Biological consequences of radiation-induced DNA damage: Relevance to radiotherapy

Clinical Oncology

Volumn 25, Issue 10, 2013, Pages 578-585

  Lomax, M E ^a   Folkes, L K ^a   O'Neill, P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Clustered DNA damage; DNA repair; Ionising radiation; Microenvironment; Radiosensitisers; Radiotherapy

Indexed keywords

4 NITROIMIDAZOLE; NIMORAZOLE; NITRIC OXIDE; NITROTRIAZOLE; RADIOSENSITIZING AGENT; REACTIVE OXYGEN METABOLITE; SANAZOLE; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ARTICLE; CELL DEATH; CELL SURVIVAL; COLON CANCER; CYTOTOXICITY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; HUMAN; ION THERAPY; IONIZING RADIATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RADIATION DOSE; RADIATION INJURY; RADIOSENSITIZATION; TUMOR CELL;

CLUSTERED DNA DAMAGE; DNA REPAIR; IONISING RADIATION; MICROENVIRONMENT; RADIOSENSITISERS; RADIOTHERAPY;

DNA DAMAGE; DNA, NEOPLASM; HUMANS; NEOPLASMS; RADIOTHERAPY;

EID: 84883288290     PISSN: 09366555     EISSN: 14332981     Source Type: Journal    
DOI: 10.1016/j.clon.2013.06.007     Document Type: Article

References (94)

