Mechanism of formation of (deoxy)guanosine adducts derived from peroxidase-catalyzed oxidation of the carcinogenic nonaminoazo dye 1-phenylazo-2-hydroxynaphthalene (Sudan I)

Chemical Research in Toxicology

Volumn 22, Issue 11, 2009, Pages 1765-1773

  Dračínský, Martin ^a   Cvačka, Josef ^a   Semanská, Marcela ^b   Martínek, Václav ^b   Frei, Eva ^c   Stiborová, Marie ^b  

^a INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXONAPHTHALENE; AZO COMPOUND; CARBON; DEOXYGUANOSINE; GUANINE; HYDROXYL GROUP; NAPHTHALENE; NITROGEN; OXYGEN; PEROXIDASE; RADICAL; SPIRONAPHTHOOXADIAZINE; SPIRONAPTHOOXADIAZINE; SUDAN I; SULFADIAZINE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLITE; OXIDATION; SENSITIZATION; THIN LAYER CHROMATOGRAPHY;

BIOCATALYSIS; CARCINOGENS; COLORING AGENTS; DEOXYGUANOSINE; DNA ADDUCTS; NAPHTHOLS; OXIDATION-REDUCTION; PEROXIDASE;

RODENTIA;

EID: 72749119239     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx900201q     Document Type: Article

References (50)

