Chemical Reactions of the Radical Cations of Nucleobases in Isolated and Cellular DNA. Formation of Single-Base Lesions

Radical and Radical Ion Reactivity in Nucleic Acid Chemistry

Volumn , Issue , 2009, Pages 69-97

  Cadet, Jean ^a,b   Douki, Thierry ^a   Gasparutto, Didier ^a   Ravanat, Jean Luc ^a   Wagner, J Richard ^b  

^a CEA GRENOBLE   (France)

^b UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Chemical reactions of radical cations of nucleobases; One electron oxidation pathways and five main DNA bases; One electron oxidation reactions of normal pyrimidine

Indexed keywords

EID: 77953026794     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470526279.ch3     Document Type: Chapter

References (151)

1. Cadet, J.; Berger, M.; Douki, T.; Ravanat, J.-L. Oxidative damage toDNA: Formation, measurement and biological significance. Rev. Physiol. Biochem. Pharmacol. 1997, 131, 1-87.
2. Cadet, J.; Douki, T.; Gasparutto, D.; Ravanat, J.-L. Oxidative damage to DNA:Formation, measurement and biochemical features. Mutat. Res. 2003, 531, 5-23.
3. Gimisis, T.; Cismas, C. Isolation, characterization, and independent synthesis of guanine oxidation products. Eur. J. Org. Chem. 2006, 1351-1378.
4. Pratviel, G.; Meunier, B. Guanine oxidation: one-and two-electron reactions. Chem. Eur. J. 2006, 12, 6018-6030.
5. von Sonntag C. in Free-Radical Induced DNA Damage and Its Repair. A Chemical Perspective, Springer, Heidelberg, 2006.
6. Cadet, J.; Douki, T.; Ravanat, J.-L. Oxidatively generated damage to the guanine moiety of DNA: Mechanistic aspects and formation in cells. Acc. Chem. Res. 2008, 41, 1075-1083.
7. Chatgilialoglu, C., Ferreri, C.; Bazzanini, R.; Guerra, M.; Choi, S.-Y.; Emanuel, C. J.; Horner, J. H. Newcomb, M. Models of DNA C10 radicals. Structural, spectral, and chemical properties of the thyminylmethyl radical and the 20-deoxyuridin-10-yl radical. J. Am. Chem. Soc. 2002, 122, 9525-9533.
8. Dedon, P.C. The chemical toxicology of 2-deoxyribose oxidation in DNA. Chem. Res. Toxicol. 2008, 21, 206-219.
9. Cadet, J., Ravanat, J.-L, Martinez, G.R., Medeiros, M.H.G., Di Mascio, P. Singlet oxygen oxidation of isolated and cellular DNA: Product formation and mechanistic insights. Photochem. Photobiol. 2006, 82, 1219-1225.
10. Girault, I.; Fort, S.; Molko, D.; Cadet, J. Ozonolysis of 20-deoxycytidine: isolation and identification of the main oxidation products. Free Radic. Res. 1997, 26, 257-266.
11. Dedon, P. C.; Tannenbaum, S. R. Reactive nitrogen species in the chemical biology of inflammation. Arch. Biochem. Biophys. 2004, 423, 12-22.
12. Niles, J. C.;Wishnok, . S.; Tannenbaum, S. R. Peroxynitrite-induced oxidation and nitration products of guanine and 8-oxoguanine: structures and mechanisms of product formation. Nitric Oxide 2006, 14, 109-121.
13. Neeley, W. L.; Essigmann, J. M. Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem. Res. Toxicol., 2006, 19, 491-505.
14. Masuda, M.; Suzuki, T.; Friesen, M. D.; Ravanat, J.-L.; Cadet, J.; Pignatelli, B.; Nishino, H.; Ohshima, H. Chlorination of guanosine and other nucleosides by hypochlorous acid and myeloperoxidase of activated human neutrophils. Catalysis by nicotine and trimethylamine. J. Biol. Chem. 2001, 276, 40486-40496.
15. Badouard, C.; Masuda, M.; Nishino, H.; Cadet, J.; Favier, A.; Ravanat, J.-L. Detection of chlorinated DNA and RNAnucleosides byHPLCcoupled to tandem mass spectrometry as potential biomarkers of inflammation. J. Chromatogr. B 2005, 827, 26-31.
16. Steenken, S.; Jovanovic, S. V. How easily oxidizable is DNA? One-electron reduction potentials of adenosine and guanosine radicals in aqueous solutions. J. Am. Chem. Soc. 1997, 119, 617-618.
17. Becker, D.; Sevilla, M. Adv. Radiat. Biol. 1993, 17, 121-180.
18. Symons, M. C. R. Electron-spin-resonance studies of radiation-damage to DNA and proteins. Radiat. Phys. Chem. 1995, 45, 837-845.
19. Debije, M.G.; Bernhard, W. Free radical yields in crystalline DNA X-irradiated at 4K. Radiat. Res. 1999, 152, 583-589.
20. Adhikary, A.; Kumar, A.; Becker, Sevilla, M. D. The guanine cation radical: investigation of deprotonation states by ESR and DFT. J. Phys. Chem B 2006, 110, 24171-24180.
