Bioactivation versus detoxication of the urothelial carcinogen aristolochic acid i by human cytochrome P450 1A1 and 1A2

Toxicological Sciences

Volumn 125, Issue 2, 2012, Pages 345-358

  Stiborová, Marie ^a   Levová, Katerǐna ^a   Bárta, František ^a   Shi, Zhanquan ^b   Frei, Eva ^c   Schmeiser, Heinz H ^d   Nebert, Daniel W ^b   Phillips, David H ^e,f   Arlt, Volker M ^e,f  

^a CHARLES UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^c Division of Preventive Oncology   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^f KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Aristolochic acid ia; Aristolochic acid nephropathy; Balkan endemic nephropathy; Cyp1a humanized mouse models; Cytochrome P450; Dna adducts; Metabolism

Indexed keywords

8 HYDROXYARISTOLOCHIC ACID; ALPHA NAPHTHOFLAVONE; AMANTADINE; ARISTOLOCHIC ACID; ARISTOLOCHIC ACID I; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; DIETHYLDITHIOCARBAMIC ACID; FURAFYLLINE; KETOCONAZOLE; QUINIDINE; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHILD; CONTROLLED STUDY; DETOXIFICATION; DNA ADDUCT; FEMALE; GENETIC VARIABILITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; METABOLISM; MICROSOME; MOUSE; NONHUMAN; ORTHOLOGY; OXIDATION; PRESCHOOL CHILD; RISK ASSESSMENT; SCHOOL CHILD;

MUS;

EID: 84856118524     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr306     Document Type: Article

References (40)

