Pyrimidine Nucleobase Radical Reactivity

Radical and Radical Ion Reactivity in Nucleic Acid Chemistry

Volumn , Issue , 2009, Pages 135-162

  Greenberg, Marc M ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Diastereomeric nucleobase peroxyl radicals and conformational isomers; Nucleobase radicals reactive intermediate components in nucleic acids; Pyrimidine nucleobase radical reactivity

Indexed keywords

EID: 84865964341     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470526279.ch5     Document Type: Chapter

References (110)

1. von Sonntag, C. The Chemical Basis of Radiation Biology; Taylor & Francis, London, 1987.
2. Pogozelski, W. K.; McNeese, T. J.; Tullius, T. D. What species is responsible for strand scission in the reaction of [FeIIEDTA]2- and H2O2 with DNA? J. Am. Chem. Soc. 1995, 117, 6428-6433.
3. Trzupek, J. D.; Gottesfeld, J. M.; Boger, D. L. Alkylation of duplex DNA in nucleosome core particles by duocarmycin SA and yatakemycin. Nat. Chem. Biol. 2006, 2, 79-82.
4. Boger, D. L.; Garbaccio, R. M. Shape-dependent catalysis: Insights into the source of catalysis for the CC-1065 and duocarmycin DNA alkylation reaction. Acc. Chem. Res. 1999, 32, 1043-1052.
5. Chen, J.; Stubbe, J. Bleomycins: Towards better therapeutics. Nature Rev. Cancer 2005, 5, 102-112.
6. Xi, Z.; Goldberg, I. H. In Comprehensive Natural Products Chemistry, Vol. 7; Kool, E. T., Ed.; Elsevier, Amsterdam, 1999, pp. 553-592.
7. von Sonntag, C. Free-Radical-Induced DNA Damage and Its Repair; Springer-Verlag, Berlin, 2006.
8. Greenberg, M. M. Investigating nucleic acid damage processes via independent generation of reactive intermediates. Chem. Res. Toxicol. 1998, 11, 1235-1248.
9. Greenberg, M. M. In Comprehensive Natural Products Chemistry, Vol. 7, DNA and Aspects of Molecular Biology; Kool, E. T., Ed.; Elsevier, Amsterdam, 1999, pp. 371-426.
10. Giese, B.; Dussy, A.; Meggers, E.; Petretta, M.; Schwitter, U. Conformation, lifetime, and repair of 40-DNA radicals. J. Am. Chem. Soc. 1997, 119, 11130-11131.
11. Dussy, A.; Meggers, E.; Giese, B. Spontaneous cleavage of 40-DNA radicals under aerobic conditions: Apparent discrepancy between trapping rates and cleavage products. J. Am. Chem. Soc. 1998, 120, 7399-7403.
12. Giese, B. Long-distance charge transport in DNA: The hopping mechanism. Acc. Chem. Res. 2000, 33, 631-636.
13. Bryant-Friedrich, A. C. Generation of a C-30-thymidinyl radical in single-stranded oligonucleotides under anaerobic conditions, Org. Lett. 2004, 6, 2329-2332.
14. Zhang, Q.;Wang,Y. Independent generation of 5-(20deoxycytidinyl)methyl radical and the formation of a novel cross-link lesion between 5-methylcytosine and guanine. J. Am. Chem. Soc. 2003, 125, 12795-12802.
15. Greenberg, M. M. Elucidating DNA damage and repair processes by independently generating reactive and metastable intermediates. Org. Biomol. Chem. 2007, 5, 18-30.
16. Wang, Y. Bulky DNA lesions induced by reactive oxygen species. Chem. Res. Toxicol. 2008, 21, 276-281.
17. Dizdaroglu, M.; Jaruga, P.; Birincioglu, M.; Rodriguez, H. Free radical-induced damage to DNA: Mechanisms and measurements. Free Rad. Biol. Med. 2002, 32, 1102-1115.
18. Adhikary, A.; Kumar, A.; Sevilla, M. D.; Adhikary, A.; Malkhasian, A. Y. S.; Collins, S.; Koppen, J.; Becker, D.; Sevilla, M. D. Photo-induced hole transfer from base to sugar in DNA: Relationship to primary radiation damage UVA-visible photo-excitation of guanine radical cations produces sugar Radicals in DNA and model structures. Radiat. Res. 2006, 165, 479-484.
19. Hildenbrand, K.; Schulte-Frohlinde, D. E.S.R. Studies on the mechanism of hydroxyl radical-induced strand breakage of polyuridylic acid. Int. J. Radiat. Biol. 1989, 55, 725-738.
