DNA Lesions Derived from the Site Selective Oxidation of Guanine by Carbonate Radical Anions

Chemical Research in Toxicology

Volumn 16, Issue 12, 2003, Pages 1528-1538

  Joffe, Avrum ^a   Geacintov, Nicholas E ^a   Shafirovich, Vladimir ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANINE; CARBONIC ACID; DNA; GUANINE; HYDANTOIN DERIVATIVE; OLIGONUCLEOTIDE; RADICAL; SULFATE;

ABSORPTION; ARTICLE; CIRCULAR DICHROISM; CORRELATION ANALYSIS; DISSOCIATION; DNA DAMAGE; ELECTRON; LASER; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MONITORING; OXIDATION; PHOTOLYSIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SCALE UP; STEREOCHEMISTRY; STEREOISOMERISM;

ANIMALS; ANIONS; BASE SEQUENCE; CARBONATES; CATTLE; CIRCULAR DICHROISM; DNA; DNA DAMAGE; FREE RADICALS; GUANINE; GUANOSINE; KINETICS; NUCLEIC ACID CONFORMATION; OLIGODEOXYRIBONUCLEOTIDES; OXIDATION-REDUCTION; PHOSPHORIC DIESTER HYDROLASES; PHOTOLYSIS; SNAKE VENOMS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPIRO COMPOUNDS;

EID: 0347629021     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx034142t     Document Type: Article

References (56)

