Deoxyguanosine forms a bis-adduct with E, E-muconaldehyde, an oxidative metabolite of benzene: Implications for the carcinogenicity of benzene

Chemical Research in Toxicology

Volumn 24, Issue 11, 2011, Pages 1944-1956

  Harris, Constance M ^a   Stec, Donald F ^a   Christov, Plamen P ^a   Kozekov, Ivan D ^a   Rizzo, Carmelo J ^a   Harris, Thomas M ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZENE; DEOXYGUANOSINE; DNA; HISTIDINE; IMIDAZOLE; LYSINE; MUCONALDEHYDE; NUCLEOSIDE; PEPTIDE; SODIUM DERIVATIVE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARCINOGEN DNA INTERACTION; CHEMICAL CARCINOGENESIS; CHEMICAL MODEL; CHEMICAL REACTION; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; DEGLYCOSYLATION; DIASTEREOISOMER; DNA CROSS LINKING; DNA REPAIR; DNA REPLICATION; EPIMERIZATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PROTEIN CROSS LINKING; REDUCTION KINETICS;

ALDEHYDES; AMINO ACIDS; BENZENE; BIOTRANSFORMATION; CARCINOGENS; CIRCULAR DICHROISM; DEOXYGUANOSINE; DNA; DNA ADDUCTS; ENVIRONMENTAL POLLUTION; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; NUCLEIC ACID CONFORMATION; OXIDATION-REDUCTION; PEPTIDES; SOLUTIONS; SPIRO COMPOUNDS; STEREOISOMERISM;

EID: 81755182525     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx2002838     Document Type: Article

References (69)

1. Whysner, J., Reddy, M. V., Ross, P. M., Mohan, M., and Lax, E. A. (2004) Genotoxicity of benzene and its metabolites Mutat. Res. 566, 99-130 (Pubitemid 38185874)
2. Bayliss, D. L., Chen, C., Jarabek, A., Sonawane, B., and Valcovic, L. (1998) Carcinogenic effects of benzene: An update. U.S. Environmental Protection Agency, EPA/600/P-97/001F (http://www.epa.gov/ncea/pdfs/benzenef.pdf).
3. Bond, J. A. and Rice, J. M., Eds. (2010) Benzene 2009-Health effects and mechanisms of bone marrow toxicity: Implications for t-AML and the mode of action framework. Chem.-Biol. Interact. 184, 1-312.
4. McMichael, A. J. (1988) Carcinogenicity of benzene, toluene and xylene: epidemiological and experimental evidence IARC Sci. Publ. 3-18
5. Henderson, R. F., Sabourin, P. J., Medinsky, M. A., Birnbaum, L. S., and Lucier, G. L. (1992) Benzene dosimetry in experimental animals: Relevance for risk assessment Prog. Clin. Biol. Res. 374, 93-105
6. Lan, Q., Zhang, L., Li, G., Vermeulen, R., Weinberg, R. S., Dosemeci, M., Rappaport, S. M., Shen, M., Alter, B. P., Wu, Y., Kopp, W., Waidyanatha, S., Rabkin, C., Guo, W., Chanock, S., Hayes, R. B., Linet, M., Kim, S., Yin, S., Rothman, N., and Smith, M. T. (2004) Hematotoxicity in workers exposed to low levels of benzene Science 306, 1774-1776 (Pubitemid 39601394)
7. Kim, S., Vermeulen, R., Waidyanatha, S., Johnson, B. A., Lan, Q., Rothman, N., Smith, M. T., Zhang, L., Li, G., Shen, M., Yin, S., and Rappaport, S. M. (2006) Using urinary biomarkers to elucidate dose-related patterns of human benzene metabolism Carcinogenesis 27, 772-781
8. Snyder, R. (2004) Xenobiotic metabolism and the mechanism(s) of benzene toxicity Drug Metab. Rev. 36, 531-547 (Pubitemid 39453061)
9. Smith, M. T. (1996) The mechanism of benzene-induced leukemia: a hypothesis and speculations on the causes of leukemia Environ. Health Perspect. 104 (Suppl. 6) 1219-1225 (Pubitemid 27046642)
