Metabolism of 5-methylchrysene and 6-methylchrysene by human hepatic and pulmonary cytochrome P450 enzymes

Cancer Research

Volumn 56, Issue 2, 1996, Pages 316-324

  Koehl, Werner ^a,c   Amin, Shantu ^a   Staretz, Marianne E ^a   Ueng, Yune Fang ^b   Yamazaki, Hiroshi ^b,d   Tateishi, Tomonori ^b,e   Guengerich, F Peter ^b   Hecht, Stephen S ^a  

^a AMERICAN HEALTH FOUNDATION   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c School of Medicine ^*  (Germany)

^d OSAKA PREFECTURAL INSTITUTE OF PUBLIC HEALTH   (Japan)

^e JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHRYSENE DERIVATIVE; CYTOCHROME P450;

ARTICLE; CARCINOGENICITY; DRUG METABOLISM; DRUG PROTEIN BINDING; DRUG TRANSFORMATION; ENZYME ACTIVITY; HUMAN; LIVER MICROSOME METABOLISM; LUNG CARCINOGENESIS; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

ANTIBODIES; BIOTRANSFORMATION; CARCINOGENS; CHRYSENES; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME INHIBITORS; HUMANS; ISOENZYMES; LUNG; MICROSOMES; MICROSOMES, LIVER; RECOMBINANT PROTEINS; STEREOISOMERISM;

