The shape of the radiation dose response for DNA double-strand break induction and repair

Genome Integrity

Volumn 4, Issue 1, 2013, Pages

  Barnard, Stephen ^a   Bouffler, Simon ^a   Rothkamm, Kai ^a  

^a PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

DNA double strand break; Dose response; Gamma H2AX; Ionising radiation; Low dose; Pulsed field gel electrophoresis

Indexed keywords

DNA DETERMINATION; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENE LOCUS; GENOTOXICITY; HUMAN; IONIZING RADIATION; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; RADIATION DOSE DISTRIBUTION; RADIATION INJURY; RADIATION RESPONSE; REVIEW;

EID: 84875904745     PISSN: None     EISSN: 20419414     Source Type: Journal    
DOI: 10.1186/2041-9414-4-1     Document Type: Review

References (71)

1. Mullenders L, Atkinson M, Paretzke H, Sabatier L, Bouffler S. Assessing cancer risks of low-dose radiation. Nat Rev Cancer 2009, 9:596-604. 10.1038/nrc2677, 19629073.
2. Little MP, Wakeford R, Tawn EJ, Bouffler SD, Berrington de Gonzalez A. Risks associated with low doses and low dose rates of ionizing radiation: why linearity may be (almost) the best we can do. Radiology 2009, 251:6-12. 10.1148/radiol.2511081686, 2663578, 19332841.
3. Pearce MS, Salotti JA, Little MP, McHugh K, Lee C, Kim KP, Howe NL, Ronckers CM, Rajaraman P, Sir Craft AW, Parker L, Berrington de Gonzalez A. Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet 2012, 380:499-505. 10.1016/S0140-6736(12)60815-0, 3418594, 22681860.
4. Kendall GM, Little MP, Wakeford R, Bunch KJ, Miles JCH, Vincent TJ, Meara JR, Murphy MFG. A record-based case-control study of natural background radiation and the incidence of childhood leukaemia and other cancers in Great Britain during 1980-2006. Leukemia 2013, 27:3-9. 10.1038/leu.2012.151, 22766784.
5. Little MP, Azizova TV, Bazyka D, Bouffler SD, Cardis E, Chekin S, Chumak VV, Cucinotta FA, de Vathaire F, Hall P, Harrison JD, Hildebrandt G, Ivanov V, Kashcheev VV, Klymenko SV, Kreuzer M, Laurent O, Ozasa K, Schneider T, Tapio S, Taylor AM, Tzoulaki I, Vandoolaeghe WL, Wakeford R, Zablotska LB, Zhang W, Lipshultz SE. Systematic Review and Meta-analysis of Circulatory Disease from Exposure to Low-Level Ionizing Radiation and Estimates of Potential Population Mortality Risks. Environ Health Perspect 2012, 120:1503-1511. 10.1289/ehp.1204982, 3556625, 22728254.
6. Pernot E, Hall J, Baatout S, Benotmane MA, Blanchardon E, Bouffler S, El Saghire H, Gomolka M, Guertler A, Harms-Ringdahl M, Jeggo P, Kreuzer M, Laurier D, Lindholm C, Mkacher R, Quintens R, Rothkamm K, Sabatier L, Tapio S, de Vathaire F, Cardis E. Ionizing radiation biomarkers for potential use in epidemiological studies. Mutat Res 2012, 751:258-286. 10.1016/j.mrrev.2012.05.003, 22677531.
7. Cadet J, Ravanat J, Tavernaporro M, Menoni H, Angelov D. Oxidatively generated complex DNA damage: Tandem and clustered lesions. Cancer Lett 2012, 327:5-15. 10.1016/j.canlet.2012.04.005, 22542631.
8. Eccles LJ, O'Neill P, Lomax ME. Delayed repair of radiation induced clustered DNA damage: friend or foe?. Mutat Res 2011, 711:134-141. 10.1016/j.mrfmmm.2010.11.003, 3112496, 21130102.
9. Ward JF. DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability. Prog Nucleic Acid Res Mol Biol 1988, 35:95-125.
10. Thompson LH. Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutat Res 2012, 751:158-246. 10.1016/j.mrrev.2012.06.002, 22743550.
11. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell 2010, 40:179-204. 10.1016/j.molcel.2010.09.019, 2988877, 20965415.
12. Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 2011, 25:409-433. 10.1101/gad.2021311, 3049283, 21363960.
13. Giglia-Mari G, Zotter A, Vermeulen W. DNA damage response. Cold Spring Harb Perspect Biol 2011, 3:a000745. 10.1101/cshperspect.a000745, 3003462, 20980439.
