Bystander effects as manifestation of intercellular communication of DNA damage and of the cellular oxidative status

Cancer Letters

Volumn 356, Issue 1, 2015, Pages 58-71

  Klammer, Holger ^a   Mladenov, Emil ^a   Li, Fanghua ^a   Iliakis, George ^a  

^a UNIVERSITY OF ESSEN MEDICAL SCHOOL   (Germany)

Author keywords

Bystander effects; DNA damage signaling; Ionizing radiation

Indexed keywords

ATM PROTEIN; ATR PROTEIN; BMI1 PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIN DEPENDENT KINASE; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; HISTONE H2AX; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 13; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P53; TRANSCRIPTION FACTOR NRF2; CYTOKINE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ADAPTATION; BINDING SITE; BYSTANDER EFFECT; CELL COMMUNICATION; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; DNA DAMAGE; DNA REPLICATION; ENZYME METABOLISM; ENZYME REGULATION; EXCISION REPAIR; EXTRACELLULAR MATRIX; GAP JUNCTION; GENOMIC INSTABILITY; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INNATE IMMUNITY; IONIZING RADIATION; MOLECULAR DYNAMICS; NEUROMODULATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RADIATION INJURY; RADIOBIOLOGY; RECOMBINATION REPAIR; SEQUENCE HOMOLOGY; SHORT SURVEY; SIGNAL TRANSDUCTION; SISTER CHROMATID EXCHANGE; UBIQUITINATION; UPREGULATION; APOPTOSIS; BIOSYNTHESIS; CELL TRANSFORMATION; DNA REPAIR; GENETICS; METABOLISM; OXIDATIVE STRESS; RADIATION RESPONSE; SECRETION (PROCESS);

APOPTOSIS; BYSTANDER EFFECT; CELL COMMUNICATION; CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; DNA DAMAGE; DNA REPAIR; GAP JUNCTIONS; GENOMIC INSTABILITY; HUMANS; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84912575835     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.12.017     Document Type: Review

References (219)

1. Ward J.F. DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability. Prog. Nucl. Acid Res. 1988, 35:95-125.
2. Lett J.T., Parkins G., Alexander P., Ormerod M.G. Mechanisms of sensitization to X-rays of mammalian cells by 5-bromodeoxyuridine. Nature 1964, 203:593-596.
3. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
4. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
5. Fawcett J.A., Innan H. The role of gene conversion in preserving rearrangement hotspots in the human genome. Trends Genet. 2013, 29:561-568.
6. Schipler A., Iliakis G. DNA double-strand-break complexity levels and their possible contributions to the probability for error-prone processing and repair pathway choice. Nucl. Acids Res. 2013, 41:7589-7605.
7. Prise K.M., O'Sullivan J.M. Radiation-induced bystander signalling in cancer therapy. Nat. Rev. Cancer 2009, 9:351-360.
8. Mothersill C., Kadhim M. Mechanisms involved in the induction of radiation-induced non-targeted effects. Int. J. Radiat. Biol. 2012, 88:711-712.
9. Hei T.K., Zhou H., Chai Y., Ponnaiya B., Ivanov V.N. Radiation induced non-targeted response: mechanism and potential clinical implications. Curr. Mol. Pharmacol. 2011, 4:96-105.
10. W.F. Morgan, Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro, Radiat. Res. 178 (2012) AV223-AV236.
11. Morgan W.F., Sowa M.B. Non-targeted bystander effects induced by ionizing radiation. Mutat. Res./Fund. Mol. Mech. Mutagen. 2007, 616:159-164.
12. Morgan D.O. Principles of CDK regulation. Nature 1995, 374:131-134.
13. Nurse P., Thuriaux P., Nasmyth K. Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe. Mol. Gen. Genet. 1976, 146:167-178.
14. L.H. Hartwell, J. Culotti, B. Reid, Genetic control of the cell-division cycle in yeast. I. Detection of mutants, Proc. Natl. Acad. Sci. U.S.A. 66 (1970) 352-359.
15. Elledge S.J. Cell cycle checkpoints: preventing an identity crisis. Science 1996, 274:1664-1672.
16. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 2001, 15:2177-2196.
17. Shiloh Y. ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. 2001, 11:71-77.
18. San Filippo J., Sung P., Klein H. Mechanism of eukaryotic homologous recombination. Ann. Rev. Biochem. 2008, 77:229-257.
19. Daley J.M., Palmbos P.L., Wu D., Wilson T.E. Nonhomologous end joining in yeast. Ann. Rev. Genet. 2005, 39:431-451.
20. Mladenov E., Iliakis G. Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mutat. Res./Fund. Mol. Mech. Mutagen. 2011, 711:61-72.
21. E. Mladenov, S. Magin, A. Soni, G. Iliakis, DNA double-strand break repair as determinant of cellular radiosensitivity to killing and target in radiation therapy, Front. Oncol. 3 (2013) Article 113.
22. Dueva R., Iliakis G. Alternative pathways of non-homologous end joining (NHEJ) in genomic instability and cancer. Transl. Cancer Res. 2013, 2:163-177.
23. Lane D.P. Cancer. p53, guardian of the genome. Nature 1992, 358:15-16.
24. Amundson S.A., Myers T.G., Fornace A.J. Roles for p53 in growth arrest and apoptosis: putting on the brakes after genotoxic stress. Oncogene 1998, 17:3287-3299.
25. Schwartz D., Rotter V. P53-dependent cell cycle control: response to genotoxic stress. Semin. Cancer Biol. 1998, 8:325-336.
26. Kim S.-T., Xu B., Kastan M.B. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev. 2002, 16:560-570.
27. Danial N.N. BCL-2 family proteins: critical checkpoints of apoptotic cell death. Clin. Cancer Res. 2007, 13:7254-7263.
28. Schmitz I., Kirchhoff S., Krammer P.H. Regulation of death receptor-mediated apoptosis pathways. Int. J. Biochem. Cell Biol. 2000, 32:1123-1136.
