On the species-specific biotransformation of dibenzo[a,l]pyrene

Chemico-Biological Interactions

Volumn 161, Issue 1, 2006, Pages 37-48

  Schober, Wolfgang ^a   Luch, Andreas ^b   Soballa, Volker J ^c   Raab, Gottfried ^d   Stegeman, John J ^e   Doehmer, Johannes ^f   Jacob, Jürgen ^d   Seidel, Albrecht ^d  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^c EVONIK INDUSTRIES AG   (Germany)

^d Prof Dr Gernot Grimmer Foundation   (Germany)

^e WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^f GenPharmTox BioTech AG   (Germany)

Author keywords

Cytochromes P450; Dibenzo a,l pyrene; Species specific biotransformation

Indexed keywords

CARCINOGEN; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; CYTOCHROME P450 2A6; CYTOCHROME P450 2B1; CYTOCHROME P450 2E1; CYTOCHROME P450 3A4; DIBENZO[A,L]PYRENE;

ANIMAL CELL; ARTICLE; BIOTRANSFORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENANTIOSELECTIVITY; ENZYME MECHANISM; FISH; METABOLITE; MICRONUCLEUS TEST; NONHUMAN; PROTEIN EXPRESSION; SPECIES DIFFERENCE;

ANIMALS; BENZOPYRENES; BIOTRANSFORMATION; CARCINOGENS; CELL LINE; CELL SURVIVAL; CRICETINAE; CRICETULUS; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; MICRONUCLEUS TESTS; PERCIFORMES; RATS; SPECIES SPECIFICITY;

ANIMALIA; CRICETULUS GRISEUS; RODENTIA;

EID: 33646115184     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2006.02.007     Document Type: Article

References (59)