1. Swenberg J.A., Lu K., Moeller B.C., et al. Endogenous versus exogenous DNA adducts: their role in carcinogenesis, epidemiology and risk assessment. Toxicol Sci 2011, 120:S130-S145.
2. Pouget J.-P., Frelon S., Ravanat J.-L., et al. Formation of modified DNA bases in cells exposed either to gamma radiation or to high-LET particles. Radiat Res 2002, 157:589-595.
3. 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.
4. Dizdaroglu M., Jaruga P. Mechanisms of free radical-induced damage to DNA. Free Radic Res 2012, 46:382-419.
5. Von Sonntag C. Free-radical-induced DNA damage and its repair 2006, Springer, Heidelberg.
6. O'Neill P., Wardman P. Radiation chemistry comes before radiation biology. Int J Radiat Biol 2009, 85:9-25.
7. Sutherland B.M., Bennett P.V., Sidorkina O., et al. Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation. Proc Natl Acad Sci USA 2000, 97:103-108.
8. Sutherland B.M., Bennett P.V., Sutherland J.C., et al. Clustered DNA damages induced by X-rays in human cells. Radiat Res 2002, 157:611-616.
9. Gulston M., Fulford J., Jenner T., et al. Clustered DNA damage induced by gamma radiation in human fibroblasts (HF19), hamster (V79-4) cells and plasmid DNA is revealed as Fpg and Nth sensitive sites. Nucleic Acids Res 2002, 30:3464-3472.
10. Nikjoo H., O'Neill P., Terrissol M., et al. Quantitative modelling of DNA damage using Monte Carlo track structure method. Radiat Environ Biophys 1999, 38:31-38.
11. Nikjoo H., Uehara S., Wilson W.E., et al. Track structure in radiation biology: theory and applications. Int J Radiat Biol 1998, 73:355-364.
12. Goodhead D.T. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int J Radiat Biol 1994, 65:7-17.
13. Jenner T.J., deLara C.M., O'Neill P., et al. Induction and rejoining of DNA double-strand breaks in V79-4 mammalian cells following gamma- and alpha-irradiation. Int J Radiat Biol 1993, 64:265-273.
14. Riballo E., Kuhne M., Rief N., et al. Apathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol Cell 2004, 16:715-724.
15. Eccles L.J., O'Neill P., Lomax M.E. Delayed repair of radiation induced clustered DNA damage: friend or foe?. Mutat Res 2011, 711:134-141.
16. Lomax M.E., Gulston M.K., O'Neill P. Chemical aspects of clustered DNA damage induction by ionising radiation. Radiat Prot Dosimetry 2002, 99:63-68.
17. Weinfeld M., Rasouli-Nia A., Chaudhry M.A., et al. Response of base excision repair enzymes to complex DNA lesions. Radiat Res 2001, 156:584-589.
18. Wallace S.S. Biological consequences of free radical-damaged DNA bases. Free Radic Biol Med 2002, 33:1-14.
19. Dobbs T.A., Palmer P., Maniou Z., et al. Interplay of two major repair pathways in the processing of complex double-strand DNA breaks. DNA Repair 2008, 7:1372-1383.
20. Georgakilas A.G. Processing of DNA damage clusters in human cells: current status of knowledge. Mol Biosystems 2008, 4:30-35.
21. Hanai R., Yazu M., Heida K. On the experimental distinction between ssbs and dsbs in circular DNA. Int J Radiat Biol 1998, 73:475-479.
22. van der Schans G.P. Gamma-ray induced double-strand breaks in DNA resulting from randomly-inflicted single-strand breaks: temporal local denaturation, a new radiation phenomenon?. Int J Radiat Biol Relat Stud Phys Chem Med 1978, 33:105-120.
23. Sutherland B.M., Bennett P.V., Cintron N.S., et al. Low levels of endogenous oxidative damage cluster levels in unirradiated viral and human DNAs. Free Radic Biol Med 2003, 35:495-503.
24. Bennett P.V., Cintron N.S., Gros L., et al. Are endogenous clustered DNA damages induced in human cells?. Free Radic Biol Med 2004, 37:488-499.
25. Henner W.D., Rodriguez L.O., Hecht S.M., et al. Gamma ray induced deoxyribonucleic acid strand breaks. 3' Glycolate termini. JBiol Chem 1983, 258:711-713.
26. Henner W.D., Grunberg S.M., Haseltine W.A. Sites and structure of gamma radiation-induced DNA strand breaks. JBiol Chem 1982, 257:11750-11754.
27. Datta K.P., Jaruga P., Dizaroglu M., et al. Molecular analysis of base damage clustering associated with a site-specific radiation-induced DNA double-strand break. Radiat Res 2006, 166:767-781.