1. International Agency for Research on Cancer (1975) Sudan I, in IARC Monographs, Vol.8, pp 225-231, IARC, Lyon, France.
2. Garner, R. C., Martin, C. N., and Clayson, D. B. (1984) Carcinogenic Aromatic Amines and Related Compounds, in Chemical Carcinogens (Searle, C., Ed.) 2nd ed., Vol.1, pp 175-302, CS Monograph 182, American Chemical Society, Washington, DC.
3. Westmoreland, C., and Gatehouse, D. G. (1991) The differential clastogenicity of Solvent Yellow 14 and FD & C Yellow No.6 in vivo in the rodent micronucleus test (observation of species and tissues specificity). Carcinogenesis 12, 1403-1407.
4. NCI (1982) Carcinogenesis Bioassay of C.I. Solvent Yellow 14 in F344/N Rats and B6C3F1 Mice, Technical Report No. 226, US National Cancer Institute, Bethesda, MD.
5. Moller, P., and Wallin, H. (2000) Genotoxic hazards of azo pigments and other colorants related to 1-phenylazo-2-hydroxynaphthalene. Mutat. Res. 462, 13-30. (Pubitemid 30060328)
6. An, Y., Jiang, L., Cao, J., Geng, C., and Zhong, L. (2007) Sudan I induces genotoxic effects and oxidative DNA damage in HepG2 cells. Mutat. Res. 627, 164-170. (Pubitemid 46097494)
7. Zhang, X., Jiang, L., Geng, C., Hu, C., Yoshimura, H., and Zhong, L. (2008) Inhibition of Sudan I genotoxicity in human liver-derived HepG2 cells by the antioxidant hydroxytyrosol. Free Radical Res. 42, 189-195. (Pubitemid 351298368)
8. Kozuka, T., Tashiro, M., Sano, S., Fujimoto, K., Nakamura, Y., Hashimoto, S., and Nakaminami, G. (1980) Pigmented contact dermatitis from azo dyes. I. Cross-sensitivity in humans. Contact Dermatitis 6, 330-336. (Pubitemid 11254874)
9. http://msds.chem.ox.ac.uk/SU/sudan-I.html (accessed Jun 18, 2009).
10. Mazzetti, M., Fascioli, R., Mazzoncini, I., Spinelli, G., Morelli, I., and Bertoli, A. (2004) Determination of 1-phenylazo-2-naphthol (Sudan I) in chilli powder and in chilli-containing food products by GPC clean-up and HPLC with LC/MS confirmation. Food Addit. Contam. 21, 935-941. (Pubitemid 39599989)
11. Liu, Y., Song, Z., Dong, F., and Zhang, L. (2007) Flow injection chemiluminescence determination of Sudan I in hot chilli sauce. J. Agric. Food Chem. 55, 614-617.
12. Uematsu, Y., Ogimoto, M., Kabashima, J., Suzuki, K., and Ito, K. (2007) Fast cleanup method for the analysis of Sudan I-IV and para red in various foods and paprika color (oleoresin) by high-performance liquid chromatography/diode array detection: focus on removal of fat and oil as fatty acid methyl esters prepared by transesterification of acylglycerols. J. AOAC Int. 90, 437-945. (Pubitemid 350067241)
13. Wang, S., Xu, Z., Fang, G., Duan, Z., Zhang, Y., and Chen, S. (2007) Synthesis and characterization of a molecularly imprinted silica gel sorbent for the on-line determination of trace Sudan I in Chilli powder through high-performance liquid chromatography. J. Agric. Food Chem. 55, 3869-3876. (Pubitemid 46867391)
14. Dixit, S., Khanna, S. K., and Das, M. (2008) A simple 2-directional high-performance thin-layer chromatographic method for the simultaneous determination of curcumin, metanil yellow, and Sudan dyes in turmeric, chili, and curry powders. J. AOAC Int. 91, 1387-1396.
15. Xu, H., Heinze, T. M., Chen, S., Cerniglia, C. E., and Chen, H. (2007) Anaerobic metabolism of 1-amino-2-naphthol-based azo dyes (Sudan dyes) by human intestinal microflora. Appl. Environ. Microbiol. 73, 7759-7762.
16. Wang, Y., Wei, D., Yang, H., Yang, Y., Xing, W., Li, Y., and Deng, A. (2009) Development of a highly sensitive and specific monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) for detection of Sudan I in food samples. Talanta 77, 1783-1789.
17. Federal Institute for Risk Assessment. (2003) Dyes Sudan I to IV in Food in Opinion of 10 November 2003, Federal Institute for Risk Assessment, Berlin, Germany.
18. Zeiger, E., Andersen, B., Haworth, S., Lawlor, T., and Mortelmans, K. (1988) Salmonella mutagenicity tests. IV. Results from the testing of 300 chemicals. Environ. Mutagen. 11 (Suppl. 12), 1-158.
19. ± assays. Mutat. Res. 189, 223-261.
20. Stiborová, M., Asfaw, B., Anzenbacher, P., and Hodek, P. (1988) A new way to carcinogenicity of azo dye: the benzenediazonium ion formed from non-aminoazo dye, 1-phenylazo-2-hydroxynaphthalene (Sudan I) by microsomal enzymes binds to deoxyguanosine residues of DNA. Cancer Lett. 40, 327-333. (Pubitemid 18163605)
21. Stiborová, M., Asfaw, B., Frei, E., Schmeiser, H. H., and Wiessler, M. (1995) Benzenediazonium ion derived from Sudan I forms an 8-(phenylazo)guanine adduct. Chem. Res. Toxicol. 8, 489-498.
22. 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. (Pubitemid 35204721)
23. Stiborová, M., Asfaw, B., and Anzenbacher, P. (1988) Activation of carcinogens by peroxidase. Horseradish peroxidase-mediated formation of benzenediazonium ion from a non-aminoazo dye, 1-phenylazo-2-hydroxynaphthalene (Sudan I) and its binding to DNA. FEBS Lett. 232, 387-390. (Pubitemid 18126244)
24. 32P-postlabeling of DNA adducts derived from peroxidative activation of carcinogenic non-aminoazo dye 1-phenylazo-2-hydroxynaphthalene (Sudan I). Carcinogenesis 11, 1843-1848.
25. Stiborová, M., Frei, E., Klokow, K., Wiessler, M., Šafařík, L., Anzenbacher, P., and Hradec, J. (1990) Peroxidase-mediated reaction of the carcinogenic non-aminoazo dye 1-phenylazo-2-hydroxynaphthalene with transfer ribonucleic acid. Carcinogenesis 11, 1789-1794. (Pubitemid 20331447)
