Clustered DNA lesion repair in eukaryotes: Relevance to mutagenesis and cell survival

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 711, Issue 1-2, 2011, Pages 123-133

  Sage, Evelyne ^a,b   Harrison, Lynn ^c  

^a INSTITUT CURIE   (France)

^b CNRS UMR3348   (France)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Clustered DNA lesions; DNA repair; Double strand breaks; Ionizing radiation; Mutation induction

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; XRCC4 PROTEIN;

CELL SURVIVAL; CLUSTERED DNA DAMAGE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; EXCISION REPAIR; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; IONIZING RADIATION; LINEAR ENERGY TRANSFER; MUTAGENESIS; MUTATION RATE; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OXIDATIVE STRESS; POINT MUTATION; PRIORITY JOURNAL; SHORT SURVEY; SINGLE STRANDED DNA BREAK; TUMOR CELL;

ANIMALS; CELL SURVIVAL; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA BREAKS, SINGLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; MAMMALS; MUTAGENESIS; RADIATION, IONIZING; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; MAMMALIA;

EID: 79956225907     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.12.010     Document Type: Short Survey

References (105)

1. Teoule R. Radiation induced DNA damage and its repair. Int. J. Radiat. Biol. 1987, 51:573-589.
2. Ward J.F., Evans J.W., Limoli C.L., Calabro-Jones P.M. Radiation and hydrogen peroxide induced free radical damage to DNA. Cancer 1987, 55:105-112.
3. Ward J.F. DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation and repairability. Prog. Nucleic Acids Mol. Biol. 1988, 35:95-125.
4. Goodhead D.T. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int. J. Radiat. Biol. 1994, 61:7-17.
5. Brenner D.J., Ward J.F. Constraints on energy deposition and target size of multiply damaged sites associated with DNA double-strand breaks. Int. J. Radiat. Biol. 1992, 61:737-748.
6. Muller W.E.G., Zahn R.K. Bleomycin, an antibiotic that removes thymine from double-stranded DNA. Prog. Nucleic Acid Res. Mol. Biol. 1977, 21-57. Academic Press, NY. W.E. Cohn (Ed.).
7. Sausville E.A., Horwitz S.B. A mechanism for the degradation of DNA by bleomycin. Bristol-Meyers Cancer Symposia 1979, 181-205. Academic Press, NY. M. Gordon, S.T. Cooke (Eds.).
8. von Sonntag C.V. The Chemical Basis of Radiation Biology 1987, Taylor & Francis Ltd., UK.
9. Povirk L.F., Houlgrave C.W. Effect of apurinic/apyrimidinic endonucleases and polyamines on DNA treated with bleomycin and neocarzinostatin: specific formation and cleavage of closely opposed lesions in complementary strands. Biochemistry 1988, 27:3850-3857.
10. Povirk L.F. DNA damage and mutagenesis by radiomimetic DNA-cleaving agents: bleomycin, neocarzinostatin and other enediynes. Mutat. Res. 1996, 355:71-89.
11. Olive P.L., Johnston P.J. DNA damage from oxidants: influence of lesion complexity and chromatin organization. Oncol. Res. 1997, 9:287-294.
12. Ward J.F. Radiation mutagenesis: the initial DNA lesions responsible. Radiat. Res. 1995, 142:362-368.
13. Hong I.S., Carter K.N., Sato K., Greenburg M.M. Characterization and mechanism of formation of tandem lesions in DNA by a nucleobase peroxyl radical. J. Am. Chem. Soc. 2007, 129:4089-4098.
14. Box H.C., Patrzyc H.B., Dawidzik J.B., Wallace J.C., Freund H.G., Iijima H., Budzinski E.E. Double base lesions in DNA X-irradiated in the presence or absence of oxygen. Radiat. Res. 2000, 153:442-446.
15. Bourdat A.-G., Douki T., Frelon S., Gasparutto D., Cadet J. Tandem base lesions are generated by hydroxyl radical within isolated DNA in aerated aqueous solution. J. Am. Chem. Soc. 2000, 122:4549-4556.