21. Angelov, D.; Spassky, A.; Berger, M. Cadet,J. High-intensity UV laser photolysis of DNA and purine 20-deoxyribonucleosides: Formation of 8-oxopurine damage and oligonucleotide strand cleavage as revealed by HPLC and gel electrophoresis studies. J. Am. Chem. Soc. 1997, 119, 11373-11360.
22. Douki, T.; Angelov, D.; Cadet, J. UV laser photolysis of DNA: Effect of duplex stability on charge transfer efficiency. J. Am. Chem. Soc. 2001, 123, 11360-11366.
23. Cadet, J.; Vigny, P. The photochemistry of nucleic acids. In Bioorganic Photochemistry, Photochemistry and the Nucleic Acid, Vol. 1; Morrison, H., Ed.; John Wiley & Sons, New York, 1990, pp. 1-272.
24. Fisher, G. J.; Land, . J. Photosensitization of pyrimidines by 2-methylnaphthoquinone in water: A laser flash photolysis study. Photochem. Photobiol. 1983, 37, 27-32.
25. Wagner, J. R.; van Lier, J. E.; Johnston, L. J. Quinone sensitized electron transfer photooxidation of nucleic acids: Chemistry of thymine and thymidine radical cations in aqueous solution. Photochem. Photobiol. 1990, 52, 333-343.
26. Schuster, G. B. Long-range charge transfer in DNA: Transient structural distortions control the distance dependence. Acc. Chem. Res. 2000, 33, 2253-2260.
27. Delatour T.; Douki, T.; D'Ham C.; Cadet, J. Photosensitization of thymine nucleobase by benzophenone through energy transfer, hydrogen abstraction and one-electron oxidation. J. Photochem. Photobiol. B: Biol. 1998, 44, 191-198.
28. Cadet, J.; Douki, T.; Ravanat, J.-L. The human genome as a target of oxidative modification:Damage to nucleic acids. In Redox-Genome Interactions in Health and Disease; Fuchs, J.; Podda, M.; Packer, L., Eds.; Marcel Dekker, New York, 2004, pp. 145-192.
29. Joffe, A.; Geacintov, N.E.; Shafirovich, V. DNA lesions derived from the site selective oxidationofguaninebycarbonateradicalanions. Chem.Res.Toxicol. 2003,16,1528-1538.
30. Medinas, D. B.; Cerchiaro, G.; Trindale, D. F.; Augusto, O. The carbonate radical and related oxidants derived from bicarbonate buffer. IUBMB Life 2007, 59, 255-262.
31. Giese, B.; Amaudrut, J.; Kühler, A.-K.; Spormann, M.;Wessely, S. Direct observation of hole transfer through DNA by hopping between adenine bases and by tunnelling. Nature 2001, 412, 318-320.
32. Boon, E. M.; Barton, J. K. Charge transfer in DNA. Curr. Opin. Struct. Biol. 2002, 12, 320-329.
33. Roginskaya, M.; Bernhard, W.A.; Razskazovskiy, Y. Diffusion approach to long distance charge migration in DNA:Time dependent and steady-state analytical solutions for the product yield. J. Phys. Chem. B 2004, 108, 2432-2437.
34. Osakada, Y.; Kawai, K.; Fujitsuka, M.; Majima, T. Charge transfer through DNA nanoscaled assembly programmable with DNA building blocks. Proc. Natl. Acad. Sci. USA 2006, 103, 18072-18076.
35. Debje, M. G.; Close, D. M.; Bernhard,W. A. Reductive damage in directly ionized DNA:saturation of the C5--C6 bond of cytosine in d(CGCG)2 crystals. Radiat. Res. 2002, 157, 235-242.
36. Swarts, S. G.; Becker, D.; Sevilla, M.; Wheeler,K. T. Radiat. Res. 1996, 145, 304-314.
37. Shaw,A. A.; Cadet, J. Radical combination processes under the direct effect of gamma radiation on thymidine. J. Chem. Soc. Perkin Trans. 2 1990, 2063-2070.
38. Gromova, M.; Balanzat, E.; Gervais, B.; Nardin, R.; Cadet, J. The direct effect of heavy ions and electrons on thymidine in the solid state. Int. J. Radiat. Biol. 1998, 74, 81-97.
39. Gromova, M.; Nardin, R.; Cadet, J. Direct effects of heavy ions and electrons on 20-deoxyguanosine in the solid state. J. Chem. Soc. Perkin Trans. 2 1998, 1365-1374.
40. Swarts, S. G.; Gilbert, D. C.; Sharma, K. K.; Razskazovskiy, Y.; Purkayastha, S.; Naumenko, K. A.; Bernhard, W. A. Mechanisms of direct radiation damage in DNA, based on a study of the yields of base damage, deoxyribose damage, and trapped radicals in d(GCACGCGTGC)2, Radiat. Res. 2007, 168, 367-381.
