Radiation-induced versus endogenous DNA damage: Possible effect of inducible protective responses in mitigating endogenous damage

Human and Experimental Toxicology

Volumn 22, Issue 6, 2003, Pages 290-306

  Pollycove, Myron ^a   Feinendegen, Ludwig E ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGEN; DNA; REACTIVE OXYGEN METABOLITE; TRACE ELEMENT;

ADAPTATION; AGING; APOPTOSIS; CANCER INCIDENCE; CARCINOGENESIS; CELL DAMAGE; CELL PROTECTION; CORRELATION ANALYSIS; DNA DAMAGE; DNA REPAIR; HUMAN; HYPOTHESIS; IMMUNE SYSTEM; INCIDENCE; IONIZING RADIATION; LINEAR ENERGY TRANSFER; LINEAR SYSTEM; MALIGNANT NEOPLASTIC DISEASE; MALIGNANT TRANSFORMATION; MAMMAL CELL; OUTCOMES RESEARCH; POLLUTANT; PRIORITY JOURNAL; PROBABILITY; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RADIATION ABSORPTION; RADIATION DOSE; RADIATION HAZARD; RADIATION INJURY; REVIEW; SIGNAL TRANSDUCTION; STEADY STATE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; APOPTOSIS; CELL TRANSFORMATION, NEOPLASTIC; CYTOPROTECTION; DNA; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, RADIATION; HUMANS; LINEAR MODELS; NEOPLASMS, RADIATION-INDUCED; REACTIVE OXYGEN SPECIES;

MAMMALIA;

EID: 0038730829     PISSN: 09603271     EISSN: None     Source Type: Journal    
DOI: 10.1191/0960327103ht365oa     Document Type: Review

References (112)

1. UNSCEAR. Sources and effects of ionizing radiation. Annex B: Adaptive responses to radiation in cells and organisms. New York: United Nations, 1994: 185-272.
2. ICRP (International Commission on Radiological Protection). Recommendations of the International comn-fission on radiological protection. ICRP Publication 60. Annals of the ICRP 21 (1-3), Oxford: Pergamon Press, 1991.
3. Ames BN, Gold LS, Willet WC. The causes and prevention of cancer. Proc Natl Acad Sci USA 1995; 92: 5258-65.
4. Beckman KD, Ames BN. Oxidative decay of DNA. J Biol Chem 1997; 272: 19633-36.
5. Helbock HJ, Beckman KB, Shigenaga MK, Walter PB, Woodall AA, Yeo HC, Ames BN. DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Natl Acad Sci USA 1998; 96: 288-93.
6. Blount BC, Mack MM, Wehr CM, MacGregor JT, Hiatt RA, Wang G, Wickramasinghe SN, Everson RB, Ames BN. Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc Natl Acad Sci USA 1997; 94: 3290-95.
7. Ames BN. Micronutrients prevent cancer and delay aging. Toxicol Lett 1998; 102-103: 5-18.
8. Fenech M, Aitken C, Rinaldi J. Folate, vitamin B12, homocysteine status and DNA damage in young Australian adults. Carcinogenesis 1998 19: 1163-71.
9. Potten CS. Extreme sensitivity of some intestinal crypt cells to X and ? irradiation. Nature 1977; 269: 518-21.
10. Kondo S. Health effects of low level radiation. Osaka: Kinki University Press, Madison, WI: Medical Physics Publishing, 1993.
11. Wei Q, Matanoski GM, Farmer ER, Hedayati MA, Grossman L. DNA repair and aging in basal cell carcinoma: A molecular epidemiologic study. Proc Natl Acad Sci USA 1993; 90: 1614-18.
12. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD eds. Molecular biology of the cell, third edition. New York: Garland Publishing, 1994.