16. Douki T., Rivière J., Cadet J. DNA tandem lesions containing 8-oxo-7,8-dihydroguanine and formamido residues arise from intramolecular addition of thymine peroxyl radical to guanine. Chem. Res. Toxicol. 2002, 15:445-454.
17. Bergeron F., Auvré F., Radicella J.P., Ravanat J.L. HO radicals induce an unexpected high proportion of tandem base lesions refractory to repair by DNA glycosylases. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:5528-5533.
18. Dawidzik J.B., Patrzyc H.B., Iijima H., Budzinski E.E., Higbee A.J., Cheng H.C., Box H.C. DNA damage measured by liquid chromatography-mass spectrometry in mouse fibroblast cells exposed to oxidative stress. Biochim. Biophys. Acta 2003, 1621:211-217.
19. Box H.C., Budzinski E.E., Dawidzik J., Patrzyc H.B., Freund H.G. A novel double lesion in X-irradiated DNA consists of a strand break and a base modification. Radiat. Res. 2001, 156:215-219.
20. Box H.C., Dawidzik J.B., Budzinski E.E. Free radical-induced double lesions in DNA. Free Radic. Biol. Med. 2001, 31:856-868.
21. Regulus P., Duroux B., Bayle P., Favier A., Cadet J., Ravanat J.L. Oxidation of the sugar moiety of DNA by ionizing radiation or bleomycin could induce the formation of a cluster DNA lesion. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:14032-14037.
22. Nikjoo H., O'Neill P.O., Wilson W.E., Goodhead D.T. Computational approach for determining the spectrum of DNA damage induced by ionizing radiation. Radiat. Res. 2001, 156:577-583.
23. Rydberg B. Clusters of DNA damage induced by ionizing radiation: Formation of short DNA fragments, II. Experimental detection. Radiat. Res. 1996, 145:200-209.
24. Ahnstrom G., Bryant P.E. DNA double-strand breaks generated by the repair of X-ray damage in Chinese hamster cells. Int. J. Radiat. Biol. 1982, 41:671-676.
25. Bonura T., Smith K.C., Kaplan H.S. Enzymatic induction of DNA double-strand breaks in gamma-irradiated E. coli K-12. Proc. Natl. Acad. Sci. U.S.A. 1975, 72:4265-4269.
26. Sutherland B.M., Georgakilas A.G., Bennett P.V., Laval J.C. Sutherland quantifying clustered DNA damage induction and repair by gel electrophoresis, electronic imaging and number average length analysis. Mutat. Res. 2003, 531:93-107.
27. Barnes D.E., Lindahl T. Repair and genetic consequences of endogeneous base damage in mammalian cells. Ann. Rev. Genet. 2004, 38:445-476.
28. Sutherland B.M., Bennett P.V., Sidorkina O., Laval J. Clustered damages and total lesions induced in DNA by ionizing radiation: oxidized bases and strand breaks. Biochemistry 2000, 39:8026-8031.
29. Georgakilas A.G., P V Bennett B.M. Sutherland High efficiency detection of bi-stranded abasic clusters in gamma-irradiated DNA by putrescine. Nucleic Acid Res. 2002, 30:2800-2808.
30. Sutherland B.M., Bennett P.V., Sidorkina O., Laval J. Clustered DNA damages induced in isolated cells and human cells by low doses of ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:103-108.
31. Sutherland B.M., Bennett P.V., Sutherland J.C., Laval J. Clustered DNA damages induced by X-rays in human cells. Radiat. Res. 2002, 157:611-616.
32. Hada M., Sutherland B.M. Spectrum of complex DNA damages depends on the incident radiation. Radiat. Res. 2006, 165:223-230.
33. Campa A., Ballarini F., Belli M., Cherubini R., Dini V., Esposito G., Friedland W., Gerardi S., Molinelli S., Ottolenghi A., Paretzke H., Simone G., Tabocchini M.A. DNA DSB in human cells by charged particles and gamma rays: experimental results and theoretical approaches. Int. J. Radiat. Biol. 2005, 81:841-854.