41. Greenberg, M. M. Pyrimidine nucleobase radical reactivity. Chapter 5, present volume.
42. Krishna, C. M.; Decarroz, C., Wagner, J. R.; Cadet, J.; Riesz, P. Menadione sensitized photooxidation of nucleic acid and protein constituents. An ESR and spin-trapping study. Photochem. Photobiol. 1987, 46, 175-182.
43. Decarroz, C.; Wagner, J. R.; van Lier, J. E.; Krishna, C. M.; Riesz, P.; Cadet, J. Sensitized photo-oxidation of thymidine by 2-methyl-1,4-naphthoquinone. Characterization of the stable photoproducts. Int. J. Radiat. Biol. 1986, 50, 491-505;
44. Wagner, J. R.; van Lier, J. E.; Decarroz, C.; Berger, M.; Cadet, J. Photodynamic methods for oxy radical-induced DNA damage. Methods Enzymol. 1990, 186, 502-511.
45. Isildar, M.; Schuchmann, M. N.; Schulte-Frohlinde, D.; von Sonntag, C. V. Oxygen uptake in the radiolysis of aqueous solutions of nucleic acids and their constituents. Int. J. Radiat. Biol. 1982, 41, 525-533.
46. Wagner, J. R.; van Lier, J. E.; Berger, M.; Cadet, J. Thymidine hydroperoxides, structural assignment, conformational features and thermal decomposition in water. J. Am. Chem. Soc. 1994, 116, 2235-2242.
47. Cadet, J.; Ducolomb, R.; Téeoule, R. Préeparation, isoméerisation et configuration absolue des hydrates de thymidine. Tetrahedron 1977, 33, 1603-1607.
48. Cadet, J.; Ducolomb, R.; Hruska, F. . Proton magnetic resonance studies of 5,6-saturated thymidine derivatives produced by ionizing radiation. Conformational studies of 6-hydroxylated diastereoisomers. Biochim. Biophys. Acta 1979, 563, 206-215.
49. Jolibois, F.; D'Ham, C.; Grand, A.; Subra, R.; Cadet, J. Cis-5-Hydroperoxy-6-hydroxy-5,6-dihydrothymine crystal structure and theoretical investigations of the electronic properties by DFT. J. Mol. Struct. (Theochem) 1998, 427, 143-155.
50. Russell, G. A. Deuterium-isotope effects in the autoxidation of aralkyl hydrocarbons. Mechanisms of the interaction of peroxy radicals. J. Am. Chem. Soc. 1957, 79, 3871-3877.
51. Wagner, J. R; Cadet, J.; Fisher, . J. Photo-oxidation of thymine sensitized by 2-methyl-1,4-naphthoquinone: Analysis of products including three novel photodimers. Photochem. Photobiol. 1984, 40, 589-597.
52. Miyamoto, S.; Marques, S. A.; Retton, D.; Augusto, O.; Medeiros, M. H; Di Mascio, P. Linoleic acid hydroperoxide reacts with hypochlorous acid to generate peroxyl radical intermediate and singlet oxygen. Proc. Natl. Acad. Sci. USA 2006, 103, 293-298.
53. Douki, T.; Cadet, J. Modification of DNA bases by photosensitized one-electron oxidation. Int. J. Radiat. Biol. 1999, 75, 571-581.
54. Gosh, A.; Joy, A.; Schuster, G. B.; Douki, T.; Cadet, J. Selective one-electron oxidation of duplexDNA oligomers: Reaction at thymines. Org. Biomol. Chem. 2008, 6, 916-928.
55. Frelon, S.; Douki, T.; Ravanat, J.-L.; Pouget, J.-P.; Tornabene, C.; Cadet, J. High performance liquid chromatography-Tandem mass spectrometry measurement of radiation-induced base damage to isolated and cellular DNA. Chem. Res. Toxicol. 2000, 13, 1002-1010.
56. Saito, I.; Takayama, M.; Kawanishi, S. Photoactivable DNA-cleaving amino acids: High sequence-selective DNA photocleavage by novel L-lysine derivatives. J. Am. Chem. Soc. 1995, 117, 5590-5591.
57. Wagner, J. R.; Decarroz, C.; Berger, M.; Cadet, J. Hydroxyl radical-induced decomposition of 20-deoxycytidine in aerated aqueous solutions. J. Am. Chem. Soc. 1999, 121, 4101-4110.
58. Decarroz, C.;Wagner, J. R.; Cadet, J. Specific deprotonation reactions of the pyrimidine radical cation resulting from menadione mediated photosensitization of 20-deoxycytidine. Free Rad. Res. Commun. 1987, 2, 295-301.
59. Labet, V., Grant, A., Cadet, J., Eriksson, L. . Deamination of the radical cation of the base moiety of 20-deoxycytidine: A theoretical study. ChemPhysChem 2008, 9, 1195-1203.
60. Urata, H. ;Yamamoto, K.; Akagi, M.; Hiroaki, H.; Uesugi, S.A 2-deoxyribonolactonecontaining nucleotide: Isolation and characterization of the alkali-sensitive photoproduct of the trideoxyribonucleotide d(ApCpA). Biochemistry 1989, 28, 9566-9569.