EID: 0030069518     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. International Agency for Research on Cancer. IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Polynuclear Aromatic Compounds. Part 1. Chemical, Environmental, and Experimental Data. Vol. 32. Lyon, France. LARC, 1983
2. International Agency for Research on Cancer IARC. Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans., Polynuclear Aromatic Corapounds, Part 2. Carbon Blacks. Mineral Oils and Some Nitroarenes. Vol. 33. Lyon, France. IARC, 1984.
3. International Agency for Research on Cancer IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Polynuclear Aromatic Compounds. Part 3. Industrial Exposures in Aluminum Production: Coal Gasification, Coke Production, and Iron and Steel Founding, Vol. 34. Lyon, France: IARC, 1984.
4. International Agency for Research on Cancer IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Polynuclear Aromatic Compounds, Part 4. Bitumens: Coal-Tars and Derived Products, Shale-Oils and Soots, Vol. 35. Lyon, France: IARC, 1985
5. Hoffmann, D , and Hecht, S S Advances in tobacco carcinogenesis, In: C. S. Cooper and P. L. Grover (eds.). Handbook of Experimental Pharmacology, pp. 63-102. Heidelberg: Springer-Verlag, 1990.
6. International Agency for Research on Cancer IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Tobacco Smoking, Vol 38 Lyon, France IARC, 1986.
7. Hecht, S. S. Bondinell, W. E , and Hoffmann, D. Chrysene and methylchrysenes: presence in tobacco smoke and carcinogenicity. J. Natl. Cancer Inst , 53: 1121-1133, 1974.
8. Hecht, S. S., Loy, M., Maronpot, R R., and Hoffmann, D. Comparative carcinogenicity of 5-methylchrysene, benzo[a]pyrene, and modified chrysenes. Cancer Lett., 1: 147-154, 1976.
9. Hecht, S S., Loy, M., and Hoffmann, D. On the structure and carcinogenicity of the methylchrysenes. In: R. I. Freudenthal and P. W Jones (eds). Carcinogenesis, Vol. 1. Polynuclear Aromatic Hydrocarbons: Chemistry. Metabolism, and Carcinogenesis, pp. 325-340. New York: Raven Press, 1976.
10. Hecht, S. S., Melikian, A , and Amin, S. Effects of methyl substitution on the tumorigenicity and metabolic activation of polycyclic aromatic hydrocarbons In. S. K Yang and B D Silverman (eds.), Polycyclic Aromatic Hydrocarbon Carcinogenesis: Structure-Activity Relationships, pp. 95-128. Boca Raton, FL: CRC Press, 1988.
11. Ross, J. A., Nelson, G. B., Wilson, K. H., Rabinowitz, J. R , Galati, A., Stoner, G. D., Nesnow, S , and Mass, M. J. Adenomas induced by polycyclic aromatic hydrocarbons in strain A/J mouse lune correlate with time-integrated DNA adduct levels. Cancer Res., 55: 1039-1044, 1995.
12. Melikian, A., LaVoie, E. J., Hecht, S. S., and Hoffmann, D. Influence of a bay region methyl group on formation of 5-methylchrysene dihydrodiol epoxide: DNA adducts in mouse skin Cancer Res., 42. 1239-1242, 1982
13. Meliktan, A. A., LaVoie, E J., Hecht, S. S., and Hoffmann, D. 5-Methytchrysene metabolism in mouse epidermis in vivo, diol epoxide-DNA adduct persistence, and diol epoxide reactivity with DNA as potential factors influencing the predominance of 5-methylchrysene-1,2-diol-3,4-epoxide-DNA adducts in mouse epidermis. Carcinogenesis (Lond.), 4: 843-849, 1983.
14. Hecht, S. S., Radok, L , Amin, S., Huie, K., Melikian, A. A., Hoffmann, D , Pataki, J., and Harvey, R. G. Tumorigenicity of 5-methylchrysene dihydrodiols and dihydrodiol epoxides in newborn mice and on mouse skin. Cancer Res., 45: 1449-1452, 1985.
15. Amin, S., Huie, K., Melikian, A. A., Leszczynska, J M., and Hecht, S. S. Comparative metabolic activation in mouse skin of the weak carcinogen 6-methylchrysene and the strong carcinogen 5-methylchrysene. Cancer Res., 45: 6406-6412, 1985.
16. Amin, S., Huie, K , Balanikas, G., Hecht, S. S., Pataki, J., and Harvey, R. G. High stereoselectivity in mouse skin metabolic activation of methylchrysenes to tumorigenic dihydrodiols. Cancer Res., 47: 3613-3617, 1987.
