Modification of DNA damage mechanisms by nitric oxide during ionizing radiation

Free Radical Biology and Medicine

Volumn 58, Issue , 2013, Pages 14-25

  Folkes, Lisa K ^a   O'Neill, Peter ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

2 Deoxyguanosine; DNA strand breaks; Free radicals; Hydroxyl radical; Nitric oxide; Radiosensitization

Indexed keywords

2' DEOXY 8 AZAGUANOSINE MONOPHOSPHATE; 2' DEOXYXANTHOSINE MONOPHOSPHATE; DEOXYGUANOSINE PHOSPHATE; DNA BASE; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; HISTONE H2AX; NITRIC OXIDE; PLASMID DNA; UNCLASSIFIED DRUG;

ANOXIA; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA MODIFICATION; DOUBLE STRANDED DNA BREAK; ELECTROPHORESIS; EXCISION REPAIR; GAMMA IRRADIATION; IONIZING RADIATION; OXIDATION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PULSE RADIOLYSIS; SINGLE STRANDED DNA BREAK; STEADY STATE;

ANIMALS; ANOXIA; DEOXYGUANINE NUCLEOTIDES; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, RADIATION; FREE RADICALS; GAMMA RAYS; MICE; NEOPLASMS; NITRIC OXIDE; OXIDATION-REDUCTION; PLASMIDS; RADIATION-SENSITIZING AGENTS;

MAMMALIA;

EID: 84875989232     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.01.014     Document Type: Article

References (76)

