Role of oxidatively induced DNA lesions in human pathogenesis

Mutation Research - Reviews in Mutation Research

Volumn 704, Issue 1-3, 2010, Pages 152-159

  Sedelnikova, Olga A ^a   Redon, Christophe E ^a   Dickey, Jennifer S ^a   Nakamura, Asako J ^a   Georgakilas, Alexandros G ^b   Bonner, William M ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Aging; Bystander effect; Cancer; DNA damage; DNA double strand breaks; Reactive oxygen species

Indexed keywords

HISTONE H2AX; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; REACTIVE OXYGEN METABOLITE;

AGING; BYSTANDER EFFECT; CELL POPULATION; DISEASE COURSE; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; DOUBLE STRANDED DNA BREAK; EXCISION REPAIR; FLUORESCENCE IN SITU HYBRIDIZATION; GENOMIC INSTABILITY; HUMAN; IONIZING RADIATION; NEOPLASM; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; REVIEW; SINGLE STRANDED DNA BREAK;

AGING; BYSTANDER EFFECT; CELL AGING; DNA DAMAGE; HUMANS; NEOPLASMS; OXIDATIVE STRESS;

EID: 77951977494     PISSN: 13835742     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrrev.2009.12.005     Document Type: Review

References (129)

1. Nordberg J., and Arner E.S. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic. Biol. Med. 31 (2001) 1287-1312
2. Cooke M.S., Evans M.D., Dizdaroglu M., and Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 17 (2003) 1195-1214
3. Hussain S.P., Hofseth L.J., and Harris C.C. Radical causes of cancer. Nat. Rev. Cancer 3 (2003) 276-285
4. Liu J., Qu W., and Kadiiska M.B. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol. Appl. Pharmacol. 238 (2009) 209-214
5. O'Neill P., and Wardman P. Radiation chemistry comes before radiation biology. Int. J. Radiat. Biol. 85 (2009) 9-25
6. McMillan T.J., Leatherman E., Ridley A., Shorrocks J., Tobi S.E., and Whiteside J.R. Cellular effects of long wavelength UV light (UVA) in mammalian cells. J. Pharm. Pharmacol. 60 (2008) 969-976
7. Klaunig J.E., and Kamendulis L.M. The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 239-267
8. Ott M., Gogvadze V., Orrenius S., and Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis 12 (2007) 913-922
9. Georgakilas A.G., Aziz K., Ziech D., Georgakila S., and Panayiotidis M.I. BRCA1 involvement in toxicological responses and human cancer etiology. Toxicol. Lett. 188 (2009) 77-83
10. Evans M.D., Dizdaroglu M., and Cooke M.S. Oxidative DNA damage and disease: induction, repair and significance. Mutat. Res. 567 (2004) 1-61
11. Galli F., Piroddi M., Annetti C., Aisa C., Floridi E., and Floridi A. Oxidative stress and reactive oxygen species. Contrib. Nephrol. 149 (2005) 240-260
12. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., and Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39 (2007) 44-84
13. Kohchi C., Inagawa H., Nishizawa T., and Soma G. ROS and innate immunity. Anticancer Res. 29 (2009) 817-821
14. Ward J.F. The complexity of DNA damage: relevance to biological consequences. Int. J. Radiat. Biol. 66 (1994) 427-432
15. Sutherland B.M., Bennett P.V., Sidorkina O., and Laval J. Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 103-108
16. Nakamura J., and Swenberg J.A. Endogenous apurinic/apyrimidinic sites in genomic DNA of mammalian tissues. Cancer Res. 59 (1999) 2522-2526
17. Klungland A., Hoss M., Gunz D., Constantinou A., Clarkson S.G., Doetsch P.W., Bolton P.H., Wood R.D., and Lindahl T. Base excision repair of oxidative DNA damage activated by XPG protein. Mol. Cell 3 (1999) 33-42
18. Atamna H., Cheung I., and Ames B.N. A method for detecting abasic sites in living cells: age-dependent changes in base excision repair. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 686-691
19. De Bont R., and van Larebeke N. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis 19 (2004) 169-185
