V., Schmeiser H.H., and Frei E. Mechanism of peroxidase-mediated oxidation of carcinogenic o-anisidine and its binding to DNA. Mutat. Res. 500 (2002) 49-66