1. R.M.J. Palmer, A.G. Ferrige, and S. Moncada Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor Nature 327 1987 524 526
2. P. Sonveaux, B.F. Jordan, B. Gallez, and O. Feron Nitric oxide delivery to cancer: why and how? Eur. J. Cancer 45 2009 1352 1369
3. S.G. Hummel, A.J. Fischer, S.M. Martin, F.Q. Schafer, and G.R. Buettner Nitric oxide as a cellular antioxidant: a little goes a long way Free Radic. Biol. Med. 40 2005 501 506
4. E.E. Kelley, B.A. Wagner, G.R. Buettner, and C.P. Burns Nitric oxide inhibits iron-induced lipid peroxidation in HL-60 cells Arch. Biochem. Biophys. 370 1999 97 104
5. P. Howard-Flanders Effect of nitric oxide on the radiosensitivity of bacteria Nature 180 1957 1191 1192
6. L.H. Gray, F.O. Green, and C.A. Hawes Effect of nitric oxide on the radiosensitivity of tumour cells Nature 182 1958 952 953
7. D.L. Dewey Effect of oxygen and nitric oxide on the radiosensitivity of human cells in tissue culture Nature 186 1960 780 782
8. J.B. Mitchell, D.A. Wink, W. deGraff, J. Gamson, L.K. Keefer, and M.C. Krishna Hypoxic mammalian cell radiosensitization by nitric oxide Cancer Res. 53 1993 5845 5848
9. R.J. Griffin, C.M. Makepeace, W.-J. Hur, and C.W. Song Radiosensitization of hypoxic tumor cells in vitro by nitric oxide Int. J. Radiat. Oncol. Biol. Phys. 36 1996 377 383
10. P. Wardman, K. Rothkamm, L.K. Folkes, M. Woodcock, and P.J. Johnston Radiosensitization by nitric oxide at low radiation doses Radiat. Res. 167 2007 475 484
11. G.D. Stewart, J. Nandi, E. Katz, K.J. Bowman, J.G. Christie, D.J.G. Brown, D.B. Mclaren, A.C.P. Riddick, J.A. Ross, G.D.D. Jones, and F.K. Habib DNA strand breaks and hypoxia response inhibition mediate the radisensitisation effect of nitric oxide donors on prostrate cancer under varying oxygen concentrations Biochem. Pharmacol. 81 2011 203 210
12. D.L. Wise, and G. Houghton Diffusion coefficients of neon, krypton, xenon, carbon monoxide and nitric oxide in water at 10-60 °C Chem. Eng. Sci. 23 1968 1211 1216
13. C. Shao, M. Aoki, and Y. Furusawa Bystander effect of cell growth stimulation in neoplastic HSGc cells induced by heavy-ion irradiation Radiat. Environ. Biophys. 42 2003 183 187
14. Janssens, M. Y.; Verovski, V. N.; Berge, D. L. V. d.; Monsaert, C.; Storme, G. A. Radiosensitization of hypoxic tumour cells by S-nitroso-N- acetylpenicillamine implicates a bioreductive mechanism of nitric oxide generation. Br. J. Cancer 79:1085-1089; 1999.
15. J. Worthington, T. Robson, M. O'Keeffe, and D. Hirst Tumour cell radiosensitization using constitutive (CMV) and radiation inducible (WAF1) promoters to drive the iNOS gene: a novel suicide gene therapy Gen. Ther. 9 2002 263 269
16. J. Worthington, H.O. McCarthy, E. Barrett, C. Adams, T. Robson, and D.G. Hirst Use of the radiation-inducible WAF1 promoter to drive iNOS gene therapy as a novel anti-cancer treatment J. Gene Med. 6 2004 673 680
17. (WAF1)- mediated transcriptional targeting of inducible nitric oxide synthase gene therapy sensitizes tumours to fractionated radiotherapy Gene Ther 14 2007 246 255
18. S. Singh, R.L. Cowen, E.C. Chinje, and I.J. Stratford The impact of intracellular generation of nitric oxide on the radiation response of human tumour cells Radiat. Res. 171 2009 572 580
19. B.F. Jordan, N. Beghein, M. Aubry, V. Grégoire, and B. Gallez Potentiation of radiation-induced regrowth delay by isosorbide dinitrate in FSAII murine tumors Int. J. Cancer 103 2003 138 141
20. S. Ning, M. Bednaarski, B. Oronsky, J. Scicinski, G. Saul, and S.J. Knox Dinitroazetidines are a novel class of anticancer agents and hypoxia-activated radiation sensitizers developed from highly energetic materials Cancer Res. 72 2012 2600 2608
21. T. Cook, Z. Wang, S. Alber, K. Liu, S.C. Watkins, Y. Vodovotz, T.R. Billiar, and D. Blumberg Nitric oxide and ionizing radiation synergistically promote apoptosis and growth inhibition of cancer by activating p53 Cancer Res. 64 2004 8015 8021
22. Y.-H. Chien, D.-T. Bau, and K.-Y. Jan Nitric oxide inhibits DNA-adduct excision in nucleotide excision repair Free Radic. Biol. Med. 36 2004 1011
23. B.F. Jordan, P. Sonveaux, O. Feron, V. Grégoire, N. Beghein, C. Dessy, and B. Gallez Nitric oxide as a radiosensitizer: evidence for an intrinsic role in addition to its effect on oxygen delivery and consumption Int. J. Cancer 109 2004 768 773