29. Wajant H. The Fas signaling pathway: more than a paradigm. Science 2002, 296:1635-1636.
30. Dejean L.M., Martinez-Caballero S., Manon S., Kinnally K.W. Regulation of the mitochondrial apoptosis-induced channel, MAC, by BCL-2 family proteins. Biochim. Biophys. Acta 2006, 1762:191-201.
31. Chipuk J.E., Green D.R. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization?. Trends Cell Biol. 2008, 18:157-164.
32. Leber B., Lin J., Andrews D.W. Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis 2007, 12:897-911.
33. Popov S.G., Villasmil R., Bernardi J., Grene E., Cardwell J., Wu A., Alibek D., Bailey C., Alibek K. Lethal toxin of Bacillus anthracis causes apoptosis of macrophages. Biochem. Biophys. Res. Commun. 2002, 293:349-355.
34. Brune B. Nitric oxide: NO apoptosis or turning it ON?. Cell Death Differ. 2003, 10:864-869.
35. Piret B., Schoonbroodt S., Piette J. The ATM protein is required for sustained activation of NF-kappaB following DNA damage. Oncogene 1999, 18:2261-2271.
36. Li N., Karin M. Ionizing radiation and short wavelength UV activate NF-kappaB through two distinct mechanisms. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13012-13017.
37. Huang T.T., Feinberg S.L., Suryanarayanan S., Miyamoto S. The zinc finger domain of NEMO is selectively required for NF-kappa B activation by UV radiation and topoisomerase inhibitors. Mol. Cell. Biol. 2002, 22:5813-5825.
38. Nagasawa H., Little J.B. Induction of sister chromatid exchanges by extremely low doses of α-particles. Cancer Res. 1992, 52:6394-6396.
39. Kaminski J.M., Shinohara E., Summers J.B., Niermann K.J., Morimoto A., Brousal J. The controversial abscopal effect. Cancer Treat. Rev. 2005, 31:159-172.
40. Emerit I., Garban F., Vassy J., Levy A., Filipe P., Freitas J. Superoxide-mediated clastogenesis and anticlastogenic effects of exogenous superoxide dismutase. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:12799-12804.
41. Morgan W.F. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat. Res. 2003, 159:567-580.
42. Morgan W.F. Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic factors and transgenerational effects. Radiat. Res. 2003, 159:581-596.
43. Sjostedt S., Bezak E. Non-targeted effects of ionising radiation and radiotherapy. Australas. Phys. Eng. Sci. Med. 2010, 33:219-231.
44. Morgan W.F., Hartmann A., Limoli C.L., Nagar S., Ponnaiya B. Bystander effects in radiation-induced genomic instability. Mutat. Res./Fund. Mol. Mech. Mutagen. 2002, 504:91-100.
45. Shao C., Folkard M., Michael B.D., Prise K.M. Targeted cytoplasmic irradiation induces bystander responses. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13495-13500.
46. Yang H., Assad N., Held K.D. Medium-mediated intercellular communication is involved in bystander responses of X-ray-irradiated normal human fibroblasts. Oncogene 2005, 24:2096-2103.
47. Zhou H., Randers-Pehrson G., Waldren C.A., Vannais D., Hall E.J., Hei T.K. Induction of a bystander mutagenic effect of alpha particles in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:2099-2104.
48. Huo L., Nagasawa H., Little J.B. HPRT mutants induced in bystander cells by very low fluences of alpha particles result primarily from point mutations. Radiat. Res. 2001, 156:521-525.
49. Azzam E.I., De Toledo S.M., Spitz D.R., Little J.B. Oxidative metabolism modulates signal transduction and micronucleus formation in bystander cells from alpha-particle-irradiated normal human fibroblast cultures. Cancer Res. 2002, 62:5436-5442.
50. Kashino G., Prise K.M., Schettino G., Folkard M., Vojnovic B., Michael B.D., Suzuki K., Kodama S., Watanabe M. Evidence for induction of DNA double strand breaks in the bystander response to targeted soft X-rays in CHO cells. Mutat. Res./Fund. Mol. Mech. Mutagen. 2004, 556:209-215.
51. Lorimore S.A., Kadhim M., Pocock D.A., Papworth D., Stevens D.L., Goodhead D.T., Wright E.G. Chromosomal instability in the descendants of unirradiated surviving cells after α-particle irradiation. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:5730-5733.
52. Limoli C.L., Giedzinski E. Induction of chromosomal instability by chronic oxidative stress. Neoplasia 2003, 5:339-346.
53. Sawant S.G., Randers-Pehrson G., Geard C.R., Brenner D.J., Hall E.J. The bystander effect in radiation oncogenesis: I. Transformation in C3H 10T1/2 cells in vitro can be initiated in the unirradiated neighbors of irradiated cells. Radiat. Res. 2001, 155:397-401.
54. Mothersill C., Seymour C. Medium from irradiated human epithelial cells but not human fibroblasts reduced the clonogenic survival of unirradiated cells. Int. J. Radiat. Biol. 1997, 71:421-427.
55. Belyakov O.V., Folkard M., Mothersill C., Prise K.M., Michael B.D. Bystander-induced apoptosis and premature differentiation in primary urothelial explants after charged particle microbeam irradiation. Radiat. Prot. Dosim. 2002, 99:249-251.
56. Lyng F.M., Seymour C.B., Mothersill C. Initiation of apoptosis in cells exposed to medium from the progeny of irradiated cells: a possible mechanism for bystander-induced genomic instability?. Radiat. Res. 2002, 157:365-370.
57. Iyer R., Lehnert B.E. Factors underlying the cell growth-related bystander responses to α particles. Cancer Res. 2000, 60:1290-1298.
58. Gerashchenko B.I., Howell R.W. Flow cytometry as a strategy to study radiation-induced bystander effects in co-culture systems. Cytometry 2003, 54A:1-7.
59. Iyer R., Lehnert B.E. Low dose, low-LET ionizing radiation-induced radioadaptation and associated early responses in unirradiated cells. Mutat. Res. 2002, 503:1-9.