1. Aoyama, T., Gonzalez, F. J., and Gelboin, H. V. (1989). Human cDNAexpressed cytochrome P450 IA2: Mutagen activation and substrate specificity. Mol. Carcinog. 2, 192-198.
2. Arlt, V. M., Ferluga, D., Stiborová, M., Pfohl-Leszkowicz, A., Vukelic, M., Ceovic, S., Schmeiser, H. H., and Cosyns, J. P. (2002). Is aristolochic acid a risk factor for Balkan endemic nephropathy-associated urothelial cancer? Int. J. Cancer 101, 500-502.
3. Arlt, V. M., Levová, K., Bárta, F., Shi, Z., Frei, E., Schmeiser, H. H., Nebert, D. W., Phillips, D. H., and Stiborová, M. (2011a). Role of CYP1A1 and CYP1A2 in bioactivation versus detoxication of the renal carcinogen aristolochic acid I: Studies in Cyp1a(-/-) knockout mice. Chem. Res. Toxicol. 24, 1710-1719.
4. Arlt, V. M., Stiborová, M., vom Brocke, J., Simoes, M. L., Lord, G. M., Nortier, J. L., Hollstein, M., Phillips, D. H., and Schmeiser, H. H. (2007). Aristolochic acid mutagenesis: Molecular clues to the aetiology of Balkan endemic nephropathy-associated urothelial cancer. Carcinogenesis 28, 2253-2261.
5. Arlt, V. M., Zuo, J., Trenz, K., Roufosse, C. A., Lord, G. M., Nortier, J. L., Schmeiser, H. H., Hollstein, M., and Phillips, D. H. (2011b). Gene expression changes induced by the human carcinogen aristolochic acid I in renal and hepatic tissue of mice. Int. J. Cancer 128, 21-32.
6. Atanasova, S., von Ahsen, N., Toncheva, D. I., Dimitrov, T. G., Oellerich, M., and Amstrong, V. M. (2005). Genetic polymorphism of cytochrome P450 among patients with Balkan endemic nephropathy (BEN). Clin. Biochem. 38, 223-228.
7. Chan, W., Cu, L., Xu, G., and Cai, Z. (2006). Study of the phase I and phase II metabolism of nephrotoxin aristolochic acid by liquid chromatography/ tandem mass spectrometry. Rapid Commun. Mass Spectrom. 20, 1755-1760.
8. Cheung, C., Ma, X., Krausz, K. W., Kimura, S., Feigenbaum, L., Dalton, T. P., Nebert, D. W., Idle, J. R., and Gonzalez, F. J. (2005). Differential metabolism of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in mice humanized for CYP1A1 and CYP1A2. Chem. Res. Toxicol. 18, 1471-1478.
9. Debelle, F. D., Vanherweghem, J. L., and Nortier, J. L. (2008). Aristolochic acid nephropathy: A worldwide problem. Kidney Int. 74, 158-169.
10. Dragin, N., Uno, S., Wang, B., Dalton, T. P., and Nebert, D. W. (2007). Generation of 'humanized' hCYP1A1_1A2_Cyp1a1/1a2(-/-) mouse line. Biochem. Biophys. Res. Commun. 359, 635-642.
11. Grollman, A. P., Shibutani, S., Moriya, M., Miller, F., Wu, L., Moll, U., Suzuki, N., Fernandes, A., Rosenquist, T., Medverec, Z., et al. (2007). Aristolochic acid and the etiology of endemic (Balkan) nephropathy. Proc. Natl. Acad. Sci. U.S.A. 104, 12129-12134.
12. Grosse, Y., Baan, R., Straif, K., Secretan, B., El Ghissassi, F., Bouvard, V., Benbrahim-Tallaa, L., Guha, N., Galichet, L., and Cogliano, V. (2009). A review of human carcinogens-Part A: Pharmaceuticals. Lancet Oncol. 10, 13-14.
13. Harris, A. L. (2002). Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. 2, 38-47.
14. Ikeya, K., Jaiswal, A. K., Owens, R. A., Jones, J. E., Nebert, D. W., and Kimura, S. (1989). Human CYP1A2: Sequence, gene structure, comparison with the mouse and rat orthologous gene, and differences in liver 1A2 mRNA expression. Mol. Endocrinol. 3, 1399-1408.
15. Lemy, A., Wissing, K. M., Rorive, S., Zlotta, A., Roumeguere, T., Muniz Martinez, M. C., Decaestecker, C., Salmon, I., Abramowicz, D., et al. (2008). Late onset of bladder urothelial carcinoma after kidney transplantation for end-stage aristolochic acid nephropathy: A case series with 15-year follow-up. Am. J. Kidney Dis. 51, 471-477.
16. Levová, K., Moserova, M., Kotrbova, V., Sulc, M., Henderson, C. J., Wolf, C. R., Phillips, D. H., Frei, E., Schmeiser, H. H., Mares, J., et al. (2011). Role of cytochromes P450 1A1/2 in detoxication and activation of carcinogenic aristolochic acid I: Studies with the hepatic NADPH: Cytochrome P450 reductase null (HRN) mouse model. Toxicol. Sci. 121, 43-56.
17. Mimura, I., and Nangaku, M. (2010). The suffocating kidney: Tubulointerstitial hypoxia in end-stage renal disease. Nat. Rev. Nephrol. 6, 667-678.
18. Nebert, D. W. (2006). Comparison of gene expression in cell culture to that in the intact animal: Relevance to drugs and environmental toxicants. Focus on "development of a transactivator in hepatoma cells that allows expression of phase I, phase II, and chemical defense genes." Am. J. Physiol. 290, C37-C41.
19. Nortier, J. L., Martinez, M. C., Schmeiser, H. H., Arlt, V. M., Bieler, C. A., Petein, M., Depierreux, M. F., De Pauw, L., Abramowicz, D., Vereerstraeten, P., et al. (2000). Urothelial carcinoma associated with the use of a Chinese herb (Aristolochia fangchi). N. Engl. J. Med. 342, 1686-1692.