24. J.-P. Pouget, S. Frelon, L.-L. Ravanat, I. Testard, F. Odin, and J. Cadet Formation of modified DNA bases in cells exposed either to gamma radiation or to high-LET particles Radiat. Res. 157 2002 589 595
25. M.M.M. Bamatraf, P. O'Neill, and B.S.M. Rao Redox dependence of the rate of interaction of hydroxyl radical adducts of DNA nucleobases with oxidants: consequences for DNA strand breakage J. Am. Chem. Soc. 120 1998 11852 11857
26. C. Von Sonntag Free-Radical-Induced DNA Damage and Its Repair 2006 Springer Heidelberg
27. R.L. Willson The reaction of oxygen with radiation-induced free radicals in DNA and related compounds Int. J. Radiat. Biol 17 1970 349 358
28. P. O'Neill, and S.E. Davies A pulse radiolytic study of the interaction of nitroxyls with free-radical adducts of purines: consequences for radiosensitization Int. J. Radiat. Biol 49 1986 937 950
29. S. Steenken, and S.V. Jovanovic How easily oxidizable is DNA? One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution J. Am. Chem. Soc 119 1997 617 618
30. L.P. Candeias, and S. Steenken Structure and acid-base properties of one-electron-oxidized deoxyguanosine, guanosine and 1-methylguanosine J. Am. Chem. Soc. 111 1989 1094 1099
31. M. Dizdaroglu, and P. Jaruga Mechanisms of free radical-induced damage to DNA Free Radic. Res. 46 2012 382 419
32. P. O'Neill Pulse radiolytic study of the interaction of thiols and ascorbate with OH adducts of dGMP and dG: implications for DNA repair processes Radiat. Res 96 1983 198 210
33. P. O'Neill, and P.W. Chapman Potential repair of free radical adducts of dGMP and dG by a series of reductants: a pulse radiolytic study Int. J. Radiat. Biol 47 1985 71 80
34. • Chem. Eur. J 6 2000 475 484
35. C. Chatgilialoglu, M. D'Angelantonio, M. Guerra, P. Kaloudis, and Q.G. Mulazzani A reevaluation of the ambident reactivity of the guanine moiety towards hydroxyl radicals Angew. Chem. 48 2009 2214 2217
36. C. Chatgilialoglu, M. D'Angelantonio, G. Kciuk, and K. Bobrowski New insights into the reaction paths of hydroxyl radicals with 2′ deoxyguanosine Chem. Res. Toxicol. 24 2011 2200 2206
37. A. Adhikary, A. Kumar, D. Becker, and M.D. Sevilla The guanine cation radical: investigation of deprotonation states by ESR and DFT J. Phys. Chem. B 110 2006 24171 24180
38. S. Naumov, and C.V. Sonntag Guanine-derived radicals: dielectric constant-dependent stability and UV/Vis spectral properties: a DFT study Radiat. Res. 169 2008 364 372
39. S.D. Phadatare, K.K.K. Sharma, B.S.M. Rao, S. Naumov, and G.K. Sharma Spectral characterization of guanine C4-OH adduct: a radiation and quantum chemical study J. Phys. Chem. B 115 2011 13650 13658
40. P. Wardman, and E.D. Clarke Electron transfer and radical-addition in the radiosensitization and chemotherapy of hypoxic cells A. Breccia, J.F. Fowler, New Chemo and Radiosensitizing Drugs 1985 Scarabeo Bologna 21 38
41. L.J. Eccles, P. O'Neill, and M.E. Lomax Delayed repair of radiation induced clustered DNA damage: friend or foe? Mutat. Res. 711 2011 134 141
42. P.S. Hodgkins, M.P. Fairman, and P. O'Neill Rejoining of gamma-radiation-induced single-strand breaks in plasmid DNA by human cell extracts: dependence on the concentration of the hydroxy radical scavenger Tris. Radiat. Res 145 1996 24 30
43. L.K. Folkes, and P. Wardman Kinetics of the reaction between nitric oxide and glutathione: implications for thiol depletion in cells Free Radic. Biol. Med. 37 2004 549 556
44. Spinks, J. W. T; Woods, R. J., editors. An Introduction to Radiation Chemistry, 2nd ed. Wiley-Interscience, New York; 1976.
45. Sambrook, J.; Russell, D. W. In Molecular cloning, a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, New York; 2001
46. M. Gulston, J. Fulford, T. Jenner, C. d. Lara, and P. O'Neill Clustered DNA damage induced by g-radiation in human fibroblasts (HF19), hamster (V79-4) cells and plasmid DNA is revealed as Fpg and Nth sensitive sites Nucleic Acids Res 30 2002 3464 6472
47. G. Hems Effect of ionizing radiation on aqueous solutions of guanylic acid and guanosine Nature 181 1958 1721 1722
48. H. Kasai, and S. Nishimura Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents Nucleic Acids Res 1984 2137 2145 Suppl. 12
49. T. Nguyen, D. Brunson, C.L. Crespi, B.W. Penman, J.S. Wishnok, and S.R. Tannenbaum DNA damage and mutation in human cells exposed to nitric oxide in vitro Proc. Natl. Acad. Sci. USA 89 1992 3030 3034
