Development of enzymatic probes of oxidative and nitrosative DNA damage caused by reactive nitrogen species

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 594, Issue 1-2, 2006, Pages 120-134

  Dong, Min ^a,d   Vongchampa, Viengsai ^a   Gingipalli, Lakshmaiah ^a,e   Cloutier, Jean Francois ^a,f   Kow, Yoke W ^a,b   O'Connor, Timothy ^a,c   Dedon, Peter C ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^e ARQULE INC   (United States)

^f UNIVERSITÉ LAVAL   (Canada)

Author keywords

DNA repair; Enzymatic probe of DNA damage; Kinetics; Nitrosative DNA damage; Oxidative DNA damage

Indexed keywords

2' DEOXY 8 OXOGUANOSINE; 2' DEOXYOXANOSINE; 2' DEOXYXANTHOSINE; CARBON DIOXIDE; CARBONIC ACID DERIVATIVE; DEOXYINOSINE; DEOXYURIDINE; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; DNA GLYCOSYLTRANSFERASE; GENOMIC DNA; GUANOSINE DERIVATIVE; NITRIC OXIDE; NITROSOPEROXYCARBONATE; REACTIVE OXYGEN METABOLITE; TIOPRONIN; UNCLASSIFIED DRUG; URACIL DNA GLYCOSYLTRANSFERASE;

ARTICLE; CHRONIC INFLAMMATION; COMET ASSAY; DNA DAMAGE; DNA PROBE; ENZYME ACTIVITY; ESCHERICHIA COLI; GENOTOXICITY; IN VITRO STUDY; MACROPHAGE ACTIVATION; OXIDATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ANIMALS; DNA DAMAGE; DNA PROBES; DNA REPAIR; DNA REPAIR ENZYMES; ESCHERICHIA COLI PROTEINS; HUMANS; INOSINE MONOPHOSPHATE; MICE; MOLECULAR PROBE TECHNIQUES; NITROGEN OXIDES; NITROSATION; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLASMIDS; REACTIVE NITROGEN SPECIES;

ESCHERICHIA COLI; MURINAE;

EID: 31744431923     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2005.08.008     Document Type: Article

References (86)

