Metabolic activation of the (+)-S,S-and(-)-R,R-enantiomers of trans- 11,12-dihydroxy-11,12-dihydrodibenzo[a,l]pyrene: Stereoselectivity, DNA adduct formation, and mutagenicity in Chinese hamster V79 cells

Chemical Research in Toxicology

Volumn 10, Issue 10, 1997, Pages 1161-1170

  Luch, Andreas ^a,b   Seidel, Albrecht ^a   Glatt, Hansruedi ^a,c   Platt, Karl L ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AROCLOR 1254; BENZO[A]PYRENE DERIVATIVE; DIHYDRODIOL DEHYDROGENASE; EPOXIDE; POLYCYCLIC AROMATIC HYDROCARBON;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTRANSFORMATION; CELL STRAIN V 79; CHINESE HAMSTER; CONTROLLED STUDY; DNA ADDUCT; DNA BINDING; ENANTIOMER; LIVER MICROSOME METABOLISM; MALE; METABOLIC ACTIVATION; MOUSE; MUTAGENICITY; NONHUMAN; RAT; STEREOCHEMISTRY;

ANIMALS; AROCLOR 1254; AROCLORS; BIOTRANSFORMATION; CARCINOGENS; CRICETINAE; CRICETULUS; DIHYDROXYDIHYDROBENZOPYRENES; DNA ADDUCTS; MALE; MICE; MICROSOMES, LIVER; MUTAGENS; RATS; RATS, SPRAGUE-DAWLEY; STEREOISOMERISM;

EID: 0030875361     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx970005i     Document Type: Article

References (60)

1. Carruthers, W. (1966) Synthesis of dibenzo[a,l]pyrene. J. Chem. Soc. Chem. Commun. 548-549.
2. Vingiello, F. A., Yanez, J., and Greenwood, E. J. (1966) The synthesis of dibenzo[a,l]pyrene. J. Chem. Soc. Chem. Commun. 375.
3. Masuda, Y., and Kagawa, R. (1972) A novel synthesis and carcinogenicity of dibenzo[a,l]pyrene. Chem. Pharm. Bull. 20, 2736-2737.
4. Cavalieri, E. L., Higginbotham, S., RamaKrishna, N. V. S., Devanesan, P. D., Todorovic, R., Rogan, E. G., and Salmasi, S. (1991) Comparative dose-response tumorigenicity studies of dibenzo[a,l]pyrene versus 7,12-dimethylbenz[a]anthracene, benzo-[a]pyrene and two dibenzo[a,l]pyrene dihydrodiols in mouse skin and rat mammary gland. Carcinogenesis (London) 12, 1939-1944.
5. Higginbotham, S., RamaKrishna, N. V. S., Johansson, S. L., Rogan, E. G., and Cavalieri, E. L. (1993) Tumor-initiating activity and carcinogenicity of dibenzo[a,l]pyrene versus 7,12-dimethylbenz[a]anthracene and benzo[a]pyrene at low doses in mouse skin. Carcinogenesis (London) 14, 875-878.
6. LaVoie, E. J., He, Z.-M., Meegalla, R. L., and Weyand, E. H. (1993) Exceptional tumor-initiating activity of 4-fluorobenzo[j]fluoranthene on mouse skin: comparison with benzo[j]fluoranthene, 10-fluorobenzo[j]fluoranthene, benzo[a]pyrene, dibenzo[a,l]pyrene and 7,12-dimethylbenz[a]anthracene. Cancer Lett. 70, 7-14.
7. Hughes, N. C., and Phillips, D. H. (1990) Covalent binding of dibenzpyrenes and benzo[a]pyrene to DNA: evidence for synergistic and inhibitory interactions when applied in combination to mouse skin. Carcinogenesis (London) 11, 1611-1619.
8. Arif, J.-M., Smith, W. A., and Gupta, R. C. (1997) Tissue distribution of DNA adducts in rats treated by intramammillary injection with dibenzo[a,l]pyrene, 7,12-dimethylbenz[a]anthracene and benzo[a]pyrene. Mutat. Res., in press.
