Identification and quantification of a guanine - Thymine intrastrand cross-link lesion induced by Cu(II)/H2O2/ascorbate

Chemical Research in Toxicology

Volumn 19, Issue 5, 2006, Pages 614-621

  Hong, Haizheng ^a   Cao, Huachuan ^a   Wang, Yuesong ^a   Wang, Yinsheng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (HYDROXYMETHYL) 2' DEOXYURIDINE; 5 FORMYLDEOXYURIDINE; 8 HYDROXYDEOXYGUANOSINE; ASCORBIC ACID; CARBON; CUPRIC ION; DEOXYURIDINE DERIVATIVE; DNA; GUANINE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; NUCLEIC ACID BASE; PHOSPHORUS 32; REACTIVE OXYGEN METABOLITE; THYMINE; UNCLASSIFIED DRUG;

AQUEOUS SOLUTION; ARTICLE; CATTLE; COVALENT BOND; CROSS LINKING; DNA DAMAGE; DNA STRAND; FENTON REACTION; GAMMA IRRADIATION; INTRASTRAND CROSS LINK LESION; LIQUID CHROMATOGRAPHY; QUANTITATIVE ASSAY; TANDEM MASS SPECTROMETRY; THYMUS; X IRRADIATION;

ASCORBIC ACID; CHROMATOGRAPHY, LIQUID; COPPER; CROSS-LINKING REAGENTS; DNA; DNA DAMAGE; GUANINE; HYDROGEN PEROXIDE; MASS SPECTROMETRY; THYMINE;

MAMMALIA;

EID: 33744504440     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx060025x     Document Type: Article

References (62)