60. Klammer H., Kadhim M., Iliakis G. Evidence of an adaptive response targeting DNA nonhomologous end joining and its transmission to bystander cells. Cancer Res. 2010, 70:8498-8506.
61. Kovalchuk O., Zemp F.J., Filkowski J.N., Altamirano A.M., Dickey J.S., Jenkins-Baker G., Marino S.A., Brenner D.J., Bonner W.M., Sedelnikova O.A. MicroRNAome changes in bystander three-dimensional human tissue models suggest priming of apoptotic pathways. Carcinogenesis 2010, 31:1882-1888.
62. Koturbash I., Zemp F., Kolb B., Kovalchuk O. Sex-specific radiation-induced microRNAome responses in the hippocampus, cerebellum and frontal cortex in a mouse model. Mutat. Res./Genetic Toxicol. Environ. Mutagen. 2011, 722:114-118.
63. Mothersill C., Seymour C.B. Radiation-induced bystander effects - implications for cancer. Nat. Rev. Cancer 2004, 4:158-164.
64. Koturbash I., Boyko A., Rodriguez-Juarez R., McDonald R.J., Tryndyak V.P., Kovalchuk I., Pogribny I.P., Kovalchuk O. Role of epigenetic effectors in maintenance of the long-term persistent bystander effect in spleen in vivo. Carcinogenesis 2007, 28:1831-1838.
65. Mothersill C. Are epigenetic mechanisms involved in radiation-induced bystander effects?. Front. Genet 2012, 3:e74.
66. Ilnytskyy Y., Kovalchuk O. Non-targeted radiation effects-an epigenetic connection. Mutat. Res./Fund. Mol. Mech. Mutagen. 2011, 714:113-125.
67. Azzam E.I., de Toledo S.M., Little J.B. Direct evidence for the participation of gap junction-mediated intercellular communication in the transmission of damage signals from α-particle irradiated to nonirradiated cells. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:473-478.
68. Fernandez-Palomo C., Schultke E., Smith R., Brauer-Krisch E., Laissue J., Schroll C., Fazzari J., Seymour C., Mothersill C. Bystander effects in tumor-free and tumor-bearing rat brains following irradiation by synchrotron X-rays. Int. J. Radiat. Biol. 2013, 89:445-453.
69. B. Frey, Y. Rubner, L. Kulzer, N. Werthmoller, E.M. Weiss, R. Fietkau, U.S. Gaipl, 2013. Antitumor immune responses induced by ionizing irradiation and further immune stimulation, Cancer Immunol. Immunother. (in press). [Epub ahead of print].
70. Guo X., Sun J., Bian P., Chen L., Zhan F., Wang J., Xu A., Wang Y., Hei T.K., Wu L. Radiation-induced bystander signaling from somatic cells to germ cells in Caenorhabditis elegans. Radiat. Res. 2013, 180:268-275.
71. Emerit I., Oganesian N., Sarkisian T., Arutyunyan R., Pogosian A., Asrian K., Levy A., Cernjavski L. Clastogenic factors in the plasma of chernobyl accident recovery workers: anticlastogenic effect of Ginkgo biloba extract. Radiat. Res. 1995, 144:198-205.
72. Emerit I., Quastel M., Goldsmith J., Merkin L., Levy A., Cernjavski L., Alaoui-Youssefi A., Pogossian A., Riklis E. Clastogenic factors in the plasma of children exposed at Chernobyl. Mutat. Res./Fund. Mol. Mech. Mutagen. 1997, 373:47-54.
73. Fuchs J., Oelke N., Imhof M., Ochsendorf F., Schöfer H., Oromek G., Alaoui-Youssefi A., Emerit I. Multiparameter analysis of clastogenic factors, pro-oxidant cytokines, and inflammatory markers in HIV-1-infected patients with asymptomatic disease, opportunistic infections, and malignancies. Mol. Med. 1998, 4:333-343.
74. Pant G.S., Kamada N. Chromosome aberrations in normal leukocytes induced by the plasma of exposed individuals. Hiroshima J. Med. Sci. 1977, 26:149-154.
75. Littlefield L.G., Hollowell J.G.J., Pool W.H.J. Chromosomal aberrations induced by plasma from irradiated patients: an indirect effect of X radiation. Further observations and studies of a control population. Radiology 1969, 93:879-886.
76. Alaoui Youssefi A., Arutyunyan R., Emerit I. Chromosome damage in PUVA-treated human lymphocytes is related to active oxygen species and clastogenic factors. Mutat. Res./Fund. Mol. Mech. Mutagen. 1994, 309:185-191.
77. Emerit I., Fabiani J.N., Levy A., Ponzio O., Conti M., Brasme B., Bienvenu P., Hatmi M. Plasma from patients exposed to ischemia reperfusion contains clastogenic factors and stimulates the chemiluminescence response of normal leukocytes. Free Radical Biol. Med. 1995, 19:405-415.
78. Emerit I. Clastogenic factors as potential biomarkers of increased superoxide production. Biomark Insights 2007, 2:429-438.
79. McMahon S.J., Butterworth K.T., McGarry C.K., Trainor C., O'Sullivan J.M., Hounsell A.R., Prise K.M. A computational model of cellular response to modulated radiation fields. Int. J. Radiat. Oncol. Biol. Phys. 2012, 84:250-256.
80. Trainor C., Butterworth K.T., McGarry C.K., McMahon S.J., O'Sullivan J.M., Hounsell A.R., Prise K.M. DNA damage responses following exposure to modulated radiation fields. PLoS One 2012, 7:e43326.
81. Mothersill C., Seymour C. Uncomfortable issues in radiation protection posed by low-dose radiobiology. Radiat. Environ. Biophys. 2013, 52:293-298.
82. Morgan W.F., Bair W.J. Issues in low dose radiation biology: the controversy continues. A perspective. Radiat. Res. 2013, 179:501-510.
83. Mancuso M., Pasquali E., Leonardi S., Tanori M., Rebessi S., Di Majo V., Pazzaglia S., Toni M.P., Pimpinella M., Covelli V., Saran A. Oncogenic bystander radiation effects in patched heterozygous mouse cerebellum. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:12445-12450.