1. Lacassagne A., Buu-Hoï N.P., Zajdela F., and Vigniello F.A. The true dibenzo[a,l]pyrene, a new, potent carcinogen. Naturwissenschaften 55 (1968) 43
2. Masuda Y., and Kagawa R. A novel sythesis and carcinogenicity of dibenzo[a,l]pyrene. Chem. Pharm. Bull. 20 (1972) 2736-2737
3. DeRaat W.K., Kooijman S.A.L.M., and Gielen J.W.J. Concentrations of polycyclic aromatic hydrocarbons in airborne particles in Netherlands and their correlation with mutagenicity. Sci. Total Environ. 66 (1987) 95-114
4. Mumford J.L., Harris D.B., Williams K., Chuang J.C., and Cooke M. Indoor air sampling, and mutagenicity studies of emissions from unvented coal combustion. Environ. Sci. Technol. 21 (1987) 308-311
5. Mumford J.L., Xueming L., Fuding H., Xu B.L., and Chuang J.C. 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 16 (1995) 3031-3036
6. Kozin I.S., Gooijer C., and Velthorst N.H. Direct determination of dibenzo[a,l]pyrene in crude extracts of environmental samples by laser excited Shpol'skii spectroscopy. Anal. Chem. 67 (1995) 1623-1626
7. Seidel A., Frank H., Behnke A., Schneider D., and Jacob J. Determination of dibenzo[a,l]pyrene and other fjord-region PAH isomers with MW 302 in environmental matrices. Polycycl. Aromat. Compd. 24 (2004) 759-771
8. Snook M.E., Severson R.F., Arrendale R.F., Higman H.C., and Chortyk O.T. The identification of high molecular weight polynuclear aromatic hydrocarbons in a biologically active fraction of cigarette smoke condensate. Beitr. Tabakforsch. 9 (1977) 79-101
9. Hoffmann D., and Hoffmann I. Tobacco smoke components. Beitr. Tabakforsch. 18 (1998) 49-52
10. Cavalieri E.L., Rogan E.G., Higginbotham S., Cremonesi P., and Salmasi S. Tumor-initiating activity in mouse skin and carcinogenicity in rat mammary gland of dibenzo[a]pyrenes: the very potent environmental carcinogen dibenzo[a,l]pyrene. J. Cancer Res. Clin. Oncol. 115 (1989) 67-72
11. Cavalieri E.L., Higginbotham S., RamaKrishna N.V.S., Devanesan P.D., Todorovic R., Rogan E.G., and Salmasi S. 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 12 (1991) 1939-1944
12. LaVoie E.J., He Z.M., Meegalla R.L., and Weyand E.H. 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 (1993) 7-14
13. Higginbotham S., RamaKrishna N.V.S., Johansson S.L., Rogan E.G., and Cavalieri E.L. 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 14 (1993) 875-878
14. Ralston S.L., Lau H.H.S., Seidel A., Luch A., Platt K.L., and Baird W.M. 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 (1994) 887-890
15. Ralston S.L., Seidel A., Luch A., Platt K.L., and Baird W.M. 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 16 (1995) 2899-2907
16. Devanesan P.D., Cremonesi P., Nunnally J.E., Rogan E.G., and Cavalieri E.L. Metabolism and mutagenicity of dibenzo[a,e]pyrene and the very potent environmental carcinogen dibenzo[a,l]pyrene. Chem. Res. Toxicol. 3 (1990) 580-586
17. Li K.M., Todorovic R., Rogan E.G., Cavalieri E.L., Ariese F., Suh M., Jankowiak R., and Small G.J. Identification and quantitation of dibenzo[a,l]pyrene-DNA adducts formed by rat liver microsomes in vitro: preponderance of depurinating adducts. Biochemistry 34 (1995) 8043-8049
18. 32P-postlabeling. Carcinogenesis 18 (1997) 1999-2007
19. Ralston S.L., Coffing S.L., Seidel A., Luch A., Platt K.L., and Baird W.M. Stereoselective activation of dibenzo[a,l]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 (1997) 687-693
20. Luch A., Seidel A., Glatt H., and Platt K.L. 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. Chem. Res. Toxicol. 10 (1997) 1161-1170
21. Luch A., Friesel H., Seidel A., and Platt K.L. Tumor-initiating activity of the (+)-(S,S)- and (-)-(R,R)-enantiomers of trans-11,12-dihydroxy-11,12-dihydrodibenzo[a,l]pyrene in mouse skin. Cancer Lett. 136 (1999) 119-128
22. Thakker D.R., Levin W., Yagi H., Wood A.W., Conney A.H., and Jerina D.M. Stereoselective biotransformation of polycyclic aromatic hydrocarbons to ultimate carcinogens. In: Wainer A.W., and Dryer D. (Eds). Stereochemical Aspects of Pharmacologically Active Compounds (1988), Marcel Dekker, New York
23. Hall M., and Grover P.L. Polycyclic aromatic hydrocarbons: metabolism, activation and tumour initiation. In: Cooper C.S., and Grover P.L. (Eds). Chemical Carcinogenesis and Mutagenesis vol. I (1990), Springer, Berlin 327-372