34. Semenenko V.A., Stewart R.D. A fast Monte Carlo algorithm to simulate the spectrum of DNA damages formed by ionizing radiation. Radiat. Res. 2004, 161:451-457.
35. Semenenko V.A., Stewart R.D. Fast Monte Carlo simulation of DNA damage formed by electrons and light ions. Phys. Med. Biol. 2006, 51:1693-1706.
36. Bennett P.V., Cuomo N.L., Paul S., Tafrov S.T., Sutherland B.M. Endogenous DNA damage clusters in human skin, 3-D model, and cultured cells. Free Radic. Biol. Med. 2005, 39:832-839.
37. Bennett P., Ishchenko A.A., Laval J., Paap B., Sutherland B.M. Endogenous DNA damage clusters in human hematopoietic stem and progenitor cells. Free Radic. Biol. Med. 2008, 45:1352-1359.
38. Gollapalle E., Wang R., Adetolu R., Tsao D., Francisco D., Sigounas G., Georgakilas A.G. Detection of oxidative clustered DNA lesions in X-irradiated mouse skin tissues and human MCF-7 breast cancer cells. Radiat. Res. 2007, 167:207-216.
39. Nowsheen S., Wukovich R.L., Aziz K., Kalogerinis P.T., Richardson C.C., Panayiotidis M.I., Bonner W.M., Sedelnikova O.A., Georgakilas A.G. Accumulation of oxidatively induced clustered DNA lesions in human tumor tissues. Mutat. Res./Genet. Toxicol. Environ. Mutagen. 2009, 674:131-136.
40. Redon C.E., Dickey J.S., Nakamura A.J., Kareva I.G., Naf D., Nowsheen S., Kryston T.B., Bonner W.M., Gerorgakilas A.G., Sedelnikova O.A. Tumors induce complex DNA damage in distant proliferative tissues in vivo. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17992-17997.
41. Blaisdell J.O., Wallace S.S. Abortive base-excision repair of radiation-induced clustered DNA lesions in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:7426-7430.
42. Yang N., Galick H., Wallace S.S. Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks. DNA Repair 2004, 3:1323-1334.
43. Yang N., Chaudhry M.A., Wallace S.S. Base excision repair by hNTH1 and hOGG1: a two edged sword in the processing of DNA damage in γ-irradiated human cells. DNA Repair 2006, 5:43-51.
44. Holt S.M., Georgakilas A.G. Detection of complex DNA damage in gamma-irradiated acute lymphoblastic leukemia pre-B NALM-6 cells. Radiat. Res. 2007, 168:527-534.
45. Malyarchuk S., Youngblood R., Landry A.M., Quillin E., Harrison L. The mutation frequency of 8-oxo-7,8-dihydroguanine (8-oxodG) situated in a multiply damaged site: comparison of a single and two closely opposed 8-oxodG in Escherichia coli. DNA Repair 2003, 2:695-705.
46. Malyarchuk S., Brame K.L., Youngblood R., Shi R., Harrison L. 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.
47. Pearson C.G., Shikazono N., Thacker J., O'Neill P. Enhanced mutagenic potential of 8-oxo-7,8-dihydroguanine when present within a clustered DNA damage site. Nucleic Acids Res. 2004, 32:263-270.
48. Shikazono N., Pearson C., O'Neill P., Thacker J. The roles of specific glycosylases in determining the mutagenic consequences of clustered DNA base damage. Nucleic Acids Res. 2006, 34:3722-3730.
49. Budworth H., Dianov G.L. Mode of inhibition of short-patch base excision repair by thymine glycol within clustered DNA lesions. J. Biol. Chem. 2003, 278:9378-9381.
50. 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.
51. Budworth H., Matthewman G., O'Neill P., Dianov G.L. Repair of tandem base lesions in DNA by human cell extracts generates persisting single-strand breaks. J. Mol. Biol. 2005, 351:1020-1029.