13. Friedberg EC, Walker GC, Siede W. DNA repair and mutagenesis. Washington DC: ASM Press, 1995.
14. Hanawalt PC. DNA repair comes of age. Mutat Res 1995; 336:101-13.
15. Lohman PHM., Cox R, Chadwick KH. Role of molecular biology in radiation biology. Int J Rad Biol. 1995; 68: 331-40.
16. Jaruga P, Dizdaroglu M. Repair of products of oxidative DNA base damage in human cells. Nucleic Acid Res 1996; 24: 1389-94.
17. Wallace SS. Enzymatic processing of radiation-induced free radical damage in DNA. Rad Res 1998; 150 (5 Suppl): 60-79.
18. 18 Ohyama H, Yamada T. Radiation-induced apoptosis: a review. In Yamada T, Hashimoto Y, eds. Apoptosis, its roles and mechanisms. Tokyo: Business Center for Academic Societies, 1998: 141-86.
19. Radiation Research Society (USA). Program abstracts, 46th Annual Meeting in Louisville, Kentucky. Oak Brook, IL: Radiation Research Society, 1998.
20. Eisen JA, Hanawalt PC. A phylogenomic study of DNA repair genes, proteins and processes. Mutat Res 1999; 435: 171-213.
21. Melov S, Ravenscroft J, Malik S, Gill MS, Walker DW, Clayton PE, Wallace DC, Malfroy B, Doctrow SR, Lithgow GJ. Extension of life span with superoxide dismutase/catalase mimetics. Science 2000; 289: 1567-69.
22. Wood RD, Mitchell M, Sgouros J, Lindahl T. Human DNA repair genes. Science 2001; 291: 1284-89.
23. Abbas AK, Lichtman AH, Pober JS. Cellular and molecular immunology, fourth edition. Philadelphia: Saunders Company, 2000.
24. Cleaver J. Defective repair replication of DNA in Xeroderma Pigmentosum. Nature 1968; 218: 652-56.
25. Kirkwood TBL, Austad SN. Why do we age? Nature 2000; 408: 233-38.
26. Feinendegen LE, Pollycove M. Biological responses to low doses of ionizing radiation: detriment versus hormesis. Part 1. Dose responses of cells and tissues. J Nucl Med 2001; 42(7): 17N-27N.
27. Pollycove M, Feinendegen LE. Molecular biology, epidemiology, and the demise of the linear no-threshold (LNT) hypothesis. Compt Rend Acad Sci Paris, Life Sciences 1999; 322: 197-204.
28. Pollycove M, Feinendegen LE. Biological responses to low doses of ionizing radiation: Dertriment versus hormesis. Part 2. Dose responses of organisms. J Nucl Med 2001; 42(9): 26N-37N.
29. von Sonntag C. The chemical basis for radiation biology. London, Philadelphia, New York: Taylor&Francis, 1987.
30. Beckman KD, Ames BN. The free radical theory of aging matures. Physiol Rev 1998; 78: 547-81.
31. ICRU (International Commission on Radiation Units and Measurements). Microdosimetry. Report 36. Bethesda, MD: ICRU, 1983.
32. ICRU (International Commission on Radiation Units and Measurements). Radiation quantities and units. Report 33. Bethesda, MD: ICRU, 1980.
33. Booz J, Feinendegen LE. A microdosimetric understanding of low-dose radiation effects. Int J Radiat Biol 1988; 53: 13-21.
34. Feinendegen LE, Booz J, Bond VP, Sondhaus CA. Microdosimetric approach to the analysis of cell responses at low dose and low dose rate. Rad Prot Dosim 1985; 13: 299-306.
35. Nagasawa H, Little JB. Induction of sister chromatid exchanges by extremely low doses of alpha-particles. Cancer Res 1992; 52: 6394-96.
36. Azzam EI, de Toledo SM, Gooding T, Little JB. Intercellular communication is involved in the bystander regulation of gene expression in human cells exposed to very low fluence of alpha particles. Rad Res 1998; 150: 497-504.
37. Seymour CB, Mothersill C. Relative contrribution of bystander and targeted cell killing to the low-dose region of the radiation dose-response curve. Rad Res 2000; 153: 508-11.