17. Hecht, S. S., Amin, S., Huie, K., Melikian, A. A., and Harvey, R. G. Enhancing effect of a bay region methyl group on tumorigenicity in newborn mice and mouse skin of enantiomeric bay region diol epoxides formed stereoselectively from methylchrysenes in mouse epidermis. Cancer Res., 47: 5310-5315, 1987
18. Melikian, A. A., Amin, S., Hecht, S. S., Hoffmann, D., Pataki, J , and Harvey, R G Identification of the major adducts formed by reaction of 5-methylchrysene anti-dihydrodiol epoxides with DNA in vitro. Cancer Res., 44, 2524-2529, 1984.
19. Melikian, A. A., Amin, S., Huie, K., Hecht, S. S., and Harvey, R. G. Reactivity with DNA bases and mutagenicity toward Salmonella typhimurium of methylchrysene diol epoxide enantiomers. Cancer Res., 48: 1781-1787, 1988.
20. Melikian, A. A., Prahalad, K. A., Amin, S., and Hecht, S. S. Comparative DNA binding of polynuclear aromatic hydrocarbons and their dihydrodiol and bay region diolepoxide metabolites in newborn mouse lung and liver. Carcinogenesis (Lond.), 12. 1665-1670, 1991.
21. Reardon, D. B., Prakash, A. S., Hilton, B. D., Roman, J. M., Pataki, J., Harvey, R. G., and Dipple, A. Characterization of 5-methylchrysene-1,2-dihydrodiol-3,4-epoxide-DNA adducts Carcinogenesis (Lond.), 8. 1317-1322, 1987.
22. Bigger, C A. H , Flickinger, D. J., Strandberg, J., Pataki, J , Harvey, R. G., and Dippie, A. Mutational specificity of the anti 1,2-dihydrodiol 3,4-epoxide of 5-methylchrysene. Carcinogenesis (Lond), 11: 2263-2265, 1990.
23. You, L., Wang, D., Galati, A. J., Ross, J. A., Mass, M. J , Nelson, G. B., Wilson, K. H., Amin S., Stoner, J. C., Nesnow, S., and Stoner, G D. Tumor multiplicity, DNA adducts and K-ray mutation pattern of 5-methylchrysene in strain A/J mouse lung. Carcinogenesis (Lond.), 15: 2613-2618, 1994.
24. Amin, S , Juchatz, A., Furuya, K., and Hecht, S S. Effects of fluorine substitution on the tumor initiating activity and metabolism of 5-hydroxymethylchrysene, a tumorigenic metabolite of 5-methylchrysene. Carcinogenesis (Lond.), 2: 1027-1032, 1981.
25. Okuda, H., Hiratsuka, A , Nojima, H., and Watabe, T. A hydroxymethyl sulphate ester as an active metabolite of the carcinogen, 5-hydroxymethylchrysene. Biochem Pharmacol., 35: 535-538, 1986.
26. Okuda, H., Nojima, H., Watanabe, N., Miwa, K , and Watabe, T. Activation of the carcinogen, 5-hydroxymethylchrysene, to the mutagenic sulphate ester by mouse skin sulphotransferase. Biochem. Pharmacol., 37: 970-973, 1987.
27. Okuda, H , Nojima, H. Miwa, K., Watanabe, N., and Watabe, T. Selective covalent binding of the active sulfate ester of the carcinogen 5-(hydroxymethynchrysene to the adenine residue of calf thymus DNA Chem Res Toxicol., 2: 15-22, 1989.
28. Shimada, T., Martin, M. V., Pruess-Schwartz, D., Marnett, L. J., and Guengerich, F. P. Roles of individual human cytochrome P450 enzymes in the bioactivation of benzo(a)pyrene, 7-8-dihydroxy-7,8-dihydrobenzo(a)pyrene, and other dihydrodiol derivatives of polycyclic aromatic hydrocarbons. Cancer Res., 49: 6304-6312, 1989
29. Yun, C-H., Shimada, T., and Guengerich, F P Roles of human liver cytochrome P4502C and 3A enzymes in the 3-hydroxylation of benzo(a)pyrene Cancer Res , 52, 1868-1874, 1992.
30. Shou, M., Korzekwa, K. R , Crespi, C. L., Gonzalez, F J., and Gelboin, H. V The role of 12 cDNA-expressed human, rodent, and rabbit cytochromes P450 in the metabolism of benzo[a]pyrene and benzo[a]pyrene trans-7-8-dihydrodiol Mol. Carcinog , 10: 159-168, 1994
31. Bauer, E , Guo, Z., Ueng, Y-F., Bell, L. C., Zeldin, D , and Guengench, F. P. Oxidation of benzo[a]pyrene by recombinant human cytochrome P450 enzymes. Chem Res. Toxicol., 8, 136-142, 1995.
32. Jones, J. P., Shou, M., and Korzekwa, K. R. Stereospecific activation of the procarcinogen benzo[a]pyrene: a probe for the active sites of the cytochrome P450 superfamily. Biochemistry, 34: 6596-6961, 1995.