9. Snook, M. E., Severson, R. F., Arrendale, R. F., Higman, H. C., and Chortyk, O. T. (1977) The identification of high molecular weight polynuclear aromatic hydrocarbons in a biologically active fraction of cigarette smoke condensate. Beitr. Tabakforsch. 9, 79-101.
10. Mumford, J. L., Harris, D. B., Williams, K., Chuang, J. C., and Cooke, M. (1987) Indoor air sampling and mutagenicity studies of emissions from unvented coal combustion. Environ. Sci. Technol. 21, 308-311.
11. DeRatt, W. K., Kooijman, S. A. L. M., and Gielen, J. W. J. (1987) Concentrations of polycyclic hydrocarbons in airborne particles in Netherlands and their correlation with mutagenicity. Sci. Total Environ. 66, 95-114.
12. Kozin, I. S., Gooijer, C., and Velthorst, N. H. (1995) Direct determination of dibenzo[a,l]pyrene in crude extracts of environmental samples by laser excited Shpol'skii spectroscopy. Anal. Chem. 67, 1623-1626.
13. Mumford, J. L., Xueming, L., Fuding, H., Xu, B. L., and Chuang, J. C. (1995) Human exposure and dosimetry of polycyclic aromatic hydrocarbons in urine from Xuan Wei, China with high lung cancer mortality associated with exposure to unvented coal smoke. Carcinogenesis (London) 16, 3031-3036.
14. El-Bayoumy, K. (1992) Environmental carcinogens that may be involved in human breast cancer etiology. Chem. Res. Toxicol. 5, 585-590.
15. Devanesan, P. D., Cremonesi, P., Nunnally, J. E., Rogan, E. G., and Cavalieri, E. L. (1990) Metabolism and mutagenicity of dibenzo[a,e]pyrene and the very potent environmental carcinogen dibenzo[a,l]pyrene. Chem. Res. Toxicol. 3, 580-586.
16. Shou, M., Krausz, K. W., Gonzalez, F. J., and Gelboin, H. V. (1996) Metabolic activation of the potent carcinogen dibenzo[a,l]pyrene by human recombinant cytochromes P450, lung and liver microsomes. Carcinogenesis (London) 17, 2429-2433.
17. Ralston, S. L., Lau, H. H. S., Seidel, A., Luch, A., Platt, K. L., and Baird, W. M. (1994) The potent carcinogen dibenzo[a,l]pyrene is metabolically activated to fjord-region 11,12-diol 13,14-epoxides in human mammary carcinoma MCF-7 cell cultures. Cancer Res. 54, 887-890.
18. Ralston, S. L., Seidel, A., Luch, A., Platt, K. L., and Baird, W. M. (1995) Stereoselective activation of dibenzo[a,l]pyrene to (-)-anti(11R,12S,13S,14R)- and (+)-syn(11S,12R,13S,14R)-11,12-diol-13,14-epoxides which bind extensively to deoxyadenosine residues of DNA in the human mammary carcinoma cell line MCF-7. Carcinogenesis (London) 16, 2899-2907.
19. Li, K.-M., Todorovic, R., Rogan, E. G., Cavalieri, E. L., Ariese, F., Suh, M., Jankowiak, R., and Small, G. J. (1995) Identification and quantitation of dibenzo[a,l]pyrene-DNA adducts formed by rat liver microsomes in vitro: preponderance of depurination adducts. Biochemistry 34, 8043-8049.
20. Li, K.-M., RamaKrishna, N. V. S., Padmavathi, N. S., Rogan, E. G., and Cavalieri, E. L. (1994) Synthesis and structure determination of the adducts of dibenzo[a,l]pyrene diol epoxides and deoxyadenosine and deoxyguanosine. Polycycl. Aromat. Compd. 6, 207-213.
21. Thakker, D. R., Levin, W., Yagi, H., Wood, A. W., Conney, A. H., and Jerina, D. M. (1988) Stereoselective biotransformation of polycyclic aromatic hydrocarbons to ultimate carcinogens. In Stereochemical Aspects of Pharmacologically Active Compounds (Wainer, A. W., and Dryer, D., Eds.) pp 271-296, Marcel Dekker, New York.