38. NCRP (National Council on Radiation Protection). Tritium and other radionuclide labelled organic compounds incorporated in genetic materials. Bethesda MD; NCRP, Publication 63, 1979.
39. Feinendegen LE, Bond VP, Booz J. The quantification of physical events within tissue at low levels of exposure to ionizing radiation. ICRU News 1994; 2: 9-13.
40. Ward JF. DNA damage produced by ionizing radiation in mammalian cells: Identities, mechanisms of formation, and repairability. Prog Nucleic Acid Res Mol Biol 1988; 35: 95-125.
41. Feinendegen LE, Loken M, Booz J, Muehlensiepen H, Sondhaus CA, Bond VP. Cellular mechanisms of protection and repair induced by radiation exposure and their consequences for cell system responses. Stem Cells 1995; 13: 7-20.
42. Weaver VM, Fischer AH, Peterson OW, Bissell MJ. The importance of the microenvironment in breast cancer progression: recapitulation of mammary tumorigenesis using a three-dimensional culture assay. Biochem Cell Biol 1996; 74: 833-51.
43. Barcellos-Hoff MH, Brooks AL. Extracellular signaling through the microenvironment: a hypothesis relating carcinogenesis; bystander effects, and genomic instability. Rad Res 2001; 156: 618-27.
44. Kasprzak KS, Diwan BA, Rice JM, Misra M, Olinski R, Dizdaroglu M. Nickel (11)-mediated oxidative DNA base damage in rat renal chromatin in vivo. Possible relevance to nickel (II) carcinogenesis. Chem Res Toxicol 1992; 5: 809-15.
45. Kasprzak KS, Zastawny TH, North SL, Riggs CW, Diwan BA, JM, Dizdaroglu M. Oxidative DNA base damage in renal, hepatic and pulmonary chromatin of rats after intraperitoneal injection of cobalt acetate. Chem Res Toxicol 1994; 7: 329-35.
46. Nakae D, Mizurnoto Y, Kobayashi E, Noguchi O, Konishi Y. Improved genomic/nuclear DNA extraction for 8-hydroxydeoxyguanosine analysis of small amounts of rat liver tissue. Cancer Lett 1995; 97: 233-39.
47. Olinski R, Zastawny TH, Foksinki M, Barecki A, Dizdaroglu M. DNA base modifications and antioxidant enzyme activities in human benign prostatic hyperplasia. Free Radic Biol Med 1995; 18: 807-13.
48. Nakajima M, Takeuchi T, Morimoto K. Determination of 8-hydroxydeoxguanosine in human cells under oxygen-free conditions. Carcinogenesis 1996; 17: 787-91.
49. Olinski R, Zastawny TH, Foksinski M, Windorbska W, Jaruga P, Dizdaroglu M. DNA base damage in lymphocytes of cancer patients undergoing radiation therapy. Cancer Lett 1996; 106: 207-15.
50. Wilson III DM, Barsky D. The major human abasic endonuclease formation, consequences and repair of abasic lesions in DNA. Mutat Res 2001; 485: 283-27.
51. Atamna H, Cheung I, Ames BN. A method for detecting abasic sites in living cells: Age-dependent changes in base excision repair. Proc Natl Acad Sci USA 2000; 97: 686-91.
52. Lee XC, Xing JZ, Lee J, Leadon SA, Weinfeld M. Inducible repair of thymine glycol detected by an ultrasensitive assay for DNA damage. Science 1998; 280: 1066-69.
53. Frankenberg-Schwager M. Induction, repair and biological relevance of radiation-induced DNA lesions in eukaryotic cells. Radiat Environ Biophys 1990; 29: 273-92.
54. Lindahl T. The Croonian Lecture 1996: endogenous damage to DNA. Philos Trans R Soc Lond B Biol Sci 1996; 35(1347): 1529-38.
