Benzo[a]pyrene Diol Epoxide Forms Covalent Adducts with Deoxycytidylic Acid by Alkylation at Both Exocyclic Amino N4 and Ring Imino N-3 Positions

Chemical Research in Toxicology

Volumn 17, Issue 4, 2004, Pages 476-491

  Wolfe, Alan R ^a   Smith, Timothy J ^a,b   Meehan, Thomas ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Lion Bioscience   (United States)

^c Deep Sea DNA Corp   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGEN; DEOXYCYTIDINE PHOSPHATE; DIHYDROXYBENZO[A]PYRENE OXIDE; DNA; EPOXIDE; HALIDE; PYRIMIDINE; URACIL;

ALKYLATION; ARTICLE; DEAMINATION; FLUORESCENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; MASS SPECTROMETRY; MOLECULAR MODEL; NUCLEAR OVERHAUSER EFFECT; PROTON NUCLEAR MAGNETIC RESONANCE;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; ALKYLATION; CARCINOGENS; DEOXYCYTIDINE MONOPHOSPHATE; DNA ADDUCTS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 1942486371     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx0340201     Document Type: Article

References (78)

1. Geacintov, N. E., Shahbaz, M., Ibanez, V., Moussaoui, K., and Harvey, R. G. (1988) Base-sequence dependence of noncovalent complex formation and reactivity of benzo[a]pyrene diol epoxide with polynucleotides. Biochemistry 27, 8380-8387.
2. Szeliga, J., and Dipple, A. (1998) DNA adduct formation by polycyclic aromatic hydrocarbon dihydrodiol epoxides. Chem. Res. Toxicol. 11, 1-11.
3. Jerina, D. M., Chadha, A., Cheh, A. M., Schurdak, M. E., Wood, A. W., and Sayer, J. M. (1991) Covalent bonding of bay-region diol epoxides to nucleic acids. Adv. Exp. Med. Biol. 283, 533-553.
4. 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.
5. Cheng, S. C., Hilton, B. D., Roman, J. M., and Dipple, A. (1989) DNA adducts from carcinogenic and noncarcinogenic enantiomers of benzo[a]pyrene dihydrodiol epoxide. Chem. Res. Toxicol. 2, 334-340.
6. 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.
7. Chen, L., Devanesan, P. D., Byun, J., Gooden, J. K., Gross, M. L., Rogan, E. G., and Cavalieri, E. L. (1997) Synthesis of depurinating DNA adducts formed by one-electron oxidation of 7H-dibenzo[c,g]carbazole and identification of these adducts after activation with rat liver microsomes. Chem. Res. Toxicol. 10, 225-233.
8. Penning, T. M., Burczynski, M. E., Hung, C. F., McCoull, K. D., Palackal, N. T., and Tsuruda, L. S. (1999) Dihydrodiol dehydrogenases and polycyclic aromatic hydrocarbon activation: generation of reactive and redox active o-quinones. Chem. Res. Toxicol. 12, 1-18.
9. Wolfe, A. R., Yamamoto, J., and Meehan, T. (1994) Chloride ions catalyze the formation of cis adducts in the binding of anti-benzo[a]pyrene diol epoxide to nucleic acids. Proc. Natl. Acad. Sci. U.S.A. 91, 1371-1375.
10. Wolfe, A. R., and Meehan, T. (1994) Halide-catalyzed cis product formation in the hydrolysis of anti-benzo[a]pyrene diol epoxide and its alkylation of poly(A). Chem. Res. Toxicol. 7, 110-119.
11. Wolfe, A. R., Song, Q., and Meehan, T. (1996) The effect of temperature on the stereochemistry of DNA adducts derived from benzo[a]pyrene diol epoxide in the presence and absence of halide ions. Polycyclic Aromat. Compd. 10, 203-210.
12. Meehan, T., Wolfe, A. R., Negrete, G. R., and Song, Q. (1997) Benzo[a]pyrene diol epoxide-DNA cis adduct formation through a trans chlorohydrin intermediate. Proc. Natl. Acad. Sci. U.S.A. 94, 1749-1754.
13. Song, Q., Negrete, G. N., Wolfe, A. R., Wang, K., and Meehan, T. (1998) Synthesis and characterization of bay region halohydrins derived from benzo[a]pyrene diol epoxide and their role as intermediates in halide-catalyzed cis adduct formation. Chem. Res. Toxicol. 11, 1057-1066.