22. Jones, J. P., Shou, M., and Korzekwa, K. R. (1995) Stereospecific activation of the procarcinogen benzo[a]pyrene: a probe for the active site of the cytochrome P450 superfamily. Biochemistry 34, 6956-6961.
23. Thakker, D. R., Yagi, H., Levin, W., Wood, A. W., Conney, A. H., and Jerina, D. M. (1985) Polycyclic aromatic hydrocarbons: metabolic activation to ultimate carcinogens. In Bioactivation of Foreign Compounds (Anders, M. W., Ed.) pp 177-242, Academic Press, New York.
24. Luch, A., Glatt, H. R., Platt, K. L., Oesch, F., and Seidel, A. (1994) Synthesis and mutagenicity of the diastereomeric fjord-region 11,-12-dihydrodiol 13,14-epoxides of dibenzo[a,l]pyrene. Carcinogenesis (London) 15, 2507-2516.
25. Amin, S., Desai, D., Dai, W., Harvey, R. G., and Hecht, S. S. (1995) Tumorigenicity in newborn mice of fjord region and other sterically hindered diol epoxides of benzo[g]chrysene, dibenzo[a,l]-pyrene (dibenzo[def,p]chrysene), 4H-cyclopenta[def]chrysene and fluoranthene. Carcinogenesis (London) 16, 2813-2817.
26. Amin, S., Krzeminski, J., Rivenson, A., Kurtzke, C., Hecht, S. S., and El-Bayoumy, K. (1995) Mammary carcinogenicity in female CD rats of fjord region diol epoxides of benzo[c]phenanthrene, benzo[g]chrysene and dibenzo[a,l]pyrene. Carcinogenesis (London) 16, 1971-1974.
27. Gill, H. S., Kole, P. L., Wiley, J. C., Li, K. M., Higginbotham, S., Rogan, E. G., and Cavalieri, E. L. (1994) Synthesis and tumor-initiating activity in mouse skin of dibenzo[a,l]pyrene syn- and anti-fjord-region diolepoxides. Carcinogenesis (London) 15, 2455-2460.
28. 32P-postlabeling test for structurally diverse DNA adducts. Carcinogenesis (London) 7, 1543-1551.
29. Bradley, M. O., Bhuyan, B., Francis, M. C., Langenbach, R., Peterson, A., and Huberman, E. (1981) Mutagenesis by chemical agents in V79 Chinese hamster cells: a review and analysis of the literature - a report of the Gene-Tox Program. Mutat. Res. 87, 81-142.
30. Jernström, B., and Gräslund, A. (1994) Covalent binding of benzo-[a]pyrene 7,8-dihydrodiol 9,10-epoxides to DNA: molecular structures, induced mutations and biological consequences. Biophys. Chem. 49, 185-199.
31. Wei, S.-J. C., Chang, R. L., Hennig, E., Cui, X. X., Merkler, K. A., Wong, C.-Q., Yagi, H., Jerina, D. M., and Conney, A. H. (1994) Mutagenic selectivity at the HPRT locus in V-79 cells: comparison of mutations caused by bay-region benzo[a]pyrene 7,8-diol-9,10-epoxide enantiomers with high and low carcinogenic activity. Carcinogenesis (London) 15, 1729-1735.
32. Phillips, D. H., Hewer, A., Seidel, A., Steinbrecher, T., Schrode, R., Oesch, F., and Glatt, H.-R. (1991) Relationship between mutagenicity and DNA adduct formation in mammalian cells for fjord- and bay-region diol epoxides of polycyclic aromatic hydrocarbons. Chem.-Biol. Interact. 80, 177-186.
33. Leffler, M. T., and Calkins, A. E. (1955) l-Menthoxyacetyl chloride. Org. Syntheses, Collect. Vol. 3, pp 547-548, Wiley, New York.
34. Schollmeier, M., Frank, H., Oesch, F., and Platt, K. L. (1986) Assignment of absolute configuration to metabolically formed trans-dihydrodiols of dibenz[a,h]anthracene by two distinct spectroscopic methods. J. Org. Chem. 51, 5368-5372.