1. Burrows, C. J., and Muller, J. G. (1998) Oxidative nucleobase modifications leading to strand scission. Chem. Rev. 98, 1109-1151.
2. Cadet, J., Bourdat, A. G., D'Ham, C., Duarte, V., Gasparutto, D., Romieu, A., and Ravanat, J. L. (2000) Oxidative base damage to DNA: specificity of base excision repair enzymes. Mutat. Res. 462, 121-128.
3. Beckman, K. B., and Ames, B. N. (1997) Oxidative decay of DNA. J. Biol. Chem. 272, 19633-19636.
4. Grisham, M. B., Jourd'heuil, D., and Wink, D. A. (2000) Review article: chronic inflammation and reactive oxygen and nitrogen metabolism - implications in DNA damage and mutagenesis. Aliment. Pharmacol. Ther. 14 (Suppl. 1), 3-9.
5. Steenken, S., and Jovanovic, S. V. (1997) How easily oxidizable is DNA? One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution. J. Am. Chem. Soc. 119, 617-618.
6. Cadet, J., Bellon, S., Berger, M., Bourdat, A. G., Douki, T., Duarte, V., Frelon, S., Gasparutto, D., Muller, E., Ravanat, J. L., and Sauvaigo, S. (2002) Recent aspects of oxidative DNA damage: guanine lesions, measurement and substrate specificity of DNA repair glycosylases. Biol. Chem. 383, 933-943.
7. Augusto, O., Bonini, M. G., Amanso, A. M., Linares, E., Santos, C. C., and De Menezes, S. L. (2002) Nitrogen dioxide and carbonate radical anion: two emerging radicals in biology. Free Radical Biol. Med. 32, 841-859.
8. Goss, S. P., Singh, R. J., and Kalyanaraman, B. (1999) Bicarbonate enhances the peroxidase activity of Cu, Zn-superoxide dismutase. Role of carbonate anion radical. J. Biol. Chem. 274, 28233-28239.
9. Zhang, H., Joseph, J., Felix, C., and Kalyanaraman, B. (2000) Bicarbonate enhances the hydroxylation, nitration, and peroxidation reactions catalyzed by copper, zinc superoxide dismutase. Intermediacy of carbonate anion radical. J. Biol. Chem. 275, 14038-14045.
10. Zhang, H., Joseph, J., Gurney, M., Becker, D., and Kalyanaraman, B. (2002) Bicarbonate enhances peroxidase activity of Cu, Zn-superoxide dismutase. Role of carbonate anion radical and scavenging of carbonate anion radical by metalloporphyrin antioxidant enzyme mimetics. J. Biol. Chem. 277, 1013-1020.
11. Lymar, S. V., and Hurst, J. K. (1995) Rapid reaction between peroxonitrite ion and carbon dioxide: Implications for biological activity. J. Am. Chem. Soc. 117, 8867-8868.
12. 2-Catalyzed One-Electron Oxidations by Peroxynitrite: Properties of the Reactive Intermediate. J. Am. Chem. Soc. 37, 294-301.
13. Bonini, M. G., Radi, R., Ferrer-Sueta, G., Ferreira, A. M., and Augusto, O. (1999) Direct EPR detection of the carbonate radical anion produced from peroxynitrite and carbon dioxide (published erratum appears in J. Biol. Chem. 1999, 274 (27), 19508). J. Biol. Chem. 274, 10802-10806.
14. Bonini, M. G., Radi, R., Ferrer-Sueta, G., Ferreira, A. M., and Augusto, O. (1999) Direct EPR detection of the carbonate radical anion produced from peroxynitrite and carbon dioxide (published erratum appears in J. Biol. Chem. 1999, 274 (27), 19508). J. Biol. Chem. 274, 10802-10806.
15. 2: energetics, reactive species, and biological implications. Chem. Res. Toxicol. 15, 885-895.
16. Huie, R. E., Clifton, C. L., and Neta, P. (1991) Electron-transfer reaction rates and equilibria of the carbonate and sulfate radical anions. Radiat. Phys. Chem. 38, 477-481.
17. Neta, P., Huie, R. E., and Ross, A. B. (1988) Rate constants for reactions of inorganic radicals in aqueous solution. J. Phys. Chem. Ref. Data 17, 1027-1284.
18. Burney, S., Caulfield, J. L., Niles, J. C., Wishnok, J. S., and Tannenbaum, S. R. (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat. Res. 424, 37-49.
19. Tien, M., Berlett, B. S., Levine, R. L., Chock, P. B., and Stadtman, E. R. (1999) Peroxynitrite-mediated modification of proteins at physiological carbon dioxide concentration: pH dependence of carbonyl formation, tyrosine nitration, and methionine oxidation. Proc. Natl. Acad. Sci. U.S.A. 96, 7809-7814.
20. Davis, K. L., Martin, E., Turko, I. V., and Murad, F. (2001) Novel effects of nitric oxide. Annu. Rev. Pharmacol. Toxicol. 41, 203-236.