28. Datta K., Neumann R.D., Winters T.A. Characterization of complex apurinic/apyrimidinic-site clustering associated with an authentic site-specific radiation-induced DNA double-strand break. Proc Natl Acad Sci USA 2005, 102:10569-10574.
29. Datta K., Purkayastha S., Newmann R.D., et al. Base damage immediately upstream from double-strand break ends is a more severe impediment to nonhomologous end joining than blocked 3'-termini. Radiat Res 2011, 175:97-112.
30. Rothkamm K., Lobrich M. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low X-ray doses. Proc Natl Acad Sci USA 2003, 100:5057-5062.
31. Claesson K., Magnander K., Kahu H., et al. RBE of alpha-particles from (211)At for complex DNA damage and cell survival in relation to cell cycle position. Int J Radiat Biol 2011, 87:372-384.
32. Magnander K., Hultborn R., Claesson K., et al. Clustered DNA damage in irradiated human diploid fibroblasts: influence of chromatin organization. Radiat Res 2010, 173:272-282.
33. van Gent D.C., Hoeijmakers J.H., Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat Rev Genet 2001, 2:196-206.
34. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 2010, 79:181-211.
35. Schmid T.E., Dollinger G., Beisher W., et al. Differences in the kinetics of gamma-H2AX fluorescence decay after exposure to low and high LET radiation. Int J Radiat Biol 2010, 86:682-691.
36. Reynolds P., Anderson J.A., Harper J.V., et al. The dynamics of Ku70/80 and DNA-PKcs at DSBs induced by ionizing radiation is dependent on the complexity of damage. Nucleic Acids Res 2012, 40:10821-10831.
37. Asaithamby A., Uematsu N., Chatterjee A., et al. Repair of HZE-particle-induced DNA double-strand breaks in normal human fibroblasts. Radiat Res 2008, 169:437-446.
38. Botchway S.W., Stevens D.L., Hill M.A., et al. Induction and rejoining of DNA double-strand breaks in Chinese hamster V79-4 cells irradiated with characteristic aluminum K and copper L ultrasoft X rays. Radiat Res 1997, 148:317-324.
39. Jeggo P.A., Lobrich M. Artemis links ATM to double strand break rejoining. Cell Cycle 2005, 4:359-362.
40. Jakob B., Splinter J., Conrad S., et al. DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res 2011, 39:6489-6499.
41. Mladenov E., Iliakis G. Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mutat Res 2011, 711:61-72.
42. Peddi P., Francisco D.C., Cecil A.M., et al. Processing of clustered DNA damage in human breast cancer cells MCF-7 with partial DNA-PKcs deficiency. Cancer Lett 2008, 269:174-183.
43. Covo S., de Villartay J.P., Jeggo P.A., et al. Translesion DNAsynthesis-assisted non-homologous end-joining of complex double-strand breaks prevents loss of DNA sequences in mammalian cells. Nucleic Acids Res 2009, 37:6737-6745.
44. Nikjoo H., O'Neill P., Wilson W.E., et al. Computational approach for determining the spectrum of DNA damage induced by ionizing radiation. Radiat Res 2001, 156:577-583.
45. Zharkov D.O. Base excision DNA repair. Cell Mol Life Sci 2008, 65:1544-1565.
46. Harrison L., Hatahet Z., Wallace S.S., et al. Invitro repair of synthetic ionizing radiation-induced multiply damaged DNA sites. JMol Biol 1999, 290:667-684.
47. David-Cordonnier M.-H., Laval J., O'Neill P. Clustered DNA damage, influence on damage excision by XRS5 nuclear extracts and Escherichia coli Nth and Fpg proteins. JBiol Chem 2000, 275:11865-11873.
48. Lomax M.E., Cunniffe S., O'Neill P. 8-OxoG retards the activity of the ligase III/XRCC1 complex during the repair of a single-strand break, when present within a clustered DNA damage site. DNA Repair 2004, 3:289-299.
49. Eccles L.J., Lomax M.E., O'Neill P. Hierarchy of lesion processing governs the repair, double-strand break formation and mutability of three-lesion clustered DNA damage. Nucleic Acids Res 2010, 38:1123-1134.
50. Lomax M., Cunniffe S., O'Neill P. Efficiency of repair of an abasic site within DNA clustered damage sites by mammalian cell nuclear extracts. Biochemistry 2004, 43:11017-11026.
