The role of DNA single- and double-strand breaks in cell killing by ionizing radiation

Radiation Research

Volumn 150, Issue 5 SUPPL., 1998, Pages

  Olive, Peggy L ^a  

^a BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; SINGLE STRANDED DNA;

ARTICLE; BASE MISPAIRING; CELL KILLING; CELL SURVIVAL; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CHROMOSOME DAMAGE; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; IONIZING RADIATION; PRIORITY JOURNAL; RADIATION RESPONSE; RADIOSENSITIVITY;

EID: 0031742958     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.2307/3579807     Document Type: Article

References (87)

1. R. A. McGrath and R. W. Williams, Reconstruction in vivo of irradiated Escherichia coli deoxyribonucleic acid: the rejoining of broken pieces. Nature 212, 534-535 (1966).
2. G. P. van der Schans, M. C. Paterson and W. G. Cross, DNA strand break and rejoining in cultured human fibroblasts exposed to fast neutrons or gamma rays. Int. J. Radiat. Biol. 44, 75-85 (1983).
3. A. J. Fornace and J. B. Little, Normal repair of DNA single-strand breaks in patients with ataxia telangiectasia. Biochim. Biophys. Acta 607, 432-437 (1980).
4. A. J. Ward, P. L. Olive, A. H. Burr and M. P. Rosin, Response of fibroblast cultures from ataxia-telangiectasia patients to reactive oxygen species generated during inflammatory reactions. Environ. Mol. Mutagen. 24, 103-111 (1994).
5. J. Thacker and A. N. Ganesh, DNA break repair, radioresistance of DNA synthesis, and camptothecin sensitivity in the radiation-sensitive irs mutants: comparisons to ataxia-telangiectasia cells. Mutat. Res. 235, 49-58 (1990).
6. E. Dikomey, J. Dahm-Daphi, I. Brammer, R. Martensen and B. Kaina, Correlation between cellular radiosensitivity and non-repaired double-strand breaks studied in nine mammalian cell lines. Int. J. Radiat. Biol. 73, 269-278 (1998).
7. J. S. Bedford and M. N. Cornforth, Relationship between the recovery from sublethal X-ray damage and the rejoining of chromosome breaks in normal human fibroblasts. Radiat. Res. 111, 406-423 (1987).
8. Y. Shibamoto, T. Shibata, S. Miyatake, Y. Oda, T. Manabe, G. Ohshio, K. Yagi, C. Streffer, M. Takahashi and M. Abe, Assessment of the proliferative activity and radiosensitivity of human tumours using the cytokinesis-block micronucleus assay. Br. J. Cancer 70, 67-71 (1994).
9. J. Thacker, The use of integrating DNA vectors to analyse the molecular defects in ionizing radiation-sensitive mutants of mammalian cells including ataxia-telangiectasia. Mutat. Res. 220, 187-204 (1989).
10. M. P. Fairman, A. P. Johnson and J. Thacker, Multiple components are involved in the efficient joining of double stranded DNA in human cell extracts. Nucleic Acids Res. 25, 4145-4152 (1992).
11. T. Ganguly and G. Iliakis, A cell-free assay using cytoplasmic cell extracts to study rejoining of radiation-induced DNA double-strand breaks in human cell nuclei. Int. J. Radiat. Biol. 68, 447-457 (1995).
12. S. N. Powell and T. J. McMillan, The repair fidelity of restriction enzyme-induced double strand breaks in plasmid DNA correlates with radioresistance in human tumor cell lines. Int. J. Radiat. Oncol. Biol. Phys. 29, 1035-1040 (1994).
13. J. Smith-Ravin and P. A. Jeggo, Use of damaged plasmid to study DNA repair in X-ray sensitive (xrs) strains of Chinese hamster ovary (CHO) cells. Int. J. Radiat. Biol. 56, 951-961 (1989).
14. M. Löbrich, S. Ikpeme and J. Kiefer, 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. 65, 623-630 (1994).
15. M. Löbrich, B. Rydberg and P. K. Cooper, 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 92, 12050-12054 (1995).