84. Rödel F., Frey B., Gaipl U., Keilholz L., Fournier C., Manda K., Schollnberger H., Hildebrandt G., Rodel C. Modulation of inflammatory immune reactions by low-dose ionizing radiation: molecular mechanisms and clinical application. Curr. Med. Chem. 2012, 19:1741-1750.
85. Rödel F., Keilholz L., Herrmann M., Sauer R., Hildebrandt G. Radiobiological mechanisms in inflammatory diseases of low-dose radiation therapy. Int. J. Radiat. Biol. 2007, 83:357-366.
86. Mothersill C., Seymour R.J., Seymour C.B. Bystander effects in repair-deficient cell lines. Radiat. Res. 2004, 161:256-263.
87. Coates P.J., Lorimore S.A., Wright E.G. Damaging and protective cell signalling in the untargeted effects of ionizing radiation. Mutat. Res./Fund. Mol. Mech. Mutagen. 2004, 568:5-20.
88. Shibutani S., Takeshita M., Grollman A.P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 1991, 349:431-434.
89. Dreher D., Junod A.F. Role of oxygen free radicals in cancer development. Eur. J. Cancer 1996, 32A:30-38.
90. Dröge W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82:47-95.
91. Alexander R.W. Hypertension and the pathogenesis of atherosclerosis: oxidative stress and the mediation of arterial inflammatory response: a new perspective. Hypertension 1995, 25:155-161.
92. Harman D. The aging process. Proc. Natl. Acad. Sci. U.S.A. 1981, 78:7124-7128.
93. R.B. Hamanaka, A. Glasauer, P. Hoover, S. Yang, H. Blatt, A.R. Mullen, S. Getsios, C.J. Gottardi, R.J. DeBerardinis, R.M. Lavker, N.S. Chandel, Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development, Sci. Signal. 6 (2013) ra8-.
94. Wagener F.A., Carels C.E., Lundvig D.M. Targeting the redox balance in inflammatory skin conditions. Int. J. Mol. Sci. 2013, 14:9126-9167.
95. Schaue D., McBride W.H. Links between innate immunity and normal tissue radiobiology. Radiat. Res. 2010, 173:406-417.
96. Stuehr D.J., Santolini J., Wang Z.Q., Wei C.C., Adak S. Update on mechanism and catalytic regulation in the NO synthases. J. Biol. Chem. 2004, 279:36167-36170.
97. Guzik T.J., West N.E.J., Pillai R., Taggart D.P., Channon K.M. Nitric oxide modulates superoxide release and peroxynitrite formation in human blood vessels. Hypertension 2002, 39:1088-1094.
98. O'Donnell V.B., Eiserich J.P., Chumley P.H., Jablonsky M.J., Krishna N.R., Kirk M., Barnes S., Darley-Usmar V.M., Freeman B.A. Nitration of unsaturated fatty acids by nitric oxide-derived reactive nitrogen species peroxynitrite, nitrous acid, nitrogen dioxide, and nitronium ion. Chem. Res. Toxicol. 1998, 12:83-92.
99. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
100. Han D., Antunes F., Canali R., Rettori D., Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem. 2003, 278:5557-5563.
101. Fridovich I. Superoxide anion radical (O2-), superoxide dismutases, and related matters. J. Biol. Chem. 1997, 272:18515-18517.
102. Okado-Matsumoto A., Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu,Zn-SOD in mitochondria. J. Biol. Chem. 2001, 276:38388-38393.
103. Orrenius S. Reactive oxygen species in mitochondria-mediated cell death. Drug Metab. Rev. 2007, 39:443-455.
104. Imlay J.A. Cellular defenses against superoxide and hydrogen peroxide. Ann. Rev. Biochem. 2008, 77:755-776.
105. Imlay J.A., Chin S.M., Linn S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 1988, 240:640-642.
106. Bokoch G.M. Regulation of the human neutrophil NADPH oxidase by the Rac GTP-binding proteins. Curr. Opin. Cell Biol. 1994, 6:212-218.
107. Sundaresan M., Yu Z.X., Ferrans V.J., Sulciner D.J., Gutkind J.S., Irani K., Goldschmidt-Clermont P.J., Finkel T. Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. Biochem. J. 1996, 318:379-382.
108. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999, 13:76-86.
109. Miyata T., Takizawa S., van Ypersele de Strihou C. Hypoxia 1. Intracellular sensors for oxygen and oxidative stress: novel therapeutic targets. Am. J. Physiol. Cell Physiol. 2011, 300:C226-C231.
110. Kobayashi M., Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 2005, 7:385-394.
111. Masuda T., Ito Y., Terada T., Shibata T., Mikawa T. A non-canonical DNA structure enables homologous recombination in various genetic systems. J. Biol. Chem. 2009, 284:30230-30239.
112. Venugopal R., Jaiswal A.K. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:14960-14965.
113. Solis W.A., Dalton T.P., Dieter M.Z., Freshwater S., Harrer J.M., He L., Shertzer H.G., Nebert D.W. Glutamate-cysteine ligase modifier subunit: mouse Gclm gene structure and regulation by agents that cause oxidative stress. Biochem. Pharmacol. 2002, 63:1739-1754.
114. Wang J., Doré S. Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain 2007, 130:1643-1652.
115. Hayes J.D., Chanas S.A., Henderson C.J., McMahon M., Sun C., Moffat G.J., Wolf C.R., Yamamoto M. The Nrf2 transcription factor contributes both to the basal expression of glutathione S-transferases in mouse liver and to their induction by the chemopreventive synthetic antioxidants, butylated hydroxyanisole and ethoxyquin. Biochem. Soc. Trans. 2000, 28:33-41.
116. DeNicola G.M., Karreth F.A., Humpton T.J., Gopinathan A., Wei C., Frese K., Mangal D., Yu K.H., Yeo C.J., Calhoun E.S., Scrimieri F., Winter J.M., Hruban R.H., Iacobuzio-Donahue C., Kern S.E., Blair I.A., Tuveson D.A. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011, 475:106-109.