10. Valentine, J. L., Lee, S. S., Seaton, M. J., Asgharian, B., Farris, G., Corton, J. C., Gonzalez, F. J., and Medinsky, M. A. (1996) Reduction of benzene metabolism and toxicity in mice that lack CYP2E1 expression Toxicol. Appl. Pharmacol. 141, 205-213 (Pubitemid 26414367)
11. Jowa, L., Witz, G., Snyder, R., Winkle, S., and Kalf, G. F. (1990) Synthesis and characterization of deoxyguanosine-benzoquinone adducts J. Appl. Toxicol. 10, 47-54 (Pubitemid 20200274)
12. Lindsey, R. H., Bender, R. P., and Osheroff, N. (2005) Stimulation of topoisomerase II-mediated DNA cleavage by benzene metabolites Chem.-Biol. Interact. 153-154, 197-205 (Pubitemid 40797811)
13. McDonald, T. A., Holland, N. T., Skibola, C., Duramad, P., and Smith, M. T. (2001) Hypothesis: Phenol and hydroquinone derived mainly from diet and gastrointestinal flora activity are causal factors in leukemia Leukemia 15, 10-20 (Pubitemid 32140322)
14. 6]benzene to rats Carcinogenesis 14, 1921-1925 (Pubitemid 23290910)
15. 6]benzene Cancer Res. 54, 4907-4914
16. Goldstein, B. D., Witz, G., Javid, J., Amoruso, M. A., Rossman, T., and Wolder, B. (1981) Muconaldehyde, a potential toxic intermediate of benzene metabolism Adv. Exp. Med. Biol. 136 (Part A) 331-339
17. 14C-deoxyguanosine 5′-phosphate Environ. Health Perspect. 82, 249-251 (Pubitemid 19231556)
18. Witz, G., Latriano, L., and Goldstein, B. D. (1989) Metabolism and toxicity of trans, trans -muconaldehyde, an open-ring microsomal metabolite of benzene Environ. Health Perspect. 82, 19-22 (Pubitemid 19231530)
19. Amin, R. P. and Witz, G. (2001) DNA-protein crosslink and DNA strand break formation in HL-60 cells treated with trans, trans -muconaldehyde, hydroquinone and their mixtures Int. J. Toxicol. 20, 69-80 (Pubitemid 32422312)
20. Davies, S. G. and Whitham, G. H. (1977) Benzene oxide-oxepin. Oxidation to muconaldehyde J. Chem. Soc., Perkins I 1346-1347
21. Bleasdale, C., Kennedy, G., MacGregor, J. O., Nieschalk, J., Pearce, K., Watson, W. P., and Golding, B. T. (1996) Chemistry of muconaldehydes of possible relevance to the toxicology of benzene Environ. Health Perspect. 104 (Suppl. 6) 1201-1209 (Pubitemid 27046641)
22. Henderson, A. P., Bleasdale, C., Delaney, K., Lindstrom, A. B., Rappaport, S. M., Waidyanatha, S., Watson, W. P., and Golding, B. T. (2005) Evidence for the formation of Michael adducts from reactions of (E, E)-muconaldehyde with glutathione and other thiols Bioorg. Chem. 33, 363-373 (Pubitemid 41405701)
23. Latriano, L., Goldstein, B. D., and Witz, G. (1986) Formation of muconaldehyde, an open-ring metabolite of benzene, in mouse liver microsomes: An additional pathway for toxic metabolites Proc. Natl. Acad. Sci. U.S.A. 83, 8356-8360 (Pubitemid 17182499)
24. 1) benzene Biochem. J. 54, 231-238
25. Witz, G., Maniara, W., Mylavarapu, V., and Goldstein, B. D. (1990) Comparative metabolism of benzene and trans, trans -muconaldehyde to trans, trans -muconic acid in DBA/2N and C57BL/6 mice Biochem. Pharmacol. 40, 1275-1280 (Pubitemid 20311938)
26. Gad-El Karim, M. M., Ramanujam, V. M., and Legator, M. S. (1985) trans, trans -Muconic acid, an open-chain urinary metabolite of benzene in mice. Quantification by high-pressure liquid chromatography Xenobiotica 15, 211-220 (Pubitemid 15050129)
27. Weaver, V. M., Buckley, T., and Groopman, J. D. (2000) Lack of specificity of trans,trans -muconic acid as a benzene biomarker after ingestion of sorbic acid-preserved foods Cancer Epidemiol. Biomarkers Prev. 9, 749-755 (Pubitemid 30482708)