50. J.L. Caulfield, J.S. Wishnok, and S.R. Tannenbaum Nitric oxide-induced deamination of cytosine and guanine in deoxynucleosides and oligonucleosides J. Biol. Chem. 273 1998 12689 12695
51. T. Suzuki, R. Yamaoka, M. Nishi, H. Ide, and K. Makino Isolation and characterization of a novel product, 2′-deoxyoxanosine, from 2′-deoxyguanosine, oligodeoxynucleotide, and calf thymus DNA treated by nitrous acid and nitric oxide J. Am. Chem. Soc. 118 1996 2515 2516
52. P. Majumdar, H. Wu, P. Tipton, and R. Glaser Oxanosine is a substrate of adenosine deaminase: implications for the quest for a toxicological marker for nitrosation activity Chem. Res. Toxicol. 18 2005 1830 1841
53. R.L. Willson, K.-D. Asmus, and P. Wardman Interaction of a dGMP radical with cysteamine and promethazine: a possible model of DNA repair Nature 252 1974 323 324
54. T. Suzuki, H. Ide, M. Yamada, N. Endo, K. Kanaori, K. Tajima, T. Morii, and K. Makino Formation of 2′deoxyoxanosine from 2′-deoxyguanosine and nitrous acid: mechanisms and intermediates Nucleic Acids Res. 28 2000 544 551
55. G. Czapski, J. Holcman, and B.H.J. Bielski Reactivity of nitric oxide with simple short-lived radicals in aqueous solutions J. Am. Chem. Soc. 116 1994 11465 11469
56. A.R. Richardson, K.C. Soliven, M.E. Castor, P.D. Barnes, S.J. Libby, and F.C. Fang The base excision repair system of Salmonella enterica serovar Typhimurium counteracts DNA damage by host nitric oxide PLoS Pathog. 5 2009 e1000451
57. 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
58. k ultrasoft X-rays and a-particles: comparison of experimental and simulated yields Int. J. Radiat. Biol 77 2001 1053 1066
59. A.A. Rafi, and C.M. Wheeler On the radiation-induced hyperchromicity of DNA Int. J. Radiat. Biol. 24 1973 321 323
60. S.R. Tannenbaum, S. Tamir, T. de Rojas-Walker, and J.S. Wishnok DNA damage and cytotoxicity caused by nitric oxide R.N. Loeppky, C.J. Michejda, Nitrosamines and Related N-nitroso Compounds: Chemistry and Biochemistry 1994 Am. Chem. Soc Washington, DC 120 135
61. S. Tamir, S. Burney, and S.R. Tannenbaum DNA damage by nitric oxide Chem. Res. Toxicol. 9 1996 821 827
62. S. Burney, J.L. Caulfield, J.C. Niles, J.S. Wishnok, and S.R. Tannenbaum The chemistry of DNA damage from nitric oxide and peroxynitrite Mutat. Res. 424 1999 37 49
63. - and OH adducts Chem. Rev 89 1989 503 520
64. T. Suzuki, K. Iwakura, Y. Takashima, N. Kasajima, and M. Inukai Formation of diazoate intermediate upon nitrous acid and nitric oxide treatment of 2′-deoxyadenosine Bioorg. Med. Chem. Lett. 19 2009 788 791
65. M. Berger, and J. Cadet Isolation and characterization of the radiation-induced degradation products of 2′-deoxyguanosine in oxygen-free aqueous solutions Z. Naturforsch. 40b 1985 1519 1531
66. K. Miaskiewicz, and R. Osman Theoretical study on the deoxyribose radicals formed by hydrogen abstraction J. Am. Chem. Soc. 116 1994 232 238
67. A.P. Breen, and J.A. Murphy Reactions of oxyl radicals with DNA Free Radic. Biol. Med. 18 1995 1033 1077
68. M.M. Greenberg Elucidating DNA damage and repair processes by independently generating reactive and metastable intermediates Org. Biomol. Chem 5 2007 18 30
69. F. Seela, and S. Lampe Synthesis, base pairing and structural transitions of oligodeoxyribonucleotides containing 8-aza-2′-deoxyguanosine Helv. Chim. Acta 77 1994 1003 1017
70. F. Seela, I. Munster, U. Lochner, and H. Rosemeyer 8-Azaadenosine and its 2′-deoxyribonucleoside: synthesis and oligonucleotide base-pair stability Helv. Chim. Acta 81 1998 1139 1155
71. J.G. Contreras, and S.T. Madariaga Structure and the energy of base pairing in non-natural bases of nucleic acids: the azaguanine-cytosine and azaadenine-thymine base pairs Bioorg. Chem 31 2003 367 377
72. E. Sage, and L. Harrison Clustered DNA lesion repair in eukaryotes: relevance to mutagenesis and cell survival Mutat. Res. 711 2011 123 133
73. •NO in aqueous solution: intermediacy of organic peroxynitrate and peroxynitrite species J. Phys. Chem 108 2004 1719 1725
74. G.W. Kidder, V.C. Dewey, R.E. Parks, and G.L. Woodside Further evidence on the mode of action of 8-azaguanine (Guanazolo) in tumour inhibition Cancer Res. 11 1951 204 211
75. 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
76. L.M. Coussens, and Z. Werb Inflammation and cancer Nature 420 2002 860 867