52. Eot-Houillier G., Eon-Marchais S., Gasparutto D., Sage E. Processing of a complex multiply damaged site by human cell extracts and purified repair proteins. Nucleic Acids Res. 2005, 33:260-271.
53. Eot-Houillier G., Gonera M., Gasparutto D., Giustranti C., Sage E. Interplay between DNA N-glycosylases/AP lyases at multiply damaged sites and biological consequences. Nucleic Acids Res. 2007, 35:3355-3366.
54. Paap G., 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.
55. Parsons J.L., Zharkov D.O., Dianov G.L. NEIL1 excises 3′ end proximal oxidative DNA lesions resistant to cleavage by NTH1 and OGG1. Nucleic Acids Res. 2005, 33:4849-4856.
56. Parsons J.L., Dianova I.I., Boswell E., Weinfeld M., Dianov G.L. End-damage-specific proteins facilitate recruitment or stability of X-ray cross-complementing protein 1 at the sites of DNA single-strand break repair. FEBS J. 2005, 272:5753-5763.
57. Dobbs T.A., Palmer P., Maniou Z., Lomax M.E., O'Neill P. Interplay of two major repair pathways in the processing of complex double-strand DNA breaks. DNA Repair 2008, 7:1372-1383.
58. Kozmin S., Sedletska Y., Reynaud-Angelin A., Gasparutto D., Sage E. 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.
59. Moscariello M., Sutherland B. Saccharomyces cerevisiae-based system for studying clustered DNA damages. Radiat. Environ. Biophys. 2010, 49:447-456.
60. Bao G., Kow Y.W. Effect of sequence context and direction of replication on AP site bypass in Saccharomyces cerevisiae. Mutat. Res. 2009, 669:147-154.
61. Cappelli E., Degan P., Frosina G. Comparative repair of the endogenous lesions 8-oxo-7, 8-dihydroguanine (8-oxoG), uracil and abasic site by mammalian cell extracts: 8-oxoG is poorly repaired by human cell extracts. Carcinogenesis 2000, 21:1135-1141.
62. Cappelli E., Hazra T., Hill J.W., Slupphaug G., Bogliolo M., Frosina G. Rates of base excision repair are not solely dependent on levels of initiating enzymes. Carcinogenesis 2001, 22:387-393.
63. D'Souza D.I., Harrison L. Repair of clustered uracil DNA damages in Escherichia coli. Nucleic Acids Res. 2003, 31:4573-4581.
64. Harrison L., Brame K.L., Geltz L.E., Landry A.M. 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 2006, 5:324-335.
65. Shikazono N., O'Neill P. Biological consequences of potential repair intermediates of clustered base damage site in Escherichia coli. Mutat. Res. 2009, 669:162-168.
66. Dianov G.L., Timchenko T.V., Sinitsina O.I., Kuzminov A.V., Medvedev O.A., Salganik R.I. Repair of uracil residues closely spaced on the opposite strands of plasmid DNA results in double-strand break and deletion formation. Mol. Gen. Genet. 1991, 225:448-452.
67. Bellon S., Shikazono N., Cunniffe S., Lomax M., O'Neill P. Processing of thymine glycol in a clustered DNA damage site: mutagenic or cytotoxic. Nucleic Acids Res. 2009, 37:4430-4440.
68. Cuniffe S.M.T., Lomax M.E., O'Neill P. An AP site can protect against the mutagenic potential of 8-oxoG when present within a tandem clustered site in E. coli. DNA Repair 2007, 6:1839-1849.
69. Yuan B., Jiang Y., Wang Y., Wang Y. Efficient formation of the tandem thymine glycol/8-oxo-7,8-dihydroguanine lesion in isolated DNA and the mutagenic and cytotoxic properties of the tandem lesions in Escherichia coli cells. Chem. Res. Toxicol. 2010, 23:11-19.