24. Phillips D.H., and Grover P.L. Polycyclic hydrocarbon activation: bay regions and beyond. Drug Metab. Rev. 26 (1994) 443-467
25. Luch A., and Baird W.M. Metabolic activation and detoxification of polycyclic aromatic hydrocarbons. In: Luch A. (Ed). The Carcinogenic Effects of Polycyclic Aromatic Hydrocarbons (2005), Imperial College Press, London 19-96
26. Doehmer J. V79 Chinese hamster cells genetically engineered for cytochrome P450 and their use in mutagenicity and metabolism studies. Toxicology 82 (1993) 105-118
27. Grimmer G., Stober W., Jacob J., Mohr U., Schoene K., Brune H., and Misfeld J. Inventory and biological impact of polycyclic carcinogens in the environment. Exp. Pathol. 24 (1983) 3-13
28. Stegeman J.J., and Kloepper-Sams P.J. Cytochrome P-450 isozymes and monooxygenase activity in aquatic animals. Environ. Health Perspect. 71 (1987) 87-95
29. Meador J.P., Stein J.E., Reichert W.L., and Varanasi U. Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms. Rev. Environ. Contam. Toxicol. 143 (1995) 79-165
30. Morrison H.G., Oleksiak M.F., Cornell N.W., Sogin M.L., and Stegeman J.J. Identification of cytochrome P-450 1A (CYP1A) genes from two teleost fish, toadfish (Opsanus tau) and scup (Stenotomus chrysops), and phylogenetic analysis of CYP1A genes. Biochem. J. 308 (1995) 97-104
31. Luch A., Glatt H.R., Platt K.L., Oesch F., and Seidel A. Synthesis and mutagenicity of the diastereomeric fjord-region 11,12-dihydrodiol-13,14-epoxides of dibenzo[a,l]pyrene. Carcinogenesis 15 (1994) 2507-2516
32. Luch A., Schober W., Soballa V.J., Raab G., Greim H., Jacob J., Doehmer J., and Seidel A. Metabolic activation of dibenzo[a,l]pyrene by human cytochrome P450 1A1 and 1B1 expressed in V79 Chinese hamster cells. Chem. Res. Toxicol. 12 (1999) 353-364
33. Glatt H.R., Gemperlein I., Turchi G., Heinritz H., Doehmer J., and Oesch F. Search for cell culture systems with diverse xenobiotic-metabolizing activities and their use in toxicological studies. Mol. Toxicol. 1 (1987) 313-334
34. Schmalix W.A., Maser H., Kiefer F., Reen R., Wiebel F.J., Gonzalez F.J., Seidel A., Glatt H.R., and Doehmer J. Stable expression of human cytochrome P450 1A1 cDNA in V79 Chinese hamster cells and metabolic activation of benzo[a]pyrene. Eur. J. Pharmacol. 248 (1993) 251-261
35. Wölfel C., Heinrich-Hirsch B., Schultz-Schalge T., Seidel A., Frank H., Ramp U., Wächter F., Wiebel F.J., Greim H., and Doehmer J. Genetically engineered V79 Chinese hamster cells for stable expression of human cytochrome P450 1A2. Eur. J. Pharmacol. 228 (1992) 95-102
36. Luch A., Coffing S.L., Tang Y.M., Schneider A., Soballa V., Greim H., Jefoate C.R., Seidel A., Greenlee W.F., Baird W.M., and Doehmer J. Stable expression of human cytochrome P450 1B1 in V79 Chinese hamster cells and metabolically catalyzed DNA adduct formation of dibenzo[a,l]pyrene. Chem. Res. Toxicol. 11 (1998) 686-695
37. Schneider A., Schmalix W.A., Siruguri V., de Groene E.M., Horbach G.J., Kleingeist B., Lang D., Böcker R., Belloc C., Beaune P., Greim H., and Doehmer J. Stable expression of human cytochrome P450 3A4 in conjunction with human NADPH-cytochrome P450 oxidoreductase in V79 Chinese hamster cells. Arch. Biochem. Biophys. 332 (1996) 295-304
38. Schmalix W.A., Barrenscheen M., Landsiedel R., Janzowski C., Eisenbrand G., Gonzalez F., Eliasson E., Ingelman-Sundberg M., Perchermeier M., Greim H., and Doehmer J. Stable expression of human cytochrome P450 2E1 in V79 Chinese hamster cells. Eur. J. Pharmacol. 293 (1995) 123-131
39. Dogra S., Doehmer J., Glatt H.R., Molders H., Siegert P., Friedberg T., Seidel A., and Oesch F. Stable expression of rat cytochrome P-450IA1 cDNA in V79 Chinese hamster cells and their use in mutagenicity testing. Mol. Pharmacol. 37 (1990) 608-613
40. Wölfel C., Platt K.L., Dogra S., Glatt H.R., Wächter F., and Doehmer J. Stable expression of rat cytochrome P450IA2 cDNA and hydroxylation of 17β-estradiol and 2-aminofluorene in V79 Chinese hamster cells. Mol. Carcinogen. 4 (1991) 489-498
41. 1. Proc. Natl. Acad. Sci. USA 85 (1988) 5769-5773