21. Ischiropoulos, H., and Beckman, J. S. (2003) Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J. Clin. Invest. 111, 163-169.
22. Shafirovich, V., Dourandin, A., Huang, W., and Geacintov, N. E. (2001) Carbonate radical is a site-selective oxidizing agent of guanines in double-stranded oligonucleotides. J. Biol. Chem. 276, 24621-24626.
23. Shafirovich, V., Dourandin, A., Huang, W., Luneva, N. P., and Geacintov, N. E. (1999) Oxidation of guanine at a distance in oligonucleotides induced by two-photon photoionization of 2-aminopurine. J. Phys. Chem. B 103, 10924-10933.
24. Ravanat, J. L., and Cadet, J. (1995) Reaction of singlet oxygen with 2′-deoxyguanosine and DNA. Isolation and characterization of the main oxidation products. Chem. Res. Toxicol. 8, 379-388.
25. Berger, M., Anselmino, C., Mouret, J.-F., and Cadet, J. (1990) High performance liquid chromatography-electrochemical assay for monitoring the formation of 8-oxo-7,8-dihydroadenine and its related 2′ -deoxyribonucleoside. J. Liq. Chromatogr. 13, 929-940.
26. Zhang, L. K., Ren, Y., Rempel, D., Taylor, J. S., and Gross, M. L. (2001) Determination of photomodified oligodeoxynucleotides by exonuclease digestion, matrix-assisted laser desorption/ionization and post-source decay mass spectrometry. J. Am. Soc. Mass Spectrom. 12, 1127-1135.
27. Ivanov, K. L., Glebov, E. M., Plyusnin, V. F., Ivanov, Y. V., Grivin, V. P., and Bazhin, N. M. (2000) Laser flash photolysis of sodium persulfate in aqueous solution with additions of dimethylformamide. J. Photochem. Photobiol., A 133, 99-104.
28. McElroy, W. J. (1990) A laser photolysis study of the reaction of sulfate(1-) with chloride and the subsequent decay of chlorine-(1-) in aqueous solution. J. Phys. Chem. 94, 2435-2441.
29. Lymar, S. V., Schwarz, H. A., and Czapski, G. (2000) Medium effects on reactions of the carbonate radical with thiocyanate, iodide, and ferrocyanide ions. Radiat. Phys. Chem. 59, 387-392.
30. Steenken, S., Jovanovic, S. V., Bietti, M., and Bernhard, K. (2000) The trap depth (in DNA) of 8-oxo-7,8-dihydro-2′deoxyguanosine as derived from electron-transfer equilibria in aqueous solution. J. Am. Chem. Soc. 122, 2373-2374.
31. Shafirovich, V., Cadet, J., Gasparutto, D., Dourandin, A., Huang, W., and Geacintov, N. E. (2001) Direct spectroscopic observation of 8-oxo-7,8-dihydro-2′-deoxyguanosine radicals in double-stranded DNA generated by one-electron oxidation at a distance by 2-aminopurine radicals. J. Phys. Chem. B 105, 586-592.
32. .- with deoxynucleosides. Possible implications for direct energy deposition. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 52, 577-587.
33. Wolf, P., Jones, G. D., Candeias, L. P., and O'Neill, P. (1993) Induction of strand breaks in polyribonucleotides and DNA by the sulphate radical anion: role of electron loss centres as precursors of strand breakage. Int. J. Radiat. Biol. 64, 7-18.
34. Candeias, L. P., and Steenken, S. (1993) Electron transfer in di-(deoxy)nucleoside phosphates in aqueous solution: rapid migration of oxidative damage (via adenine) to guanine. J. Am. Chem. Soc. 115, 2437-2440.
35. Luo, W., Muller, J. G., Rachlin, E. M., and Burrows, C. J. (2000) Characterization of spiroiminodihydantoin as a product of one-electron oxidation of 8-oxo-7,8-dihydroguanosine. Org. Lett. 2, 613-616.
36. Leipold, M. D., Muller, J. G., Burrows, C. J., and David, S. S. (2000) Removal of hydantoin products of 8-oxoguanine oxidation by the escherichia coli DNA repair enzyme, FPG. Biochemistry 39, 14984-14992.
37. Luo, W., Muller, J. G., Rachlin, E. M., and Burrows, C. J. (2001) Characterization of hydantoin products from one-electron oxidation of 8- oxo-7,8-dihydroguanosine in a nucleoside model. Chem. Res. Toxicol. 14, 927-938.
38. Luo, W., Muller, J. G., and Burrows, C. J. (2001) The pH-Dependent Role of Superoxide in Riboflavin-Catalyzed Photooxidation of 8-Oxo-7,8-dihydroguanosine. Org. Lett. 3, 2801-2804.