70. Imoto S., Bransfield L.A., Croteau D.L., Van Houten B., Greenberg M.M. DNA tandem lesion repair by strand displacement synthesis and nucleotide excision repair. Biochemistry 2008, 47:4306-4316.
71. Bourdat A.-G., Gasparutto D., Cadet J. Synthesis and enzymatic processing of oligodeoxynucleotides containing tandem base damage. Nucleic Acids Res. 1999, 27:1015-1024.
72. Gentil A., Le Page F., Cadet J., Sarasin A. Mutation spectra induced by replication of two vicinal oxidative DNA lesions in mammalian cells. Mutat. Res. 2000, 452:51-56.
73. Gulston M., de Lara C., Jenner T., Davis E., O'Neill P. Processing of clustered DNA damage generates additional double-strand breaks in mammalian cells post-irradiation. Nucleic Acids Res. 2004, 32:1602-1609.
74. Georgakilas A.G., Bennett P.V., Wilson D.M., Sutherland B.M. Processing of bistranded abasic DNA clusters in γ-irradiated human hematopoietic cells. Nucleic Acids Res. 2004, 32:5609-5620.
75. Harrison L., Skorvaga M., Cunningham R.P., Hendry J.H., Margison G.P. Transfection of the E. coli nth gene into radiosensitive Chinese Hamster cells: effects on sensitivity to radiation, hydrogen peroxide and bleomycin sulfate. Radiat. Res. 1992, 132:30-39.
76. Paul S., Gros L., Laval J., Sutherland B.M. Expression of the E. coli Fpg protein in CHO cells lowers the endogenous oxypurine clustered damage levels and decreases the accumulation of endogenous Hprt mutations. Environ. Mol. Mutagen. 2006, 47:311-319.
77. Malyarchuk S., Castore R., Harrison L. Apex1 can cleave complex clustered lesions in cells. DNA Repair 2009, 8:1343-1354.
78. Saxowsky T.T., Meadows K.L., Klungland A., Doetsch P.W. 8-Oxoguanine-mediated transcriptional mutagenesis causes Ras activation in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18877-18882.
79. Malyarchuk S., Harrison L. DNA repair of clustered uracils in HeLa cells. J. Mol. Biol. 2005, 345:731-743.
80. 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.
81. David-Cordonnier M.-H., Boiteux S., O'Neill P. Efficiency of excision of 8-oxoguanine within DNA clustered damage by XRS5 nuclear extracts and purified human OGG1 protein. Biochemistry 2001, 40:11811-11818.
82. Hashimoto M., Donald C.D., Yannone S.M., Chen D.J., Roy R., Kow Y.W. A possible role of Ku in mediating sequential repair of closely opposed lesions. J. Biol. Chem. 2001, 276:12827-12831.
83. Di Noia J.M., Neuberger M.S. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 2007, 76:161-1622.
84. Schrader C.E., Guikema J.E.J., Wu X., Stavnezer J. The roles of APE1, APE2, DNA polymerase β and mismatch repair in creating S region DNA breaks during antibody class switch. Phil. Trans. R. Soc. B 2009, 364:645-652.
85. Han L., Yu K. Altered kinetics of nonhomologous end joining and class switch recombination in ligase IV-deficient B cells. J. Exp. Med. 2008, 205:2745-2753.
86. Nakamura M., Kondo S., Sugai M., Nazarea M., Imamura S., Honjo T. High frequency class switching of an IgM+ B lymphoma clone CH12F3 to IgA+ cells. Int. Immunol. 1996, 8:193-201.
87. Wilson S.H., Kunkel T.A. Passing the baton in base excision repair. Nat. Struct. Biol. 2000, 7:176-178.
88. Waters T.R., Gallinari P., Jiricny J., Swann P.F. Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1. J. Biol. Chem. 1999, 274:67-74.
89. Parikh S.S., Mol C.D., Slupphaug G., Bharati S., Krokan H.E., Tainer J.A. Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J. 1998, 17:5214-5226.