1. Lindahl, T. (1999) DNA lesions generated in vivo by reactive oxygen species, their accumulation and repair. NATO ASl Ser., Ser. A 302, 251-257.
2. Finkel, T., and Holbrook, N. J. (2000) Oxidants, oxidative stress and the biology of aging. Nature 408, 239-247.
3. Marnett, L. J. (2000) Oxyradicals and DNA damage. Carcinogenesis 21, 361-370.
4. Feig, D. I., Reid, T. M., and Loeb, L. A. (1994) Reactive oxygen species in tumorigenesis. Cancer Res. 54, 1890s-1894s.
5. Lee, D. H., O'Connor, T. R., and Pfeifer, G. P. (2002) Oxidative DNA damage induced by copper and hydrogen peroxide promotes CG→TT tandem mutations at methylated CpG dinucleotides in nucleotide excision repair-deficient cells. Nucleic Acids Res. 30, 3566-3573.
6. Reid, T. M., and Loeb, L. A. (1993) Tandem double CC-TT mutations are produced by reactive oxygen species. Proc. Natl. Acad. Sci. U.S.A. 90, 3904-3907.
7. Newcomb, T. G., Allen, K. J., Tkeshelashvili, L., and Loeb, L. A. (1999) Detection of tandem CC→TT mutations induced by oxygen radicals using mutation-specific PCR. Mutat. Res. 427, 21-30.
8. Box, H. C., Budzinski, E. E., Dawidzik, J. D., Wallace, J. C., Evans, M. S., and Gobey, J. S. (1996) Radiation-induced formation of a cross-link between base moieties of deoxyguanosine and thymidine in deoxygenated solutions of d(CpGpTpA). Radiat. Res. 145, 641-643.
9. Box, H. C., Budzinski, E. E., Dawidzik, J. B., Gobey, J. S., and Freund, H. G. (1997) Free radical-induced tandem base damage in DNA oligomers. Free Radical Biol. Med. 23, 1021-1030.
10. Box, H. C., Budzinski, E. E., Dawidzik, J. B., Wallace, J. C., and Iijima, H. (1998) Tandem lesions and other products in X-irradiated DNA oligomers. Radiat. Res. 149, 433-439.
11. Budzinski, E. E., Dawidzik, J. B., Rajecki, M. J., Wallace, J. C., Schroder, E. A., and Box, H. C. (1997) Isolation and characterization of the products of anoxic irradiation of d(CpGpTpA). Int. J. Radiat. Biol. 71, 327-336.
12. Romieu, A., Bellon, S., Gasparutto, D., and Cadet, J. (2000) Synthesis and UV photolysis of oligodeoxynucleotides that contain 5-(phenylthiomethyl)- 2′-deoxyuridine: A specific photolabile precursor of 5-(2′- deoxyuridilyl)methyl radical. Org. Lett. 2, 1085-1088.
13. Bellon, S., Ravanat, J. L., Gasparutto, D., and Cadet, J. (2002) Cross-linked thymine-purine base tandem lesions: Synthesis, characterization, and measurement in gamma-irradiated isolated DNA. Chem. Res. Toxicol. 15, 598-606.
14. BrCG) and duplex DNA containing 5-bromocytosine. J. Am. Chem. Soc. 126, 6552-6553.
15. Zhang, Q., and Wang, Y. (2003) Independent generation of 5-(2′-deoxycytidinyl)methyl radical and the formation of a novel cross-link lesion between 5-methylcytosine and guanine. J. Am. Chem. Soc. 125, 12795-12802.
16. Zhang, Q., and Wang, Y. (2004) Independent generation of the 5-hydroxy-5,6-dihydrothymidin-6-yl radical and its reactivity in dinucleoside monophosphates. J. Am. Chem. Soc. 126, 13287-13297.
17. Zhang, Q., and Wang, Y. (2005) Generation of 5-(2′-deoxycytidyl)- methyl radical and the formation of intrastrand cross-link lesions in oligodeoxyribonucleotides. Nucleic Acids Res. 33, 1593-1603.
18. Liu, Z., Gao, Y., and Wang, Y. (2003) Identification and characterization of a novel cross-link lesion in d(CpC) upon 365-nm irradiation in the presence of 2-methyl-1,4-naphthoquinone. Nucleic Acids Res. 31, 5413-5424.
19. Liu, Z., Gao, Y., Zeng, Y., Fang, F., Chi, D., and Wang, Y. (2004) Isolation and characterization of a novel cross-link lesion in d(CpC) induced by one-electron photooxidation. Photochem. Photobiol. 80, 209-215.
20. Gu, C., and Wang, Y. (2004) LC-MS/MS identification and yeast polymerase eta bypass of a novel γ-irradiation-induced intrastrand cross-link lesion G[8-5]C. Biochemistry 43, 6745-6750.
21. von Sonntag, C. (1987) The Chemical Basis of Radiation Biology, Talor & Francis, London.
22. Aruoma, O. I., Halliwell, B., Gajewski, E., and Dizdaroglu, M. (1991) Copper-ion-dependent damage to the bases in DNA in the presence of hydrogen peroxide. Biochem. J. 273, 601-604.