20. Hildenbrand, K.; Behrens, G.; Schulte-Frohlinde, D. Comparison of the reaction of .OH and of SO4-. radicals with pyrimidine nucleosides. An electron spin resonance study in aqueous solution. J. Chem. Soc. Perkin Trans. II 1989, 283-289.
21. Lemaire, D. G. E.; Bothe, E.; Schulte-Frohlinde, D.Yields of radiation-induced main chain scission of poly U in aqueous solution: Strand break formation via base radicals. Int. J. Radiat. Biol. 1984, 45, 351-358.
22. Barvian, M. R.; Greenberg, M. M. Independent generation of the major adduct of hydroxyl radical and thymidine. Examination of intramolecular hydrogen atom transfer in competition with thiol trapping. Tetrahedron Lett. 1992, 33, 6057-6060.
23. Barvian, M. R.; Barkley, R. M.; Greenberg, M. M. Reactivity of 5,6-dihydro-5-hydroxythymid-6-yl generated via photoinduced single electron transfer and the role of cyclohexa-1,4-diene in the photodeoxygenation process. J. Am. Chem. Soc. 1995, 117, 4894-4904.
24. Zhang, Q.; Wang, Y. Independent generation of the 5-hydroxy-5,6-dihydrothymidin-6-yl radical and its reactivity in dinucleoside morophosphates. J. Am. Chem. Soc. 2004, 126, 13287-13297.
25. Box, H. C.; Wallace, J. C. Free radical-induced double base lesions, Radiat. Res. 1995, 141, 91.
26. Box, H. C.; Patrzyc, H. B.; Dawidzik, J. B.; Wallace, J. C.; Freund, H. G.; Iijima, H.; Budzinski, E. E. Double base lesions in DNA X-irradiated in the presence or absence of oxygen, Radiat. Res. 2000, 153, 442-446.
27. Dianov, G. L.; O'Neill, P.; Goodhead, D. T. Securing genome stability by orchestrating DNA Repair: Removal of Radiation-induced clustered lesions in DNA, BioEssays 2001, 23, 745-749.
28. Lomax, M. E.; Gulston, M. K.; O'Neill, P. Chemical aspects of clustered DNA damage induction by ionising radiation. Radiation Protection Dosimetry 2002, 99, 63-68.
29. Weinfeld, M.; ResouliNia, A.; Chaudhry, M. A.; Britten, R. A. Response of base excision repair enzymes to complex DNA lesions. Radiat. Res. 2001, 156, 584-589.
30. Jenner, T. J.; Fulford, J.; O'Neill, P. Contribution of base lesions to radiation-induced clustered DNA damage: Implication for models of radiation response. Radiat. Res. 2001, 156, 590-593.
31. Zhang, Q.; Wang, Y. The reactivity of the 5-hydroxy-5,6-dihydrothymidin-6-yl radical in oligodeoxyribonucleotides. Chem. Res. Toxicol. 2005, 18, 1897-1906.
32. Tallman, K. A.; Tronche, C.; Yoo, D. J.; Greenberg, M. M. Release of superoxide from nucleoside peroxyl radicals, a double-edged sword? J. Am. Chem. Soc. 1998, 120, 4903-4909.
33. Barvian, M. R.; Greenberg, M. M. Independent generation of 5,6-dihydrothymid-5-yl and investigation of its ability to effect nucleic acid strand scission via hydrogen atom abstraction. J. Org. Chem. 1995, 60, 1916-1917.
34. Carter, K. N.; Greenberg, M. M. Independent generation and study of 5,6-dihydro-20- deoxyuridin-6-yl, a member of the major family of reactive intermediates formed in DNA from the effects of g-radiolysis, J. Org. Chem. 2003, 68, 4275-4280.
35. Newcomb, M. Competition methods and scales for alkyl radical reaction kinetics. Tetrahedron 1993, 49, 1151-1176.
36. Janik, I.; Ulanski, P.; Rosiak, J. M.;Von Sonntag, C. Hydroxyl-radical-induced reactions of the poly(vinyl methyl ether) model 2,4-dimethoxypentane in the absence and presence of dioxygen: A pulse radiolysis and product study, J. Chem. Soc. Perkin Trans. 2 2000, 2034-2040.
37. Schuchmann, M. N.; Von Sonntag. Hydroxyl radical-induced oxidation of diisopropyl ether in oxygenated aqueous solution. A product and pulse radiolysis study. C. Z. Naturforsch. B 1987, 42, 495-502.