1. B. Epe, D. Ballmaier, I. Roussyn, K. Briviba, and H. Sies DNA damage by peroxynitrite characterized with DNA repair enzymes Nucleic Acids Res. 24 1996 4105 4110
2. G.K. Kuipers, and M.V. Lafleur Characterization of DNA damage induced by gamma-radiation-derived water radicals, using DNA repair enzymes Int. J. Radiat. Biol. 74 1998 511 519
3. B. Epe, and J. Hegler Oxidative DNA damage: endonuclease fingerprinting Methods Enzymol. 234 1994 122 131
4. A. Hartwig, H. Dally, and R. Schlepegrell Sensitive analysis of oxidative DNA damage in mammalian cells: use of the bacterial Fpg protein in combination with alkaline unwinding Toxicol. Lett. 88 1996 85 90
5. A.R. Collins The comet assay for DNA damage and repair: principles, applications, and limitations Mol. Biotechnol. 26 2004 249 261
6. I. Hininger, A. Chollat-Namy, S. Sauvaigo, M. Osman, H. Faure, J. Cadet, A. Favier, and A.M. Roussel Assessment of DNA damage by comet assay on frozen total blood: method and evaluation in smokers and non-smokers Mutat. Res. 558 2004 75 80
7. S. Sauvaigo, C. Petec-Calin, S. Caillat, F. Odin, and J. Cadet Comet assay coupled to repair enzymes for the detection of oxidative damage to DNA induced by low doses of gamma-radiation: use of YOYO-1, low-background slides, and optimized electrophoresis conditions Anal. Biochem. 303 2002 107 109
8. J.P. Pouget, T. Douki, M.J. Richard, and J. Cadet DNA damage induced in cells by gamma and UVA radiation as measured by HPLC/GC-MS and HPLC-EC and Comet assay Chem. Res. Toxicol. 13 2000 541 549
9. S. Czene, and M. Harms-Ringdahl Detection of single-strand breaks and formamidopyrimidine-DNA glycosylase-sensitive sites in DNA of cultured human fibroblasts Mutat. Res. 336 1995 235 242
10. C. Collins, M.M. Awada, X. Zhou, and P.C. Dedon Analysis of 3′-phosphoglycolaldehyde residues in oxidized DNA by gas chromatography/negative chemical ionization/mass spectrometry Chem. Res. Toxicol. 16 2003 1560 1566
11. L.H. Breimer, and T. Lindahl Thymine lesions produced by ionizing radiation in double-stranded DNA Biochemistry 24 1985 4018 4022
12. S. Tornaletti, and G.P. Pfeifer Slow repair of pyrimidine dimers at p53 mutation hotspots in skin cancer Science 263 1994 1436 1438
13. J. Xu, J. Wu, and P.C. Dedon DNA damage produced by enediynes in the human phosphoglycerate kinase gene in vivo: esperamicin A1 as a nucleosome footprinting agent Biochemistry 37 1998 1890 1897
14. J. Tchou, S. Bodepudi, S. Shibutani, S. Antoshechkin, J. Miller, A.P. Grollman, and F. Johnson Substrate specificity of Fpg protein J. Biol. Chem. 269 1994 15318 15324
15. S. Boiteux, E. Gajewski, J. Laval, and M. Dizdaroglu Substrate specificity of the Escherichia coli Fpg protein (formamidopyrimidine-DNA glycosylase): excision of purine lesions in DNA produced by ionizing radiation or photosensitization Biochemistry 31 1992 106 110
16. S. Boiteux Properties and biological functions of the NTH and FPG proteins of Escherichia coli: two DNA glycosylases that repair oxidative damage in DNA J. Photochem. Photobiol. B 19 1993 87 96
17. M.F. Denissenko, A. Pao, M.-s. Tang, and G.P. Pfeifer Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53 Science 274 1996 430 432
18. H. Ohshima, and H. Bartsch Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis Mutat. Res. 305 1994 253 264
19. G.H. Cassell Infectious causes of chronic inflammatory diseases and cancer Emerg. Infect. Dis. 4 1998 475 487
20. P.C. Dedon, and S.R. Tannenbaum Reactive nitrogen species in the chemical biology of inflammation Arch. Biochem. Biophys. 423 2004 12 22
21. M. Dong, C. Wang, W.M. Deen, and P.C. Dedon Absence of 2′-deoxyoxanosine and presence of abasic sites in DNA exposed to nitric oxide at controlled physiological concentrations Chem. Res. Toxicol. 16 2003 1044 1055
22. C.A. Reynaud, S. Aoufouchi, A. Faili, and J.C. Weill What role for AID: mutator, or assembler of the immunoglobulin mutasome? Nat. Immunol. 4 2003 631 638
23. S. Anant, and N.O. Davidson Molecular mechanisms of apolipoprotein B mRNA editing Curr. Opin. Lipidol. 12 2001 159 165