61. Roupioz, Y.; Lhomme, J.; Kotera, M. Chemistry of the 2-deoxyribonolactone lesion in oligonucleotides: cleavage kinetics and products analysis. J. Am. Chem. Soc. 2002, 124, 9129-9135.
62. Xue, L.; Greenberg, M. . Use of fluorescence sensors to determine that 2-deoxyribonolactone is the major alkali-labile deoxyribose lesion produced in oxidatively damaged DNA. Angew. Chem. Int. Ed. Engl. 2007, 46, 561-564.
63. Schweibert, M.C; Daniels, M. 60Co gamma-ray-induced peroxidation ofDNAin aqueous solution. Int. J. Radiat. Phys. Chem. 1971, 3, 353-366.
64. Tremblay, S.;Wagner, J. Dehydration, deamination, and enzymatic repair of cytosine glycols from oxidized poly(dC-dG) and poly(dC-dI). Nucleic Acids Res. 2008, 36, 284-293.
65. Tremblay, S.; Douki, T.; Cadet, J.;Wagner, J. R. 20-Deoxycytidine glycols, a missing link in the free radical-mediated oxidation of DNA. J. Biol. Chem. 1999, 274, 20833-20838.
66. Tremblay, S.; Gantchev, T.; Tremblay, L.; Lavigne, P.; Cadet, J.;Wagner, J. . Oxidation of 20-deoxycytidine to four interconverting diastereomers of N-1-carbamoyl-4,5-dihydroxy-2-oxoimidazolidine nucleosides. J. Org. Chem. 2007, 72, 3672-3678.
67. Polverelli, M. Modification radio-induites de la cytosine en solution aqueuse aéeréee et après irradiation gamma d'Escherichia coli, Thesis Universitée Joseph Fourier, Grenoble, 1983.
68. Leonard, N. J., Wiemer, D. F. Synthesis of cytosine radiolysis products: cis-and trans-1-carbamoyl-4,5-dihydroxyimidazolidin-2-one. J. Am. Chem. Soc. 1976, 98, 8218-8221.
69. Paul, C. R.; Arakali, A. V.; Wallace, J. C.; McReynolds, J.; Box, H. C. Radiation chemistry of 20-deoxycytidylyl-'30-50)-20-deoxyguanosine and its sequence isomer in N2O and O2-saturated solutions. Radiat. Res. 1987, 112, 464-477.
70. Wagner, J. R.; Blount, B. C.; Weinfeld, M. Excision of oxidative cytosine modifications from gamma irradiated DNA by Escherichia coli endonuclease III and human whole cell extracts. Anal. Biochem. 1996, 233, 73-86.
71. Paul, C. R.;Wallace, J. C.; Alderfer, J. L.; Box, H. C. Radiation chemistry of d(TpApCpG) in oxygenated solutions. Int. J. Radiat. Biol. 1988, 54, 403-415.
72. Bienvenu, C.; Wagner, J. R.; Cadet J. Photosensitized oxidation of 5-methyl-20-deoxycytidine by 2-methyl-1,4-naphthoquinone-Characterization of 5-(hydroperoxymethyl)-20-deoxycytidine and stable methyl group oxidation products. J. Am. Chem. Soc. 1996, 118, 11406-11411.
73. Bienvenu, C.; Cadet, J. Synthesis and kinetic study of the deamination of the cis diastereomers of 5,6-dihydroxy-5,6-dihydro-5-methyl-20-deoxycytidine. J. Org. Chem. 1996, 61, 2632-2637.
74. Bareyt, S.; Carell, T. Selective detection of 5-methylcytosine sites in DNA. Angew. Chem. Int. Engl. Ed. 2008, 47, 181-184.
75. Tanabe, K.; Yamada, H.; Nishimoto, S. Oneelectron photooxidation and site-selective strand cleavage at 5-methylcytosine inDNAby sensitization with 2-methyl-1,4-naphthoquinone-tethered oligonucleotides. J. Am. Chem. Soc. 2007, 129, 8034-8040.
76. Cadet, J.; Berger, M.; Buchko, G.W.; Joshi, P.; Raoul, S.; Ravanat, J.-L. 2,2-Diamino-4-(3,5-di-O-acetyl-2-deoxy-b-D-erythro-pentofuranosyl)amino]-5-(2H)-oxazolone: A novel and predominant radical oxidation product of 30,50-di-O-acetyl-20-deoxyguanosine. J. Am. Chem. Soc. 1994, 116, 7403-7404.
77. Raoul, S.; Berger, M.; Buchko, G.W.; Joshi, P. C.; Morin, B., Weinfeld, M., Cadet, J. 1H, 13C and 15N NMR analysis and chemical features of the two main radical oxidation products of 20-deoxyguanosine: Oxazolone and imidazolone nucleosides. J. Chem. Soc. Perkin Trans. 2 1996, 371-381.
78. Candeias, L. P.; Steenken, S. Reaction of HO. with guanine derivatives in aqueous solution: formation of two different redox-active OH-adduct radical and their unimolecular transformation reactions. Properties of G(-H). Chem. Eur. J. 2000, 6, 475-484.