42. Seidel A., Soballa V.J., Raab G., Frank H., Greim H., Grimmer G., Jacob J., and Doehmer J. Regio- and stereoselectivity in the metabolism of benzo[c]phenanthrene mediated by genetically engineered V79 Chinese hamster cells expressing rat and human cytochrome P450. Environ. Toxicol. Pharmacol. 5 (1998) 179-196
43. Schmalix W.A., Lang D., Schneider A., Bocker R., Greim H., and Doehmer J. Stable expression and coexpression of human cytochrome P450 oxidoreductase and cytochrome P4501A2 in V79 Chinese hamster cells: sensitivity to quinons and biotransformation of 7-alkoxy and triazines. Drug Metab. Disp. 24 (1996) 1314-1319
44. Roscher E., and Wiebel F.J. Mutagenicity, clastogenicity and cytotoxicity of procarcinogens in a rat hepatoma cell line competent for xenobiotic metabolism. Mutagenesis 3 (1988) 269-276
45. Jacob J., and Grimmer G. Capillary gas chromatography analysis and mass spectrometric identification of polycyclic aromatic hydrocarbon metabolites from biological materials. Rev. Anal. Chem. 9 (1988) 49-58
46. Luch A., Platt K.L., and Seidel A. Synthesis of fjord region tetraols and their use in hepatic biotransformation studies of dihydrodiols of benzo[c]chrysene, benzo[g]chrysene and dibenzo[a,l]pyrene. Carcinogenesis 19 (1998) 639-648
47. 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 (1994) 159-168
48. Bauer E., Guo Z., Ueng Y.F., Bell L.C., Zeldin D., and Guengerich F.P. Oxidation of benzo[a]pyrene by recombinant human cytochrome P450 enzymes. Chem. Res. Toxicol. 8 (1995) 136-142
49. Shou M., Krausz K.W., Gonzalez F.J., and Gelboin H.V. Metabolic activation of the potent carcinogen dibenzo[a,l]pyrene by human recombinant cytochromes P450, lung and liver microsomes. Carcinogenesis 17 (1996) 2429-2433
50. Luch A., Kishiyama S., Seidel A., Doehmer J., Greim H., and Baird W.M. The K-region trans-8,9-diol does not significantly contribute as an intermediate in the metabolic activation of dibenzo[a,l]pyrene to DNA-binding metabolites by human cytochrome P450 1A1 or 1B1. Cancer Res. 59 (1999) 4603-4609
51. Penning T.M., Burczynski M.E., Hung C.F., McCoull K., Palackal N.T., and Tsuruda L.S. Dihydrodiol dehydrogenases and polycyclic aromatic hydrocarbons: generation of reactive and redox active o-quinones. Chem. Res. Toxicol. 12 (1999) 1-18
52. Palackal N.T., Burczynski M.E., Harvey R.G., and Penning T.M. The ubiquitous aldehyde reductase (AKR1A1) oxidizes proximate carcinogen trans-dihydrodiols to o-quinones: potential role in polycyclic aromatic hydrocarbon activation. Biochemistry 40 (2001) 10901-10910
53. Shou M., Gonzalez F.J., and Gelboin H.V. Stereoselective epoxidation and hydration at the K-region of polycyclic aromatic hydrocarbons by cDNA-expressed cytochromes P450 1A1, 1A2, and epoxide hydrolase. Biochemistry 35 (1996) 15807-15813
54. Jacob J., Raab G., Schober W., Frank H., Luch A., Doehmer J., and Seidel A. Species-dependent metabolism of benzo[c]chrysene mediated by c-DNA-expressed human, rodent and fish cytochrome P450 enzymes. Polycycl. Aromat. Compd. 21 (2000) 109-121
55. Balani S.K., van Bladeren P.J., Shirai N., and Jerina D.M. Resolution and absolute configuration of K-region trans-dihydrodiols from polycyclic aromatic hydrocarbons. J. Org. Chem. 51 (1986) 1773-1778
56. Jacob J., Raab G., Soballa V.J., Luch A., Grimmer G., Greim H., Doehmer J., Morrison H.G., Stegeman J.J., and Seidel A. Species-dependent metabolism of benzo[c]phenanthrene and dibenzo[a,l]pyrene by various CYP450 isoforms. Polycycl. Aromat. Compd. 16 (1999) 191-203
57. Doehmer J., Holtkamp D., Soballa V., Raab G., Schmalix W., Seidel A., Greim H., and Jacob J. Cytochrome P450 mediated reactions studied in genetically engineered V79 Chinese hamster cells. Pharmacogenetics 5 (1995) S91-S96
58. Ittah Y., Thakker D.R., Levin W., Croisy-Delcey M., Ryan D.E., Thomas P.E., Conney A.H., and Jerina D.M. Metabolism of benzo[c]phenanthrene by rat liver microsomes and by a purified monooxygenase system reconstituted with different isozymes of cytochrome P-450. Chem. Biol. Interact. 45 (1983) 15-28
59. Lorentzen R.J., Caspary W.J., Lesko S.A., and Ts'o P.O.P. The autoxidation of 6-hydroxybenzo[a]pyrene and 6-oxobenzo[a]pyrene radical, reactive metabolites of benzo[a]pyrene. Biochemistry 14 (1975) 3970-3977