14. Vock, E. H., Wolfe, A. R., and Meehan, T. (2001) Trans- and cis-DNA adduct concentration in epidermis from mouse and rat skin treated ex vivo with benzo[a]pyrene diol epoxide and its corresponding chlorohydrin. Mutat. Res. 478, 199-206.
15. - content controls cell volume in single salivary acinar cells during fluid secretion. Am. J. Physiol. 259, C998-C1004.
16. Takemura, T., Sato, F., Saga, K., Suzuki, Y., and Sato, K. (1991) Intracellular ion concentrations and cell volume during cholinergic stimulation of eccrine secretory coil cells. J. Membr. Biol. 119, 211-219.
17. Meehan, T., Straub, K., and Calvin, M. (1977) Benzo[a]pyrene diol epoxide covalently binds to deoxyguanosine and deoxyadenosine in DNA. Nature (London) 269, 725-727.
18. Straub, K. M., Meehan, T., Burlingame, A. L., and Calvin, M. (1977) Identification of the major adducts formed by reaction of benzo[a]pyrene diol epoxide with DNA in vitro. Proc. Natl. Acad. Sci. U.S.A. 74, 5285-5289.
19. Jennette, K. W., Jeffrey, A. M., Blobstein, S. H., Beland, F. A., Harvey, R. G., and Weinstein, I. B. (1977) Nucleoside Adducts from the in vitro reaction of benzo[a]pyrene-7,8-dihydrodiol 9,10-oxide or benzo[a]pyrene 4,5-oxide with nucleic acids. Biochemistry 16, 932-938.
20. Brown, H. S., Jeffrey, A. M., and Weinstein, I. B. (1979) Formation of DNA adducts in 10T1/2 mouse embryo fibroblasts incubated with benzo[a]pyrene or dihydrodiol oxide derivatives. Cancer Res. 39, 1673-1677.
21. Sayer, J. M., Chadha, A., Agarwal, S. K., Yeh, H. J. C., Yagi, H., and Jerina, D. M. (1991) Covalent nucleoside adducts of benzo[a]pyrene 7,8-diol 9,10-epoxides: structural reinvestigation and characterization of a novel adenosine adduct on the ribose moiety. J. Org. Chem. 56, 20-29.
22. Yamamoto, J., Subramaniam, R., Wolfe, A. R., and Meehan, T. (1990) The formation of covalent adducts between benzo[a]pyrenediol epoxide and RNA: structural analysis by mass spectrometry. Biochemistry 29, 3966-3972.
23. Chadha, A., Sayer, J. M., Yeh, H. J. C., Yagi, H., Cheh, A. M., Pannell, L. K., and Jerina, D. M. (1989) Structures of covalent nucleoside adducts formed from adenine, guanine, and cytosine bases of DNA and the optically active bay-region 3,4-diol 1,2-epoxides of dibenz[a,j]anthracene. J. Am. Chem. Soc. 111, 5456-5463.
24. Chadha, A., Sayer, J. M., Agarwal, S. K., Cheh, A. M., Yagi, H., Yeh, H. J. C., and Jerina, D. M. (1991) Formation of covalent adducts between DNA and optically active bay-region diol epoxides of dibenzo[a,j]anthracene. In Polynuclear Aromatic Hydrocarbons: Measurements, Means and Metabolism (Eleventh International Symposium) (Cook, M., Loening, K., and Merritt, J., Eds.) pp 179-193, Battelle Press, Columbus, OH.
25. Cheh, A. M., Chadha, A., Sayer, J. M., Yeh, H. J. C., Yagi, H., Pannell, L. K., and Jerina, D. M. (1993) Structures of covalent nucleoside adducts formed from adenine, guanine, and cytosine bases of DNA and the optically active bay-region 3,4-diol 1,2-epoxides of benz[a]anthracene. J. Org. Chem. 58, 4013-4022.
26. Jerina, D. M., Sayer, J. M., Agarwal, S. K., Yagi, H., Levin, W., Wood, A. W., Conney, A. H., Pruess-Schwartz, D., Baird, W. M., Pigott, M. A., and et al. (1986) Reactivity and tumorigenicity of bay-region diol epoxides derived from polycyclic aromatic hydrocarbons. Adv. Exp. Med. Biol. 197, 11-30.
27. Dipple, A., Pigott, M. A., Agarwal, S. K., Yagi, H., Sayer, J. M., and Jerina, D. M. (1987) Optically active benzo[c]phenanthrene diol epoxides bind extensively to adenine in DNA. Nature 327, 535-536.
28. Sage, E., and Haseltine, W. A. (1984) High ratio of alkali-sensitive lesions to total DNA modification induced by benzo[a]pyrene diol epoxide. J. Biol. Chem. 259, 11098-11102.