79. Kobayashi, K.; Tagawa, S. Direct observation of guanine radical cation deprotonation in duplex DNA using pulse radiolysis. J. Am. Chem. Soc. 2003, 125, 10213-10218.
80. Steenken, S. Purine bases, nucleosides, and nucleotides: aqueous solution redox chemistry and transformation reactions of their radical cations and e-and OH adducts. Chem. Rev. 1989, 89, 503-520.
81. Al-Sheikhly,M. The reactivity of adenyl and guanyl radicals towards oxygen. Rad. Phys. Chem. 1994, 44, 297-301.
82. Chatgiglialoglu, C.; Caminal, C.; Altieri, A.; Vougiokalakis, G. C.; Mulazzani, Q. G.; Gimisis, T.; Guerra, M. Tautomerism in the guanyl radical. J. Am. Chem. Soc. 2006, 128, 13796-13805.
83. Misiaszek, R.; Crean, C.; Joffe, A.; Geacintov N. E.; Shafirovich, V. Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping. J. Biol. Chem. 2004, 279, 32106-32115.
84. Vialas, C.; Pratviel, G.; Claparols, C.; Meunier, B. Efficient oxidation of 20-deoxyguanosine by Mn-TMPyP/KHSO5 to imidazolone dIz without formation of 8-Oxo-dG. J. Am. Chem. Soc. 1998, 120, 11548-11553.
85. Ravanat, J.-L., Saint-Pierre, C.; Cadet, J. One-electron oxidation of the guanine moiety of 20-deoxyguanosine: Influence of 8-oxo-7,8-dihydroguanine. J. Am. Chem. Soc. 2003, 125, 2030-2031.
86. Gasparutto, D.; Ravanat, J.-L.; Géerot, O.; Cadet, J. Characterization and chemical stability of photooxidized oligonucleotides that contain 2,2-diamino-4-[(deoxy-b-Derythro-pentofuranosyl)-amino]-5(2H)-oxazolone. J. Am. Chem. Soc. 1998, 120, 10283-10286.
87. Kino, K.; Saito, I.; Sugyiama, H. Product analysis of GG-specific photooxidation of DNA via electron transfer: 2-aminoimidazolone as a major guanine oxidation product. J. Am. Chem. Soc. 1998, 120, 7373-7374.
88. Cullis, P. M., Malone, M. E., Merson-Davies, L. A. Guanine radical cations are precursors of 7,8-dihydro-8-oxo-20-deoxyguanosine but are not precursors of immediate strand breaks in DNA. J. Am. Chem. Soc. 1996, 118, 2775-2781.
89. Buchko, G. W.; Cadet, J.; Ravanat, J.-L.; Labataille, P. Isolation and characterization of a new product produced by ionizing radiation and type I photosensitization of 20-deoxyguanosine in oxygen-saturated aqueous solution: (2S)-2,50-anhydro-1-(20-deoxy-b-D-erythro-pentofuranosyl)-5-guanidinylidene-2-hydroxy-4-oxoimidazolidine. Int. J. Radiat. Biol. 1993, 63, 669-676.
90. Morin, B.; Cadet, J. Type I benzophenone mediated nucleophilic reaction of 50-amino-20,50-dideoxyguanosine. Chem. Res. Toxicol. 1995, 8, 792-799.
91. Morin, B.; Cadet, J. Chemical aspects of the benzophenone photosensitized formation of two lysine-20-deoxyguanosine crosslinks. J. Am. Chem. Soc. 1995, 117, 12408-12415.
92. Giese, B.; Spichy, M. Long-distance charge transport through DNA: Quantification and extension of the hopping model. ChemPhysChem. 2000, 1, 195-198.
93. Barnett, R. N.; Bongiorno, A.; Cleveland, C. L.; Joy, A.; Landman, U.; Schuster, G. B. Oxidative damage toDNA: Counterion-assisted addition of water to ionizedDNA. J. Am. Chem. Soc. 2006, 128, 10795-10800.
94. Kasai, H.; Yamaizumi, Z.; Berger, M.; Cadet, J. Photosensitized formation of 7,8-dihydro-8-oxo-20-deoxyguanosine (8-hydroxy-20-deoxyguanosine) in DNA by riboflavin:A non-singlet oxygen mediated reaction. J. Am. Chem. Soc. 1992, 114, 9692-9694.
95. Munk, B. H.; Burrows, C. J.; Schlegel, H. B. Exploration of mechanisms for the transformation of 8-hydroxy guanine radical to FAPyG by density functional theory. Chem. Res. Toxicol. 2007, 20, 432-444.
96. Steenken, S.; Jovanovic, S. B.; Bietti, M.; Bernhard, K. The trap death (inDNA) of 8-oxo-7,8-dihydro-20-deoxyguanosine as derived from electron transfer equilibria in aqueous solution. J. Am. Chem. Soc. 2000, 122, 2373-2374.
97. Douki, T.; Cadet, J. Modification of DNA bases by photosensitized one-electron oxidation. Int. J. Radiat. Biol. 1999, 75, 571-581.