117. Wang T., Li F., Xu S., Bian P., Wu Y., Wu L., Yu Z. The time course of long-distance signaling in radiation-induced bystander effect in vivo in arabidopsis thaliana demonstrated using root micro-grafting. Radiat. Res. 2011, 176:234-243.
118. Evert B.A., Salmon T.B., Song B., Jingjing L., Siede W., Doetsch P.W. Spontaneous DNA damage in Saccharomyces cerevisiae elicits phenotypic properties similar to cancer cells. J. Biol. Chem. 2004, 279:22585-22594.
119. Salmon T.B., Evert B.A., Song B., Doetsch P.W. Biological consequences of oxidative stress-induced DNA damage in Saccharomyces cerevisiae. Nucl. Acids Res. 2004, 32:3712-3723.
120. Choi K.M., Kang C.M., Cho E.S., Kang S.M., Lee S.B., Um H.D. Ionizing radiation-induced micronucleus formation is mediated by reactive oxygen species that are produced in a manner dependent on mitochondria, Nox1, and JNK. Oncol. Rep. 2007, 17:1183-1188.
121. Schaue D., Kachikwu E.L., McBride W.H. Cytokines in radiobiological responses: a review. Radiat. Res. 2012, 178:505-523.
122. Todd D.G., Mikkelsen R.B., Rorrer W.K., Valerie K., Schmidt-Ullrich R.K. Ionizing radiation stimulates existing signal transduction pathways involving the activation of epidermal growth factor receptor and ERBB-3, and changes of intracellular calcium in A431 human squamous carcinoma cells. J. Recept. Signal. Transduct. Res. 1999, 19:885-908.
123. Ohshima Y., Tsukimoto M., Takenouchi T., Harada H., Suzuki A., Sato M., Kitani H., Kojima S. Γ-Irradiation induces P2X7 receptor-dependent ATP release from B16 melanoma cells. Biochim. Biophys. Acta 1800, 2010:40-46.
124. Zhang X., Rosenstein B.S., Wang Y., Lebwohl M., Wei H. Identification of possible reactive oxygen species involved in ultraviolet radiation-induced oxidative DNA damage. Free Radic. Biol. Med. 1997, 23:980-985.
125. MacNaughton W.K., Aurora A.R., Bhamra J., Sharkey K.A., Miller M.J. Expression, activity and cellular localization of inducible nitric oxide synthase in rat ileum and colon post-irradiation. Int. J. Radiat. Biol. 1998, 74:255-264.
126. Tateishi Y., Sasabe E., Ueta E., Yamamoto T. Ionizing irradiation induces apoptotic damage of salivary gland acinar cells via NADPH oxidase 1-dependent superoxide generation. Biochem. Biophys. Res. Commun. 2008, 366:301-307.
127. Kang M.A., So E.Y., Simons A.L., Spitz D.R., Ouchi T. DNA damage induces reactive oxygen species generation through the H2AX-Nox1/Rac1 pathway. Cell Death Dis. 2012, 3:e249.
128. Zhang X., Ng W.-L., Wang P., Tian L., Werner E., Wang H., Doetsch P., Wang Y. MicroRNA-21 modulates the levels of reactive oxygen species by targeting SOD3 and TNFα. Cancer Res. 2012, 72:4707-4713.
129. Liu J., Cao L., Chen J., Song S., Lee I.H., Quijano C., Liu H., Keyvanfar K., Chen H., Cao L.-Y., Ahn B.-H., Kumar N.G., Rovira I.I., Xu X.-L., van Lohuizen M., Motoyama N., Deng C.-X., Finkel T. Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 2009, 459:387-392.
130. Lehnert B.E., Goodwin E.H. Extracellular factor(s) following exposure to α particles can cause sister chromatid exchanges in normal human cells. Cancer Res. 1997, 57:2164-2171.
131. Brach M., Hass R., Sherman M.L., Gunji H., Weichselbaum R., Kufe D. Ionizing radiation induces expression and binding activity of the nuclear factor kB. J. Clin. Invest. 1991, 88:691-695.
132. Weichselbaum R.R., Hallahan D., Fuks Z., Kufe D. Radiation induction of immediate early genes: effectors of the radiation-stress response. Int. J. Radiat. Oncol. Biol. Phys. 1994, 30:229-234.
133. Lee S.-J., Dimtchev A., Lavin M.F., Dritschilo A., Jung M. A novel ionizing radiation-induced signaling pathway that activates the transcription factor NF-κB. Oncogene 1998, 17:1821-1826.
134. Schieven G., Kirihara J., Myers D., Ledbetter J., Uckun F. Reactive oxygen intermediates activate NF-kappa B in a tyrosine kinase-dependent mechanism and in combination with vanadate activate the p56lck and p59fyn tyrosine kinases in human lymphocytes. Blood 1993, 82:1212-1220.
135. Hallahan D.E., Spriggs D.R., Beckett M.A., Kufe D.W., Weichselbaum R.R. Increased tumor necrosis factor alpha mRNA after cellular exposure to ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:10104-10107.
136. Chiang C.S., McBride W.H., Withers H.R. Radiation-induced astrocytic and microglial responses in mouse brain. Radiother. Oncol. 1993, 29:60-68.
137. Baker W.H., Limanni A., Chang C.M., Jackson W.E., Seemann R., Patchen M.L. Comparison of interleukin-1 alpha gene expression and protein levels in the murine spleen after lethal and sublethal total-body irradiation. Radiat. Res. 1995, 143:320-326.
138. Hosoi Y., Miyachi H., Matsumoto Y., Enomoto A., Nakagawa K., Suzuki N., Ono T. Induction of interleukin-1β and interleukin-6 mRNA by low doses of ionizing radiation in macrophages. Int. J. Cancer 2001, 96:270-276.
139. Johnston C.J., Williams J.P., Okunieff P., Finkelstein J.N. Radiation-induced pulmonary fibrosis: examinatin of chemokine and chemokine receptor families. Radiat. Res. 2002, 157:256-265.