35. Frank, H., Luch, A., Oesch, F., and Seidel, A. (1996) 4-[4-(Dimethylamino)-phenylazo]benzoate, a new red-shifted chromophore for use in the exciton chirality method: assignment of absolute configuration to fjord-region metabolites of dibenzo[a,l]-pyrene. Polycycl. Aromat. Compd. 10, 109-116.
36. Estabrook, R. W., and Werringloer, J. (1978) The measurement of difference. In Methods in Enzymology (Fleischer, S., and Packer, L., Eds.) Vol. 52, pp 212-220, Academic Press, New York.
37. Mlcoch, J., Fuchs, J., Oesch, F., and Platt, K. L. (1993) Characterization of DNA adducts at the bay region of dibenz[a,h]-anthracene formed in vitro. Carcinogenesis (London) 14, 469-473.
38. 32P-Postlabeling analysis of DNA adducts persisting for up to 42 weeks in the skin, epidermis and dermis of mice treated topically with 7,12-dimethylbenz[a]anthracene. Carcinogenesis (London) 6, 1117-1126.
39. Platt, K. L., and Schollmeier, M. (1994) Bisdihydrodiols, rather than dihydrodiol oxides, are the principal microsomal metabolites of tumorigenic trans-3,4-dihydroxy-3,4-dihydrodibenz[a,h]anthracene. Chem. Res. Toxicol. 7, 89-97.
40. Thakker, D. R., Levin, W., Yagi, H., Yeh, H. J. C., Ryan, D. E., Thomas, P. E., Conney, A. H., and Jerina, D. M. (1986) Stereoselective metabolism of the (+)-(S,S)- and (-)-(R,R)-enantiomers of trans-3,4-dihydroxy-3,4-dihydrobenzo[c]phenanthrene by rat and mouse liver microsomes and by a purified and reconstituted cytochrome P-450 system. J. Biol. Chem. 261, 5404-5413.
41. Dock, L., Waern, F., Martinez, M., Grover, P. L., and Jernstrom, B. (1986) Studies on the further activation of benzo[a]pyrene diol epoxides by rat liver microsomes and nuclei. Chem.-Biol. Interact. 58, 301-318.
42. Skipper, P. L., Peng, X., SooHoo, C. K., and Tannenbaum, S. R. (1994) Protein adducts as biomarkers of human carcinogen exposure. Drug Metab. Rev. 26, 111-124.
43. Di Raddo, P., and Chan, T.-H. (1983) Reactions of phosphodiesters with epoxides of polycyclic aromatic hydrocarbons. J. Chem. Soc. Chem. Commun. 16-17.
44. Glatt, H. R., Piée, A., Pauly, K., Steinbrecher, T., Schrode, R., Oesch, F., and Seidel, A. (1991) Fjord- and bay-region diol-epoxides investigated for stability, SOS induction in Escherichia coli, and mutagenicity in Salmonella typhimurium and mammalian cells. Cancer Res. 51, 1659-1667.
45. DiGiovanni, J., Slaga, T. J., and Boutwell, R. K. (1980) Comparison of the tumor initiating activity of 7,12-dimethylbenz[a]-anthracene and benzo[a]pyrene in female Sencar and CD-1 mice. Carcinogenesis (London) 1, 381-389.
46. Levin, W., Wood, A. W., Chang, R. L., Ittah, Y., Croisy-Delcey, M., Yagi, H., Jerina, D. M., and Conney, A. H. (1980) Exceptionally high tumor-initiating activity of benzo[c]phenanthrene bay-region diol-epoxides on mouse skin. Cancer Res. 40, 3910-3914.
47. Phillips, D. H., and Grover, P. L. (1994) Polycyclic hydrocarbon activation: bay regions and beyond. Drug Metab. Rev. 26, 443-467.
48. Levin, W., Chang, R. L., Wood, A. W., Thakker, D. R., Yagi, H., Jerina, D. M., and Conney, A. H. (1986) Tumorigenicity of optical isomers of the diastereomeric bay-region 3,4-diol-1,2-epoxides of benzo[c]phenanthrene in murine tumor models. Cancer Res. 46, 2257-2261.