14. Asaithamby A, Chen DJ. Mechanism of cluster DNA damage repair in response to high-atomic number and energy particles radiation. Mutat Res 2011, 711:87-99. 10.1016/j.mrfmmm.2010.11.002, 3318975, 21126526.
15. Milligan JR, Ng JY, Wu CC, Aguilera JA, Fahey RC, Ward JF. DNA repair by thiols in air shows two radicals make a double-strand break. Radiat Res 1995, 143:273-280. 10.2307/3579213, 7652164.
16. Peoples AR, Mercer KR, Bernhard WA. What fraction of DNA double-strand breaks produced by the direct effect is accounted for by radical pairs?. J Phys Chem B 2010, 114:9283-9288. 10.1021/jp103362z, 2914509, 20583765.
17. Dahm-Daphi J, Sass C, Alberti W. Comparison of biological effects of DNA damage induced by ionizing radiation and hydrogen peroxide in CHO cells. Int J Radiat Biol 2000, 76:67-75. 10.1080/095530000139023, 10665959.
18. Löbrich M, Rydberg B, Cooper P. Repair of x-ray-induced DNA double-strand breaks in specific Not I restriction fragments in human fibroblasts: joining of correct and incorrect ends. Proc Natl Acad Sci USA 1995, 92:12050-12054. 10.1073/pnas.92.26.12050, 40294, 8618842.
19. Balagurumoorthy P, Adelstein SJ, Kassis AI. Novel method for quantifying radiation-induced single-strand-break yields in plasmid DNA highlights 10-fold discrepancy. Anal Biochem 2011, 417:242-246. 10.1016/j.ab.2011.06.023, 3184882, 21741945.
20. Gradzka I, Iwanenko T. A non-radioactive, PFGE-based assay for low levels of DNA double-strand breaks in mammalian cells. DNA Repair (Amst) 2005, 4:1129-1139.
21. Costes SV, Chiolo I, Pluth JM, Barcellos-Hoff MH, Jakob B. Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutat Res 2010, 704:78-87. 10.1016/j.mrrev.2009.12.006, 20060491.
22. Bekker-Jensen S, Mailand N. Assembly and function of DNA double-strand break repair foci in mammalian cells. DNA Repair 2010, 9:1219-1228. 10.1016/j.dnarep.2010.09.010, 21035408.
23. Feuerhahn S, Egly J. Tools to study DNA repair: what's in the box?. Trends Genet 2008, 24:467-474. 10.1016/j.tig.2008.07.003, 18675488.
24. Rothkamm K, Horn S. Gamma-H2AX as protein biomarker for radiation exposure. Ann Ist Super Sanita 2009, 45:265-271.
25. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998, 273:5858-5868. 10.1074/jbc.273.10.5858, 9488723.
26. Mah L, Orlowski C, Ververis K, El-Osta A, Karagiannis TC. Utility of gammaH2AX as a molecular marker of DNA double-strand breaks in nuclear medicine: applications to radionuclide therapy employing auger electron-emitting isotopes. Curr Radiopharm 2011, 4:59-67. 10.2174/1874471011104010059, 22191615.
27. So S, Davis AJ, Chen DJ. Autophosphorylation at serine 1981 stabilizes ATM at DNA damage sites. J Cell Biol 2009, 187:977-990. 10.1083/jcb.200906064, 2806275, 20026654.
28. Noon AT, Goodarzi AA. 53BP1-mediated DNA double strand break repair: insert bad pun here. DNA Repair 2011, 10:1071-1076. 10.1016/j.dnarep.2011.07.012, 21868291.
29. Neumaier T, Swenson J, Pham C, Polyzos A, Lo AT, Yang P, Dyball J, Asaithamby A, Chen DJ, Bissell MJ, Thalhammer S, Costes SV. Evidence for formation of DNA repair centers and dose-response nonlinearity in human cells. Proc Natl Acad Sci USA 2012, 109:443-448. 10.1073/pnas.1117849108, 3258602, 22184222.
30. Asaithamby A, Chen DJ. Cellular responses to DNA double-strand breaks after low-dose gamma-irradiation. Nucleic Acids Res 2009, 37:3912-3923. 10.1093/nar/gkp237, 2709554, 19401436.
31. Ager DD, Dewey WC. Calibration of pulsed field gel electrophoresis for measurement of DNA double-strand breaks. Int J Radiat Biol 1990, 58:249-259. 10.1080/09553009014551601, 1974573.
32. Rothkamm K, Löbrich M. Misrejoining of DNA double-strand breaks in primary and transformed human and rodent cells: a comparison between the HPRT region and other genomic locations. Mutat Res 1999, 433:193-205. 10.1016/S0921-8777(99)00008-7, 10343652.