98. Perrier, S.; Hau, J.; Gasparutto, D.; Cadet, J.; Favier, A.; Ravanat, J.-L. Characterization of lysine-guanine cross-links upon one-electron oxidation of a guanine-containing oligonucleotides in the presence of a trilysine peptide. J. Am. Chem. Soc. 2006, 128, 5703-5710.
99. Xu, X.; Muller, J. G.; Ye, Y.; Burrows, C. J. DNA-protein cross-links between guanine and lysine depend on the mechanism of oxidation for formation of C5 Vs C8 guanosine adducts. J. Am. Chem. Soc. 2008, 130, 703-709.
100. Crean, C.; Uvaydov,Y.; Geacintov,N. E.; Shafirovich,V. Oxidation of single-stranded oligonucleotides by carbonate radical anions: Generating intrastrand cross-links between guanine and thymine bases separated by cytosines. Nucleic Acids Res. 2008, 36, 742-755.
101. Crean, C.; Geacintov, N. E.; Shafirovich,V. Intrastrand G-U cross-links generated by the oxidation of guanine in 50-d(GCU) and 50-r(GCU). Free Radic. Biol. Med. 2008, 45, 1125-1134.
102. O'Neill, P.; Parker, A. W.; Plumb, M. A., Siebbeles, L. D. A. Guanine modifications following ionization of DNA occurs predominantly via intra-and not interstrand charge migration: An experimental and theoretical study. J. Phys. Chem. B 2001, 105, 5283-5290.
103. Berger, M.; de Hazen, M.; Nejjari, A.; Fournier, J.; Guignard, J.; Pezerat, H.; Cadet, J. Radical oxidation reactions of the purine moiety of 20-deoxyribonucleosides andDNAby iron-containing minerals. Carcinogenesis 1993, 14, 41-46.
104. Raoul, S.; Bardet, M.; Cadet, J. Gamma irradiation of 20-deoxyadenosine in oxygen-free aqueous solutions:Identification and conformational features of formamidopyrimidine nucleoside derivatives. Chem. Res. Toxicol. 1995, 8, 924-933.
105. Frelon, S.; Douki, T.; Cadet, J. Radical oxidation of the adenine moiety of nucleoside and DNA: 2-hydroxy-20-deoxyadenosine is a minor decomposition product. Free Radic. Res. 2002, 36, 499-508.
106. Wang,Y.; Liu, Z.; Dixon, C. Major adenine products from 2-methyl-1,4-naphthoquinonesensitized photoirradiation at 365 nm. Biochem. Biophys. Res. Commun. 2002, 91, 1252-1257.
107. Wagner, J. R.; Hu, C. C.; Ames, B.N. Endogenous oxidative damage of deoxycytidine in DNA. Proc. Natl. Acad. Sci. U.S.A., 1992, 89, 3380-3384.
108. Rivière, J.; Ravanat, J.L.; Wagner, J.R. Ascorbate and H2O2 induced oxidative DNA damage in Jurkat cells. Free Rad. Biol. Med. 2006, 40, 2071-2079.
109. Fujimoto, J.; Tran, L.; Sowers, L.C. Synthesis and cleavage of oligodeoxynucleotides containing a 5-hydroxyuracil residue at defined site. Chem. Res. Toxicol. 1997, 10, 1254-1258.
110. Wolfe, J. L.; Kawate, T.; Sarracino, D. A.; Zillmann, M.; Olson, J.; Stanton,V. P.;Verdine, G. L. A genotyping strategy based on incorporation and cleavage of chemically modified nucleotides. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 11073-11078.
111. Rivière, J.; Bergeron, F.; Tremblay, S.; Gasparutto, D.; Cadet, J.;Wagner, J.R. Oxidation of 5-hydroxy-20-deoxyuridine into isodialuric acid, dialuric acid, and hydantoin products. J. Am. Chem. Soc. 2004, 126, 6548-6549.
112. Rivière, J.; Klarskov, K.;Wagner, J.R. Oxidation of 5-hydroxypyrimidine nucleosides to 5-hydroxyhydantoin and its alpha-hydroxy-ketone isomer. Chem. Res. Toxicol. 2005, 18, 1332-1338.
113. Simon, P.; Gasparutto, D.; Gambarelli, S.; Saint-Pierre, C.; Favier, A.; Cadet, J. Formation of isodialuric acid lesion within DNA oligomers via one-electron oxidation of 5-hydroxyuracil: Characterization, stability and excision repair. Nucleic Acids Res. 2006, 34, 3660-3669.
114. Joffe, A.; Geacintov, N. E.; Shafirovich, V. DNA lesions derived from the site selective oxidation of guanine by carbonate radical anions. Chem. Res. Toxicol. 2003, 16, 1528-1538.
115. Cadet, J.; Douki, T.; Ravanat, J.-L. Onet-electron oxidation of DNA and inflammation processes. Nat. Chem. Biol. 2006, 2, 348-349.
116. Luo, W.; Muller, J. G.; Burrows, C. The pH-dependent role of superoxide in riboflavin-catalyzed photooxidation of 8-oxo-7,8-dihydroguanosine. Org. Lett. 2001, 3, 2801-2804.