23. Drouin, R., Rodriguez, H., Gao, S. W., Gebreyes, Z., O'Connor, T. R., Holmquist, G. P., and Akman, S. A. (1996) Cupric ion/ascorbate/hydrogen peroxide-induced DNA damage: DNA-bound copper ion primarily induces base modifications. Free Radical Biol. Med. 21, 261-273.
24. Agarwal, K., Sharma, A., and Talukder, G. (1989) Effects of copper on mammalian cell components. Chem.-Biol. Interact. 69, 1-16.
25. Bach, D., and Miller, I. R. (1967) Polarographic investigation of binding of Cu++ and Cd++ by DNA. Biopolymers 5, 161-172.
26. Bryan, S. E., and Frieden, E. (1967) Interaction of copper(II) with deoxyribonucleic acid below 30°. Biochemistry 6, 2728-2734.
27. Prutz, W. A., Butler, J., and Land, E. J. (1990) Interaction of copper(I) with nucleic acids. Int. J. Radiat. Biol. 58, 215-234.
28. Barbouti, A., Doulias, P. T., Zhu, B. Z., Frei, B., and Galaris, D. (2001) Intracellular iron, but not copper, plays a critical role in hydrogen peroxide-induced DNA damage. Free Radical Biol. Med. 31, 490-498.
29. Bar-Or, D., and Winkler, J. V. (2002) Copper is involved in hydrogen-peroxide-induced DNA damage. Free Radical Biol. Med. 32, 197-199.
30. Ames, B. N., and Gold, L. S. (1991) Endogenous mutagens and the causes of aging and cancer. Mutat. Res. 250, 3-16.
31. Sagripant, J. L., and Kraemer, K. H. (1989) Site-specific oxidative DNA damage at polyguanosines produced by copper plus hydrogen peroxide. J. Biol. Chem. 264, 1729-1734.
32. Liang, Q., and Dedon, P. C. (2001) Cu(II)/H2O2-induced DNA damage is enhanced by packaging of DNA as a nucleosome. Chem. Res. Toxicol. 14, 416-422.
33. Nackerdien, Z., Rao, G., Cacciuttolo, M. A., Gajewski, E., and Dizdaroglu, M. (1991) Chemical nature of DNA-protein cross-links produced in mammalian chromatin by hydrogen peroxide in the presence of iron or copper ions. Biochemistry 30, 4873-4879.
34. Lloyd, D. R., and Phillips, D. H. (1999) Oxidative DNA damage mediated by copper(II), iron(II) and nickel(II) fenton reactions: Evidence for site-specific mechanisms in the formation of double-strand breaks, 8-hydroxydeoxyguanosine and putative intrastrand cross-links. Mutat. Res. 424, 23-36.
35. Oikawa, S., and Kawanishi, S. (1998) Distinct mechanisms of site-specific DNA damage induced by endogenous reductants in the presence of iron(III) and copper(II). Biochim. Biophys. Acta 1399, 19-30.
36. Yamamoto, K., and Kawanishi, S. (1989) Hydroxyl free radical is not the main active species in site-specific DNA damage induced by copper(II) ion and hydrogen peroxide. J. Biol. Chem. 264, 15435-15440.
37. Dizdaroglu, M., Gajewski, E., Reddy, P., and Margolis, S. A. (1989) Structure of a hydroxyl radical induced DNA-protein cross-link involving thymine and tyrosine in nucleohistone. Biochemistry 28, 3625-3628.
38. Randerath, K., Reddy, M. V., and Disher, R. M. (1986) Age- and tissue-related DNA modifications in untreated rats: Detection by 32P-postlabeling assay and possible significance for spontaneous tumor induction and aging. Carcinogenesis 7, 1615-1617.
39. Randerath, K., Yang, P. F., Danna, T. F., Reddy, R., Watson, W. P., and Randerath, E. (1991) Bulky adducts detected by 32P-postlabeling in DNA modified by oxidative damage in vitro. Comparison with rat lung I-compounds. Mutat. Res. 250, 135-144.
40. Randerath, E., Watson, W. P., Zhou, G. D., Chang, J., and Randerath, K. (1995) Intensification and depletion of specific bulky renal DNA adducts (I-compounds) following exposure of male F344 rats to the renal carcinogen ferric nitrilotriacetate (Fe-NTA). Mutat. Res. 341, 265-279.
41. Randerath, K., Randerath, E., Smith, C. V., and Chang, J. (1996) Structural origins of bulky oxidative DNA adducts (type II I-compounds) as deduced by oxidation of oligonucleotides of known sequence. Chem. Res. Toxicol. 9, 247-254.
42. Randerath, K., Randerath, E., Zhou, G. D., and Li, D. (1999) Bulky endogenous DNA modifications (I-compounds) -possible structural origins and functional implications. Mutat. Res. 424, 183-194.