24. H. Jacobs, and L. Bross Towards an understanding of somatic hypermutation Curr. Opin. Immunol. 13 2001 208 218
25. S. Maas, and A. Rich Changing genetic information through RNA editing Bioessays 22 2000 790 802
26. W.A. Pryor, R. Cueto, X. Jin, W.H. Koppenol, M. Ngu-Schwemlein, G.L. Squadrito, P.L. Uppu, and R.M. Uppu A practical method for preparing peroxynitrite solutions of low ionic strength and free of hydrogen peroxide Free Rad. Biol. Med. 18 1995 75 83
27. J.S. Beckman, H. Ischiropoulos, L. Zhu, M. Van der Woerd, C. Smith, J. Chen, J. Harrison, J.C. Martin, and M. Tsai Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite Arch. Biochem. Biophys. 2 1992 438 445
28. D.M. Wilson III., M Takeshita, A.P. Grollman, and B. Demple Incision activity of human apurinic endonuclease (Ape) at abasic site analogs in DNA J. Biol. Chem. 270 1995 16002 16007
29. M. Yao, and Y.W. Kow Further characterization of Escherichia coli endonuclease V. Mechanism of recognition for deoxyinosine, deoxyuridine, and base mismatches in DNA J. Biol. Chem. 272 1997 30774 30779
30. S. Ikeda, T. Biswas, R. Roy, T. Izumi, I. Boldogh, A. Kurosky, A.H. Sarker, S. Seki, and S. Mitra Purification and characterization of human NTH1, a homolog of Escherichia coli endonuclease III. Direct identification of Lys-212 as the active nucleophilic residue J. Biol. Chem. 273 1998 21585 21593
31. V. Vongchampa, M. Dong, L. Gingipalli, and P. Dedon Stability of 2′-deoxyxanthosine in DNA Nucleic Acids Res. 31 2003 1045 1051
32. R. Eritja, D.M. Horowitz, P.A. Walker, J.P. Ziehler-Martin, M.S. Boosalis, M.F. Goodman, K. Itakura, and B.E. Kaplan Synthesis and properties of oligonucleotides containing 2′-deoxynebularine and 2′- deoxyxanthosine Nucleic Acids Res. 14 1986 8135 8153
33. F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl Current Protocols in Molecular Biology 1989 John Wiley and Sons New York
34. T. Lindahl, and A. Andersson Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid Biochemistry 11 1972 3618 3623
35. L. Yu, J. Golik, R. Harrison, and P. Dedon The deoxyfucose-anthranilate of esperamicin A1 confers intercalative DNA binding and causes a switch in the chemistry of bistranded DNA lesions J. Am. Chem. Soc. 116 1994 9733 9738
36. J.S. Beckman, J. Chen, J.P. Crow, and Y.Z. Ye Reactions of nitric oxide, superoxide and peroxynitrite with superoxide dismutase in neurodegeneration Prog. Brain Res. 103 1994 371 380
37. J. Hegler, D. Bittner, S. Boiteux, and B. Epe Quantification of oxidative DNA modifications in mitochondria Carcinogenesis 14 1993 2309 2312
38. B. He, H. Qing, and Y.W. Kow Deoxyxanthosine in DNA is repaired by Escherichia coli endonuclease V Mutat. Res. 459 2000 109 114
39. G.E. Wuenschell, T.R. O'Connor, and J. Termini Stability, miscoding potential, and repair of 2′-deoxyxanthosine in DNA: implications for nitric oxide-induced mutagenesis Biochemistry 42 2003 3608 3616
40. H. Feng, A.M. Klutz, and W. Cao Active site plasticity of endonuclease V from Salmonella typhimurium Biochemistry 44 2005 675 683
41. H. Kamiya, H. Yakushiji, L. Dugue, M. Tanimoto, S. Pochet, Y. Nakabeppu, and H. Harashima Probing the substrate recognition mechanism of the human MTH1 protein by nucleotide analogs J. Mol. Biol. 336 2004 843 850
42. H. Terato, A. Masaoka, K. Asagoshi, A. Honsho, Y. Ohyama, T. Suzuki, M. Yamada, K. Makino, K. Yamamoto, and H. Ide Novel repair activities of AlkA (3-methyladenine DNA glycosylase II) and endonuclease VIII for xanthine and oxanine, guanine lesions induced by nitric oxide and nitrous acid Nucleic Acids Res. 30 2002 4975 4984
43. Y.W. Kow Repair of deaminated bases in DNA Free Radic. Biol. Med. 33 2002 886 893
44. K.A. Schouten, and B. Weiss Endonuclease V protects Escherichia coli against specific mutations caused by nitrous acid Mutat. Res. 435 1999 245 254
45. M. Saparbaev, J.C. Mani, and J. Laval Interactions of the human, rat, Saccharomyces cerevisiae and Escherichia coli 3-methyladenine-DNA glycosylases with DNA containing dIMP residues Nucleic Acids Res. 28 2000 1332 1339