38. Emanuel, C. J.; Newcomb, M.; Ferreri, C.; Chatgilialoglu, C. kinetics of 20-deoxyuridin-10- yl radical reactions. J. Am. Chem. Soc. 1999, 121, 2927-2928.
39. Hashimoto, M.; Greenberg, M. M.; Kow, Y. W.; Hwang, J.-T.; Cunningham, R. P. The 2- deoxyribonolactone lesion produced in DNA by neocarzinostatin and other DNA damaging agents forms cross-links with the base-excision repair enzyme endonuclease III. J. Am. Chem. Soc. 2001, 123, 3161-3162.
40. DeMott, M. S.; Beyret, E.; Wong, D.; Bales, B. C.; Hwang, J.-T.; Greenberg, M. M.; Demple, B. Covalent trapping of humanDNApolymerase b by the oxidativeDNAlesion 2- deoxyribonolactone. J. Biol. Chem. 2002, 277, 7637-7640.
41. Huang, H.; Greenberg, M. M. Hydrogen bonding contributes to the selectivity of nucleotide incorporation opposite an oxidized abasic lesion, J. Am. Chem. Soc. 2008, 130, 6080-6081.
42. Barvian, M. R.; Greenberg, M. M. Independent generation of 5,6-dihydrothymid-5-yl in single-stranded polythymidylate. O2 is necessary for strand scission. J. Am. Chem. Soc. 1995, 117, 8291-8292.
43. Greenberg, M. M.; Barvian, M. R.; Cook, G. P.; Goodman, B. K.; Matray, T. J.; Tronche, C.; Venkatesan, H. DNA damage induced via 5,6-dihydrothymidin-5-yl in single-stranded oligonucleotides. J. Am. Chem. Soc. 1997, 119, 1828-1839.
44. Carter, K. N.; Greenberg, M. M. Tandem lesions are the major products resulting from a pyrimidine nucleobase radical. J. Am. Chem. Soc. 2003, 125, 13376-13378.
45. Hong, I. S.; Carter, K. N.; Greenberg, M. M. Evidence for glycosidic bond rotation in a nucleobase peroxyl radical and its effect on tandem lesion formation. J. Org. Chem. 2004, 69, 6974-6978.
46. Hwang, J.-T.; Tallman, K. A.; Greenberg, M. M. The reactivity of the 2-deoxyribonolactone lesion in single-stranded DNA and its implication in reaction mechanisms of DNA damage and repair. Nucleic Acids Res. 1999, 27, 3805-3810.
47. Sato, K.; Greenberg, M. M. Selective detection of 2-deoxyribonolactone in DNA. J. Am. Chem. Soc. 2005, 127, 2806-2807.
48. Hong, I. S.; Carter, K. N.; Sato, K.; Greenberg, M. M. Characterization and mechanism of formation of tandem lesions in DNA by a nucleobase peroxyl radical. J. Am. Chem. Soc. 2007, 129, 4089-4098.
49. Miaskiewicz, K.; Osman, R. Theoretical study on the deoxyribose radicals formed by hydrogen abstraction. J. Am. Chem. Soc. 1994, 116, 232-238.
50. Colson, A. O.; Sevilla, M. D. Structure and relative stability of deoxyribose radicals in a model DNA backbone: Ab initio molecular orbital calculations. J. Phys. Chem. 1995, 99, 3867-3874.
51. Dizdaroglu, M.; Schulte-Frohlinde, D.; Von Sonntag, C. Isolation of 2-deoxy-D-erythropentonic acid from an alkali-labile site in g-irradiated DNA. Int. J. Radiat. Biol. 1977, 32, 481-483.
52. Roginskaya, M.; Razskazovskiy, Y.; Bernhard,W. A. 2-Deoxyribonolactone lesions in Xray- irradiated DNA: Quantitative determination by catalytic 5-methylene-2-furanone release. Angew. Chem. Int. Ed. 2005, 44, 6210-6213.
53. Xue, L.; Greenberg, M. 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. 2007, 46, 561-564.
54. Imoto, S.; Bransfield, L. A.; Croteau, D. L.; Van Houten, B.; Greenberg, M. M. DNA tandem lesion repair by strand displacement synthesis and nucleotide excision repair. Biochemistry 2008, 47, 4306-4316.
55. Joy, A.; Ghosh, A. K.; Schuster, G. B. One-electron oxidation of DNA oligomers that lack guanine: Reaction and strand cleavage at remote thymines by long-distance radical cation hopping. J. Am. Chem. Soc. 2006, 128, 5346-5347.