43. 32P-postlabeling of DNA adducts induced by a Fenton-type oxygen radical-generating system. Carcinogenesis 13, 1127-1135.
44. 32P-postlabeling. Mutat. Res. 291, 147-159.
45. 32P-postlabeling assay for the oxidative DNA lesion 8,5′-cyclo-2′-deoxyadenosine in mammalian tissues: evidence that four type II I-compounds are dinucleotides containing the lesion in the 3′ nucleotide. J. Biol. Chem. 276, 36051-36057.
46. LaFrancois, C. J., Fujimoto, J., and Sowers, L. C. (1998) Synthesis and characterization of isotopically enriched pyrimidine deoxynucleoside oxidation damage products. Chem. Res. Toxicol. 11, 75-83.
47. Gillet, L. C., and Scharer, O. D. (2002) Preparation of C8-amine and acetylamine adducts of 2′-deoxyguanosine suitably protected for DNA synthesis. Org. Lett. 4, 4205-4208.
48. Nampalli, S., and Kumar, S. (2000) Efficient synthesis of 8-oxo-dGTP: A mutagenic nucleotide. Bioorg. Med. Chem. Lett. 10, 1677-1679.
49. Frelon, S., Douki, T., Ravanat, J. L., Pouget, J. P., Tornabene, C., and Cadet, J. (2000) High-performance liquid chromatography-tandem mass spectrometry measurement of radiation-induced base damage to isolated and cellular DNA. Chem. Res. Toxicol. 13, 1002-1010.
50. BrCA) and duplex DNA containing a 5-bromocytosine. J. Am. Chem. Soc. 127, 13969-13977.
51. Trumbore, C. N., Ehrlich, R. S., and Myers, Y. N. (2001) Changes in DNA conformation induced by gamma irradiation in the presence of copper. Radiat. Res. 155, 453-465.
52. Frelon, S., Douki, T., Favier, A., and Cadet, J. (2003) Hydroxyl radical is not the main reactive species involved in the degradation of DNA bases by copper in the presence of hydrogen peroxide. Chem. Res. Toxicol. 16, 191-197.
53. Lloyd, D. R., Carmichael, P. L., and Phillips, D. H. (1998) Comparison of the formation of 8-hydroxy-2′-deoxyguanosine and single- and double-strand breaks in DNA mediated by fenton reactions. Chem. Res. Toxicol. 11, 420-427.
54. Shi, M., Xu, B., Azakami, K., Morikawa, T., Watanabe, K., Morimoto, K., Komatsu, M., Aoyama, K., and Takeuchi, T. (2005) Dual role of vitamin C in an oxygen-sensitive system: Discrepancy between DNA damage and cell death. Free Radical Res. 39, 213-220.
55. Ravanat, J. L., Di Mascio, P., Martinez, G. R., Medeiros, M. H. G., and Cadet, J. (2000) Singlet oxygen induces oxidation of cellular DNA. J. Biol. Chem. 275, 40601-40604.
56. Kuraoka, I., Bender, C., Romieu, A., Cadet, J., Wood, R. D., and Lindahl, T. (2000) Removal of oxygen free-radical-induced 5′,8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc. Natl. Acad. Sci. U.S.A. 97, 3832-3837.
57. Brooks, P. J., Wise, D. S., Berry, D. A., Kosmoski, J. V., Smerdon, M. J., Somers, R. L., Mackie, H., Spoonde, A. Y., Ackerman, E. J., Coleman, K., Tarone, R. E., and Robbins, J. H. (2000) The oxidative DNA lesion 8,5′-(S)-cyclo-2′-deoxyadenosine is repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells. J. Biol. Chem. 275, 22355-22362.
58. Yang, Z., Colis, L. C., Basu, A. K., and Zou, Y. (2005) Recognition and incision of gamma-radiation-induced cross-linked guanine-thymine tandem lesion G[8,5-Me]T by UvrABC nuclease. Chem. Res. Toxicol. 18, 1339-1346.
59. Gu, C., and Wang, Y. (2005) Thermodynamic and in vitro replication studies of an intrastrand G[8-5]C cross-link lesion. Biochemistry 44, 8883-8889.
60. Berneburg, M., and Lehmann, A. R. (2001) Xeroderma pigmentosum and related disorders: Defects in DNA repair and transcription. Adv. Genet. 43, 71-102.
61. Satoh, M. S., Jones, C. J., Wood, R. D., and Lindahl, T. (1993) DNA excision-repair defect of xeroderma pigmentosum prevents removal of a class of oxygen free radical-induced base lesions. Proc. Natl. Acad. Sci. U.S.A. 90, 6335-6339.
62. Cleaver, J. E., and Kraemer, K. H. (1989) In The Metabolic Basis of Inherited Disease (Scriver, C., Beaudet, A. L., Sly, W. S., and Vale, D., Eds.) pp 2949-2971, McGraw-Hill, New York.