29. Bigger, C. A. H., Cheh, A. M., Dipple, A., Yagi, H., Sayer, J. M., and Jerina, D. M. (1986) Sites of alkali-sensitive DNA lesions induced by enantiomers of the diastereomeric bay-region benzo[c]phenanthrene (B[c]Ph) 3,4-diol-1,2-epoxides. Proc. Am. Assoc. Cancer Res. 27, 88.
30. 2-deoxyguanosine adducts derived from the highly carcinogenic fjord-region benzo[c]phenanthrene 3,4-diol 1,2-epoxides. Chem. Res. Toxicol. 15, 1619-1626.
31. Peltonen, K., Cheng, S. C., Hilton, B. D., Lee, H., Cortez, C., Harvey, R. G., and Dipple, A. (1991) Effect of bay region methyl group on reactions of anti-benz[a]anthracene 3,4-dihydrodiol 1,2-epoxides with DNA. J. Org. Chem. 56, 4181-4188.
32. Wei, S. J., Chang, R. L., Bhachech, N., Cui, X. X., Merkler, K. A., Wong, C. Q., Hennig, E., Yagi, H., Jerina, D. M., and Conney, A. H. (1993) Dose-dependent differences in the profile of mutations induced by (+)-7R,SS-dihydroxy-9S,10R-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene in the coding region of the hypoxanthine (guanine) phosphoribosyltransferase gene in Chinese hamster V-79 cells. Cancer Res. 53, 3294-3301.
33. Yagi, H., Akagi, H., Thakker, D. R., Mah, H. D., Koreeda, M., and Jerina, D. M. (1977) Absolute stereochemistry of the highly mutagenic 7,8-diol 9,10-epoxides derived from the potent carcinogen trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene. J. Am. Chem. Soc. 99, 2358-2359.
34. Moore, P. D., and Koreeda, M. (1976) Application of the change in partition coefficient with pH to the structure determination of alkyl substituted guanosines. Biochem. Biophys. Res. Commun. 73, 459-464.
35. Dudek, M. J., and Ponder, J. W. (1995) Accurate modeling of the intramolecular electrostatic energy of proteins. J. Comput. Chem. 16, 791-816.
36. Stewart, J. J. P. (1989) Optimization of parameters for semiempirical methods I. Method. J. Comput. Chem. 10, 210-220.
37. Stewart, J. J. (1990) MOPAC: a semiempirical molecular orbital program. J. Comput.-Aided Mol. Des. 4, 1-105.
38. Klamt, A., and Shüürmann, G. (1993) COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient. J. Chem. Soc. Perk. Trans. 2, 799-805.
39. Jeffrey, A. M., Jennette, K. W., Blobstein, S. H., Weinstein, I. B., Beland, F. A., Harvey, R. G., Kasai, H., Miura, I., and Nakanishi, K. (1976) Benzo[a]pyrene-nucleic acid derivative found in vivo: structure of a benzo[a]pyrenetetrahydrodiol epoxide-guanosine adduct. J. Am. Chem. Soc. 98, 5714-5715.
40. Jeffrey, A. M., Grzeskowiak, K., Weinstein, I. B., Nakanishi, K., Roller, P., and Harvey, R. G. (1979) Benzo[a]pyrene-7,8-dihydrodiol 9,10-oxide adenosine and deoxyadenosine adducts: structure and stereochemistry. Science 206, 1309-1311.
41. Dunn, D. B., and Hall, H. R. (1975) Purines, pyrimidines, nucleosides and nucleotides: physical constants and spectral properties. In CRC Handbook of Biochemistry and Molecular Biology, 3rd ed. (Fasman, G. D., Ed.) Vol. 2:1, pp 65-215, CRC Press, Cleveland.
42. Solomon, J. J., Mukai, F., Fedyk, J., and Segal, A. (1988) Reactions of propylene oxide with 2′-deoxynucleosides and in vitro with calf thymus DNA. Chem.-Biol. Interact. 67, 275-294.
43. Solomon, J. J., and Segal, A. (1989) DNA adducts of propylene oxide and acrylonitrile epoxide: hydrolytic deamination of 3-alkyl-dCyd to 3-alkyl-dUrd. Environ. Health Perspect. 81, 19-22.
44. Solomon, J. J., Singh, U. S., and Segal, A. (1993) In vitro reactions of 2-cyanoethylene oxide with calf thymus DNA. Chem.-Biol. Interact. 88, 115-135.