51. Bellon S., Shikazonon N., Cunniffe S., et al. Processing of thymine glycol in a clustered DNA damage site: mutagenic or cytotoxic. Nucleic Acids Res 2009, 37:4430-4440.
52. Malyarchuk S., Castore R., Harrison L. DNA repair of clustered lesions in mammalian cells: involvement of non-homologous end-joining. Nucleic Acids Res 2008, 36:4872-4882.
53. Eot-Houllier G., Eon-Marchais S., Gasparutto D., et al. Processing of a complex multiply damaged DNA site by human cell extracts and purified repair proteins. Nucleic Acids Res 2005, 33:260-271.
54. Eot-Houllier G., Gonera M., Gasparutto D., et al. Interplay between DNA N-glycosylases/AP lyases at multiply damaged sites and biological consequences. Nucleic Acids Res 2007, 35:3355-3366.
55. Malyarchuk S., Brame K.L., Youngblood R., et al. Two clustered 8-oxo-7,8-dihydroguanine (8-oxodG) lesions increase the point mutation frequency of 8-oxodG, but do not result in double strand breaks or deletions in Escherichia coli. Nucleic Acids Res 2004, 32:5721-5731.
56. Pearson C.G., Shikazono N., Thacker J., et al. Enhanced mutagenic potential of 8-oxo-7,8-dihydroguanine when present within a clustered DNA damage site. Nucleic Acids Res 2004, 32:263-270.
57. Paap B., Wilson D.M., Sutherland B.M. Human abasic endonuclease action on multilesion abasic clusters: implications for radiation-induced biological damage. Nucleic Acids Res 2008, 36:2717-2727.
58. Harrison L., Brame K.L., Geltz L.E., et al. Closely opposed apurinic/apyrimidinic sites are converted to double strand breaks in Escherichia coli even in the absence of exonuclease III, endonuclease IV, nucleotide excision repair and AP lyase cleavage. DNA Repair (Amst) 2006, 5:324-335.
59. Kozmin S.G., Sedletska Y., Reynaud-Angelin A., et al. The formation of double-strand breaks at multiply damaged sites is driven by the kinetics of excision/incision at base damage in eukaryotic cells. Nucleic Acids Res 2009, 37:1767-1777.
60. Malyarchuk S., Harrison L. DNA repair of clustered uracils in HeLa cells. JMol Biol 2005, 345:731-743.
61. Malyarchuk S., Castore R., Harrison L. Apex1 can cleave complex clustered DNA lesions in cells. DNA Repair (Amst) 2009, 8:1343-1354.
62. Georgakilas A.G., Bennett P.V., Wilson D.M., et al. Processing of bistranded abasic DNA clusters in gamma-irradiated human hematopoietic cells. Nucleic Acids Res 2004, 32:5609-5620.
63. Gulston M., de Lara C., Jenner T., et al. Processing of clustered DNA damage generates additional double-strand breaks in mammalian cells post-irradiation. Nucleic Acids Res 2004, 32:1602-1609.
64. Anderson J.A., Harper J.V., Cucinotta F.A., et al. Participation of DNA-PKcs in DSB repair after exposure to high- and low-LET radiation. Radiat Res 2010, 174:195-205.
65. Harper J.V., Anderson J.A., O'Neill P. Radiation induced DNA DSBs: contribution from stalled replication forks?. DNA Repair (Amst) 2010, 9:907-913.
66. Groth P., Orta M.L., Elvers I., et al. Homologous recombination repairs secondary replication induced DNA double-strand breaks after ionizing radiation. Nucleic Acids Res 2012, 40:6585-6594.
67. Arnaudeau C., Lundin C., Helleday T. DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. JMol Biol 2001, 307:1235-1245.
68. Hair J.M., Terzoudi G.I., Hatzi V.I., et al. BRCA1 role in the mitigation of radiotoxicity and chromosomal instability through repair of clustered DNA lesions. Chem Biol Interact 2010, 188:350-358.
69. Bryant H.E., Schultz N., Thomas H.D., et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
70. Farmer H., McCabe N., Lord C.J., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
71. Thomlinson R.H., Gray L.H. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br J Cancer 1955, 9:539-549.
72. Nordsmark M., Bentzen S.M., Rudat V., et al. Prognostic value of tumor oxygenation in 397 head and neck tumors after primary radiation therapy. An international multi-center study. Radiother Oncol 2005, 77:18-24.
