Oxidative damage to DNA and antioxidant status in aging and age-related diseases

• Authors: Ryszard Olinski , Agnieszka Siomek , Rafal Rozalski , Daniel Gackowski , Marek Foksinski , Jolanta Guz , Tomasz Dziaman , Anna Szpila , Barbara Tudek
• Languages of publication: EN

Abstracts

EN

Aging is a complex process involving morphologic and biochemical changes in single cells and in the whole organism. One of the most popular explanations of how aging occurs at the molecular level is the oxidative stress hypothesis. Oxidative stress leads in many cases to an age-dependent increase in the cellular level of oxidatively modified macromolecules including DNA, and it is this increase which has been linked to various pathological conditions, such as aging, carcinogenesis, neurodegenerative and cardiovascular diseases. It is, however, possible that a number of short-comings associated with gaps in our knowledge may be responsible for the failure to produce definite results when applied to understanding the role of DNA damage in aging and age-related diseases.

Keywords

EN

ROS; aging; oxidative DNA damage; age-related diseases; BER; GO system

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2007
• Volume: 54
• Issue: 1
• Pages: 11-26

Dates

published

2007

received

2006-10-23

revised

2006-11-27

accepted

2006-12-18

(unknown)

2007-01-09

Contributors

author

Ryszard Olinski

• Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Toruń, Poland

author

Agnieszka Siomek

• Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Toruń, Poland

author

Rafal Rozalski

• Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Toruń, Poland

author

Daniel Gackowski

• Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Toruń, Poland

author

Marek Foksinski

• Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Toruń, Poland

author

Jolanta Guz

• Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Toruń, Poland

author

Tomasz Dziaman

• Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Toruń, Poland

author

Anna Szpila

• Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Toruń, Poland

author

Barbara Tudek

• Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warszawa, Poland

References

• Al-Tassan N, Chmiel NH, Maynard J, Fleming N, Livingston AL, Williams GT, Hodges AK, Davies DR, David SS, Sampson JR, Cheadle JP (2002) Inherited variants of MYH associated with somatic G:C→T:A mutations in colorectal tumors. Nat Genet 30: 227-232.
• Ambs S, Bennett WP, Merriam WG, Ogunfusika MO, Oser SM, Khan MA, Jones RT, Harris CC (1998) Vascular endothelial growth factor and nitric oxide synthase expression in human lung cancer and the relation to p53. Br J Cancer 78: 233-239.
• Anson RM, Senturker S, Dizdaroglu M, Bohr VA (1999) Measurement of oxidatively induced base lesions in liver from Wistar rats of different ages. Free Radic Biol Med 27: 456-462.
• Barja G, Herrero A (2000) Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 14: 312-318.
• Bialkowski K, Bialkowska A, Anderson LM, Kasprzak KS (1999) Higher activity of 8-oxo-2'-deoxyguanosine 5'-triphosphate pyrophosphohydrolase (8-oxo-dGTPase) coincides with lower background levels of 8-oxo-2'-deoxyguanosine in DNA of fetal compared with maternal mouse organs. Free Radic Biol Med 27: 90-94.
• Butkiewicz D, Rusin M, Enewold L, Shields PG, Chorazy M, Harris CC (2001) Genetic polymorphisms in DNA repair genes and risk of lung cancer. Carcinogenesis 22: 593-597.
• Chen KH, Srivastava DK, Singhal RK, Jacob S, Ahmed AE, Wilson SH (2000) Modulation of base excision repair by low density lipoprotein, oxidized low density lipoprotein and antioxidants in mouse monocytes. Carcinogenesis 21: 1017-1022.