28. Lindstrom, A. B., Yeowell-O'Connell, K., Waidyanatha, S., Golding, B. T., Tornero-Velez, R., and Rappaport, S. M. (1997) Measurement of benzene oxide in the blood of rats following administration of benzene Carcinogenesis 18, 1637-1641 (Pubitemid 28134790)
29. Lovern, M. R., Turner, M. J., Meyer, M., Kedderis, G. L., Bechtold, W. E., and Schlosser, P. M. (1997) Identification of benzene oxide as a product of benzene metabolism by mouse, rat, and human liver microsomes Carcinogenesis 18, 1695-1700 (Pubitemid 28134673)
30. Turteltaub, K. W. and Mani, C. (2003) Benzene metabolism in rodents at doses relevant to human exposure from urban air. Res. Rep. Health Eff. Inst., 1-26; discussion 27-35.
31. Henderson, R. F., Sabourin, P. J., Bechtold, W. E., Griffith, W. C., Medinsky, M. A., Birnbaum, L. S., and Lucier, G. W. (1989) The effect of dose, dose rate, route of administration, and species on tissue and blood levels of benzene metabolites Environ. Health Perspect. 82, 9-17 (Pubitemid 19231529)
32. Sabourin, P. J., Bechtold, W. E., Griffith, W. C., Birnbaum, L. S., Lucier, G., and Henderson, R. F. (1989) Effect of exposure concentration, exposure rate, and route of administration on metabolism of benzene by F344 rats and B6C3F1 mice Toxicol. Appl. Pharmacol. 99, 421-444 (Pubitemid 19189756)
33. Weisel, C., Yu, R., Roy, A., and Georgopoulos, P. (1996) Biomarkers of environmental benzene exposure Environ. Health Perspect. 104 (Suppl. 6) 1141-1146 (Pubitemid 27046139)
34. Yu, R. and Weisel, C. P. (1996) Measurement of benzene in human breath associated with an environmental exposure J. Exposure Anal. Environ. Epidemiol. 6, 261-277 (Pubitemid 26345815)
35. Rappaport, S. M., Kim, S., Lan, Q., Vermeulen, R., Waidyanatha, S., Zhang, L., Li, G., Yin, S., Hayes, R. B., Rothman, N., and Smith, M. T. (2009) Evidence that humans metabolize benzene via two pathways Environ. Health Perspect. 117, 946-952
36. Au, W. W., Ramanujam, V. M., Ward, J. B., Jr., and Legator, M. S. (1991) Chromosome aberrations in lymphocytes of mice after sub-acute low-level inhalation exposure to benzene Mutat. Res. 260, 219-224
37. Ward, J. B., Jr., Ammenheuser, M. M., Ramanujam, V. M., Morris, D. L., Whorton, E. B., Jr., and Legator, M. S. (1992) The mutagenic effects of low level sub-acute inhalation exposure to benzene in CD-1 mice Mutat. Res. 268, 49-57
38. Chang, R. L., Wong, C. Q., Kline, S. A., Conney, A. H., Goldstein, B. D., and Witz, G. (1994) Mutagenicity of trans, trans -muconaldehyde and its metabolites in V79 cells Environ. Mol. Mutagen. 24, 112-115 (Pubitemid 24317111)
39. Glatt, H. and Witz, G. (1990) Studies on the induction of gene mutations in bacterial and mammalian cells by the ring-opened benzene metabolites trans, trans -muconaldehyde and trans, trans -muconic acid Mutagenesis 5, 263-266 (Pubitemid 20329944)
40. Zhang, L., Eastmond, D. A., and Smith, M. T. (2002) The nature of chromosomal aberrations detected in humans exposed to benzene Crit. Rev. Toxicol. 32, 1-42 (Pubitemid 34132781)
41. Eastmond, D. A., Schuler, M., Frantz, C., Chen, H., Parks, R., Wang, L., and Hasegawa, L. (2001) Characterization and mechanisms of chromosomal alterations induced by benzene in mice and humans. Res. Rep. Health Eff. Inst., 1-68; discussion 69-80.