16. A. Sak and M. Stuschke, Repair of ionizing radiation induced DNA double-strand breaks (dsb) at the c-myc locus in comparison to the overall genome. Int. J. Radiat. Biol. 73, 35-43 (1998).
17. J. F. Ward, Some biochemical consequences of the spatial distribution of ionizing radiation-produced free radicals. Radiat. Res. 86, 185-195 (1981).
18. B. Rydberg, M. Löbrich and P. K. Cooper, DNA double-strand breaks induced by high energy neon and iron ions in human fibroblasts. I. Pulsed-field gel electrophoresis method. Radiat. Res. 139, 133-141 (1994).
19. J. F. Ward, DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and repairability. Prog. Nucleic Acid Res. 35, 95-124 (1988).
20. B. Rydberg, Clusters of DNA damage induced by ionizing radiation: Formation of short DNA fragments. II. Experimental detection. Radiat. Res. 145, 200-209 (1996).
21. M. Löbrich, P. K. Cooper and B. Rydberg, Non-random distribution of DNA double-strand breaks induced by particle irradiation. Int. J. Radiat. Biol. 70, 493-503 (1996).
22. W. R. Holley and A. Chatterjee, Clusters of DNA damage induced by ionizing radiation: Formation of short DNA fragments. I. Theoretical modeling. Radiat. Res. 145, 188-199 (1996).
23. P. J. Johnston and P. E. Bryant, A component of DNA double-strand break repair is dependent on the spatial orientation of the lesions within the high-order structures of chromatin. Int. J. Radiat. Biol. 66, 531-536 (1994).
24. P. J. Johnston, S. H. MacPhail, T. D. Stamato, C. U. Kirchgessner and P. L. Olive, Higher-order chromatin structure-dependent repair of DNA double-strand breaks: Involvement of the V(D)J recombination double-strand break repair pathway. Radiat. Res. 149, 455-462 (1998).
25. P. L. Olive, J. Hilton and R. E. Durand, DNA conformation of Chinese hamster V79 cells and sensitivity to ionizing radiation. Radiat. Res. 107, 115-124 (1986).
26. M. Flentje, B. Asadpour, D. Latz and K. J. Weber, Sensitivity of neutral filter elution but not PFGE can be modified by non-dsb chromatin damage. Int. J. Radiat. Biol. 63, 715-724 (1993).
27. J. L. Schwartz and A. T. M. Vaughan, DNA-nuclear matrix interactions and ionizing radiation sensitivity. Environ. Mol. Mutagen. 22, 231-233 (1993).
28. P. L. Olive, S. Vanderbyl and S. H. MacPhail, Resistance to DNA denaturation in irradiated Chinese hamster V79 fibroblasts is linked to cell shape. Exp. Cell Res. 193, 330-345 (1991).
29. J. L. Schwartz and A. T. M. Vaughan, Association between DNA/chromosome break rejoining rates, chromatin structure alterations and radiation sensitivity in human tumor cell lines. Cancer Res. 49, 5054-5057 (1989).
30. T. H. Lynch, P. Anderson, D. M. Wallace, G. M. Kondratowicz, R. P. Beaney and A. T. M. Vaughan, A correlation between nuclear supercoiling and the response of patients with bladder cancer to radiotherapy. Br. J. Cancer 64, 867-871 (1991).
31. R. S. Malyapa, W. D. Wright and J. L. Roti Roti, DNA supercoiling changes and nucleoid protein composition in a group of L5178Y cells of varying radiosensitivity. Radiat. Res. 145, 239-242 (1996).
32. R. L. Warters and B. W. Lyons, Detection of ionizing radiation-induced DNA double-strand breaks by filter elution is affected by nuclear chromatin structure. Radiat. Res. 124, 309-316 (1990).
33. D. Wlodek and P. L. Olive, Basis for detecting DNA double-strand breaks using neutral filter elution. Radiat. Res. 124, 326-333 (1990).
34. A. J. Giaccia, J. Schwartz, J. Shieh and J. M. Brown, The use of asymmetric-field inversion gel electrophoresis to predict tumor cell radiosensitivity. Radiother. Oncol. 24, 231-238 (1992).