20. Cadet J., Douki T., Gasparutto D., and Ravanat J.L. Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res. 531 (2003) 5-23
21. Poulsen H.E. Oxidative DNA modifications. Exp. Toxicol. Pathol. 57 Suppl. 1 (2005) 161-169
22. Gedik C.M., and Collins A. Establishing the background level of base oxidation in human lymphocyte DNA: results of an interlaboratory validation study. FASEB J. 19 (2005) 82-84
23. Bennett P.V., Cintron N.S., Gros L., Laval J., and Sutherland B.M. Are endogenous clustered DNA damages induced in human cells?. Free Radic. Biol. Med. 37 (2004) 488-499
24. Bennett P.V., Cuomo N.L., Paul S., Tafrov S.T., and Sutherland B.M. Endogenous DNA damage clusters in human skin, 3-D model, and cultured skin cells. Free Radic. Biol. Med. 39 (2005) 832-839
25. Nowsheen S., Wukovich R.L., Aziz K., Kalogerinis P.T., Richardson C.C., Panayiotidis M.I., Bonner W.M., Sedelnikova O.A., and Georgakilas A.G. Accumulation of oxidatively induced clustered DNA lesions in human tumor tissues. Mutat. Res. 674 (2009) 131-136
26. Ward J.F. Some biochemical consequences of the spatial distribution of ionizing radiation-produced free radicals. Radiat. Res. 86 (1981) 185-195
27. Harrison L., Hatahet Z., and Wallace S.S. In vitro repair of synthetic ionizing radiation-induced multiply damaged DNA sites. J. Mol. Biol. 290 (1999) 667-684
28. David-Cordonnier M.H., Cunniffe S.M., Hickson I.D., and O'Neill P. Efficiency of incision of an AP site within clustered DNA damage by the major human AP endonuclease. Biochemistry 41 (2002) 634-642
29. Georgakilas A.G., Bennett P.V., and Sutherland B.M. High efficiency detection of bi-stranded abasic clusters in gamma-irradiated DNA by putrescine. Nucleic Acids Res. 30 (2002) 2800-2808
30. Eot-Houllier G., Eon-Marchais S., Gasparutto D., and Sage E. Processing of a complex multiply damaged DNA site by human cell extracts and purified repair proteins. Nucleic Acids Res. 33 (2005) 260-271
31. Cunniffe S.M., Lomax M.E., and 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 (Amst.) 6 (2007) 1839-1849
32. Bonner W.M., Redon C.E., Dickey J.S., Nakamura A.J., Sedelnikova O.A., Solier S., and Pommier Y. GammaH2AX and cancer. Nat. Rev. Cancer 8 (2008) 957-967
33. Wilstermann A.M., and Osheroff N. Base excision repair intermediates as topoisomerase II poisons. J. Biol. Chem. 276 (2001) 46290-46296
34. Pommier Y., Barcelo J.M., Rao V.A., Sordet O., Jobson A.G., Thibaut L., Miao Z.H., Seiler J.A., Zhang H., Marchand C., Agama K., Nitiss J.L., and Redon C. Repair of topoisomerase I-mediated DNA damage. Prog. Nucleic Acid Res. Mol. Biol. 81 (2006) 179-229
35. Sordet O., Redon C.E., Guirouilh-Barbat J., Smith S., Solier S., Douarre C., Conti C., Nakamura A.J., Das B.B., Nicolas E., Kohn K.W., Bonner W.M., and Pommier Y. Ataxia telangiectasia mutated activation by transcription- and topoisomerase I-induced DNA double-strand breaks. EMBO Rep. 10 (2009) 887-893
36. Yang N., Galick H., and Wallace S.S. Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks. DNA Repair (Amst.) 3 (2004) 1323-1334
37. Khanna K.K., and Jackson S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27 (2001) 247-254
38. Memisoglu A., and Samson L. Base excision repair in yeast and mammals. Mutat. Res. 451 (2000) 39-51
39. Wilson III D.M., Sofinowski T.M., and McNeill D.R. Repair mechanisms for oxidative DNA damage. Front. Biosci. 8 (2003) d963-981
40. Slupphaug G., Kavli B., and Krokan H.E. The interacting pathways for prevention and repair of oxidative DNA damage. Mutat. Res. 531 (2003) 231-251
41. Lindahl T., and Wood R.D. Quality control by DNA repair. Science 286 (1999) 1897-1905
42. Demple B., and DeMott M.S. Dynamics and diversions in base excision DNA repair of oxidized abasic lesions. Oncogene 21 (2002) 8926-8934