42. Nakayama, A., Noguchi, Y., Mori, T., Morisawa, S., and Yagi, T. (2004) Comparison of mutagenic potentials and mutation spectra of benzene metabolites using supF shuttle vectors in human cells Mutagenesis 19, 91-97 (Pubitemid 38380285)
43. Schoenfeld, H. A. and Witz, G. (2000) Structure-activity relationships in the induction of DNA-protein cross-links by hematotoxic ring-opened benzene metabolites and related compounds in HL60 cells Toxicol. Lett. 116, 79-88 (Pubitemid 30440770)
44. Schoenfeld, H. A. and Witz, G. (1999) DNA-protein cross-link levels in bone marrow cells of mice treated with benzene or trans, trans -muconaldehyde J. Toxicol. Environ. Health A 56, 379-395 (Pubitemid 29149894)
45. Frantz, C. E., Chen, H., and Eastmond, D. A. (1996) Inhibition of human topoisomerase II in vitro by bioactive benzene metabolites Environ. Health Perspect. 104 (Suppl. 6) 1319-1323 (Pubitemid 27046162)
46. Bleasdale, C., Golding, B. T., Kennedy, G., MacGregor, J. O., and Watson, W. P. (1993) Reactions of muconaldehyde isomers with nucleophiles including tri- O -acetylguanosine: Formation of 1,2-disubstituted pyrroles from reactions of the (Z, Z)-isomer with primary amines Chem. Res. Toxicol. 6, 407-412 (Pubitemid 23212504)
47. 2-deoxyguanosine adducts of the α,β-unsaturated aldehydes acrolein, crotonaldehyde, and 4-hydroxynonenal Chem. Res. Toxicol. 22, 759-778
48. Stone, M. P., Cho, Y. J., Huang, H., Kim, H. Y., Kozekov, I. D., Kozekova, A., Wang, H., Minko, I. G., Lloyd, R. S., Harris, T. M., and Rizzo, C. J. (2008) Interstrand DNA cross-links induced by α,β-unsaturated aldehydes derived from lipid peroxidation and environmental sources Acc. Chem. Res. 41, 793-804
49. 2-propano-2′-deoxyguanosine DNA adduct J. Am. Chem. Soc. 127, 17686-17696 (Pubitemid 43003382)
50. Nechev, L. V., Harris, C. M., and Harris, T. M. (2000) Synthesis of nucleosides and oligonucleotides containing adducts of acrolein and vinyl chloride Chem. Res. Toxicol. 13, 421-429 (Pubitemid 30327163)
51. 2-propano-2′-deoxyguanosine J. Am. Chem. Soc. 124, 9324-9325 (Pubitemid 34856190)
52. Golding, B. T., Kennedy, G., and Watson, W. P. (1988) Simple syntheses of isomers of muconaldehyde and 2-methylmuconaldehyde Tetrahedron Lett. 29, 5991-5994
53. Ihara, M., Katogi, M., Fukumoto, K., and Kametani, T. (1987) Total synthesis of (±)-pentalenic acid via intramolecular double Michael reaction J. Chem. Soc., Chem. Commun. 721-722 (Pubitemid 17073280)
54. Tobe, Y., Iseki, T., Kakiuchi, K., and Odaira, Y. (1984) A new strategy for construction of angularly fused tricyclic ring systems. Transannular bond formation of bicyclic enones via photochemical intramolecular hydrogen abstraction Tetrahedron Lett. 25, 3895-3896
55. Humski, K., Sendijarevic, V., and Shiner, V. J. (1976) Stereochemistry of solvolytic substitution of cyclopentyl p -bromobenzenesulfonate J. Am. Chem. Soc. 98, 2865-2868
56. 1H-NMR analyses, shielding mechanisms, coupling-constants, and conformations in steroids bearing halogen, hydroxy, oxo groups, and double bonds J. Am. Chem. Soc. 107, 7027-7039
57. Paasivirta, J. (1987) Solutions to stereochemical problems. In Lanthanide Shift Reagents in Stereochemical Analysis (Morrill, T. C., Ed.) p 121, Wiley-VCH Pubs., New York.