35. P. L. Olive, S. H. MacPhail and J. P. Banáth, Lack of correlation between DNA double-strand break induction/rejoining and radiosensitivity in six human tumor cell lines. Cancer Res. 54, 3939-3946 (1994).
36. M. Ronne, A. O. Gyldenholm and C. O. Storm, Minibands and chromosome structure. A theory. Anticancer Res. 15, 249-254 (1995).
37. I. R. Radford, The level of induced DNA double-strand breakage correlates with cell killing after X-irradiation. Int. J. Radiat. Biol. 48, 45-54 (1985).
38. L. R. Kelland, S. M. Edwards and G. G. Steel, Induction and rejoining of DNA double-strand breaks in human cervix carcinoma cell lines of differing radiosensitivity. Radiat. Res. 116, 526-538 (1988).
39. T. J. McMillan, A. M. Cassoni, S. Edwards, A. Holmes and J. H. Peacock, The relationship of DNA double-strand break induction to radiosensitivity in human tumour cell lines. Int. J. Radiat. Biol. 58, 427-438 (1990).
40. K. W. Kohn, Principles and practice of DNA filter elution. Pharmacol. Ther. 49, 55-77 (1991).
41. S. C. vanAnkeren, D. Murray and R. E. Meyn. Induction and rejoining of gamma-ray-induced DNA single- and double-strand breaks in Chinese hamster AA8 cells and in two radiosensitive clones. Radiat. Res. 116, 511-525 (1988).
42. J. H. van Touw, J. B. Verberne, J. Retèl and H. Loman, Radiation-induced strand breaks in φX174 replicative form DNA: an improved experimental and theoretical approach. Int. J. Radiat. Biol. 48, 567-578 (1985).
43. G. P. van der Schans, 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. 33, 105-120 (1978).
44. B. S. Kaur and E. R. Blazek, Subdenaturing (pH 11.1) filter elution: More sensitive quantification of DNA double-strand breaks. Radiat. Res. 147, 569-578 (1997).
45. R. Okayasu and G. Iliakis, Linear DNA elution dose response curves obtained in CHO cells with non-unwinding filter elution after appropriate selection of the lysis conditions. Int. J. Radiat. Biol. 55, 569-581 (1989).
46. G. Iliakis, D. Blöcher, L. Metzger and G. Pantelias, Comparison of DNA double-strand break rejoining as measured by pulsed field gel electrophoresis, neutral sucrose gradient centrifugation, and non-unwinding filter elution in irradiated plateau-phase CHO cells. Int. J. Radiat. Biol. 59, 927-939 (1991).
47. K. T. Wheeler and J. V. Wierowski, DNA repair kinetics in irradiated undifferentiated and terminally differentiated cells. Radiat. Environ. Biophys. 22, 3-19 (1983).
48. D. Blöcher and W. Pohlit, DNA double-strand breaks in Ehrlich ascites tumour cells at low doses of X-rays. II. Can cell death be attributed to double-strand breaks? Int. J. Radiat. Biol. 42, 329-338 (1982).
49. S. A. Leadon and P. K. Cooper, Preferential repair of ionizing radiation-induced damage in the transcribed strand of an active human gene is defective in Cockayne syndrome. Proc. Natl. Acad. Sci. USA 90, 10499-10503 (1993).
50. J. L. Schwartz, J. Rotmensch, S. Giovanazzi, M. B. Cohen and R. R. Weichselbaum, Faster repair of DNA double-strand breaks in radioresistant human tumor cells. Int. J. Radiat. Oncol. Biol. Phys. 15, 907-912 (1988).
51. J. L. Schwartz, R. Mustafi, M. A. Beckett and R. R. Weichselbaum, DNA double-strand break rejoining rates, inherent radiation sensitivity and human tumour response to radiotherapy. Br. J. Cancer 74, 37-42 (1996).
52. N. Zaffaroni, L. Orlandi, R. Villa, A. Bearzatto, E. K. Rofstad and R. Silvestrini, DNA double-strand break repair and radiation response in human tumour primary cultures. Int. J. Radiat. Biol. 66, 279-285 (1994).