55. Ottolenghi A, Merzagora M, Tallone L, Durante M, Paretzke HG, Wilson WE. The quality of DNA double-strand breaks: a Monte Carlo simulation of the end-structure of strand breaks produced by protons and alpha particles. Radiat Environ Biophys 1995; 34: 239-44.
56. Ward JF, Blakely WJ, Joner EI. Mammalian cells are not killed by DNA single-strand breaks caused by hydroxyl radicals from hydrogen peroxide. Rad Res 1985; 103: 383-92.
57. Chance B, Sies H, Boveris A. Hydroperoxide Metabolism in Mammalian Organs. Physiol Rev 1979; 59: 527-605.
58. von Sonntag C, Hagen U, Schoen-Bopp A, Schulte-Frohlinde D. Radiation-induced strand breaks in DNA: chemical and enzymatic analysis of end groups and mechanistic aspects. Adv Rad Biol 1981; 9: 109-42.
59. MacGregor JT, Wehr CM, Hiatt RA, Peters B, Tucker JD, Langlois RG, Jacob RA, Jensen RH, Yager JW, Shigenaga MK, Frei B, Eynon BP, Ames BN. Spontaneous genetic damage in man: evaluation of inter-individual variability, relationship among markers of damage, and influence of nutritional status. Mutat Res 1997; 377: 125-35.
60. Fenech M. Micronucleus frequency in human lymphocytes is related to plasma vitamin B12 and homocysteine. Mutat Res 1999; 428: 299-304.
61. Block G, Patterson B, Subar A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr Cancer 1992; 18: 1-29.
62. Chaudhry MA, Weinfeld M. The action of Escherichia coli endonuclease III on multiply damaged sites in DNA. J Mol Biol 1995; 249: 914-22.
63. Schuenemann S, Schulte-Frohlinde D. Survival of phage M13 with uracils on one or both DNA strands. Mol Gen Genet 1992; 233: 348-54.
64. Ventur Y, Schulte-Frohlinde D. Does enzymatic conversion of DNA single strand damage into double strand breaks contribute to biological inactivation of gamma-irradiated plasmid DNA? Intern J Rad Biol 1993; 63: 167-71.
65. Ventur Y, Schulte-Frohlinde D. Biological inactivation of pBr322 plasmid DNA by enzyme- and radiation-induced single strand damage under various conditions. Mutat Res DNA Repair 1994; 315: 65-74.
66. Stewart RD. On the complexity of the DNA damages created by endogenous processes. Rad Res 1999; 152: 1101-102.
67. Anderson RE. Effects of low-dose radiation on the immune response. In Calabrese EJ ed. Biological effects of low level exposures to chemicals and radiation. Chelsea, MI: Lewis Publishing Inc., 1992: 95-112.
68. Makinodan T. Cellular and subcellular alteration in immune cells induced by chronic, intermittent exposure in vivo to very low dose of ionizing radiation (ldr) and its ameliorating effects on progression of autoimmune disease and mammary tumor growth. In Sugahara T, Sagan LA, Aoyama T eds. Low-dose irradiation and biological defense mechanisms. Amsterdam, London, New York, Tokyo: Exerpta Medica, 1999: 233-37.
69. Sakamoto K, Myojin M, Hosoi Y, Ogawa Y, Nemoto K, Takai Y, Kakuto Y, Yamada S, Watabe N. Fundamental and clinical studies on cancer control with total or upper half body irradiation. J Jpn Soc Ther Radiol Oncol 1997; 9: 161-75.
70. Hashimoto S, Shirato H, Hosokawa M, Nishioka T, Kuramitsu Y, Matushita K, Kobayashi M, Miyasaka K. The suppression of metastases and the change in host immune response after low-dose total-body irradiation in tumor-bearing rats. Rad Res 1999; 151: 717-24.
71. Ramana CV, Boldogh I, Izumi T, Mira S. Activation of apurinic/aprymidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotocicity of free radicals. Proc Natl Acad Sci USA 1998; 95: 5061-66.