73. Wardman P. The mechanism of radiosensitization by electron-affinic compounds. Int J Radiat Phys Chem 1987, 30:423-432.
74. Wardman P. Chemical radiosensitizers for use in radiotherapy. Clin Oncol 2007, 19:397-417.
75. Overgaard J., Eriksen J.G., Nordsmark M., et al. Plasma osteopontin, hypoxia, and response to the hypoxia sensitiser nimorazole in radiotherapy of head and neck cancer: results from the DAHANCA 5 randomised double-blind placebo-controlled trial. Lancet Oncol 2005, 6:757-764.
76. Dobrowsky W., Huigol N.G., Jayatilake R.S., et al. AK-2123 (Sanazol) as a radiation sensitizer in the treatment of stage III cervical cancer: results of an IAEA multicentre randomised trial. Radiother Oncol 2007, 82:24-29.
77. Howard Flanders P. Effect of nitric oxide on the radiosensitivity of bacteria. Nature 1957, 180:1191-1192.
78. Oronsky B.T., Knox S.J., Scicinski J.J. Is nitric oxide (NO) the last word in radiosensitization? A review. Transl Oncol 2012, 5:66-71.
79. Wardman P., Rothkamm K., Folkes L.K., et al. Radiosensitization by nitric oxide at low radiation doses. Radiat Res 2007, 167:475-484.
80. Stewart G.D., Nandi J., Katz E., et al. DNA strand breaks and hypoxia response inhibition mediate the radiosensitisation effect of nitric oxide donors on prostate cancer under varying oxygen concentrations. Biochem Pharmacol 2011, 81:203-210.
81. Folkes L.K., O'Neill P. Modification of DNA damage mechanisms by nitric oxide during ionizing radiation. Free Radic Biol Med 2013, 58:14-25.
82. Folkes L.K., O'Neill P. DNA damage induced by nitric oxide during ionizing radiation is enhanced at replication. Nitric Oxide 2013, Apr 26. pii: S1089-8603(13)00132-8. http://dx.doi.org/10.1016/j.niox.2013.04.005. [Epub ahead of print].
83. Bamatraf M.M.M., O'Neill P., Rao B.S.M. Redox dependence of the rate of interaction of hydroxyl radical adducts of DNA nucleobases with oxidants: consequences for DNA strand breakage. JAm Chem Soc 1998, 120:11852-11857.
84. Das P., Sutherland B.M. Processing of abasic DNA clusters in hApeI-silenced primary fibroblasts exposed to low doses of X-irradiation. JBiosci 2011, 36:105-116.
85. Panda H., Jaiswal A.S., Corsino P.E., et al. Amino acid Asp181 of 5'-flap endonuclease 1 is a useful target for chemotherapeutic development. Biochemistry 2009, 48:9952-9958.
86. Mitchell J.B., Wink D.A., deGraff W., et al. Hypoxic mammalian cell radiosensitization by nitric oxide. Cancer Res 1993, 53:5845-5848.
87. Gao X., Saha D., Kapur P., et al. Radiosensitization of HT-29 cells and xenografts by the nitric oxide donor DETANONOate. JSurg Oncol 2009, 100:149-158.
88. Frérart F., Sonveaux P., Rath G., et al. The acidic tumor microenvironment promotes the reconversion of nitrite into nitric oxide: towards a new and safe radiosensitizing strategy. Clin Can Res 2008, 14:2768-2774.
89. Ning S., Bednaarski M., Oronsky B., et al. Dinitroazetidines are a novel class of anticancer agents and hypoxia-activated radiation sensitizers developed from highly energetic materials. Cancer Res 2012, 72:2600-2608.
90. Jordan B.F., Sonveaux P., Feron O., et al. Nitric oxide as a radiosensitizer: evidence for an intrinsic role in addition to its effect on oxygen delivery and consumption. Int J Cancer 2004, 109:768-773.
91. Jiang H., Ridder M.D., Verovski V.N., et al. Activated macrophages as a novel determinant of tumor cell radioresponse: the role of nitric oxide-mediated inhibition of cellular respiration and oxygen sparing. Int J Oncol Biol Phys 2010, 76:1520-1527.
92. Denny W.A., Wilson W.R., Hay M.P. Recent developments in the design of bioreductive drugs. Br J Cancer 1996, 74(Suppl. XXVII):S32-S38.
93. Weiss G.J., Infante J.R., Chiorean E.G., et al. Phase I study of the safety, tolerability, and pharmacokinetics of TH-302, a hypoxia-activated prodrug, in patients with advanced solid malignancies. Cancer Ther: Clinical 2011, 17:2997-3004.
94. Sharma K., Iyer A., Sengupta K., et al. INDQ/NO, a bioreductively activated nitric oxide prodrug. Org Lett 2013, 15:2636-2639.