140. Wang T., Zhang X., Li J.J. The role of NF-κB in the regulation of cell stress responses. Int. Immunopharmacol. 2002, 2:1509-1520.
141. Baldwin A.S. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 1996, 14:649-681.
142. Jones P.L., Ping D., Boss J.M. Tumor necrosis factor alpha and interleukin-1beta regulate the murine manganese superoxide dismutase gene through a complex intronic enhancer involving C/EBP-beta and NF-kappaB. Mol. Cell. Biol. 1997, 17:6970-6981.
143. Wang C.-Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress Caspase-8 activation. Science 1998, 281:1680-1683.
144. Mayo M.W., Wang C.-Y., Cogswell P.C., Rogers-Graham K.S., Lowe S.W., Der C.J., Baldwin A.S. Requirement of NF-κB activation to suppress p53-independent apoptosis induced by oncogenic ras. Science 1997, 278:1812-1815.
145. Wang C.-Y., Guttridge D.C., Mayo M.W., Baldwin A.S. NF-κB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol. Cell. Biol. 1999, 19:5923-5929.
146. Simon H.-U., Haj-Yehia A., Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5:415-418.
147. Bragado P., Armesilla A., Silva A., Porras A. Apoptosis by cisplatin requires p53 mediated p38alpha MAPK activation through ROS generation. Apoptosis 2007, 12:1733-1742.
148. Liu B., Chen Y., St D.K. Clair, ROS and p53: a versatile partnership. Free Radic. Biol. Med. 2008, 44:1529-1535.
149. Sablina A.A., Budanov A.V., Ilyinskaya G.V., Agapova L.S., Kravchenko J.E., Chumakov P.M. The antioxidant function of the p53 tumor suppressor. Nat. Med. 2005, 11:1306-1313.
150. Tomko R.J.J., Bansal P., Lazo J.S. Airing out an antioxidant role for the tumor suppressor p53. Mol. Interv. 2006, 6:23-25.
151. Stambolsky P., Weisz L., Shats I., Klein Y., Goldfinger N., Oren M., Rotter V. Regulation of AIF expression by p53. Cell Death Differ. 2006, 13:2140-2149.
152. Drane P., Bravard A., Bouvard V., May E. Reciprocal down-regulation of p53 and SOD2 gene expression-implication in p53 mediated apoptosis. Oncogene 2001, 20:430-439.
153. Dhar S.K., Xu Y., Chen Y., Clair D.K.S. Specificity protein 1-dependent p53-mediated suppression of human manganese superoxide dismutase gene expression. J. Biol. Chem. 2006, 281:21698-21709.
154. Polyak K., Xia Y., Zweier J.L., Kinzler K.W., Vogelstein B. A model for p53-induced apoptosis. Nature 1997, 389:300-305.
155. Rivera A., Maxwell S.A. The p53-induced gene-6 (proline oxidase) mediates apoptosis through a calcineurin-dependent pathway. J. Biol. Chem. 2005, 280:29346-29354.
156. Liu Z., Lu H., Shi H., Du Y., Yu J., Gu S., Chen X., Liu K.J., Hu C.-A.A. PUMA overexpression induces reactive oxygen species generation and proteasome-mediated stathmin degradation in colorectal cancer cells. Cancer Res. 2005, 65:1647-1654.
157. Tawa R., Kimura Y., Komura J.-I., Miyamura Y., Kurishita A., Sasaki M.S., Sakurai H., Ono T. Effects of X-ray irradiation on genomic DNA methylation levels in mouse tissues. J. Radiat. Res. 1998, 39:271-278.
158. Franco R., Schoneveld O., Georgakilas A.G., Panayiotidis M.I. Panayiotidis, oxidative stress, DNA methylation and carcinogenesis. Cancer Lett. 2008, 266:6-11.
159. Niture S.K., Khatri R., Jaiswal A.K. Regulation of Nrf2-an update. Free Rad. Biol. Med. 2014, 66:36-44.
160. Bauer A.K., Cho H.-Y., Miller-DeGraff L., Walker C., Helms K., Fostel J., Yamamoto M., Kleeberger S.R. Targeted deletion of Nrf2 reduces urethane-induced lung tumor development in mice. PLoS One 2011, 6:e26590.
161. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
162. Kim J.W., Dang C.V. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 2006, 66:8927-8930.
163. Bauer G. Low dose radiation and intercellular induction of apoptosis: potential implications for the control of oncogenesis. Int. J. Radiat. Biol. 2007, 83:887-902.
164. Schaue D., Xie M.W., Ratikan J.A., McBride W.H. Regulatory T cells in radiotherapeutic responses. Front. Oncol. 2012, 2:90.
165. Lyng F.M., Howe O.L., McClean B. Reactive oxygen species-induced release of signalling factors in irradiated cells triggers membrane signalling and calcium influx in bystander cells. Int. J. Radiat. Biol. 2011, 87:683-695.
166. Shao C., Lyng F.M., Folkard M., Prise K.M. Calcium fluxes modulate the radiation-induced bystander responses in targeted glioma and fibroblast cells. Radiat. Res. 2006, 166:479-487.
167. Banaz-Yasar F., Lennartz K., Winterhager E., Gellhaus A. Radiation-induced bystander effects in malignant trophoblast cells are independent from gap junctional communication. J. Cell. Biochem. 2008, 103:149-161.
168. Dieriks B., De Vos W.H., Derradji H., Baatout S., Van Oostveldt P. Medium-mediated DNA repair response after ionizing radiation is correlated with the increase of specific cytokines in human fibroblasts. Mutat. Res./Fund. Mol. Mech. Mutagen. 2010, 687:40-48.
169. Mariotti L.G., Bertolotti A., Ranza E., Babine G., Ottolenghi A. Investigation of the mechanisms underpinning IL-6 cytokine release in bystander responses: the roles of radiation dose, radiation quality and specific ROS/RNS scavengers. Int. J. Radiat. Biol. 2012, 88:751-762.
170. Chou C.H., Chen P.-J., Lee P.-H., Cheng A.-L., Hsu H.-C., Cheng J.C.-H. Radiation-induced hepatitis B virus reactivation in liver mediated by the bystander effect from irradiated endothelial cells. Clin. Cancer Res. 2007, 13:851-857.