20. Phillips, D. H., and Arlt, V. M. (2007). The 32P-postlabeling assay for DNA adducts. Nat. Protoc. 2, 2772-2781.
21. Rendic, S., and DiCarlo, F. J. (1997). Human cytochrome P450 enzymes: A status report summarizing their reactions, substrates, inducers, and inhibitors. Drug Metab. Rev. 29, 413-480.
22. Rosenquist, T. A., Einolf, H. J., Dickman, K. G., Wang, L., Smith, A., and Grollman, A. P. (2010). Cytochrome P450 1A2 detoxicates aristolochic acid in the mouse. Drug Metab. Dispos. 38, 761-768.
23. Schmeiser, H. H., Bieler, C. A., Wiessler, M., van Ypersele de Strihou, C., and Cosyns, J. P. (1996). Detection of DNA adducts formed by aristolochic acid in renal tissue from patients with Chinese herbs nephropathy. Cancer Res. 56, 2025-2028.
24. Schmeiser, H. H., Stiborová, M., and Arlt, V. M. (2009). Chemical and molecular basis of the carcinogenicity of Aristolochia plants. Curr. Opin. Drug Discov. Devel. 12, 141-148.
25. Shi, Z., Chen, Y., Dong, H., Amos-Kroohs, R. M., and Nebert, D. W. (2008). Generation of a 'humanized' hCYP1A1_1A2_Cyp1a1/1a2(-/-)_Ahrd mouse line harboring the poor-affinity aryl hydrocarbon receptor. Biochem. Biophys. Res. Commun. 376, 775-780.
26. Shibutani, S., Bonala, R. R., Rosenquist, T., Rieger, R., Suzuki, N., Johnson, F., Miller, F., and Grollman, A. P. (2010). Detoxification of aristolochic acid I by O-demethylation: Less nephrotoxicity and genotoxicity of aristolochic acid Ia in rodents. Int. J. Cancer 127, 1021-1027.
27. Sistkova, J., Hudecek, J., Hodek, P., Frei, E., Schmeiser, H. H., and Stiborová, M. (2008). Human cytochromes P450 1A1 and 1A2 participate in detoxication of carcinogenic aristolochic acid. Neuro. Endocrinol. Lett. 29, 733-737.
28. Stiborová, M., Frei, E., Arlt, V. M., and Schmeiser, H. H. (2008). Metabolic activation of carcinogenic aristolochic acid, a risk factor for Balkan endemic nephropathy. Mutat. Res. 658, 55-67.
29. Stiborová, M., Frei, E., Hodek, P., Wiessler, M., and Schmeiser, H. H. (2005a). 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, 189-197.
30. Stiborová, M., Frei, E., Sopko, B., Sopkova, K., Markova, V., Lankova, M., Kumstyrova, T., Wiessler, M., and Schmeiser, H. H. (2003). 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, 1695-1703.
31. Stiborová, M., Frei, E., Wiessler, M., and Schmeiser, H. H. (2001). Human enzymes involved in the metabolic activation of carcinogenic aristolochic acids: Evidence for reductive activation by cytochromes P450 1A1 and 1A2. Chem. Res. Toxicol. 14, 1128-1137.
32. Stiborová, M., Mares, J., Frei, E., Arlt, V. M., Martínek, V., and Schmeiser, H. H. (2011). The human carcinogen aristolochic acid I is activated to form DNA adducts by human NAD(P)H:quinone oxidoreductase without the contribution of acetyltransferases or sulfotransferases. Environ. Mol. Mutagen. 52, 448-459.
33. Stiborová, M., Martínek, V., Rýdlová, H., Hodek, P., and Frei, E. (2002). 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, 5678-5684.
34. Stiborová, M., Martínek, V., Rýdlová, H., Koblas, T., and Hodek, P. (2005b). 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, 145-154.
35. Stiborová, M., Sejbal, J., Borek-Dohalska, L., Aimova, D., Poljakova, J., Forsterova, K., Rupertova, M., Wiesner, J., Hudecek, J., Wiessler, M., et al. (2004). The anticancer drug ellipticine forms covalent DNA adducts, mediated by human cytochromes P450, through metabolism to 13-hydroxyellipticine and ellipticine N2-oxide. Cancer Res. 64, 8374-8380.
36. Stiborová, M., Sopko, B., Hodek, P., Frei, E., Schmeiser, H. H., and Hudecek, J. (2005c). The binding of aristolochic acid I to the active site of human cytochromes P450 1A1 and 1A2 explains their potential to reductively activate this human carcinogen. Cancer Lett. 229, 193-204.
37. Toncheva, D. I., von Ahsen, N., Atanasova, S. Y., Dimitrov, T. G., and Amstrong, V. M. (2004). Identification of NQO1 and GSTs genotype frequencies in Bulgarian patients with Balkan endemic nephropathy. J. Nephrol. 17, 384-389.
38. Turesky, R. J. (2005). Interspecies metabolism of heterocyclic aromatic amines and the uncertainties in extrapolation of animal toxicity data for human risk assessment. Mol. Nutr. Food Res. 49, 101-117.
39. Vanherweghem, J. L., Depierreux, M., Tielemans, C., Abramowicz, D., Dratwa, M., Jadoul, M., Richard, C., Vandervelde, D., Verbeelen, D., Vanhaelen-Fastre, R., et al. (1993). Rapidly progressive interstitial renal fibrosis in young women: Association with slimming regimen including Chinese herbs. Lancet 341, 387-391.
40. Xue, X., Xiao, Y., Zhu, H., Wang, H., Liu, Y., Xie, T., and Ren, J. (2008). Induction of P450 1A by 3-methylcholanthrene protects mice from aristolochic acid-I-induced acute renal injury. Nephrol. Dial. Transplant. 23, 3074-3081.