46. M. Saparbaev, and J. Laval Excision of hypoxanthine from DNA containing dIMP residues by the Escherichia coli, yeast, rat, and human alkylpurine DNA glycosylase Proc. Natl. Acad. Sci. U.S.A. 91 1994 5873 5877
47. S. Burney, J.C. Niles, P.C. Dedon, and S.R. Tannenbaum DNA damage in deoxynucleosides and oligonucleotides treated with peroxynitrite Chem. Res. Toxicol. 12 1999 513 520
48. N.Y. Tretyakova, J.C. Niles, S. Burney, J.S. Wishnok, and S.R. Tannenbaum Peroxynitrite-induced reactions of synthetic oligonucleotides containing 8-oxoguanine Chem. Res. Toxicol. 12 1999 459 466
49. N.Y. Tretyakova, S. Burney, B. Pamir, J.S. Wishnok, P.C. Dedon, G.N. Wogan, and S.R. Tannenbaum Peroxynitrite-induced DNA damage in the supF gene: correlation with the mutational spectrum Mutat. Res. 447 2000 287 303
50. R. Kissner, and W.H. Koppenol Product distribution of peroxynitrite decay as a function of pH, temperature, and concentration J. Am. Chem. Soc. 124 2002 234 239
51. M. Saparbaev, and J. Laval Excision of hypoxanthine from DNA containing dIMP residues by the Escherichia coli, yeast, rat, and human alkylpurine DNA glycosylases Proc. Natl. Acad. Sci. U.S.A. 91 1994 5873 5877
52. H. Rodriguez, G.P. Holmquist, R.J. D'Agostino, J. Keller, and S.A. Akman Metal ion-dependent hydrogen peroxide-induced DNA damage is more sequence specific than metal specific Cancer Res. 57 1997 2394 2403
53. K.G. Berdal, R.F. Johansen, and E. Seeberg Release of normal bases from intact DNA by a native DNA repair enzyme EMBO J. 17 1998 363 367
54. M.D. Wyatt, and L.D. Samson Influence of DNA structure on hypoxanthine and 1,N6-ethenoadenine removal by murine 3-methyladenine DNA glycosylase Carcinogenesis 21 2000 901 908
55. R. Roy, S.J. Kennel, and S. Mitra Distinct substrate preference of human and mouse N-methylpurine-DNA glycosylases Carcinogenesis 17 1996 2177 2182
56. M. Saparbaev, K. Kleibl, and J. Laval Escherichia coli, Saccharomyces cerevisiae, rat and human 3-methyladenine DNA glycosylases repair 1,N6-ethenoadenine when present in DNA Nucleic Acids Res. 23 1995 3750 3755
57. M.K. Dosanjh, R. Roy, S. Mitra, and B. Singer 1,N6-Ethenoadenine is preferred over 3-methyladenine as substrate by a cloned human N-methylpurine-DNA glycosylase (3-methyladenine-DNA glycosylase) Biochemistry 33 1994 1624 1628
58. T.R. O'Connor Purification and characterization of human 3-methyladenine-DNA glycosylase Nucleic Acids Res. 21 1993 5561 5569
59. L. Samson, B. Derfler, M. Boosalis, and K. Call Cloning and characterization of a 3-methyladenine DNA glycosylase cDNA from human cells whose gene maps to chromosome 16 Proc. Natl. Acad. Sci. U.S.A. 88 1991 9127 9131
60. D. Chakravarti, G.C. Ibeanu, K. Tano, and S. Mitra Cloning and expression in Escherichia coli of a human cDNA encoding the DNA repair protein N-methylpurine-DNA glycosylase J. Biol. Chem. 266 1991 15710 15715
61. A. Asaeda, H. Ide, K. Asagoshi, S. Matsuyama, K. Tano, A. Murakami, Y. Takamori, and K. Kubo Substrate specificity of human methylpurine DNA N-glycosylase Biochemistry 39 2000 1959 1965
62. M.K. Dosanjh, A. Chenna, E. Kim, H. Fraenkel-Conrat, L. Samson, and B. Singer All four known cyclic adducts formed in DNA by the vinyl chloride metabolite chloroacetaldehyde are released by a human DNA glycosylase Proc. Natl. Acad. Sci. U.S.A. 91 1994 1024 1028
63. F. Miao, M. Bouziane, and T.R. O'Connor Interaction of the recombinant human methylpurine-DNA glycosylase (MPG protein) with oligodeoxyribonucleotides containing either hypoxanthine or abasic site Nucleic Acids Res. 26 1998 4034 4041
64. L. Xia, L. Zheng, H.W. Lee, S.E. Bates, L. Federico, B. Shen, and T.R. O'Connor Human 3-methyladenine-DNA glycosylase: effect of sequence context on excision association with PCNA, and stimulation by AP endonuclease J. Mol. Biol. 346 2005 1259 1274
65. A.A. Salzberg, and P.C. Dedon DNA bending is a determinant of calicheamicin target recognition Biochemistry 39 2000 7605 7612
66. H.J. Helbock, K.B. Beckman, M.K. Shigenaga, P.B. Walter, A.A. Woodall, H.C. Yeo, and B.N. Ames DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxoguanine Proc. Natl. Acad. Sci. U.S.A. 95 1998 288 293