45. Li, F., Segal, A., and Solomon, J. J. (1992) In vitro reaction of ethylene oxide with DNA and characterization of DNA adducts. Chem.-Biol. Interact. 83, 35-54.
46. Bhanot, O. S., Singh, U. S., and Solomon, J. J. (1994) The role of 3-hydroxyethyldeoxyuridine in mutagenesis by ethylene oxide. J. Biol. Chem. 269, 30056-30064.
47. Snow, E. T., Singh, J., Koenig, K. L., and Solomon, J. J. (1994) Propylene oxide mutagenesis at template cytosine residues. Environ. Mol. Mutagen. 23, 274-280.
48. Singh, U. S., Decker-Samuelian, K., and Solomon, J. J. (1996) Reaction of epichlorohydrin with 2′-deoxynucleosides: characterization of adducts. Chem.-Biol. Interact. 99, 109-128.
49. Selzer, R. R., and Elfarra, A. A. (1997) Chemical modification of deoxycytidine at different sites yields adducts of different stabilities: characterization of N3- and O2-deoxycytidine and N3-deoxyuridine adducts of butadiene monoxide. Arch. Biochem. Biophys. 343, 63-72.
50. Barlow, T., and Dipple, A. (1999) Formation of deaminated products in styrene oxide reactions with deoxycytidine. Chem. Res. Toxicol. 12, 883-886.
51. Koskinen, M., Calebiro, D., and Hemminki, K. (2000) Styrene oxide-induced 2′-deoxycytidine adducts: implications for the mutagenicity of styrene oxide. Chem.-Biol. Interact. 126, 201-213.
52. Segal, A., Solomon, J. J., and Mukai, F. (1990) In vitro reactions of glycidol with pyrimidine bases in calf thymus DNA. Cancer Biochem. Biophys. 11, 59-67.
53. Geacintov, N. E., Mao, B., France, L. L., Zhao, R., Chen, J., Liu, T. M., Ya, N.-Q., Margulis, L. A., and Sutherland, J. C. (1992) Photoinduced electron transfer and fluorescence mechanisms in covalently linked polynuclear aromatic-nucleotide complexes. SPIE Vol. 1640, Time-Resolved Laser Spectroscopy in Biochemistry III, 774-783.
54. Sayer, J. M., Yagi, H., Silverton, J. V., Friedman, S. L., Whalen, D. L., and Jerina, D. M. (1982) Conformational effects in the hydrolyses of rigid benzylic epoxides: implications for diol epoxides of polycyclic hydrocarbons. J. Am. Chem. Soc. 104, 1972-1978.
55. Sayer, J. M., Whalen, D. L., Friedman, S. L., Paik, A., Yagi, H., Vyas, K. P., and Jerina, D. M. (1984) Conformational effects in the hydrolyses of benzo-ring diol epoxides that have bay-region diol groups. J. Am. Chem. Soc. 106, 226-233.
56. Doan, L., Yagi, H., Jerina, D. M., and Whalen, D. L. (2002) Chloride Ion Catalyzed Conformational Inversion of Carbocation Intermediates in the Hydrolysis of a Benzo[a]pyrene 7,8-Diol 9,10-Epoxide. J. Am. Chem. Soc. 124, 14382-14387.
57. Singer, B. (1975) The chemical effects of nucleic acid alkylation and their relation to mutagenesis and carcinogenesis. Prog. Nucleic Acid Res. Mol. Biol. 15, 219-284.
58. Singer, B. (1986) O-alkyl pyrimidines in mutagenesis and carcinogenesis: occurrence and significance. Cancer Res. 46, 4879-4885.
59. Sun, L., and Singer, B. (1974) Reaction of cytidine with ethylating agents. Biochemistry 13, 1905-1913.
60. Dipple, A., Brookes, P., Mackintosh, D. S., and Rayman, M. P. (1971) Reaction of 7-bromomethylbenz[a]anthracene with nucleic acids, polynucleotides, and nucleosides. Biochemistry 10, 4323-4330.
61. Shapiro, R., and Shiuey, S.-J. (1976) Reactions of cytidine with 7-bromomethylbenz[a]anthracene, benzyl bromide, and p-methoxybenzyl bromide. Ratio of amino to 3 substitution. J. Org. Chem. 41, 1597-1600.
62. Dipple, A. (1995) DNA adducts of chemical carcinogens. Carcinogenesis (London) 16, 437-441.
63. 4-alkyl pyrimidine nucleosides: stability of the glycosyl bond and of the alkyl group as a function of pH. Biochemistry 17, 1246-1250.