117. Luo,W.; Muller, J. G.; Rachlin, E. M.; Burrows, C. J. Characterization of hydantoin products from one-electron oxidation of 8-oxo-7,8-dihydroguanosine in a nucleoside model. Chem. Res. Toxicol. 2001, 14, 927-938.
118. Munk, B. H.; Burrows, C. J.; Schlegel, H. B. An exploration of mechanisms for the transformation of 8-oxoguanine to guanidinohydantoin and spiroiminodihydantoin by density functional theory. J. Am. Chem. Soc. 2008, 130, 5245-5256.
119. McCallum, J. E.; Kuniyoshi, C.Y.; Foote, C. S. Characterization of 5-hydroxy-8-oxo-7,8-dihydroguanosine in the photosensitized oxidation of 8-oxo-7,8-dihydroguanosine and its rearrangement to spiroiminodihydantoin. J. Am. Chem. Soc. 2004, 126, 16777-16782.
120. Hosford, M. E.; Muller, J. G.; Burrows, C. J. Spermine participates in oxidative damage of guanosine and 8-oxoguanosine leading to deoxyribosylurea formation. J. Am. Chem. Soc. 2004, 126, 9540-9541.
121. Johansen, M. E., Muller, J. G.; Xu, X.; Burrows, C. J. Oxidatively induced DNA-protein cross-linking between single-stranded binding protein and oligodeoxynucleotides containing 8-oxo-7,8-dihydro-20-deoxyguanosine. Biochemistry 2005, 44, 5660-5671.
122. Durandin, A.; Jia, L.; Crean, C.; Kolbanovskiy, A.; Ding, S.; Shafirovich, V.; Broyde, S.; Geacintov, N. E. Assignment of absolute configuration of the enantiomeric spiroiminodihydantoin nucleobase by experimental and computational optical rotatory dispersion methods. Chem. Res. Toxicol. 2006, 19, 908-913.
123. Karwowski, B.; Dupeyrat, F.; Bardet, M.; Ravanat, J.-L.; Krajewski, P.; Cadet, J. Nuclear magnetic resonance studies of the 4R and 4S diastereomers of spiroiminodihydantoin 20-deoxyribonucleosides:Absolute configuration and conformational features. Chem. Res. Toxicol. 2006, 19, 1357-1365.
124. Shafirovich, V. ; Cadet, J.; Gasparutto, D.; Dourandin, A.; Huang, W.; Geacintov,N. E. Direct spectroscopic observation of 8-oxo-7,8-dihydro-20-deoxyguanosine radicals in double-stranded DNA generated by one-electron oxidation at a distance by 2-aminopurine radicals. J. Phys. Chem. B 2001, 105, 586-592.
125. Misiaszek, R. ; Uvaydov, Y.; Crean, C.; Geacintov, N. E.; Shafirovich, V. Combination reactions of superoxide with 8-oxo-7,8-dihydroguanine radicals in DNA: Kinetics and end products. J. Biol. Chem. 2005, 280, 6293-6300.
126. Buchko, G. W.; Cadet,J. Identification of the alpha and beta anomers of 1-(2-deoxy-Derythro-pentofuranosyl)-oxaluric acid at the site of riboflavin-mediated photooxidation of guanine in 20-deoxyguanosine and thymidylyl-(30-50)-20-deoxyguanosine. J. Photochem. Photobiol. 2006, 82, 191-199.
127. Duarte, V. ; Gasparutto, D.; Yamaguchi, Y. F.; Ravanat, J.-F.; Martinez, G. R.; Medeiros, M. H. G.; Di Mascio, P.; Cadet, J. Oxaluric acid as the major product of singlet oxygenmediated oxidation of 8-oxo-7,8-dihydroguanine in DNA. J. Am. Chem. Soc. 2000, 122, 12622-12628.
128. Shafirovich, V. ; Cadet, J.; Gasparutto, D.; Durandin, A.; Geracintov,N. E. Nitrogen dioxide as an oxidizing agent of 8-oxo-7,8-dihydro-20-deoxyguanosine oxidation but not of 20-deoxyguanosine. Chem. Res. Toxicol. 2001, 14, 233-241.
129. Hickerson, R. P.; Prat, F.; Muller, J. G.; Foote, C. S.; Burrows, C. J. Sequence and stacking dependence of 8-oxoG oxidation: Comparison of one-electron vs singlet oxygen mechanisms. J. Am. Chem. Soc. 1999, 121, 9423-9428.
130. Floyd, R. A.;Watson, J. J.;Wong, P.K.; Atmiller, D. H.; Rickard, R. C. Hydroxyl free radical adduct of deoxyguanosine: Sensitive detection and mechanism of formation. Free Rad. Res Commun. 1986, 1, 163-172.
131. Kasai, H. Analysis of a form of oxidative DNA damage, 8-hydroxy-20-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat. Res. 1997, 387, 147-163.
132. Frelon, S. ; Douki, T.; Ravanat, J.-L.; Pouget, J.-P.; Tornabene, C.; Cadet, J. Highperformance liquid chromatography-tandem mass spectrometry measurement of radiation-induced base damage to isolated and cellular DNA. Chem. Res. Toxicol. 2000, 13, 1002-1010.