171. Ivanov V.N., Zhou H., Ghandhi S.A., Karasic T.B., Yaghoubian B., Amundson S.A., Hei T.K. Radiation-induced bystander signaling pathways in human fibroblasts: a role for interleukin-33 in the signal transmission. Cell. Signal. 2010, 22:1076-1087.
172. Shao C., Folkard M., Prise K.M. Role of TGF-β1 and nitric oxide in the bystander response of irradiated glioma cells. Oncogene 2008, 27:434-440.
173. 21. Radiat. Res. 2010, 173:769-778.
174. Desai S., Kumar A., Laskar S., Pandey B.N. Cytokine profile of conditioned medium from human tumor cell lines after acute and fractionated doses of gamma radiation and its effect on survival of bystander tumor cells. Cytokine 2013, 61:54-62.
175. Zhou H., Ivanov V.N., Lien Y.-C., Davidson M., Hei T.K. Mitochondrial function and nuclear factor-κB-mediated signaling in radiation-induced bystander effects. Cancer Res. 2008, 68:2233-2240.
176. Karin M. Nuclear factor-κB in cancer development and progression. Nature 2006, 441:431-436.
177. Karin M., Yamamoto Y., Wang Q.M. The IKK NF-κB system: a treasure trove for drug development. Nat. Rev. Drug Discov. 2004, 3:17-26.
178. Ghandhi S.A., Yaghoubian B., Amundson S.A. Global gene expression analyses of bystander and alpha particle irradiated normal human lung fibroblasts: synchronous and differential responses. BMC Med. Genomics 2008, 1:63.
179. Zhou H., Ivanov V.N., Gillespie J., Geard C.R., Amundson S.A., Brenner D.J., Yu Z., Lieberman H.B., Hei T.K. Mechanism of radiation-induced bystander effect: role of the cyclooxygenase-2 signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:14641-14646.
180. Picchio M.C., Scala E., Pomponi D., Caprini E., Frontani M., Angelucci I., Mangoni A., Lazzeri C., Perez M., Remotti D., Bonoldi E., Benucci R., Baliva G., Lombardo G.A., Napolitano M., Russo G., Narducci M.G. CXCL13 is highly produced by sézary cells and enhances their migratory ability via a synergistic mechanism involving CCL19 and CCL21 chemokines. Cancer Res. 2008, 68:7137-7146.
181. Ditch S., Paull T.T. The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem. Sci. 2012, 37:15-22.
182. Guo Z., Kozlov S., Lavin M.F., Person M.D., Paull T.T. ATM activation by oxidative stress. Science 2010, 330:517-521.
183. Hei T.K., Zhou H., Ivanov V.N., Hong M., Lieberman H.B., Brenner D.J., Amundson S.A., Geard C.R. Mechanism of radiation-induced bystander effects: a unifying model. J. Pharm. Pharmacol. 2008, 60:943-950.
184. Mothersill C., Bristow R.G., Harding S.M., Smith R.W., Mersov A., Seymour C.B. A role for p53 in the response of bystander cells to receipt of medium borne signals from irradiated cells. Int. J. Radiat. Biol. 2011, 87:1120-1125.
185. Camphausen K., Moses M.A., Menard C., Sproull M., Beecken W.-D., Folkman J., O'Reilly M.S. Radiation abscopal antitumor effect is mediated through p53. Cancer Res. 2003, 63:1990-1993.
186. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.-Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckmann L., Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103-113.
187. Kashino G., Prise K.M., Suzuki K., Matsuda N., Kodama S., Suzuki M., Nagata K., Kinashi Y., Masunaga S.-I., Ono K., Watanabe M. Effective suppression of bystander effects by DMSO treatment of irradiated CHO cells. J. Radiat. Res. 2007, 48:327-333.
188. Burdak-Rothkamm S., Rothkamm K., Prise K.M. ATM acts downstream of ATR in the DNA damage response signaling of bystander cells. Cancer Res. 2008, 68:7059-7065.
189. Koturbash I., Rugo R.E., Hendricks C.A., Loree J., Thibault B., Kutanzi K., Pogribny I., Yanch J.C., Engelward B.P., Kovalchuk O. Irradiation induces DNA damage and modulates epigenetic effectors in distant bystander tissue in vivo. Oncogene 2006, 25:4267-4275.
190. Dickey J.S., Baird B.J., Redon C.E., Avdoshina V., Palchik G., Wu J., Kondratyev A., Bonner W.M., Martin O.A. Susceptibility to bystander DNA damage is influenced by replication and transcriptional activity. Nucl. Acids Res. 2012, 40:10274-10286.
191. S.I. Grivennikov, K. Wang, D. Mucida, C.A. Stewart, B. Schnabl, D. Jauch, K. Taniguchi, G.-Y. Yu, C.H. Osterreicher, K.E. Hung, C. Datz, Y. Feng, E.R. Fearon, M. Oukka, L. Tessarollo, V. Coppola, F. Yarovinsky, H. Cheroutre, L. Eckmann, G. Trinchieri, M. Karin, Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth, Nature, advance online publication (2012), Cancer - PDF.
192. Pikarsky E., Porat R.M., Stein I., Abramovitch R., Amit S., Kasem S., Gutkovich-Pyest E., Urieli-Shoval S., Galun E., Ben-Neriah Y. NF-κB functions as a tumour promoter in inflammation-associated cancer. Nature 2004, 431:461-466.
193. Dickey J.S., Baird B.J., Redon C.E., Sokolov M.V., Sedelnikova O.A., Bonner W.M. Intercellular communication of cellular stress monitored by {gamma}-H2AX induction. Carcinogenesis 2009, 30:1686-1695.
194. Davalos A.R., Coppe J.-P., Campisi J., Desprez P.-Y. Senescent cells as a source of inflammatory factors for tumor progression. Cancer Metastasis Rev. 2010, 29:273-283.