43. Ocampo M.T., Chaung W., Marenstein D.R., Chan M.K., Altamirano A., Basu A.K., Boorstein R.J., Cunningham R.P., and Teebor G.W. Targeted deletion of mNth1 reveals a novel DNA repair enzyme activity. Mol. Cell. Biol. 22 (2002) 6111-6121
44. Marenstein D.R., Chan M.K., Altamirano A., Basu A.K., Boorstein R.J., Cunningham R.P., and Teebor G.W. Substrate specificity of human endonuclease III (hNTH1). Effect of human APE1 on hNTH1 activity. J. Biol. Chem. 278 (2003) 9005-9012
45. Matsumoto Y., Kim K., and Bogenhagen D.F. Proliferating cell nuclear antigen-dependent abasic site repair in Xenopus laevis oocytes: an alternative pathway of base excision DNA repair. Mol. Cell. Biol. 14 (1994) 6187-6197
46. Blum A. Heart failure-new insights. Isr. Med. Assoc. J. 11 (2009) 105-111
47. Reddy V.P., Zhu X., Perry G., and Smith M.A. Oxidative stress in diabetes and Alzheimer's disease. J. Alzheimers Dis. 16 (2009) 763-774
48. Rao K.S. Free radical induced oxidative damage to DNA: relation to brain aging and neurological disorders. Indian J. Biochem. Biophys. 46 (2009) 9-15
49. Augoulea A., Mastorakos G., Lambrinoudaki I., Christodoulakos G., and Creatsas G. The role of the oxidative-stress in the endometriosis-related infertility. Gynecol. Endocrinol. 25 (2009) 75-81
50. Ruder E.H., Hartman T.J., and Goldman M.B. Impact of oxidative stress on female fertility. Curr. Opin. Obstet. Gynecol. 21 (2009) 219-222
51. Franco R., Schoneveld O., Georgakilas A.G., and Panayiotidis M.I. Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett. 266 (2008) 6-11
52. Nakamura A.J., Chiang Y.J., Hathcock K.S., Horikawa I., Sedelnikova O.A., Hodes R.J., and Bonner W.M. Both telomeric and non-telomeric DNA damage are determinants of mammalian cellular senescence. Epigenetics Chromatin 1 (2008) 6
53. Muller F.L., Lustgarten M.S., Jang Y., Richardson A., and Van Remmen H. Trends in oxidative aging theories. Free Radic. Biol. Med. 43 (2007) 477-503
54. Parrinello S., Samper E., Krtolica A., Goldstein J., Melov S., and Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5 (2003) 741-747
55. Bradley T.R., and Metcalf D. The growth of mouse bone marrow cells in vitro. Aust. J. Exp. Biol. Med. Sci. 44 (1966) 287-299
56. Bradley T.R., Hodgson G.S., and Rosendaal M. The effect of oxygen tension on haemopoietic and fibroblast cell proliferation in vitro. J. Cell Physiol. 97 (1978) 517-522
57. Wion D., Christen T., Barbier E.L., and Coles J.A. PO(2) matters in stem cell culture. Cell Stem Cell 5 (2009) 242-243
58. Erker L., Schubert R., Yakushiji H., Barlow C., Larson D., Mitchell J.B., and Wynshaw-Boris A. Cancer chemoprevention by the antioxidant tempol acts partially via the p53 tumor suppressor. Hum. Mol. Genet. 14 (2005) 1699-1708
59. Elchuri S., Oberley T.D., Qi W., Eisenstein R.S., Jackson Roberts L., Van Remmen H., Epstein C.J., and Huang T.T. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24 (2005) 367-380
60. Xie Y., Yang H., Cunanan C., Okamoto K., Shibata D., Pan J., Barnes D.E., Lindahl T., McIlhatton M., Fishel R., and Miller J.H. Deficiencies in mouse Myh and Ogg1 result in tumor predisposition and G to T mutations in codon 12 of the K-ras oncogene in lung tumors. Cancer Res. 64 (2004) 3096-3102
61. d'Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., Saretzki G., Carter N.P., and Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426 (2003) 194-198
62. Bakkenist C.J., and Kastan M.B. Initiating cellular stress responses. Cell 118 (2004) 9-17
63. Herbig U., Jobling W.A., Chen B.P., Chen D.J., and Sedivy J.M. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14 (2004) 501-513
64. Sedelnikova O.A., Horikawa I., Zimonjic D.B., Popescu N.C., Bonner W.M., and Barrett J.C. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell. Biol. 6 (2004) 168-170
