Identification and quantification of the depurinating DNA adducts formed in mouse skin treated with dibenzo[a,l]pyrene (DB[a,l]P) or its metabolites and in rat mammary gland treated with DB[a,l]P

Chemical Research in Toxicology

Volumn 18, Issue 6, 2005, Pages 976-983

  Cavalieri, Ercole L ^a   Rogan, Eleanor G ^a   Li, Kai Ming ^b   Todorovic, Rosa ^e   Ariese, Freek ^c   Jankowiak, Ryszard ^d   Grubor, Nenad ^d   Small, Gerald J ^d  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b ASH STEVENS INC   (United States)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d IOWA STATE UNIVERSITY   (United States)

^e NONE

Author keywords

[No Author keywords available]

Indexed keywords

DIBENZO[A,L]PYRENE; EPOXIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CONTROLLED STUDY; DNA ADDUCT; ELECTRON; FEMALE; FLUORESCENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LOW TEMPERATURE; MAMMARY GLAND; MOUSE; MUTATION; NONHUMAN; OXIDATION; QUANTITATIVE ANALYSIS; RAT; SPECTROSCOPY;

ANIMALS; APURINIC ACID; BENZOPYRENES; CARCINOGENS; DNA; DNA ADDUCTS; FEMALE; MAMMARY GLANDS, ANIMAL; MICE; RATS; RATS, SPRAGUE-DAWLEY; SKIN;

EID: 21144434859     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx049682k     Document Type: Article

References (46)