49. Thakker, D. R., Yagi, H., Akagi, H., Koreeda, M., Lu, A. Y. H., Levin, W., Wood, A. W., Conney, A. H., and Jerina, D. M. (1977) Metabolism of benz[a]pyrene VI. Stereoselective metabolism of benzo[a]pyrene and benzo[a]pyrene 7,8-dihydrodiol to diol epoxides. Chem.-Biol. Interact. 16, 281-300.
50. van Bladeren, P. J., Balani, S. K., Sayer, J. M., Thakker, D. R., Boyd, D. R., Ryan, D. E., Thomas, P. E., Levin, W., and Jerina, D. M. (1987) Stereoselective formation of benzo[c]phenanthrene (+)-(3S,4R) and (+)-(5R,6R)-oxides by cytochrome P450c in a highly purified and reconstituted system. Biochem. Biophys. Res. Commun. 145, 160-167.
51. Vericat, J. A., Cheng, S. C., and Dipple, A. (1989) Absolute stereochemistry of the major 7,12-dimethylbenz[a]anthracene-DNA adducts formed in mouse cells. Carcinogenesis (London) 10, 567-570.
52. Shou, M. G., Korzekwa, K. R., Crespi, C. L., Gonzalez, F. J., and Gelboin, H. V. (1994) 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. Carcinogen. (London) 10, 159-168.
53. Shimada, T., Hayes, C. L., Yamazaki, H., Amin, S., Hecht, S. S., and Guengerich, F. P. (1996) Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 56, 2979-2984.
54. Pruess-Schwartz, D., Baird, W. M., Yagi, H., Jerina, D. M., Pigott, M. A., and Dipple, A. (1987). Stereochemical specifity in the metabolic activation of benzo[c]phenanthrene to metabolites that covalently bind to DNA in rodent embryo cell cultures. Cancer Res. 47, 4032-4037.
55. Einolf, H. J., Amin, S., Yagi, H., Jerina, D. M., and Baird, W. M. (1996) Benzo[c]phenanthrene is activated to DNA-binding diol epoxides in the human mammary carcinoma cell line MCF-7 but only limited activation occurs in mouse skin. Carcinogenesis (London) 17, 2237-2244.
56. Pruess-Schwartz, D., Sebti, S. M., Gilham, P. T., and Baird, W. M. (1984) Analysis of benzo[a]pyrene:DNA adducts formed in cells in culture by immobilized boronate chromatography. Cancer Res. 44, 4104-4110.
57. Ralston, S., Coffing, S., Seidel, A., Luch, A., Platt, K. L., and Baird, W. M. (1997) Stereoselective activation of dibenzo[a]pyrene and its trans-11,12-dihydrodiol to fjord-region 11,12-diol 13,14-epoxides in a human mammary carcinoma MCF-7 cell-mediated V79 cell mutation assay. Chem. Res. Toxicol. 10, 687-693.
58. Parkinson, A., Safe, S. H., Robertson, L. W., Thomas, P. E., Ryan, D. E., Reik, L. M., and Levin, W. (1983) Immunochemical quantitation of cytochrome P-450 isozymes and epoxide hydrolase in liver microsomes from polychlorinated or polybrominated biphenyl-treated rats. J. Biol. Chem. 258, 5967-5976.
59. Thomas, P. E., Reik, L. M., Ryan, D. E., and Levin, W. (1983) Induction of two immunochemically related rat liver cytochrome P-450 isozymes, cytochromes P-450c and P-450d, by structurally diverse xenobiotics. J. Biol. Chem. 258, 4590-4598.
60. Thakker, D. R., Levin, W., Yagi, H., Tada, M., Ryan, D. E., Thomas, P. E., Conney, A. H., and Jerina, D. M. (1982) Stereoselective metabolism of the (+)- and (-)-enantiomers of trans-3,4-dihydroxy-3,4-dihydrobenz[a]anthracene by rat liver microsomes and by a purified and reconstituted cytochrome P-450 system. J. Biol. Chem. 257, 5103-5110.