65. Sedelnikova O.A., Horikawa I., Redon C., Nakamura A., Zimonjic D.B., Popescu N.C., and Bonner W.M. Delayed kinetics of DNA double-strand break processing in normal and pathological aging. Aging Cell 7 (2008) 89-100
66. Riches L.C., Lynch A.M., and Gooderham N.J. Early events in the mammalian response to DNA double-strand breaks. Mutagenesis 23 (2008) 331-339
67. Nakamura A., Sedelnikova O.A., Redon C., Pilch D.R., Sinogeeva N.I., Shroff R., Lichten M., and Bonner W.M. Techniques for gamma-H2AX detection. Methods Enzymol. 409 (2006) 236-250
68. Klapper W., Parwaresch R., and Krupp G. Telomere biology in human aging and aging syndromes. Mech. Ageing Dev. 122 (2001) 695-712
69. Steenken S., and Jovanovic S.V. 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
70. Lewis F.D., Liu X., Liu J., Hayes R.T., and Wasielewski M.R. Dynamics and equilibria of oxidation of G, GG, and GGG sequences in DNA hairpins. J. Am. Chem. Soc. 122 (2000) 12037-12038
71. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem. Sci. 27 (2002) 339-344
72. von Zglinicki T., Saretzki G., Docke W., and Lotze C. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence?. Exp. Cell Res. 220 (1995) 186-193
73. Vaziri H., West M.D., Allsopp R.C., Davison T.S., Wu Y.S., Arrowsmith C.H., Poirier G.G., and Benchimol S. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J. 16 (1997) 6018-6033
74. Greider C.W., and Blackburn E.H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43 (1985) 405-413
75. Furumoto K., Inoue E., Nagao N., Hiyama E., and Miwa N. Age-dependent telomere shortening is slowed down by enrichment of intracellular vitamin C via suppression of oxidative stress. Life Sci. 63 (1998) 935-948
76. Matoba S., Kang J.G., Patino W.D., Wragg A., Boehm M., Gavrilova O., Hurley P.J., Bunz F., and Hwang P.M. p53 regulates mitochondrial respiration. Science 312 (2006) 1650-1653
77. Druzhyna N.M., Wilson G.L., and LeDoux S.P. Mitochondrial DNA repair in aging and disease. Mech. Ageing Dev. 129 (2008) 383-390
78. Wei Y.H., and Lee H.C. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp. Biol. Med. (Maywood) 227 (2002) 671-682
79. Taylor R.W., and Turnbull D.M. Mitochondrial DNA mutations in human disease. Nat. Rev. Genet. 6 (2005) 389-402
80. Maynard S., Schurman S.H., Harboe C., de Souza-Pinto N.C., and Bohr V.A. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis (2008)
81. Ellsworth D.L., Ellsworth R.E., Liebman M.N., Hooke J.A., and Shriver C.D. Genomic instability in histologically normal breast tissues: implications for carcinogenesis. Lancet Oncol. 5 (2004) 753-758
82. Gackowski D., Speina E., Zielinska M., Kowalewski J., Rozalski R., Siomek A., Paciorek T., Tudek B., and Olinski R. Products of oxidative DNA damage and repair as possible biomarkers of susceptibility to lung cancer. Cancer Res. 63 (2003) 4899-4902
83. Dizdaroglu M., Jaruga P., and Rodriguez H. Measurement of 8-hydroxy-2′-deoxyguanosine in DNA by high-performance liquid chromatography-mass spectrometry: comparison with measurement by gas chromatography-mass spectrometry. Nucleic Acids Res. 29 (2001) E12
84. Sedelnikova O.A., and Bonner W.M. GammaH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle 5 (2006) 2909-2913
85. Szatrowski T.P., and Nathan C.F. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 51 (1991) 794-798
86. Kawanishi S., Hiraku Y., Pinlaor S., and Ma N. Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol. Chem. 387 (2006) 365-372
87. Verrax J., Pedrosa R.C., Beck R., Dejeans N., Taper H., and Calderon P.B. In situ modulation of oxidative stress: a novel and efficient strategy to kill cancer cells. Curr. Med. Chem. 16 (2009) 1821-1830
88. Liang Y., Lin S.Y., Brunicardi F.C., Goss J., and Li K. DNA damage response pathways in tumor suppression and cancer treatment. World J. Surg. 33 (2009) 661-666
89. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., Orntoft T., Lukas J., and Bartek J. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434 (2005) 864-870
90. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio Jr. R.A., Kastrinakis N.G., Levy B., Kletsas D., Yoneta A., Herlyn M., Kittas C., and Halazonetis T.D. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434 (2005) 907-913
91. Banath J.P., Macphail S.H., and Olive P.L. Radiation sensitivity, H2AX phosphorylation, and kinetics of repair of DNA strand breaks in irradiated cervical cancer cell lines. Cancer Res. 64 (2004) 7144-7149
92. Yu T., MacPhail S.H., Banath J.P., Klokov D., and Olive P.L. Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability. DNA Repair (Amst.) 5 (2006) 935-946
93. Nakamura A.J., Redon C.E., Bonner W.M., and Sedelnikova O.A. Telomere-dependent and telomere-independent origins of endogenous DNA damage in tumor cells. Aging 1 (2009) 212-218
94. Hastie N.D., Dempster M., Dunlop M.G., Thompson A.M., Green D.K., and Allshire R.C. Telomere reduction in human colorectal carcinoma and with ageing. Nature 346 (1990) 866-868
95. Lindsey J., McGill N.I., Lindsey L.A., Green D.K., and Cooke H.J. In vivo loss of telomeric repeats with age in humans. Mutat. Res. 256 (1991) 45-48
96. Risques R.A., Lai L.A., Brentnall T.A., Li L., Feng Z., Gallaher J., Mandelson M.T., Potter J.D., Bronner M.P., and Rabinovitch P.S. Is ulcerative colitis a disease of accelerated colon aging? Evidence from telomere attrition and DNA damage. Gastroenterology (2008)
97. Trachootham D., Lu W., Ogasawara M.A., Nilsa R.D., and Huang P. Redox regulation of cell survival. Antioxid. Redox Signal 10 (2008) 1343-1374
98. Prise K.M., and O'Sullivan J.M. Radiation-induced bystander signalling in cancer therapy. Nat. Rev. Cancer 9 (2009) 351-360
99. Dickey J.S., Baird B.J., Redon C.E., Sokolov M.V., Sedelnikova O.A., and Bonner W.M. Intercellular communication of cellular stress monitored by {gamma}-H2AX induction. Carcinogenesis (2009)
100. Sowa Resat M.B., and Morgan W.F. Radiation-induced genomic instability: a role for secreted soluble factors in communicating the radiation response to non-irradiated cells. J. Cell. Biochem. 92 (2004) 1013-1019
101. Sokolov M.V., Dickey J.S., Bonner W.M., and Sedelnikova O.A. Gamma-H2AX in bystander cells: not just a radiation-triggered event, a cellular response to stress mediated by intercellular communication. Cell Cycle 6 (2007) 2210-2212
102. Zhou H., Ivanov V.N., Gillespie J., Geard C.R., Amundson S.A., Brenner D.J., Yu Z., Lieberman H.B., and Hei T.K. Mechanism of radiation-induced bystander effect: role of the cyclooxygenase-2 signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 14641-14646
103. Hei T.K., Zhou H., Ivanov V.N., Hong M., Lieberman H.B., Brenner D.J., Amundson S.A., and Geard C.R. Mechanism of radiation-induced bystander effects: a unifying model. J. Pharm. Pharmacol. 60 (2008) 943-950
104. Azzam E.I., de Toledo S.M., and Little J.B. Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect. Oncogene 22 (2003) 7050-7057
105. Lu W., Ogasawara M.A., and Huang P. Models of reactive oxygen species in cancer. Drug Discov. Today Dis. Models 4 (2007) 67-73
106. Lala P.K., and Chakraborty C. Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol. 2 (2001) 149-156
107. Tartier L., Gilchrist S., Burdak-Rothkamm S., Folkard M., and Prise K.M. Cytoplasmic irradiation induces mitochondrial-dependent 53BP1 protein relocalization in irradiated and bystander cells. Cancer Res. 67 (2007) 5872-5879
108. Shao C., Prise K.M., and Folkard M. Signaling factors for irradiated glioma cells induced bystander responses in fibroblasts. Mutat. Res. 638 (2008) 139-145