133. Singh, R. ; McEwan, M.; Lamb, J.H.; Santella, R. M.; Farmer, P. B. An improved liquid chromatography/tandem mass spectrometry method for the determination of 8-oxo-7,8-dihydro-20-deoxyguanosine in DNA samples using immunoaffinity column purification. Rapid Commun. Mass Spectrom. 2003, 17, 126-134.
134. Ravanat, J. -L.; Douki, T.; Duez, P.; Gremaud, E.; Herbert, K.; Hofer, T.; Lasserre, L.; Saint-Pierre, C.; Favier, A.; Cadet, J. Cellular background of 8-oxo-7,8-dihydro-20-deoxyguanosine: An isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up. Carcinogenesis 2002, 23, 1911-1918.
135. ESCODD. Measurement of DNA oxidation in human cells by chromatographic and enzymic methods. Free Radic. Biol. Med. 2003, 34, 1089-1099.
136. Collins, A. R.; Cadet, J.; Müller, L.; Poulsen, H. E.; Viña, J. Are we sure we know how to measure 8-oxo-7,8-dihydroguanine in DNA from human cells? Arch. Biochem. Biophys. 2004, 423, 57-65.
137. Murata M. , Bansho Y., Inoue S., Ito K., Ohnishi S., Midorikawa K., Kawanishi S. Requirement of glutathione and cysteine in guanine-specific oxidation of DNA by carcinogenic potassium bromate. Chem. Res. Toxicol. 2001, 14, 678-685.
138. Kawanishi, S. ; Murata,M. Mechanism ofDNAdamage induced by bromate differs from general types of oxidative stress. Toxicology 2006, 221, 172-178.
139. Ballmaier, D. ; Epe, B. Oxidative DNA damage induced by potassium bromate under cell-free conditions and in mammalian cells. Carcinogenesis 1995, 16, 335-342.
140. Ballmaier, D. ; Epe, B. DNA damage by bromate: mechanism and consequences. Toxicology 2006, 221, 166-171.
141. Jałoszyński, P. ; Murata, S.; Shinkai, Y.; Takahashi, S.; Kumagai, Y.; Nishimura, S.; Yamamoto, M. Dysfunction of Nrf2 decreases KBrO3-induced oxidativeDNAdamage in Ogg1-null mice. Biochem. Biophys. Res. Commun. 2007, 364, 966-971.
142. Chipman, J. K.; Parsons, J. L.; Beddowes, E. J. The multiple influences of glutathione on bromate genotoxicity: Implications for the dose-response relationship. Toxicology 2006, 221, 187-189.
143. Douki, T. ; Ravanat, J.-L; Pouget, J.-P.; Testard, I.; Cadet, J. Minor contribution of direct ionization to DNA base damage induced by heavy ions. Int. J. Radiat. Biol. 2006, 82, 119-127.
144. Pouget, J. P.; Frelon, S.; Ravanat, J.-L.; Testard, I.; Odin, F.; Cadet, J. Formation of modified DNA to DNA in cells exposed to either gamma radiation or high-LET particles. Radiat. Res. 2002, 157, 589-595.
145. Slade, P. G.; Hailer, M. K.; Martin, B. D.; Sugden, K. D. Guanine-specific oxidation of double-stranded DNA by Cr(VI) and ascorbic acid forms spiroiminodihydantoin and 8-oxo-20-deoxyguanosine. Chem. Res. Toxicol. 2005, 18, 1140-1149.
146. Hailer,M. K.; Slade, P. G.; Martin, B. D.; Sugden, K. D. Nei deficient Escherichia coli are sensitive to chromate and accumulate the oxidized guanine lesion spiroiminodihydantoin. Chem. Res. Toxicol. 2005, 18, 1378-1383.
147. Tuo, J. ; Jaruga, P.; Rodriguez, H.; Dizdaroglu, M.; Bohr, V. A. The Cockayne syndrome group B gene product is involved in cellular repair of 8-hydroxyadenine in DNA. J. Biol. Chem. 2002, 277, 30832-30837.
148. Tuo, J. ; Jaruga, P.; Rodriguez, H.; Bohr,V. A.; Dizdaroglu, M. Primary fibroblasts of Cockayne syndrome patients are defective in cellular repair of 8-hydroxyguanine and 8-hydroxyadenine from oxidative stress. FASEB J. 2003, 17, 668-674.
149. Friedman, K. A.; Keller, A. On the nonuniform distribution of guanine in introns of human genes: Possible protection of exons against oxidation by proximal introns poly-G sequences. J. Phys. Chem. B 2001, 105, 11859-11865.
150. Friedman, K. A.; Keller, A. Guanosine distribution and oxidation resistance in eight eukaryotic genomes. J. Am. Chem. Soc. 2004, 126, 2368-2371.
151. Kanvah, S. ; Schuster, G. B. The sacrificial role of easily oxidizable sites in the protection of DNA from damage. Nucleic Acids Res. 2005, 33, 5133-5138.