1. Cavalieri, E. L., Rogan, E. G., Higginbotham, S., Cremonesi, P., and Salmasi, S. (1989) 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, 67-72.
2. 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 12, 1939-1944.
3. 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-dimethyl-benz[a]anthracene and benzo[a]pyrene at low doses in mouse skin. Carcinogenesis 14, 875-878.
4. LaVoie, E. J., He, J.-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-dimethyl-benz[a]anthracene. Cancer Lett. 70, 7-14.
5. 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 mourse skin of dibenzo[a,l]pyrene syn- and anti-fjord-region diolepoxides. Carcinogenesis 15, 2455-2460.
6. 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. Beitrag. Tabakforsch. 9, 79-101.
7. IARC (1983) IARC Monographs on the Evaluation of Carcinogenic Risk of Chemicals to Humans, Vol. 32: Polynuclear Aromatic Compounds, Part 1, Chemical, Environmental and Experimental Data, pp 33-104, 327-347, IAEC, Lyon.
8. Mumford, J. L., He, X. Z., Chapman, R. S., Cao, S. R., Harris, D. B., Li, X. M., Xian, Y. L., Jiang, W. Z., Xu, C. W., Chuang, J. C., Wilson, W. E., and Cooke, M. (1987) Lung cancer and indoor air pollution in Xuan Wei, China. Science 235, 217-220.
9. Mumford, J. L., Li, X., Hu, F., Lu, X. B., 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 16, 3031-3036.
10. Schubert, P., Schantz, M. M., Sander, L. C., and Wise, S. A. (2003) Determination of polycyclic aromatic hydrocarbons with molecular weight 300 and 302 in environmental-matrix standard reference materials by gas chromatography/mass spectrometry. Anal. Chem. 75, 234-246.
11. 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 depurinating adducts. Biochemistry 34, 8043-8049.
12. Devanesan, P., Ariese, F., Jankowiak, R., Small, G. J., Rogan, E. G., and Cavalieri, E. L. (1999) A novel method for the isolation and identification of stable DNA adducts formed by dibenzo[a,l]-pyrene and dibenzo[a,l]pyrene 11,12-dihydrodiol 13,14-epoxides in vitro. Chem. Res. Toxicol. 12, 796-801.
13. Todorovic, R., Devanesan, P., Rogan, E. G., and Cavalieri, E. L. (2005) Identification and quantification of stable DNA adducts of dibenzo[a,l]pyrene formed in mouse skin and rat mammary gland. Chem. Res. Toxicol. 18, 984-990.
14. RamaKrishna, N. V. S., Padmavathi, N. S., Cavalieri, E. L., Rogan, E. G., Cerny, R. L., and Gross, M. L. (1993) Synthesis and structure determination of the adducts formed by electrochemical oxidation of the potent carcinogen dibenzo[a,l]pyrene in the presence of nucleosides. Chem. Res. Toxicol. 6, 554-560.
15. Hanson, A. A., Rogan, E. G., and Cavalieri, E. L. (1998) Synthesis of adducts formed by iodine oxidation of aromatic hydrocarbons in the presence of deoxyribonucleosides and nucleobases. Chem. Res. Toxicol. 11, 1201-1208.
16. Li, K.-M., Byun, J., Gross, M., Zamzow, D., Jankowiak, R., Rogan, E. G., and Cavalieri, E. L. (1999) Synthesis and structure determination of the adducts formed by electrochemical oxidation of dibenzo[a,l]pyrene in the presence of adenine. Chem. Res. Toxicol. 12, 749-757.
17. 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 or deoxyguanosine. Polycyclic Aromat. Compd. 6, 207-213.
18. Li, K.-M., George, M., Gross, M. L., Seidel, A., Luch, A., Rogan, E. G., and Cavalieri, E. L. (1999) Structure elucidation of the adducts formed by fjord region dibenzo[a,l]pyrene 11,12-dihydrodiol 13,14-epoxides with deoxyadenosine. Chem. Res. Toxicol. 12, 758-767.
19. Li, K-M., George, M., Gross, M. L., Lin, C.-H., Jankowiak, R., Small, G. J., Seidel, A., Kroth, H., Rogan, E. G., and Cavalieri, E. L. (1999) Structure elucidation of the adducts formed by fjord region dibenzo[a,l]pyrene 11,12-dihydrodiol 13,14-epoxides with deoxyguanosine. Chem. Res. Toxicol. 12, 778-788.
20. 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.
21. Mulder, P. P. J., Chen, L., Sekhar, B. C., George, M., Gross, M. L., Rogan, E. G., and Cavalieri, E. L. (1996) Synthesis and structure determination of the adducts formed by electrochemical oxidation of 1,2,3,4-tetrahydro-7,12- dimethylbenz[a]anthracene in the presence of deoxyribonucleosides or adenine. Chem. Res. Toxicol. 9, 1264-1277.
22. Li, K-M., Todorovic, R., Devanesan, P., Higginbotham, S., Köfeler, H., Ramanathan, R., Gross, M. L., Rogan, E. G., and Cavalieri, E. L. (2004) Metabolism and DNA binding studies of 4-hydroxy-estradiol and estradiol-3,4-quinone in vitro and in female ACI rat mammary gland in vivo. Carcinogenesis 25, 289-297.
23. NIH Guidelines for the Laboratory Use of Chemical Carcinogens (1981) NIH Publication No. 81-2385, U.S. Government Printing Office, Washington, DC.
24. Jankowiak, R., and Small, G. J. (1989) Fluorescence line narrowing spectroscopy in the study of chemical carcinogenesis. Anal. Chem. 60, 1023A-1032A.