58. Hess, B. A. (2011) Personal communication.
59. 2-deoxyguanosine adducts of the lipid peroxidation product trans-4-hydroxynonenal J. Am. Chem. Soc. 125, 5687-5700 (Pubitemid 36592892)
60. 2-etheno-2′-deoxyguanosine formation from epoxyaldehydes Chem. Res. Toxicol. 20, 1685-1692
61. Harada, N. and Nakanishi, K. (1969) A method for determining the chirality of two aromatic chromophores and the absolute configurations of chromomycin A3 and related antibiotics J. Am. Chem. Soc. 91, 5896-5898
62. Berova, N., Nakanishi, K., and Woody, R. (2000) Circular Dichroism: Principles and Applications, 2 nd ed., Wiley-VCH, New York.
63. Pohl, F. M. and Jovin, T. M. (1972) Salt-induced co-operative conformational change of a synthetic DNA: Equilibrium and kinetic studies with poly (dG-dC) J. Mol. Biol. 67, 375-396
64. Byrns, M. C., Predecki, D. P., and Peterson, L. A. (2002) Characterization of nucleoside adducts of cis -2-butene-1,4-dial, a reactive metabolite of furan Chem. Res. Toxicol. 15, 373-379 (Pubitemid 34241376)
65. Rindgen, D., Nakajima, M., Wehrli, S., Xu, K., and Blair, I. A. (1999) Covalent modifications to 2′-deoxyguanosine by 4-oxo-2-nonenal, a novel product of lipid peroxidation Chem. Res. Toxicol. 12, 1195-1204 (Pubitemid 30013530)
66. 2- ethenodeoxyguanosine as a potential marker for DNA adduct formation by trans -4-hydroxy-2-nonenal Cancer Res. 48, 320-323 (Pubitemid 18045764)
67. Norman, D., Live, D., Sastry, M., Lipman, R., Hingerty, B. E., Tomasz, M., Broyde, S., and Patel, D. J. (1990) NMR and computational characterization of mitomycin cross-linked to adjacent deoxyguanosines in the minor groove of the d(T-A-C-G-T-A) ·d(T-A-C-G-T-A) duplex Biochemistry 29, 2861-2875 (Pubitemid 20122623)
68. Spielmann, H. P., Dwyer, T. J., Sastry, S. S., Hearst, J. E., and Wemmer, D. E. (1995) DNA structural reorganization upon conversion of a psoralen furan-side monoadduct to an interstrand cross-link: Implications for DNA repair Proc. Natl. Acad. Sci. U.S.A. 92, 2345-2349
69. Hwang, G. S., Kim, J. K., and Choi, B. S. (1996) The solution structure of a psoralen cross-linked DNA duplex by NMR and relaxation matrix refinement Biochem. Biophys. Res. Commun. 219, 191-197