72. Feinendegen LE, Muehlensiepen H, Bond VP, Sondhaus CA. Intracellular stimulation of biochemical control mechanisms by low-dose low-LET irradiation. Health Phys 1987; 52: 663-69.
73. Hohn-El-Karim K, Muehlensiepen H, Altman KI, Feinendegen LE. Modification of effects of radiation on thymidine kinase. Int J Radiat Biol 1990; 58: 97-110.
74. Chandra J, Samali A, Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 2000; 29: 323-33.
75. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000; 408: 239-47.
76. Feinendegen LE, Bond VP, Booz J, Muehlensiepen H. Biochemical and cellular mechanisms of low-dose effects. Int J Radiat Biol 1988; 53: 23-37.
77. Yamaoka K. Increased SOD activities and decreased lipid peroxide in rat organs induced by low X-irradiation. Free Radic Biol Med 1991; 11: 3-7.
78. Kojima S, Matsuki O, Nomura T, Kubodera A, Honda Y, Honda S, Tanooka H, Wakasugi H, Yamaoka K. Induction of mRNAs for glutathione synthesis-related proteins in the mouse liver by low doses of g-rays. Biochim Biophys Acta 1998; 1381: 312-18.
79. Wolff S, Afzal V, Wienke JK, Olivieri G, Michaeli A. Human lymphocytes exposed to low doses of ionizing radiations become refractory to high doses of radiation as well as to chemical mutagens that induce double-strand breaks in DNA. Int J Radiat Biol 1988; 53: 39-49.
80. Shadley JD, Wienke, JK. Induction of the adaptive response by X-rays is dependent on radiation intensity. Int J Radiat Biol 1989; 56: 107-18.
81. Ikushima T, Aritomi H, Morisita J. Radioadaptive response: Efficient repair of radiation-induced DNA damage in adapted cells. Mutat Res 1996; 358: 193-98.
82. Norimura T, Nomoto S, Katsuki M, Gondo Y, Kondo S. p 53 dependent apoptosis supresses radiation teratogenesis. Nature Med 1996; 2: 577-80.
83. Kondo S. Evidence that there are threshold effects in risk of radiation. J Nucl Sci Technol 1999; 36: 1-9.
84. Joiner MC, Larnbin P, Malaise EP, Robson T, Arrand JE, Skov KA, Marples B. Hypersensitivity to very low single radiation doses: its relationship to the adaptive response and induced radioresistance. Mutat Res 1996; 358: 171-83.
85. Joiner MC, Lambin P, Marples B. Adaptive response and induced resistance. Compt Rend Acad Sci Paris Life Sciences 1999; 322: 167-75.
86. James SJ, Makinodan T. T-cell potentiation by low dose ionizing radiation: possible mechanisms. Health Phys 1990; 59: 29-34.
87. Feinendegen LE, Bond VP, Sondhaus CA, Altman KI. Cellular signal adaptation with damage control at low doses versus the predominance of DNA damage at high doses. Compt Rend Acad Sci Paris Life Sciences 1999; 322: 245-51.
88. Miller WS, Green CA, Kitchen H. Byphasic action of penicillin and other sulphonamide similarity. Nature 1945; 1945: 210-11.
89. Gell-Mann M. The quark and the jaguar. New York: W.H. Freeman and Company, 1994.
90. Azzam EI, de Toledo SM, Raaphorst GP, Mitchel REJ. Low-dose ionizing radiation decreases the frequency of neoplastic transformation to a level below the spontaneous rate in C3H 10T1/2 cells. Rad Res 1996; 146: 369-33.
91. Redpath JL, Antoniono RJ. Introduction of an adaptive response against spontaneous neoplastic transformation in vitro by low-dose gamma radiation. Rad Res 1998; 149: 517-20.
92. Kesavan PC. Indian research on high levels of natural radiation: pertinent observations for further studies. In Wei L, Sugahara T, Tao Z. High levels of natural radiation. Radiation dose and health effects. Amsterdam, Beijing, China: Elsevier, 1996: 111-17.