33. Morrison, V. M , Burnett, A K , Forrester, L M., Wolf, C. R., and Craft, J. A The contribution of cytochromes P450 in the metabolism of 7,12-dimethylbenz[a]anthracene in rat and human liver microsomal membranes. Chem.-Biol. Interact, 79; 179-196, 1991.
34. Roberts-Thompson, S. J., McManus, M. E., Tukey, R. H., Gonzalez, F. J., and Holder, G M. Metabolism of polycyclic aza-aromatic carcinogens catalyzed by four expressed human cytoehromes P450. Cancer Res., 55: 1052-1059, 1995
35. Chae, Y-H., Yun, C-H., Guengerich, F P., Kadlubar, F F , and El-Bayoumy, K. Roles of human hepatic and pulmonary cytochrome P450 enzymes in the metabolism of the environmental carcinogen 6-nitrochrysene. Cancer Res., 53: 2028-2034, 1993.
36. Yamazaki, H , Mimura, M., Oda, Y., Gonzalez, F. J., El-Bayoumy, K., Chae, Y-H., Guengerich, F. P., and Shimada, T. Activation of trans-1,2-dihydro-1,2-dihydroxy-6-aminochrysene to genotoxic metabolites by rat and human cytochromes P450. Carcinogenesis (Lond.), 15: 465-470, 1994.
37. Silvers, K. J., Chazinski, T., McManus, M. E., Bauer, S. L., Gonzalez, F. J., Gelboin, H. V., Maurel, P., and Howard, P. C. Cytochrome P450 3A4 (nifedipine oxidase) is responsible for the C-oxidative metabolism of 1-nitropyrene in human liver microsomal samples. Cancer Res., 52: 6237-6243, 1992.
38. Harvey, R. G , Pataki, J., and Lee, H Synthesis of the dihydrodiol and diol epoxide metabolites of chrysene and 5-methylchrysene. J. Org. Chem., 51: 1407-1412, 1986.
39. Amin, S., Camanzo, J , Huie, K., and Hecht, S. S. Improved photochemical synthesis of 5-methylchrysene derivatives and its application to the preparation of 7,8-dihydro7,8-dihydroxy-5-methylchrysene J Org. Chem, 49: 381-384, 1984.
40. Amin, S., Hecht, S. S., and Hoffmann, D. Synthesis of angular ring methoxy-5-methylchrysenes and 5-methylchrysenols. J. Org. Chem., 46: 2394-2398, 1981.
41. Amin, S., Hecht, S S., LaVoie, E , and Hoffmann, D. Synthesis and mutagenicity of 5,11-dimethylchrysene and some methyl-oxidized derivatives of 5-methylchrysene. J. Med. Chem., 22: 1336-1340, 1979.
42. Guengerich, F. P. Analysis and characterization of enzymes. In: A. W. Hayes (ed.), Principles and Methods of Toxicology, Ed. 3, pp. 1259-1313. New York: Raven Press, 1994.
43. Rutten, A. A. J. J. L., Falke, H. E., Catsburg, J. F., Topp, R., Blaauboer, B. J., van Holsteijn, I., Doom, L , and van Leeuwen, F. X. R. Interlaboratory comparison of total cytochrome P450 and protein determinations in rat liver microsomes. Arch. Toxicol., 61: 27-33, 1987.
44. Schoene, B., Fleischman, R. A., Remmer, H , and van Olderhausen, H. F. Determination of drug metabolizing enzymes in needle biopsies of human liver. Eur. J Clin Pharmacol., 4: 65-73, 1972.
45. Yasukochi, Y , and Masters, B. S. Some properties of a detergent-solubilized NADPH-cytochrome c (cytochrome P450) reductase purified by biospecific affinity chromatography. J. Biol Chem., 251: 5337-5344, 1976.
46. Guengerich, F. P. Oxidation of toxic and carcinogenic chemicals by human cytochrome P450 enzymes. Chem Res. Toxicol., 4: 391-407, 1991
47. Shimada, T., and Guengerich, F. P. Activation of amino-α-carboline, 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine, and a copper phthalocyanine cellulose extract of cigarette smoke condensate by cytochrome P450 enzymes in rat and human liver microsomes. Cancer Res., 51: 5284-5291, 1991.
48. Funae, Y., and Imaoka, S. Simultaneous purification of multiple forms of rat liver and microsomal cytochrome P450 by high performance liquid chromatography. Biophys. Acta. 842: 119-132, 1985.
49. Guengench, F. P., Wang, P , Mitchell, M. B., and Mason, P. S Rat and human liver microsomal epoxide hydratase: purification and evidence for the existence of multiple forms. J. Biol. Chem., 254: 12248-12254, 1979.
50. Guo, Z., Gillam, E. M. J., Ohmori, S., Tukey, R H., and Guengerich, F. P. Expression of modified human cytochrome P450 1A1 in Escherichia coli: effects of 5′ substitution, stabilization, purification, spectral characterization, and catalytic properties. Arch. Biochem. Biophys., 312: 436-446, 1994.