56. Ghosh, A.; Joy, A.; Schuster,G. B.; Douki, T.; Cadet, J. Selective one-electron oxidation of duplex DNA oligomers: Reaction at thymines. Org. Biomol. Chem. 2008, 6, 916-928.
57. Anderson, A. S.; Hwang, J. T.; Greenberg, M. M. Independent generation and reactivity of 20-Deoxy-5-methyleneuridin-5-yl, a significant reactive intermediate produced from thymidine as a result of oxidative stress. J. Org. Chem. 2000, 65, 4648-4654.
58. Hong, I. S.; Greenberg, M. M. Efficient DNA interstrand cross-link formation from a nucleotide radical. J. Am. Chem. Soc. 2005, 127, 3692-3693.
59. Hong, I. S.; Ding, H.; Greenberg, M. M. Oxygen independent DNA interstrand cross-link formation by a nucleotide radical. J. Am. Chem. Soc. 2006, 128, 485-491.
60. Ding, H.; Majumdar, A.; Tolman, J. R.; Greenberg, M. M. Multinuclear NMR and kinetic analysis of DNA interstrand cross-link formation. J. Am. Chem. Soc. in press, 130.
61. Romieu, A.; Bellon, S.; Gasparutto, D.; Cadet, J. Synthesis and UV photolysis of oligodeoxynucleotides that contain 5-(phenylthiomethyl)-20-deoxyuridine: A specific photolabile precursor of 5-(20-deoxyuridilyl)methyl radical. Org. Lett. 2000, 2, 1085-1088.
62. Bellon, S.; Gasparutto, D.; Romieu, A.; Cadet, J. 5-(Phenylthiomethyl)-20-deoxyuridine as an efficient photoreactive precursor to generate single and multiple lesions within DNA fragments. Nucleosides, Nucleotides & Nucleic Acids 2001, 20, 967-971.
63. Zhang, Q.; Wang, Y. Independent generation of 5-(20-deoxycytidinyl)methyl radical and the formation of a novel cross-link lesion between 5-methylcytosine and guanine. J. Am. Chem. Soc. 2003, 125, 12795-12802.
64. Box, H. C.; Budzinski, E. E.; Dawidzik, J. B.;Wallace, J. C.; Iijima, H. Tandem lesions and other products in X-irradiated DNA oligomers. Radiat. Res. 1998, 149, 433-439.
65. Delatour, T.; Douki, T.; Gasparutto, D.; Brochier, M.-C.; Cadet, J. A novel vicinal lesion obtained from the oxidative photosensitization of TpdG: Characterization and mechanistic aspects. Chem. Res. Toxicol. 1998, 11, 1005-1013.
66. Hong, H.; Cao, H.; Wang, Y. Identification and quantification of a guanine-thymine intrastrand cross-link lesion induced by Cu(II)/H2O2/ascorbate. Chem. Res. Toxicol. 2006, 19, 614-621.
67. Jiang, Y.; Hong, H.; Cao, H.; Wang, Y. In vivo formation and in vitro replication of a guanine-thymine intrastrand cross-link lesion. Biochemistry 2007, 46, 12757-12763.
68. Bellon, S.; Ravanat, J.-L.; Gasparutto, D.; Cadet, J. Cross-linked thymine-purine base tandem lesions: Synthesis, characterization, and measurement in gamma-irradiated isolated DNA. Chem. Res Toxicol. 2002, 15, 598-606.
69. Zhang, Q.;Wang, Y. Generation of 5-(20-deoxycytidyl)methyl radical and the formation of intrastrand cross-link lesions in oligodeoxyribonucleotides. Nucleic Acids Res. 2005, 33, 1593-1603.
70. Cao, H.;Wang, Y. Quantification of oxidative single-base and intrastrand cross-link lesions in unmethylated and CpG-methylated DNA Induced by Fenton-type reagents. Nucleic Acids Res. 2007, 35, 4833-4844.
71. Cheek, J.; Broderick, J. B. Direct Hatom abstraction from spore photoproduct C-6 initiates DNA repair in the reaction catalyzed by spore photoproduct lyase: Evidence for a reversibly generated adenosyl radical intermediate. J. Am. Chem. Soc. 2002, 124, 2860-2861.
72. Friedel, M. G.; Pieck, J. C.; Klages, J.; Dauth, C.; Kessler, H.; Carell, T. Synthesis and stereochemical assignment of DNA spore photoproduct analogues. Chem. Eur. J. 2006, 12, 6081-6094.