53. M. Frankenberg-Schwager, Review of repair kinetics for DNA damage induced in eukaryotic cells in vitro by ionizing radiation. Radiother. Oncol. 14, 307-320 (1989).
54. B. Cedervall, P. Kallman and W. C. Dewey, Repair of DNA double-strand breaks: Errors encountered in the determination of half-life times in pulsed-field gel electrophoresis and neutral filter elution. Radiat. Res. 142, 23-28 (1995).
55. H. Zheng and P. L. Olive, Influence of oxygen on radiation-induced DNA damage and repair in testicular cells of C3H mice. Int. J. Radiat. Biol. 71, 275-282 (1997).
56. K. M. Wilson and P. C. Keng, Radiation-induced DNA damage and repair in quiescent and proliferating human tumor cells in vitro. Int. J. Radiat. Biol. 55, 385-395 (1989).
57. J. P. Banath, M. Fushiki and P. L. Olive, Rejoining of DNA single- and double-strand breaks in human white blood cells exposed to ionizing radiation. Int. J. Radiat. Biol. 73, 649-660 (1998).
58. S. Tashiro, N. Kotomura, A. Shinohara, K. Tanaka, K. Ueda and N. Kamada, S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene 12, 2165-2170 (1996).
59. P. E. Bryant and D. Blöcher, Measurement of the kinetics of DNA double-strand break repair in Ehrlich ascites tumour cells using the unwinding method. Int. J. Radiat. Biol. 38, 335-347 (1980).
60. E. Dikomey and J. Lorenzen, Saturated repair of DNA strand breaks in CHO cells after X-irradiation with doses ranging from 3 to 90 Gy. Int. J. Radiat. Biol. 64, 659-667 (1993).
61. C. Fohe and E. Dikomey, Induction and repair of DNA base damage studied in X-irradiated CHO cells using the M. luteus extract. Int. J. Radiat. Biol. 66, 697-704 (1994).
62. P. L. Olive and J. P. Banath, Induction and rejoining of radiation-induced DNA single-strand breaks: "Tail moment" as a function of position in the cell cycle. Mutat. Res. 294, 275-283 (1993).
63. E. Dikomey and J. Franzke, Three classes of DNA strand breaks induced by X-irradiation and internal beta rays. Int. J. Radiat. Biol. 50, 893-908 (1986).
64. P. J. Johnston and P. E. Bryant, Lack of interference of DNA single-strand breaks with the measurement of double-strand breaks in mammalian cells using the neutral filter elution assay. Nucleic Acids Res. 19, 2735-2738 (1991).
65. N. J. Kleiman, R. R. Wang and A. Spector, Hydrogen peroxide-induced DNA damage in bovine lens epithelial cells. Mutat. Res. 240, 35-45 (1990).
66. P. L. Olive and P. J. Johnston, DNA damage from oxidants: Lesion complexity and chromatin organization. Oncol. Res. 9, 287-294 (1997).
67. Q. Hu and R. P. Hill, Radiosensitivity, apoptosis and repair of DNA double-strand breaks in radiation-sensitive Chinese hamster ovary cell mutants treated at different dose rates. Radiat. Res. 146, 636-645 (1996).
68. N. Foray, A. Priestley, G. Alsbeih, C. Badie, E. P. Capulas, C. F. Arlett and E. P. Malaise, Hypersensitivity of ataxia telangiectasia fibroblasts to ionizing radiation is associated with a repair deficiency of DNA double-strand breaks. Int. J. Radiat. Biol. 72, 271-283 (1997).
69. R. Wurm, N. G. Burnet, N. Duggal, J. R. Yarnold and J. H. Peacock, Cellular radiosensitivity and DNA damage in primary human fibroblasts. Int. J. Radiat. Oncol. Biol. Phys. 30, 625-633 (1994).
70. M. A. Ritter, J. E. Cleaver and C. A. Tobias, High LET radiations induce a large proportion of non-rejoining DNA breaks. Nature 266, 653-655 (1977).