64. 2-alkylcytidine-a new major product of neutral, aqueous reaction of cytidine with carcinogens. FEBS Lett. 63, 85-88.
65. Koreeda, M., Moore, P. D., Yagi, H., Yeh, H. J., and Jerina, D. M. (1976) Alkylation of polyguanylic acid at the 2-amino group and phosphate by the potent mutagen (±)-7β,8α-dihydroxy-9β,10β -epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene. J. Am. Chem. Soc. 98, 6720-6722.
66. Geacintov, N. E., Cosman, M., Mao, B., Alfano, A., Ibanez, V., and Harvey, R. G. (1991) Spectroscopic characteristics and site I/site II classification of cis and trans benzo[a]pyrene diolepoxide enantiomer-guanosine adducts in oligonucleotides and polynucleotides. Carcinogenesis (London) 12, 2099-2108.
67. Meehan, T., Gamper, H., and Becker, J. F. (1982) Characterization of reversible, physical binding of benzo[a]pyrene derivatives to DNA. J. Biol. Chem. 257, 10479-10485.
68. Geacintov, N. E., Yoshida, H., Ibanez, V., and Harvey, R. G. (1982) Noncovalent binding of 7β,8α-dihydroxy-9α,10α -epoxytetrahydrobenzo[a]pyrene to deoxyribonucleic acid and its catalytic effect on the hydrolysis of the diol epoxide to tetrol. Biochemistry 21, 1864-1869.
69. Geacintov, N. E., Zhao, R., Kuzmin, V. A., Kim, S. K., and Pecora, L. J. (1993) Mechanisms of quenching of the fluorescence of a benzo[a]pyrene tetraol metabolite model compound by 2′-deoxynucleosides. Photochem. Photobiol. 58, 185-194.
70. Shafirovich, V. Y., Levin, P. P., Kuzmin, V. A., Thorgeirsson, T. E., Kliger, D. S., and Geacintov, N. E. (1994) Photoinduced electron transfer and enhanced triplet yields in benzo[a]pyrene derivative-nucleic acid complexes and covalent adducts. J. Am. Chem. Soc. 116, 63-72.
71. Xie, X. M., Geacintov, N. E., and Broyde, S. (1999) Stereochemical origin of opposite orientations in DNA adducts derived from enantiomeric anti-benzo[a]pyrene diol epoxides with different tumorigenic potentials. Biochemistry 38, 2956-2968.
72. Xie, X. M., Geacintov, N. E., and Broyde, S. (1999) Origins of conformational differences between cis and trans DNA adducts derived from enantiomeric anti-benzo[a]pyrene diol epoxides. Chem. Res. Toxicol. 12, 597-609.
73. Tan, J., Geacintov, N. E., and Broyde, S. (2000) Principles governing conformations in stereoisomeric adducts of bay region benzo[a]pyrene diol epoxides to adenine in DNA: steric and hydrophobic effects are dominant. J. Am. Chem. Soc. 122, 3021-3032.
74. Tan, J., Geacintov, N. E., and Broyde, S. (2000) Conformational determinants of structures in stereoisomeric cis-opened anti-benzo[a]pyrene diol epoxide adducts to adenine in DNA. Chem. Res. Toxicol. 13, 811-822.
75. Rayman, M. P., and Dipple, A. (1973) Structure and activity in chemical carcinogenesis. Comparison of the reactions of 7-bromomethylbenz[a]anthracene and 7-bromomethyl-12-methylbenz[a]anthracene with deoxyribonucleic acid in vitro. Biochemistry 12, 1202-1207.
76. Geacintov, N. E., Cosman, M., Hingerty, B. E., Amin, S., Broyde, S., and Patel, D. J. (1997) NMR solution structures of stereoisometric covalent polycyclic aromatic carcinogen-DNA adduct: principles, patterns, and diversity. Chem. Res. Toxicol. 10, 111-146.
77. Mao, B., Gu, Z., Gorin, A., Chen, J., Hingerty, B. E., Amin, S., Broyde, S., Geacintov, N. E., and Patel, D. J. (1999) Solution structure of the (+)-cis-anti-benzo[a]pyrene-dA ([BP]dA) adduct opposite dT in a DNA duplex. Biochemistry 38, 10831-10842.
78. Hess, M. T., Gunz, D., Luneva, N., Geacintov, N. E., and Naegeli, H. (1997) Base pair conformation-dependent excision of benzo[a]pyrene diol epoxide-guanine adducts by human nucleotide excision repair enzymes. Mol. Cell. Biol. 17, 7069-7076.