73. Boussicault, F.; Kaloudis, P.; Caminal, C.; Mulazzani, Q. G.; Chatgilialoglu, C. The fate of C50 radicals of purine nucleosides under oxidative conditions. J. Am. Chem. Soc. 2008, 130, 8377-8385.
74. Chatgilialoglu, C.; Bazzanini, R.; Jimenez, L. B.; Miranda, M. A. (50 S)- and (50 R)-50, 8- cyclo-20-deoxyguanosine: Mechanistic insights on the 20-deoxyguanosin-50-yl radical cyclization. Chem. Res. Toxicol. 2007, 20, 1820-1824.
75. Tomasz, M.; Palom, Y. The mitomycin bioreductive antitumor agents: Crosslinking and alkylation of DNA as the molecular basis of their activity. Pharmacol. Therapeut. 1997, 76, 73-87.
76. Noll, D. M.; Mason, T. M.; Miller, P. S. Formation and repair of interstrand cross-links in DNA, Chem. Rev. 2006, 106, 277-301.
77. von Sonntag, C.; Schuchmann, H.-P. The elucidation of peroxyl radical reactions in aqueous solution with the help of radiation-chemical methods. Angew. Chem. Int. Ed. 1991, 30, 1229-1253.
78. Millard, J. T.; Weidner, M. F.; Kirchner, J. J.; Ribeiro, S.; Hopkins, P. B. Sequence preferences of DNA interstrand crosslinking agents: Quantitation of interstrand crosslink locations in DNA duplex fragments containing multiple crosslinkable sites. Nucleic Acids Res. 1991, 19, 1885-1892.
79. Ding, H.; Greenberg, M. M. Gamma-radiolysis and hydroxyl radical produce interstrand cross-links in DNA involving thymidine. Chem. Res. Toxicol. 2007, 20, 1623-1628.
80. Guéron, M.; Leroy, J. Studies of base pair kinetics by NMR measurement of proton exchange. Methods Enzymol. 1995, 261, 383-413.
81. Snoussi, K.; Leroy, J. L. Alteration of A.T base-pair opening kinetics by the ammonium cation in DNA A-tracts. Biochemistry 2002, 41, 12467-12474.
82. Parker, J. B.; Bianchet, M. A.; Krosky, D. J.; Friedman, J. I.; Amzel, L. M.; Stivers, J. T. Enzymatic capture of an extrahelical thymine in the search for uracil inDNA. Nature 2007, 449, 433-437.
83. Luger, K.; Mader, A. W.; Richmond, R. K.; Sargent, D. F.; Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 1997, 389, 251-260.
84. Pogozelski, W. K.; Tullius, T. D. Oxidative strand scission of nucleic acids:Routes initiated by hydrogen abstraction from the sugar moiety. Chem. Rev. 1998, 98, 1089-1107.
85. Price, M. A.; Tullius, T. D. Using hydroxyl radical to probe DNA structure, Methods Enzymol. 1992, 212, 194-219.
86. Rees, W. A.;Keller, R.W. Evidence ofDNAbending in transcription complexes imaged by scanning force microscopy. Science 1993, 260, 1646.
87. Mouw, K. W.; Rice, P. A. Shaping the Borrelia burgdorferi genome: crystal structure and binding properties of the DNA-bending protein Hbb, Mol. Microbiol. 2007, 63, 1319-1330.
88. Swinger, K. K.; Rice, P. A. IHF and HU: Flexible architects of bentDNA. Curr. Op. Struct. Biol. 2004, 14, 28-35.
89. Peng, X.; Hong, I. S.; Li, H.; Seidman, M. M.; Greenberg, M. M. Interstrand cross-link formation in duplex and triplex DNA by modified pyrimidines. J. Am. Chem. Soc. 2008, 130, 10299-10306.
90. Brown, J. M.; Wilson, W. R. Exploiting tumor hypoxia in cancer treatment. Nature Reviews: Cancer 2004, 4, 437-447.
91. Sugiyama, H.; Saito, I. Highly sequence selective photoreaction of 5-bromouracil-containing deoxyhexanucleotides. J. Am. Chem. Soc. 1990, 112, 6720.
92. Cook, G. P.; Greenberg, M. M.Anovel mechanism for the formation of direct strand breaks upon anaerobic photolysis of duplexDNAcontaining 5-bromodeoxyuridine. J. Am. Chem. Soc. 1996, 118, 10025-10030.