51. Sandhu, P., Guo, Z., Baba, T., Martin, M. V., Tukey, R. H., and Guengench, F. P. Expression of modified human cytochrome P450 1A2 in Escherichia coli, stabilization, purification, spectral characterization, and catalytic activities of the enzyme. Arch Biochem. Biophys., 309, 168-177, 1994.
52. Sandhu, P., Baba, T., and Guengerich, F. P. Expression of modified cytochrome P450 2C10 (2C9) in Escherichia coli, purification, and reconstitution of catalytic activity. Arch. Biochem. Biophys., 306: 443-450, 1993.
53. Gillam, E. M. J , Guo, Z., and Guengerich, F P. Expression of modified human cytochrome P450 2E1 in Escherichia coli, purification, and spectral and catalytic properties. Arch. Biochem. Biophys., 312, 59-66, 1994.
54. Gillam, E. M. J., Guo, Z., Martin, M. V., Jenkins, C. M., and Guengerich, F. P Expression of cytochrome P450 2D6 in Escherichia coli, purification, and spectral and catalytic characterization. Arch. Biochem. Biophys , 319, 540-550, 1995
55. Gillam, E M J , Baba, T., Kim, B-R., Ohmori, S., and Guengench, F. P. Expression of modified human cytochrome P450 3A4 in Escherichia coli and purification and reconstitution of the enzyme. Arch Biochem. Biophys., 305: 123-131, 1993
56. Gillam, E. M. J., Guo, Z., Ueng, Y-F., Yamazaki, H., Cock, I , Reilly, P. E. B., Hooper, W. D., and Guengench, F. P. Expression of cytochrome P45G 3A5 in Escherichia coli: effects of 5′ modification, purification, spectral characterization, reconstitution conditions, and catalytic activities. Arch. Biochem Biophys., 317: 374-384, 1995.
57. Guengench, F. P. Human cytochrome P450s. In: P. R. Ortiz de Montellano (ed.), Cytochrome P450, pp. 473-535. New York: Plenum Publishing Corp., 1995.
58. Harris, C C., Autrup, H., Connor, R., Barren, L. A., McDowell, E. M., and Trump. B. F. Interindividual variation in binding of benzo[a]pyrene to DNA in cultured human bronchi. Science (Washington DC). 194. 1067-1069, 1976.
59. Shimada, T., Misono, K S., and Guengerich, F. P. Human liver microsomal cytochrome P450 mephenytoin 4-hydroxylase, a prototype of generic polymorphism in oxidative drug metabolism. J Biol. Chem., 261. 909-921, 1986.
60. Shimada, T., Yun, C-H., Yamazaki, H., Gautier, J-C., Beaune, P H., and Guengerich, F. P. Characterization of human lung microsomal cytochrome P4501A1 and its role in the oxidation of chemical carcinogens. Mol. Pharmacol., 41: 856-864, 1992.
61. Wheeler, C. W., and Guenthner, T. M Cytochrome P450-dependent metabolism of xenobiotics in human lung. J Biochem. Toxicol., 6: 163-169, 1991
62. Anttila, S , Vainio, H , Hietanen, E., Camus, A. M., Malaveille, C., Brun, G. Husgafvel-Pursiainen, K., Heikkila, L., Karjalainen, A., and Bartsch, H. Immunohistochemical detection of pulmonary cytochrome P450IA and metabolic activities associated with P450IA1 and P450IA2 isozymes in lung cancer patients Environ Health Perspect., 98: 179-182, 1992.
63. PA (P450 IA2), the phenacetin O-deethylase, is primarily responsible for the hepatic 3-demethylation of caffeine and N-oxidation of carcinogenic arylamines Proc Natl. Acad. Sci. USA, 86: 7696-7700, 1989.
64. Turesky, R. J., Lang, N. P., Butler, M. A., Teitel, C. H., and Kadlubar, F. F. Metabolic activation of carcinogenic heterocyclic aromatic amines by human liver and colon. Carcinogenesis (Lond), 12: 1839-1845, 1991
65. Shou, M., Korzekua, K R., Krausz, K. W., Crespi, C. L., Gonzalez, F. J., and Gelboin, H. V. Regio- and stereo-selective metabolism of phenanthrene by twelve cDNA-expressed human, rodent, and rabbit cytochromes P450. Cancer Lett., 83: 305-313, 1994.
66. Shou, M., Grogan, J , Mancewicz, J. A., Krausz, K. W., Gonzalez, F. J., Gelboin, H. V., and Korzekwa, K. R. Activation of CYP3A4: evidence for the simultaneous binding of two substrates in a cytochrome P450 active site. Biochemistry, 33: 6450-6455, 1994.
67. 1 by bacterial recombinant human cytochrome P450 enzymes. Chem. Res. Toxicol , 8: 218-225, 1995.