33. Löbrich M, Ikpeme S, Kiefer J. DNA double-strand break measurement in mammalian cells by pulsed-field gel electrophoresis: an approach using restriction enzymes and gene probing. Int J Radiat Biol 1994, 65:623-630. 10.1080/09553009414550731, 7912711.
34. Löbrich M, Cooper P, Rydberg B. Non-random distribution of DNA double-strand breaks induced by particle irradiation. Int J Radiat Biol 1996, 70:493-503. 10.1080/095530096144680, 8947529.
35. Mateos S, Gordon AT, Steel GG, McMillan TJ. Cell-cycle variation in DNA migration in pulsed-field gel electrophoresis. Int J Radiat Biol 1996, 69:687-693. 10.1080/095530096145427, 8691020.
36. Stenerlöw B, Karlsson KH, Cooper B, Rydberg B. Measurement of prompt DNA double-strand breaks in mammalian cells without including heat-labile sites: results for cells deficient in nonhomologous end joining. Radiat Res 2003, 159:502-510. 10.1667/0033-7587(2003)159[0502:MOPDDS]2.0.CO;2, 12643795.
37. Balart J, Pueyo G, de Llobet LI, Baro M, Sole X, Marin S, Casanovas O, Mesia R, Capella G. The use of caspase inhibitors in pulsed-field gel electrophoresis may improve the estimation of radiation-induced DNA repair and apoptosis. Radiat Oncol 2011, 6:6. 10.1186/1748-717X-6-6, 3025872, 21235815.
38. Rothkamm K, Krüger I, Thompson LH, Löbrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol 2003, 23:5706-5715. 10.1128/MCB.23.16.5706-5715.2003, 166351, 12897142.
39. Wardman P, Rothkamm K, Folkes LK, Woodcock M, Johnston PJ. Radiosensitization by nitric oxide at low radiation doses. Radiat Res 2007, 167:475-484. 10.1667/RR0827.1, 17388699.
40. Bauerschmidt C, Arrichiello C, Burdak-Rothkamm S, Woodcock M, Hill MA, Stevens DL, Rothkamm K. Cohesin promotes the repair of ionizing radiation-induced DNA double-strand breaks in replicated chromatin. Nucleic Acids Res 2010, 38:477-487. 10.1093/nar/gkp976, 2811025, 19906707.
41. Horn S, Barnard S, Rothkamm K. Gamma-H2AX-based dose estimation for whole and partial body radiation exposure. PLoS One 2011, 6:e25113. 10.1371/journal.pone.0025113, 3179476, 21966430.
42. de Feraudy S, Revet I, Bezrookove V, Feeney L, Cleaver JE. A minority of foci or pan-nuclear apoptotic staining of gammaH2AX in the S phase after UV damage contain DNA double-strand breaks. Proc Natl Acad Sci USA 2010, 107:6870-6875. 10.1073/pnas.1002175107, 2872460, 20351298.
43. Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 1992, 103:857-862.
44. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 2004, 86:3993-4003. 10.1529/biophysj.103.038422, 1304300, 15189895.
45. Sedelnikova OA, Nakamura A, Kovalchuk O, Koturbash I, Mitchell SA, Marino SA, Brenner DJ, Bonner WM. DNA double-strand breaks form in bystander cells after microbeam irradiation of three-dimensional human tissue models. Cancer Res 2007, 67:4295-4302. 10.1158/0008-5472.CAN-06-4442, 17483342.
46. Groth P, Orta ML, Elvers I, Majumder MM, Lagerqvist A, Helleday T. Homologous recombination repairs secondary replication induced DNA double-strand breaks after ionizing radiation. Nucleic Acids Res 2012, 40:6585-6594. 10.1093/nar/gks315, 3413124, 22505579.
47. Burdak-Rothkamm S, Short SC, Folkard M, Rothkamm K, Prise KM. ATR-dependent radiation-induced gamma H2AX foci in bystander primary human astrocytes and glioma cells. Oncogene 2007, 26:993-1002. 10.1038/sj.onc.1209863, 16909103.
48. Dickey JS, Baird BJ, Redon CE, Avdoshina V, Palchik G, Wu J, Kondratyev A, Bonner WM, Martin OA. Susceptibility to bystander DNA damage is influenced by replication and transcriptional activity. Nucleic Acids Res 2012, 40:10274-10286. 10.1093/nar/gks795, 3488239, 22941641.
49. Cleaver JE. gammaH2Ax: biomarker of damage or functional participant in DNA repair "all that glitters is not gold!". Photochem Photobiol 2011, 87:1230-1239. 10.1111/j.1751-1097.2011.00995.x, 21883247.
50. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 2000, 275:9390-9395. 10.1074/jbc.275.13.9390, 10734083.