93. Sugiyama, H.; Fujimoto, K.; Saito, I. Evidence for intrastrand C20 hydrogen abstraction in photoirradiation of 5-halouracil-containing oligonucleotides by using stereospecifically C20-deuterated deoxyadenosine. Tetrahedron Lett. 1996, 37, 1805-1808.
94. Franken, N. A. P.; Bree, C. V.; Veltmaat, M. A. T.; Rodermond, H. M.; Haveman, J.; Barendsen, G. W. Radiosensitization by bromodeoxyuridine and hyperthermia: Analysis of linear and quadratic parameters of radiation survival curves of two human tumor cell lines. J. Radiat. Res. 2001, 42, 179-190.
95. Ling, L. L.; Ward, J. F. Radiosensitization of Chinese hamster V79 cells by bromodeoxyuridine substitution of thymidine: Enhancement of radiation-induced toxicity and DNA strand break production by monofilar and bifilar substitution. Radiat. Res. 1990, 121, 76-83.
96. Hong, I. S.; Ding, H.; Greenberg, M. M. Radiosensitization by a modified nucleotide that produces DNA interstrand cross-links under hypoxic conditions. J. Am. Chem Soc. 2006, 128, 2230-2231.
97. Krief, A.; Lonez, F. Singlet oxygen oxidation of selenides to selenoxides. Tetrahedron Lett. 2002, 43, 6255-6257.
98. Hong, I. S.; Greenberg, M. M. DNA Interstrand cross-link formation initiated by reaction between singlet oxygen and a modified nucleotide. J. Am. Chem. Soc. 2005, 127, 10510-10511.
99. Sharman, W. M.; Allen, C. M.; van Lier, J. E. Role of activated oxygen species in photodynamic therapy. Methods Enzymol. 2000, 319, 376-400.
100. Dolmans, D. E.; Fukumura, D.; Jain, R. Photodynamic therapy for cancer. Nature Rev. Cancer 2003, 3, 380-387.
101. Peng, X.; Greenberg, M. M. Facile SNP detection using bifunctional, cross-linking oligonucleotide probes. Nucleic Acids Res. 2008, 36, e31.
102. Bastia, D.; Zzaman, S.; Krings, M.; Peng, X.; Greenberg, M. M. Replication termination mechanism as revealed by Tus-mediated polar arrest of a sliding helicase. Proc. Natl. Acad. Sci. USA 2008, 105, 12831-12836.
103. Box, H. C.; Budzinski, E. E.; Dawidzik, J. B.; Gobey, J., S.; Freund, H. G. Free radicalinduced tandem base damage in DNA oligomers. Free Rad. Biol. Med. 1997, 23, 1021-1030.
104. Zeng, Y.;Wang, Y. Facile formation of an intrastrand cross-link lesion between cytosine and guanine upon Pyrex-filtered UV light irradiation of d{eth}BrCG{Thorn} and duplex DNA containing 5-bromocytosine. J. Am. Chem. Soc. 2004, 126, 6552-6553.
105. Hong, H.; Wang, Y. Formation of intrastrand cross-link products between cytosine and adenine from UVirradiation of d(BrCA) and duplex DNA containing a 5-bromocytosine. J. Am. Chem. Soc. 2005, 127, 13969-13977.
106. Zeng, Y.;Wang, Y. Sequence-dependent formation of intrastrand crosslink products from the UVB irradiation of duplex DNA containing a 5-bromo-20-deoxyuridine or 5-bromo-20-deoxycytidine. Nucleic Acids Res. 2006, 34, 6521-6529.
107. Hong, H.; Cao, H.; Wang, Y. Formation and genotoxicity of a guanine-cytosine intrastrand cross-link lesion in vivo. Nucleic Acids Res. 2007, 35, 7118-7127.
108. Delaney, J. C.; Essigmann, J. M. Biological properties of single chemical-DNA adducts:A twenty year perspective. Chem. Res. Toxicol. 2008, 21, 232-252.
109. Patro, J. N.;Wiederholt, C. J.; Jiang, Y. L.; Delaney, J. C.; Essigmann, J. M.; Greenberg, M. M. Studies on the replication of the ring opened formamidopyrimidine, Fapy.dG in Escherichia coli, Biochemistry 2007, 46, 10202-10212.
110. Gu, C.; Zhang, Q.; Yang, Z.; Wang, Y.; Zou, Y.; Wang, Y. Recognition and incision of oxidative intrastrand cross-link lesions by UvrABC nuclease. Biochemistry 2006, 45, 10739-10746.