26. 32P-Postlabeling analysis of adducts formed from 1-phenylazo-2-hydroxynaphthalene (Sudan I, Solvent Yellow 14) with DNA and homopolydeoxyribonucleotides. Carcinogenesis 13, 1221-1225.
27. Stiborová, M., Schmeiser, H. H., and Frei, E. (1999) Prostaglandin H synthase mediated oxidation and binding to DNA of a detoxication metabolite of carcinogenic Sudan I 1-(phenylazo) 2,6-dihydroxynaphthalene. Cancer Lett. 142, 53-60. (Pubitemid 29462556)
28. Stiborová, M., Asfaw, B., and Frei, E. (1995) Peroxidase-activated carcinogenic azo dye Sudan I (Solvent Yellow 14) binds to guanosine in transfer ribonucleic acid. Gen. Physiol. Biophys. 14, 39-49.
29. Stiborová, M., Frei, E., Schmeiser, H. H., Wiessler, M., and Hradec, J. (1993) Detoxication products of the carcinogenic azodye Sudan I (Solvent Yellow 14) bind to nucleic acids after activation by peroxidase. Cancer Lett. 68, 43-47. (Pubitemid 23054896)
30. 32P-Postlabelling analysis of DNA adducts with 1-(phenylazo)-2- naphthol (Sudan I, Solvent Yellow 14) formed in vivo in Fisher 344 rats. Collect. Czech. Chem. Commun. 64, 1335-1347.
31. Stiborová, M., Martínek, V., Schmeiser, H. H., and Frei, E. (2006) Modulation of CYP1A1-mediated oxidation of carcinogenic azo dye Sudan I and its binding to DNA by cytochrome b5. Neuro Endocrinol. Lett. 27 (Suppl 2), 35-39. (Pubitemid 46534333)
32. Zhang, X., Juany, L., Geng, C., Hu, C., Yoshimura, H., and Zhong, L. (2008) Inhibition of Sudan I genotoxicity in human liver-derived HepG2 cells by the antioxidant hydroxytyrosol. Free Radical Res. 42, 189-195. (Pubitemid 351298368)
33. Childs, J. J., and Clayson, D. S. (1966) The metabolism of 1-phenylazo-2-naphthol in the rabbit. Biochem. Pharmacol. 15, 1247-1258.
34. Stiborová, M., Asfaw, B., Anzenbacher, P., Lešetický , L., and Hodek, P. (1988) 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, 319-326. (Pubitemid 18163604)
35. Stiborová, M., Martínek, V., Rýdlová, H., Koblas, T., and Hodek, P. (2005) 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. (Pubitemid 40568771)
36. Stiborová, M., Frei, E., and Anzenbacher, P. (1991) Study of oxidation and binding to macromolecules of the carcinogenic non-aminoazo dye 1-phenylazo2-hydroxynaphthalene catalyzed by horseradish (Armoracia rusticana L.) peroxidase. Biochem. Physiol. Pflanz. 187, 227-236.
37. Martínek, V., and Stiborová, M. (2002) Metabolism of carcinogenic azo dye Sudan I by rat, rabbit, minipig and human hepatic microsomes. Collect. Czech. Chem. Commun. 67, 1883-1898.
38. Wise, R. W., Zenser, T. V., Kadlubar, F. F., and Davis, B. B. (1984) Metabolic activation of carcinogenic aromatic amines by dog bladder and kidney prostaglandin H synthase. Cancer Res. 44, 1893-1897.
39. Yamazoe, Y., Miller, D. W., Wies, C. C., Dooley, K. L., Zenser, T. V., Beland, F. A., and Kadlubar, F. F. (1985) DNA adducts formed by ring-oxidation of the carcinogen 2-naphthylamine with prostaglandin H synthase in vitro and in the dog urothelium in vivo. Carcinogenesis 6, 1379-1387. (Pubitemid 15013344)
40. Eling, T. E., Thompson, D. C., Foureman, G. L., Curtis, J. F., and Hughes, M. F. (1990) Prostaglandin H synthase and xenobiotic oxidation. Annu. Rev. Pharmacol. Toxicol. 30, 1-45.
41. Chen, L., Devanesan, P. D., Higginbotham, S., Ariese, F., Jankowiak, R., Small, G. J., Rogan, E. G., and Cavalieri, E. L. (1996) Expanded analysis of benzo[a]pyrene-DNA adducts formed in vitro and in mouse skin: their significance in tumor initiation. Chem. Res. Toxicol. 9, 897-903. (Pubitemid 26250585)
42. Stiborová, M., Asfaw, B., Frei, E., and Schmeiser, H. H. (1996) Oxidation of azo dyes by peroxidase: additional evidence of a one-electron mechanism of oxidation of dimethylaminoazobenzene and Sudan I (Solvent Yellow 14). Collect. Czech. Chem. Commun. 61, 962-972. (Pubitemid 126092089)
43. Semanská, M., Dračínský, M., Martínek, V., Hudeček, J., Hodek, P., Frei, E., and Stiborová, M. (2008) A one-electron oxidation of carcinogenic non-aminoazo dye Sudan I by horseradish peroxidase. Neuro Endocrinol. Lett. 29, 712-716.
44. Stiborová, M., Mikšanová, M., Martínek, V., and Frei, E. (2000) Heme peroxidases: structure, function, mechanism and involvement in activation of carcinogens. A review. Collect. Czech. Chem. Commun. 65, 297-325.
45. 32P- labeling test for DNA damage. Proc. Natl. Acad. Sci. U.S.A. 78, 6126-6129.
46. 32P-postlabeling analysis of aromatic carcinogenic:DNA adducts. Cancer Res. 45, 5656-5662.
47. Rogg, H., Wehrli, W., and Staehelin, M. (1969) Isolation of mammalian transfer RNA. Biochim. Biophys. Acta 195, 13-15.
48. 32P-postlabeling efficiencies of 2,6-dimethylaniline-DNA adducts. Chem. Res. Toxicol. 14, 165-174.
49. Breitmaier, E., and Voelter, W. (1974) Carbon-13 NMR Spectroscopy. High-Resolution Methods and Applications in Organic Chemistry and Biochemistry, 3rd ed., VCH, Weinheim, Germany.
50. Anzenbacher, P., Niwa, T., Tolbert, L. M., Sirimanne, S. R., and Guengerich, F. P. (1996) Oxidation of 9-alkylanthracenes by cytochrome P450 2B1, horseradish peroxidase, and iron tetraphenylporphine/iodosylbenzene systems: anaerobic and aerobic mechanisms. Biochemistry 35, 2512-2520. (Pubitemid 26098760)