39. Kornyushyna, O., Berges, A. M., Muller, J. G., and Burrows, C. J. (2002) In Vitro Nucleotide Misinsertion Opposite the Oxidized Guanosine Lesions Spiroiminodihydantoin and Guanidinohydantoin and DNA Synthesis Past the Lesions Using Escherichia coli DNA Polymerase I (Klenow Fragment). Biochemistry 41, 15304-15314.
40. Sugden, K. D., Campo, C. K., and Martin, B. D. (2001) Direct oxidation of guanine and 7,8-dihydro-8-oxoguanine in DNA by a high-valent chromium complex: a possible mechanism for chromate genotoxicity. Chem. Res. Toxicol. 14, 1315-1322.
41. Niles, J. C., Wishnok, J. S., and Tannenbaum, S. R. (2001) Spiroiminodihydantoin Is the Major Product of the 8-Oxo-7,8-dihydroguanosine Reaction with Peroxynitrite in the Presence of Thiols and Guanosine Photooxidation by Methylene Blue. Org. Lett. 3, 963-966.
42. - system. Chem. Res. Toxicol. 14, 1163-1169.
43. Suzuki, T., and Ohshima, H. (2002) Nicotine-modulated formation of spiroiminodihydantoin nucleoside via 8-oxo-7,8-dihydro-2′-deoxyguanosine in 2′-deoxyguanosine-hypochlorous acid reaction. FEBS Lett. 516, 67-70.
44. - System. Chem. Res. Toxicol. 16, 382-389.
45. Adam, W., Arnold, M. A., Grune, M., Nau, W. M., Pischel, U., and Saha-Moeller, C. R. (2002) Spiroiminodihydantoin is a major product in the photooxidation of 2′-deoxyguanosine by the triplet states and oxyl radicals generated from hydroxyacetophenone photolysis and dioxetane thermolysis. Org. Lett. 4, 537-540.
46. Adam, W., Arnold, M. A., Nau, W. M., Pischel, U., and Saha-Moeller, C. R. (2002) A Comparative Photomechanistic Study (Spin Trapping, EPR Spectroscopy, Transient Kinetics, Photo-products) of Nucleoside Oxidation (dG and 8-oxodG) by Triplet-Excited Acetophenones and by the Radicals Generated from a-Oxy-Substituted Derivatives through Norrish-Type I Cleavage. J. Am. Chem. Soc. 124, 3893-3904.
47. 18O]-labeled singlet oxygen as a tool for mechanistic studies of 8-oxo-7,8-dihydroguanine oxidative damage: detection of spiroiminodihydantoin, imidazolone and oxazolone derivatives. Biol. Chem. 383, 607-617.
48. Adam, W., Saha-Moeller, C. R., and Schoenberger, A. (1996) Photooxidation of 8-Oxo-7,8-dihydro-2′-deoxyguanosine by Thermally Generated Triplet-Excited Ketones from 3-(Hydroxymethyl)-3,4,4-trimethyl-1,2-dioxetane and Comparison with Type I and Type II Photosensitizers. J. Am. Chem. Soc. 118, 9233-9238.
49. Ravanat, J. L., Remaud, G., and Cadet, J. (2000) Measurement of the main photooxidation products of 2′-deoxyguanosine using chromatographic methods coupled to mass spectrometry. Arch. Biochem. Biophys. 374, 118-127.
50. Cadet, J., Berger, M., Buchko, G. W., Joshi, P. C., Raoul, S., and Ravanat, J.-L. (1994) 2,2-Diamino-4-[(3,5-di-O-acetyl-2-deoxy-β -D-erythro-pentofuranosyl)aminol-5-(2H)-oxazolone: a Novel and Predominant Radical Oxidation Product of 3′,5′-Di-O-acetyl-2′ -deoxyguanosine. J. Am. Chem. Soc. 116, 7403-7404.
51. 5: 5,8-Dihydroxy-7,8-dihydroguanine Residue as a Key Precursor of Imidazolone and Parabanic Acid Derivatives. J. Am. Chem. Soc. 122, 2157-2167.
52. Gasparutto, D., Bourdat, A. G., D'Ham, C., Duarte, V., Romieu, A., and Cadet, J. (2000) Repair and replication of oxidized DNA bases using modified oligodeoxyribonucleotides. Biochimie 82, 19-24.
53. Margerum, D. W., Chellappa, K. L., Bossu, F. P., and Burce, G. L. (1975) Characterization of a readily accessible copper(III)-peptide complex. J. Am. Chem. Soc. 97, 6894-6896.
54. Hazra, T. K., Muller, J. G., Manuel, R. C., Burrows, C. J., Lloyd, R. S., and Mitra, S. (2001) Repair of hydantoins, one electron oxidation product of 8-oxoguanine, by DNA glycosylases of Escherichia coli. Nucleic Acids Res. 29, 1967-1974.
55. Leipold, M. D., Workman, H., Muller, J. G., Burrows, C. J., and David, S. S. (2003) Recognition and Removal of Oxidized Guanines in Duplex DNA by the Base Excision Repair Enzymes hOGG1, yOGG1, and yOGG2. Biochemistry 42, 11373-11381.
56. Henderson, P. T., Delaney, J. C., Gu, F., Tannenbaum, S. R., and Essigmann, J. M. (2002) Oxidation of 7,8-Dihydro-8-oxoguanine Affords Lesions That Are Potent Sources of Replication Errors in Vivo. Biochemistry 41, 914-921.