93. Nair KMK, Nambi KSV, Amma NSSS, Gangadharan P, Jayadevan S, Cherian V, Reghuran KN. Population study in the high natural background radiation area in Kerala, India. Rad Res 1999; 152: S145-48.
94. Cheriyan VD, Kurien CJ, Das B, Ramachandran EN, Kurappasamany CV, Thampi MV, George KP, Kesavan, PC, Koya PKM, Chauhan PS. Genetic monitoring of the human population from high level natural radiation areas of Kerala on the South West Coast of India. II Incidence of the numerical and structural chromosomal aberrations in the lymphocyte of newborns. Rad Res 1999; 152: S154-58.
95. Jakrishan G et al. Genetic monitoring of the human population from high-level natural radiation area of Kerala on the South West Coast pf India. I. Prevalence of congenital malformations in newborns. Rad Res 1999; 152: S149-53.
96. Sohrabi M. Recent radiological studies of high-level natural radiation areas of Ramsar.In Sohrabi JUAM and Durran SA eds. High levels of natural radiation. Ramsar, Iran; IAEA, 1990: 39-47.
97. Ghiassi-nejad M, Mortazavi SMJ, Cameron JR, Niroomand-rad A, Karam PA. Very high background radiation area in Ramsar, Iran: preliminary biological studies. Health Phys 2002; 82: 87-93
98. Kostyuchenko VA, Krestina LY. Long term radiation effects in the population evacuated from the East Urals radioactive trace area. Sci Total Environ 1994; 142: 118-25.
99. Matanoski GM. Health effects of low level radiation in shipyard workers final report. Report No. DOE DE-AC02-79 EV 10095. Washington: US Department of Energy, 1991.
100. Tokarskaya ZB, Okladlnikova ND, Belyaeva ZD, Drozhko EG. Multifactorial analysis of lung cancer dose-response relationships for workers at the Mayak Nuclear Enterprise. Health Phys 1997; 73: 899-905.
101. Miller AB, Howe GR, Sherman GJ, Lindsay JP, Yaffe MJ, Dinner PJ, Risch HA, Preston DL. Mortality from breast cancer after irradiation during fluoroscopic examination in patients being treated for tuberculosis. N Engl J Med 1989; 321: 1285-89.
102. Webster EW. Dose risk in diagnostic radiology: how big? How little? Lauriston S Taylor lectures in radiation protection and measurements. Bethesda, MD: National Council on Radiation Protection and Measurements, 1992.
103. Rossi HH, Zaider M. Radiogenic lung cancer: the effects of low doses of low linear energy transfer (LET) radiation. Radic Environ Biophys 1997; 36: 85-88.
104. Pollycove M. Positive health effects of low level radiation in human populations. In Calabrese EJ. Biological effects of low level exposures: dose-response relationships. Chelsea, MI: Lewis Publishing Inc., 1994: 171-87.
105. Pollycove M. Nonlinearity of radiation health effects. Environ Health Perspect 1998; 106: 363-68.
106. Rattan SIS. Biogerontology: the next step. Ann N Y Acad Sci. 2000; 908: 282-90.
107. De Pinho RA. The age of cancer. Nature 2000; 408: 248-54.
108. Feinendegen LE, Bond VP, Sondhaus CA, Muehlensiepen H. Radiation effects induced by low doses in complex tissue and their relation to cellular adaptive responses. Mutat Res 1996; 358: 199-205.
109. Sawant SG, Randers-Pehrson G, Metting NF, Hall EJ. Adaptive response and the bystander effect induced by radiation in C3H 10T(1/2) cells in culture. Rad. Res. 2001; 165:177-80.
110. Narayanan PK, Goodwin EH, Lehnert BE. Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res 1997; 57: 3963-71.
111. 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 Gingko biloba extract. Rad Res 1995; 144: 198-205.
112. Cohen BL. Test of the linear no-threshold theory of radiation carcinogenesis in the low dose, low dose rate region. Health Phys 1995; 68: 157-74.