67. J.L. Caulfield, J.S. Wishnok, and S.R. Tannenbaum Nitric oxide-induced interstrand cross-links in DNA Chem. Res. Toxicol. 16 2003 571 574
68. L. Thomas, C.H. Yang, and D.A. Goldthwait Two DNA glycosylases in Escherichia coli which release primarily 3-methyladenine Biochemistry 21 1982 1162 1169
69. T. Lindahl, B. Sedgwick, M. Sekiguchi, and Y. Nakabeppu Regulation and expression of the adaptive response to alkylating agents Annu. Rev. Biochem. 57 1988 133 157
70. S. Bjelland, N.K. Birkeland, T. Benneche, G. Volden, and E. Seeberg DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the AlkA enzyme in Escherichia coli J. Biol. Chem. 269 1994 30489 30495
71. Y. Habraken, C.A. Carter, M. Sekiguchi, and D.B. Ludlum Release of N2,3-ethanoguanine from haloethylnitrosourea-treated DNA by Escherichia coli 3-methyladenine DNA glycosylase II Carcinogenesis 12 1991 1971 1973
72. J. Tuo, L. Liu, H.E. Poulsen, A. Weimann, O. Svendsen, and S. Loft Importance of guanine nitration and hydroxylation in DNA in vitro and in vivo Free Radic. Biol. Med. 29 2000 147 155
73. V. Yermilov, J. Rubio, and H. Ohshima Formation of 8-nitroguanine in DNA treated with peroxynitrite in vitro and its rapid removal from DNA by depurination FEBS Lett. 376 1995 207 210
74. M.D. Leipold, J.G. Muller, C.J. Burrows, and S.S. David Removal of hydantoin products of 8-oxoguanine oxidation by the Escherichia coli DNA repair enzyme, FPG Biochemistry 39 2000 14984 14992
75. N.Y. Tretyakova, J.S. Wishnok, and S.R. Tannenbaum Peroxynitrite-induced secondary oxidative lesions at guanine nucleobases: chemical stability and recognition by the Fpg DNA repair enzyme Chem. Res. Toxicol. 13 2000 658 664
76. V. Duarte, D. Gasparutto, M. Jaquinod, J. Ravanat, and J. Cadet Repair and mutagenic potential of oxaluric acid, a major product of singlet oxygen-mediated oxidation of 8-oxo-7, 8-dihydroguanine Chem. Res. Toxicol. 14 2001 46 53
77. E.I. Zaika, R.A. Perlow, E. Matz, S. Broyde, R. Gilboa, A.P. Grollman, and D.O. Zharkov Substrate discrimination by formamidopyrimidine-DNA glycosylase: a mutational analysis J. Biol. Chem. 279 2004 4849 4861
78. C. D'Ham, A. Romieu, M. Jaquinod, D. Gasparutto, and J. Cadet Excision of 5, 6-dihydroxy-5, 6-dihydrothymine 5, 6-dihydrothymine, and 5-hydroxycytosine from defined sequence oligonucleotides by Escherichia coli endonuclease III and Fpg proteins: kinetic and mechanistic aspects Biochemistry 38 1999 3335 3344
79. D. Gasparutto, A.G. Bourdat, C. D'Ham, V. Duarte, A. Romieu, and J. Cadet Repair and replication of oxidized DNA bases using modified oligodeoxyribonucleotides Biochimie 82 2000 19 24
80. Z. Hatahet, Y.W. Kow, A.A. Purmal, R.P. Cunningham, and S.S. Wallace New substrates for old enzymes. 5-Hydroxy-2′-deoxycytidine and 5-hydroxy-2′-deoxyuridine are substrates for Escherichia coli endonuclease III and formamidopyrimidine DNA N-glycosylase, while 5-hydroxy-2′- deoxyuridine is a substrate for uracil DNA N-glycosylase J. Biol. Chem. 269 1994 18814 18820
81. A.A. Purmal, G.W. Lampman, J.P. Bond, Z. Hatahet, and S.S. Wallace Enzymatic processing of uracil glycol, a major oxidative product of DNA cytosine J. Biol. Chem. 273 1998 10026 10035
82. A. Karakaya, P. Jaruga, V.A. Bohr, A.P. Grollman, and M. Dizdaroglu Kinetics of excision of purine lesions from DNA by Escherichia coli Fpg protein Nucleic Acids Res. 25 1997 474 479
83. J.O. Blaisdell, Z. Hatahet, and S.S. Wallace A novel role for Escherichia coli endonuclease VIII in prevention of spontaneous G → T transversions J. Bacteriol. 181 1999 6396 6402
84. S.S. Wallace Biological consequences of free radical-damaged DNA bases Free Radic. Biol. Med. 33 2002 1 14
85. J.P. Spencer, J. Wong, A. Jenner, O.I. Aruoma, C.E. Cross, and B. Halliwell Base modification and strand breakage in isolated calf thymus DNA and in DNA from human skin epidermal keratinocytes exposed to peroxynitrite or 3-morpholinosydnonimine Chem. Res. Toxicol. 9 1996 1152 1158
86. A.H. Schein Uracil in formic acid hydrolysates of deoxyribonucleic acid Biochem. J. 98 1966 311 316