109. Han W., Wu L., Chen S., Bao L., Zhang L., Jiang E., Zhao Y., Xu A., Hei T.K., and Yu Z. Constitutive nitric oxide acting as a possible intercellular signaling molecule in the initiation of radiation-induced DNA double strand breaks in non-irradiated bystander cells. Oncogene 26 (2007) 2330-2339
110. Keefer L.K., Nims R.W., Davies K.M., and Wink D.A. "NONOates" (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Methods Enzymol. 268 (1996) 281-293
111. D'Autreaux B., and Toledano M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8 (2007) 813-824
112. Kashino G., Prise K.M., Suzuki K., Matsuda N., Kodama S., Suzuki M., Nagata K., Kinashi Y., Masunaga S., Ono K., and Watanabe M. Effective suppression of bystander effects by DMSO treatment of irradiated CHO cells. J. Radiat. Res. (Tokyo) 48 (2007) 327-333
113. Shao C., Folkard M., Michael B.D., and Prise K.M. Targeted cytoplasmic irradiation induces bystander responses. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13495-13500
114. McKinnon P.J., and Caldecott K.W. DNA strand break repair and human genetic disease. Annu. Rev. Genomics Hum. Genet. 8 (2007) 37-55
115. Burdak-Rothkamm S., Rothkamm K., and Prise K.M. ATM acts downstream of ATR in the DNA damage response signaling of bystander cells. Cancer Res. 68 (2008) 7059-7065
116. Burdak-Rothkamm S., Short S.C., Folkard M., Rothkamm K., and Prise K.M. ATR-dependent radiation-induced gamma H2AX foci in bystander primary human astrocytes and glioma cells. Oncogene 26 (2007) 993-1002
117. Cheadle J.P., and Sampson J.R. Exposing the MYtH about base excision repair and human inherited disease. Hum. Mol. Genet. 12 Spec No. 2 (2003) R159-165
118. Hanada K., and Hickson I.D. Molecular genetics of RecQ helicase disorders. Cell. Mol. Life Sci. 64 (2007) 2306-2322
119. Portess D.I., Bauer G., Hill M.A., and O'Neill P. Low-dose irradiation of nontransformed cells stimulates the selective removal of precancerous cells via intercellular induction of apoptosis. Cancer Res. 67 (2007) 1246-1253
120. Jungst C., Cheng B., Gehrke R., Schmitz V., Nischalke H.D., Ramakers J., Schramel P., Schirmacher P., Sauerbruch T., and Caselmann W.H. Oxidative damage is increased in human liver tissue adjacent to hepatocellular carcinoma. Hepatology 39 (2004) 1663-1672
121. Mancuso M., Pasquali E., Leonardi S., Tanori M., Rebessi S., Di Majo V., Pazzaglia S., Toni M.P., Pimpinella M., Covelli V., and Saran A. Oncogenic bystander radiation effects in Patched heterozygous mouse cerebellum. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 12445-12450
122. Simon H.U., Haj-Yehia A., and Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5 (2000) 415-418
123. Boonstra J., and Post J.A. Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 337 (2004) 1-13
124. Knight J.A. Review: free radicals, antioxidants, and the immune system. Ann. Clin. Lab. Sci. 30 (2000) 145-158
125. Hammond E.M., Dorie M.J., and Giaccia A.J. ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. J. Biol. Chem. 278 (2003) 12207-12213
126. To K.K., Sedelnikova O.A., Samons M., Bonner W.M., and Huang L.E. The phosphorylation status of PAS-B distinguishes HIF-1alpha from HIF-2alpha in NBS1 repression. EMBO J. 25 (2006) 4784-4794
127. Bjelakovic G., Nikolova D., Gluud L.L., Simonetti R.G., and Gluud C. Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 297 (2007) 842-857
128. Kopjar N., Miocic S., Ramic S., Milic M., and Viculin T. Assessment of the radioprotective effects of amifostine and melatonin on human lymphocytes irradiated with gamma-rays in vitro. Arh. Hig. Rada. Toksikol. 57 (2006) 155-163
129. Zhao H., Shen J., Deininger P., and Hunt J.D. Abasic sites and survival in resected patients with non-small cell lung cancer. Cancer Lett. 246 (2007) 47-53