51. Beels L, Bacher K, De Wolf D, Werbrouck J, Thierens H. Gamma-H2AX foci as a biomarker for patient X-ray exposure in pediatric cardiac catheterization: are we underestimating radiation risks?. Circulation 2009, 120:1903-1909. 10.1161/CIRCULATIONAHA.109.880385, 19858412.
52. Beels L, Werbrouck J, Thierens H. Dose response and repair kinetics of gamma-H2AX foci induced by in vitro irradiation of whole blood and T-lymphocytes with X- and gamma-radiation. Int J Radiat Biol 2010, 86:760-768. 10.3109/09553002.2010.484479, 20597840.
53. Iliakis G, Wang H, Perrault AR, Boecker W, Rosidi B, Windhofer F, Wu W, Guan J, Terzoudi G, Pantelias G. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet Genome Res 2004, 104:14-20. 10.1159/000077461, 15162010.
54. Strande NT, Waters CA, Ramsden DA. Resolution of complex ends by Nonhomologous end joining - better to be lucky than good?. Genome Integr 2012, 3:10. 10.1186/2041-9414-3-10, 3547747, 23276302.
55. Cucinotta FA, Pluth JM, Anderson JA, Harper JV, O'Neill P. Biochemical kinetics model of DSB repair and induction of gamma-H2AX foci by non-homologous end joining. Radiat Res 2008, 169:214-222. 10.1667/RR1035.1, 18220463.
56. Goodarzi AA, Jeggo P, Löbrich M. The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair 2010, 9:1273-1282. 10.1016/j.dnarep.2010.09.013, 21036673.
57. Karlsson KH, Radulescu I, Rydberg B, Stenerlow B. Repair of radiation-induced heat-labile sites is independent of DNA-PKcs, XRCC1 and PARP. Radiat Res 2008, 169:506-512. 10.1667/RR1076.1, 18439038.
58. Rothkamm K, Löbrich 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. 10.1073/pnas.0830918100, 154297, 12679524.
59. Rothkamm K, Balroop S, Shekhdar J, Fernie P, Goh V. Leukocyte DNA damage after multi-detector row CT: a quantitative biomarker of low-level radiation exposure. Radiology 2007, 242:244-251. 10.1148/radiol.2421060171, 17185671.
60. Rogakou E, Boon C, Redon C, Bonner W. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 1999, 146:905-916. 10.1083/jcb.146.5.905, 2169482, 10477747.
61. Ojima M, Furutani A, Ban N, Kai M. Persistence of DNA double-strand breaks in normal human cells induced by radiation-induced bystander effect. Radiat Res 2011, 175:90-96. 10.1667/RR2223.1, 21175351.
62. Grudzenski S, Raths A, Conrad S, Rube CE, Löbrich M. Inducible response required for repair of low-dose radiation damage in human fibroblasts. Proc Natl Acad Sci USA 2010, 107:14205-14210. 10.1073/pnas.1002213107, 2922519, 20660770.
63. Shimada M, Nakanishi M. Response to DNA damage: why do we need to focus on protein phosphatases?. Front Oncol 2013, 3:8. 3560363, 23386996.
64. Savage JR. Insight into sites. Mutat Res 1996, 366:81-95. 10.1016/S0165-1110(96)90030-5, 9001576.
65. Savage JR. Cancer. Proximity matters. Science 2000, 290:62-63. 10.1126/science.290.5489.62, 11183150.
66. Savage JR. Interchange and intra-nuclear architecture. Environ Mol Mutagen 1993, 22:234-244. 10.1002/em.2850220410, 8223504.
67. Sachs RK, Chen AM, Brenner DJ. Review: proximity effects in the production of chromosome aberrations by ionizing radiation. Int J Radiat Biol 1997, 71:1-19. 10.1080/095530097144364, 9020958.
68. Rothkamm K, Löbrich M. Misrepair of radiation-induced DNA double-strand breaks and its relevance for tumorigenesis and cancer treatment. Int J Oncol 2002, 21:433-440.
69. Kühne M, Rothkamm K, Löbrich M. Physical and biological parameters affecting DNA double strand break misrejoining in mammalian cells. Radiat Prot Dosimetry 2002, 99:129-132. 10.1093/oxfordjournals.rpd.a006742, 12194264.
70. Hlatky L, Sachs RK, Vazquez M, Cornforth MN. Radiation-induced chromosome aberrations: insights gained from biophysical modeling. BioEssays 2002, 24:714-723. 10.1002/bies.10126, 12210532.
71. Branco MR, Pombo A. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol 2006, 4:e138. 10.1371/journal.pbio.0040138, 1440941, 16623600.