90. Vidal A.E., Hickson I.D., Boiteux S., Radicella J.P. Mechanism of stimulation of the DNA glycosylase activity of hOGG1 by the major human AP endonuclease: bypass of the AP lyase activity step. Nucleic Acids Res. 2001, 29:1285-1292.
91. Bennett R.A., Wilson D.M., Wong D., Demple B. Interaction of human apurinic endonuclease and DNA polymerase beta in the base excision repair pathway. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:7166-7169.
92. Kubota Y., Nash R.A., Klungland A., Schar P., Barnes D.E., Lindahl T. Reconstitution of DNA base excision repair with purified human proteins: interaction between DNA polymerase β and the XRCC1 protein. EMBO J. 1996, 15:6662-6670.
93. Caldecott K.W., Aoufouchi S., Johnson P., Shall S. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III as a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res. 1996, 24:4387-4394.
94. Prasad R., Singhal R.K., Srivastava D.K., Molina J.T., Tomkinson A.E. Specific interaction of DNA polymerase beta and DNA ligase I in a multiprotein base excision repair complex from bovine testis. J. Biol. Chem. 1996, 271:16000-16007.
95. Peddi P., Loftin C.W., Dickey J.S., Hair J.M., Burns K.J., Aziz K., Francisco D.C., Panayiotidis M.I., Sedelnikova O.A., Bonner W.M., Winters T.A., Georgakilas A.G. DNA-PKcs deficiency leads to persistence of oxidatively induced clustered DNA lesions in human tumor cells. Free Radic. Biol. Med. 2010, 48:1435-1443.
96. Covo S., de Villartay J.-P., Jeggo P.A., Livneh Z. Translesion synthesis-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.
97. Blakely E.A., Kronenberg A. Heavy-ion radiobiology: new approaches to delineate mechanisms underlying enhanced biological effectiveness. Radiat. Res. 1998, 150(Suppl.):S126-S145.
98. Kagawa Y., Shimazu T., Gordon A.J., Fukunishi N., Inabe N., Suzuki M., Hirano M., Kato T., Watanabe M., Hanaoka F., Yatagai F. Complex hprt deletion events are recovered after exposure of human lymphoblastoid cells to high-LET carbon and neon ion beams. Mutagenesis 1999, 14:199-205.
99. Masumura K., Kuniya K., Kurobe T., Fukuoka M., Yatagai F., Nohmi T. Heavy-ion-induced mutations in the gpt delta transgenic mouse: comparison of mutation spectra induced by heavy-ion, X-ray, and gamma-ray radiation. Environ. Mol. Mutagen. 2002, 40:207-215.
100. Singleton B.K., Griffin C.S., Thacker J. Clustered DNA damage leads to complex genetic changes in irradiated human cells. Cancer Res. 2002, 62:6263-6269.
101. Kronenberg A., Gauny S., Kwoh E., Connolly L., Dan C., Lasarev M., Turker M.S. Comparative analysis of cell killing and autosomal mutation in mouse kidney epithelium exposed to 1GeV/nucleon iron ions in vitro or in situ. Radiat. Res. 2009, 172:550-557.
102. Albertini R.J., Clark L.S., Nicklas J.A., O'Neill P., Hui T.E., Jostes R. Radiation quality affects the efficiency of induction and the molecular spectrum of HPRT mutations in human T cells. Radiat Res. 1997, 148(Suppl.):S76-S86.
103. Anderson J.A., Harper J.V., Cucinotta F.A., O'Neill P. Participation of DNA-PKcs in DSB repair after exposure to high- and low-LET radiation. Radiat. Res. 2010, 174:195-205.
104. Zafar F., Seidler S.B., Kronenberg A., Schild D., Wiese C. Homologous recombination contributes to the repair of DNA double-strand breaks induced by high-energy iron ions. Radiat. Res. 2010, 173:27-39.
105. Harper J.V., Anderson J.A., O'Neill P. Radiation induced DNA DSB: contribution from stalled replication forks?. DNA Repair 2010, 9:907-913.