195. Jüngst C., Cheng B., Gehrke R., Schmitz V., Nischalke H.D., Ramakers J., Schramel P., Schirmacher P., Sauerbruch T., Caselmann W.H. Oxidative damage is increased in human liver tissue adjacent to hepatocellular carcinoma. Hepatology 2004, 39:1663-1672.
196. Streffer C., van Beuningen D., Bamberg M., Eigler F.-W., Gross E., Schabronath J. An approach to the individualization of cancer therapy - determination of DNA, SH-groups and micronuclei. Strahlenther Onkol. 1984, 160:661-666.
197. Wolff S. The adaptive response in radiobiology: evolving insights and implications. Environ. Health Perspect. 1998, 106(Suppl. 1):277-283.
198. Yonezawa M., Misonoh J., Hosokawa Y. Two types of X-ray-induced radioresistance in mice: presence of 4 dose ranges with distinct biological effects. Mutat. Res./Fund. Mol. Mech. Mutagen. 1996, 358:237-243.
199. Cai L., Liu S.-Z. Induction of cytogenetic adaptive response of somatic and germ cells in vivo and in vitro by low-dose X-irradiation. Int. J. Radiat. Biol. 1990, 58:187-194.
200. Mitchel R.E.J., Azzam E.I., de Toledo S.M. Adaption to ionizing radiation in mammalian cells. Stress-Inducible Processes in Higher Eukaryotic Cells 1997, 221-243. Plenum Press, New York. T.M. Koval (Ed.).
201. Matsumoto H., Hamada N., Takahashi A., Kobayashi Y., Ohnishi T. Vanguards of paradigm shift in radiation biology: radiation-induced adaptive and bystander responses. J. Radiat. Res. 2007, 48:97-106.
202. Olivieri G., Bodycote J., Wolff S. Adaptive response of human lymphocytes to low concentrations of radioactive thymidine. Science 1984, 223:594-597.
203. Zhou H., Randers-Pehrson G., Geard C.R., Brenner D.J., Hall E.J., Hei T.K. Interaction between radiation-induced adaptive response and bystander mutagenesis in mammalian cells. Radiat. Res. 2003, 160:512-516.
204. de Toledo S.M., Asaad N., Venkatachalam P., Li L., Howell R.W., Spitz D.R., Azzam E.I. Adaptive response to low-dose/low-dose-rate γ rays in normal human fibroblasts: the role of growth architecture and oxidative metabolism. Radiat. Res. 2006, 166:849-857.
205. Yatagai F., Sugasawa K., Enomoto S., Honma M. An approach to estimate radioadaptation from DSB repair efficiency. J. Radiat. Res. 2009, 50:407-413.
206. Yatagai F., Suzuki M., Ishioka N., Ohmori H., Honma M. Repair of I-SceI Induced DSB at a specific site of chromosome in human cells: influence of low-dose, low-dose-rate gamma-rays. Radiat. Environ. Biophys. 2008, 47:439-444.
207. Kim J.J., Tannock I.F. Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat. Rev. Cancer 2005, 5:516-525.
208. Matsumoto H., Hayashi S., Hatashita M., Ohnishi K., Shioura H., Ohtsubo T., Kitai R., Ohnishi T., Kano E. Induction of radioresistance by a nitric oxide-mediated bystander effect. Radiat. Res. 2001, 155:387-396.
209. Sawant S.G., Randers-Pehrson G., Metting N.F., Hall E.J. Adaptive response and the bystander effect induced by radiation in C3H 10T1/2 cells in culture. Radiat. Res. 2001, 156:177-180.
210. Ahmed K.M., Nantajit D., Fan M., Murley J.S., Grdina D.J., Li J.J. Coactivation of ATM/ERK/NF-κB in the low-dose radiation-induced radioadaptive response in human skin keratinocytes. Free Radic. Biol. Med. 2009, 46:1543-1550.
211. Scully R., Xie A. Double strand break repair functions of histone H2AX. Mutat. Res./Fund. Mol. Mech. Mutagen. 2013, 750:5-14.
212. Cao N., Li S., Wang Z., Ahmed K.M., Degnan M.E., Fan M., Dynlacht J.R., Li J.J. NF-κB-mediated HER2 overexpression in radiation-adaptive resistance. Radiat. Res. 2009, 171:9-21.
213. Fan M., Ahmed K.M., Coleman M.C., Spitz D.R., Li J.J. Nuclear factor-κB and manganese superoxide dismutase mediate adaptive radioresistance in low-dose irradiated mouse skin epithelial cells. Cancer Res. 2007, 67:3220-3228.
214. Nguyen T., Brunson D., Crespi C.L., Penman B.W., Wishnok J.S., Tannenbaum S.R. DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:3030-3034.
215. Kundrát P., Bauer G., Jacob P., Friedland W. Mechanistic modelling suggests that the size of preneoplastic lesions is limited by intercellular induction of apoptosis in oncogenically transformed cells. Carcinogenesis 2012, 33:253-259.
216. Wink D.A., Hanbauer I., Grisham M.B., Laval F., Nims R.W., Laval J., Cook J., Pacelli R., Liebmann J., Krishna M., Ford P.C., Mitchell J.B. Chemical biology of nitric oxide: regulation and protective and toxic mechanisms. Curr. Top. Cell. Regul. 1996, 34:159-187.
217. Kim S.B., Pandita R.K., Eskiocak U., Ly P., Kaisani A., Kumar R., Cornelius C., Wright W.E., Pandita T.K., Shay J.W. Targeting of Nrf2 induced DNA damage signaling and protects colonic epithelial cells from ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E2949-2955.
218. Schwartz J.L. Variability: the common factor linking low dose-induced genomic instability, adaptation and bystander effects. Mutat. Res./Fund. Mol. Mech. Mutagen. 2007, 616:196-200.
219. Osterreicher J., Skopek J., Jahns J., Hildebrandt G., Psutka J., Vilasova Z., Tanner J.M., Vogt J., Butz T. Beta1-integrin and IL-1alphs expression as bystander effect of medium from irradiated cells: the pilot study. Acta. Histochem. 2003, 105:223-230.