25. Lu, P., Jeong, H., Jankowiak, R., Small, G. J., Kim, S. K., Cosman, M., and Geacintov, N. E. (1991) Comparative laser spectroscopic study of DNA and polynucleotide adducts from the (±)-anti-diol epoxide of benzo[a]pyrene. Chem. Res. Toxicol. 4, 58-69.
26. Devanesan, P. D., RamaKrishna, N. V. S., Todorovic, R., Rogan, E. G., and Cavalieri, E. L. (1992) Identification and quantitation of benzo[a]pyrene-DNA adducts formed by rat liver microsomes in vitro. Chem. Res. Toxicol. 5, 302-309.
27. Rogan, E. G., Devanesan, P. D., RamaKrishna, N. V. S., Higginbotham, S., Padmavathi, N. S., Chapman, K., Cavalieri, E. L., Jeong, H., Jankowiak, R., and Small, G. J. (1993) Identification and quantitation of benzo[a]pyrene-DNA adducts formed in mouse skin. Chem. Res. Toxicol. 6, 356-363.
28. Ariese, F., Small, G. J., and Jankowiak, R. (1996) Conformational studies of depurinating DNA adducts from syrc-dibenzo[a,l]pyrene diolepoxide. Carcinogenesis 17, 829-837.
29. Jankowiak, R., Ariese, F., Zamzow, D., Luch, A., Kroth, H., Seidel, A., and Small, G. J. (1997) Conformational studies of stereoisomeric tetrols derived from syn- and anti-dibenzo[a,l]pyrene diol epoxides. Chem. Res. Toxicol. 10, 677-686.
30. 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.
31. Cremonesi, P., Hietbrink, B., Rogan, E. G., and Cavalieri, E. L. (1992) One-electron oxidation of dibenzo[a]pyrene by manganic acetate. J. Org. Chem. 57, 3309-3312.
32. Todorovic, R., Ariese, F., Devanesan, P., Jankowiak, R., Small, G. J., Rogan, E., and Cavalieri, E. (1997) Determination of benzo-[a]pyrene-and 7,12-dimethylbenz[a]anthracene-DNA adducts formed in rat mammary glands. Chem. Res. Toxicol. 10, 941-947.
33. Chakravarti, D., Pelling, J. C., Cavalieri, E. L., and Rogan, E. G. (1995) Relating aromatic hydrocarbon-induced DNA adducts and c-Harvey-ras mutations in mouse skin papillomas: The role of apurinic sites. Proc. Natl. Acad. Sci. U.S.A. 92, 10422-10426.
34. Chakravarti, D., Mailander, P., Franzen, J., Higginbotham, S., Cavalieri, E. and Rogan, E. (1998) Detection of dibenzo[a,l]pyrene-induced H-ras codon 61 mutant genes in preneoplastic SENCAR mouse skin using a new PCR-RFLP method. Oncogene 16, 3203-3210.
35. Chakravarti, D., Mailander, P. C., Cavalieri, E. L., and Rogan, E. G. (2000) Evidence that error-prone DNA repair converts dibenzo[a,l]pyrene-induced depurinating lesions into mutations: Formation, clonal proliferation and regression of initiated cells carrying H-ras oncogene mutations in early preneoplasia Mutat. Res. 456, 17-32.
36. Colapietro, A.-M., Goodell, A. L., and Smart, R. C. (1993) Characterization of benzo[a]pyrene-initiated mouse skin papillomas for Ha-ras mutations and protein kinase C levels. Carcinogenesis 14, 2289-2295.
37. Slaga, T. J., Viaje, A., Berry, D. L., and Bracken, W. (1976) Skin tumor initiating ability of benzo[a]pyrene 4,5-, 7,8- and 7,8-diol-9,10-epoxides and 7,8-diol. Cancer Lett. 2, 115-122.
38. Slaga, T. L., Bracken, W. M., Viaje, A., Levin, W., Yagi, H., Jerina, D. M., and Conney, A. H. (1977) Comparison of the tumor-initiating activities of benzo[a]pyrene arene oxides and diol-epoxides. Cancer Res. 37, 4130-4133.
39. Quintanilla, M., Brown, K., Ramsden, M., and Balmain, A. (1986) Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 322, 78-80.
40. Brown, K., Buchmann, A., and Balmain, A. (1990) Carcinogen-induced mutations in the mouse c-Ha-ras gene provide evidence of multiple pathways for tumor progression. Proc. Natl. Acad. Sci. U.S.A. 87, 538-542.
41. Devanesan, P. D., RamaKrishna, N. V. S., Padmavathi, N. S., Higginbotham, S., Rogan, E. G., Cavalieri, E. L., Marsch, G. A., Jankowiak, R., and Small, G. J. (1993) Identification and quantitation of 7,12-dimethylbenz[a]anthracene-DNA adducts formed in mouse skin. Chem. Res. Toxicol. 6, 364-371.
42. Casse, C., Hu, Y. C., and Ahrendt, S. A. (2003) The XRCC1 codon 399 Gln allele is associated with adenine to guanine p53 mutations in nonsmall cell lung cancer. Mutat. Res. 528, 19-27.
43. Hofseth, L. J., Khan, M. A., Ambrose, M., Nikolayeva, O., Xu-Welliver, M., Kartalou, M., Hussain, S. P., Roth, R. B., Zhou, X., Mechanic, L. E., Zurer, I., Rotter, V., Samson, L. D., and Harris, C. C. (2003) The adaptive imbalance in base excision-repair enzymes generates microsatellite instability in chronic inflammation. J. Clin. Invest. 112, 1887-1894.
44. Sossou, M., Flohr-Beckhaus, C., Schulz, I., Daboussi, F., Epe, B., and Radicella, J. P. (2005) APE1 overexpression in XRCC1-deficient cells complements the defective repair of oxidative single strand breaks but increases genomic instability. Nucleic Acids Res. 33, 298-306.
45. Frechet, M., Canitrot, Y., Cazaux, C., and Hoffmann, J. S. (2001) DNA polymerase beta imbalance increases apoptosis and mutagenesis induced by oxidative stress. FEBS Lett. 505, 229-232.
46. Lang, T., Maitra, M., Starcevic, D., Li, S. X., and Sweasy, J. B. (2004) A DNA polymerase beta mutant from colon cancer cells induces mutations. Proc. Natl. Acad. Sci. U.S.A. 101, 6074-6079.