71. P. L. Olive, J. P. Banáth and C. D. Fjell, DNA strand breakage and DNA structure influence staining with propidium iodide using the alkaline comet assay. Cytometry 16, 305-312 (1994).
72. P. L. Olive and R. E. Durand, Apoptosis: an indicator of radiosensitivity in vitro? Int. J. Radiat. Biol. 71, 695-707 (1997). [special supplement in honor of Tikvah Alper]
73. J. L. Schwartz, R. Jordan, B. A. Sedita, M. J. Swenningson, J. P. Banath and P. L. Olive, Different sensitivity to cell killing and chromosome mutation induction by gamma rays in two human lymphoblastoid cell lines derived from a single donor: possible role of apoptosis. Mutagenesis 10, 227-233 (1995).
74. F. Xia, X. Wang, Y. H. Wang, N. M. Tsang, D. W. Yandell, K. T. Kelsey and H. L. Liber, Altered p53 status correlates with differences in sensitivity to radiation-induced mutation and apoptosis in two closely related human lymphoblast lines. Cancer Res. 55, 12-15 (1995).
75. J. A. Fritzell, L. Narayanan, S. M. Baker, C. E. Bronner, S. E. Andrew, T. A. Prolla, A. Bradley, F. R. Jirik, R. M. Liskay and P. M. Glazer, Role of DNA mismatch repair in the cytotoxicity of ionizing radiation. Cancer Res. 57, 5143-5147 (1997).
76. J. S. Murley and D. J. Grdina, The effects of cycloheximide and WR-1065 on radiation-induced repair processes: a mechanism for chemoprevention. Carcinogenesis 16, 2699-2705 (1994).
77. J. M. Vos and P. C. Hanawalt, Processing of psoralen adducts in an active human gene: repair and replication of DNA containing monoadducts and interstrand cross-links. Cell 50, 789-799 (1987).
78. W. C. Dempke, S. A. Shellard, L. K. Hosking, A. M. Fichtinger-Schepman and B. T. Hille, Mechanisms associated with the expression of cisplatin resistance in a human ovarian tumor cell line following exposure to fractionated X-irradiation in vitro. Carcinogenesis 13, 1209-1215 (1992).
79. T. J. McMillan, Residual DNA damage: What is left over and how does this determine cell fate? Eur. J. Cancer 28, 267-269 (1992).
80. A. Sancar, DNA repair in humans. Annu. Rev. Genet. 20, 69-105 (1995).
81. S. P. Jackson, The recognition of DNA damage. Curr. Opin. Genet. Dev. 6, 19-25 (1996).
82. P. L. Olive, The DNA precipitation assay: A rapid and simple method for detecting DNA damage in mammalian cells. Environ. Mol. Mutagen. 11, 487-495 (1988).
83. P. E. Bryant, R. Warring and G. Ahnstrom, DNA repair kinetics after low doses of X-rays. A comparison of results obtained by the unwinding and nucleoid sedimentation methods. Mutat. Res. 131, 19-26 (1984).
84. Y. C. Taylor, P. G. Duncan, X. Zhang and W. D. Wright, Differences in the DNA supercoiling response of irradiated cell lines from ataxia-telangiectasia versus unaffected individuals. Int. J. Radiat. Biol. 59, 359-371 (1991).
85. D. Wlodek and P. L. Olive, Chromatin structure influence on DNA damage measurements by four assays: Pulsed- and constant-field gel electrophoresis, DNA precipitation and non-denaturing filter elution. Nukleonika 41, 23-34 (1996).
86. T. Stamato, S. Guerriero and N. Denko, Two methods for assaying DNA double-strand break repair in mammalian cells by asymmetric field inversion gel electrophoresis. Radiat. Res. 133, 60-66 (1993).
87. M. I. Nunez, M. Villalobos, N. Olea, M. T. Valenzuela, V. Pedraza, T. J. McMillan and J. M. Ruiz de Almodovar, Radiation-induced DNA double-strand break rejoining in human tumor cells. Br. J. Cancer 71, 311-316 (1995).