• Chen SK, Hsieh WA, Tsai MH, Chen CC, Hong AI, Wei YH, Chang WP (2003) Age-associated decrease of oxidative repair enzymes, human 8-oxoguanine DNA glycosylases (hOgg1), in human aging. J Radiat Res (Tokyo) 44: 31-35.
• Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA (1992) 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G→T and A→C substitutions. J Biol Chem 267: 166-172.
• Chevillard S, Radicella JP, Levalois C, Lebeau J, Poupon MF, Oudard S, Dutrillaux B, Boiteux S (1998) Mutations in OGG1, a gene involved in the repair of oxidative DNA damage, are found in human lung and kidney tumors. Oncogene 16: 3083-3086.
• Cooke MS, Evans MD, Herbert KE, Lunec J (2000) Urinary 8-oxo-2'-deoxyguanosine - source, significance and supplements. Free Radic Res 32: 381-397.
• Cooke MS, Evans MD, Dove R, Rozalski R, Gackowski D, Siomek A, Lunec J, Olinski R (2005) DNA repair is responsible for the presence of oxidatively damaged DNA lesions in urine. Mutat Res 574: 58-66.
• Cooke MS, Olinski R, Evans MD (2006) Does measurement of oxidative damage to DNA have clinical significance? Clin Chim Acta 365: 30-49.
• Cutler RG (1991a) Antioxidants and aging. Am J Clin Nutr 53: 373S-379S.
• Cutler RG (1991b) Human longevity and aging: possible role of reactive oxygen species. Ann N Y Acad Sci 621: 1-28.
• De Flora S, Izzotti A, Walsh D, Degan P, Petrilli GL, Lewtas J (1997) Molecular epidemiology of atherosclerosis. FASEB J 11: 1021-1031.
• DePinho RA (2000) The age of cancer. Nature 408: 248-254.
• de Valk B, Addicks MA, Gosriwatana I, Lu S, Hider RC, Marx JJ (2000) Non-transferrin-bound iron is present in serum of hereditary haemochromatosis heterozygotes. Eur J Clin Invest 30: 248-251.
• De Vita VT Jr, Hellman S, Rosenberg SA (2001) Cancer. Principles and practice of oncology, 6th edn. Lippincott Wiliams & Wilkins, Philadelphia.
• Dianov G, Bischoff C, Piotrowski J, Bohr VA (1998) Repair pathways for processing of 8-oxoguanine in DNA by mammalian cell extracts. J Biol Chem 273: 33811-33816.
• Dizdaroglu M (1992) Oxidative damage to DNA in mammalian chromatin. Mutat Res 275: 331-342.
• Dizdaroglu M (1998) Mechanism of free radical damage to DNA. In DNA and free radicals: techniques, mechanisms and applications. Aruoma OI, Halliwell B, eds, pp 3-26. OICA International, Saint Lucia, London.
• Dizdaroglu M, Olinski R, Doroshow JH, Akman SA (1993) Modification of DNA bases in chromatin of intact target human cells by activated human polymorphonuclear leukocytes. Cancer Res 53: 1269-1272.
• Dou H, Mitra S, Hazra TK (2003) Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J Biol Chem 278: 49679-49684.
• Du MQ, Carmichael PL, Phillips DH (1994) Induction of activating mutations in the human c-Ha-ras-1 proto-oncogene by oxygen free radicals. Mol Carcinog 11: 170-175.
• Fan CY, Liu KL, Huang HY, Barnes EL, Swalsky PA, Bakker A, Woods J, Finkelstein SD (2001) Frequent allelic imbalance and loss of protein expression of the DNA repair gene hOGG1 in head and neck squamous cell carcinoma. Lab Invest 81: 1429-1438.
• Feig DI, Reid TM, Loeb LA (1994) Reactive oxygen species in tumorigenesis. Cancer Res 54: 1890s-1894s.
• Floyd RA (1990) The role of 8-hydroxyguanine in carcinogenesis. Carcinogenesis 11: 1447-1450.
• Foksinski M, Kotzbach R, Szymanski W, Olinski R (2000) The level of typical biomarker of oxidative stress 8-hydroxy-2'-deoxyguanosine is higher in uterine myomas than in control tissues and correlates with the size of the tumor. Free Radic Biol Med 29: 597-601.
• Foksinski M, Rozalski R, Guz J, Ruszkowska B, Sztukowska P, Piwowarski M, Klungland A, Olinski R (2004) Urinary excretion of DNA repair products correlates with metabolic rates as well as with maximum life spans of different mammalian species. Free Radic Biol Med 37: 1449-1454.
• Fraga CG, Shigenaga MK, Park JW, Degan P, Ames BN (1990) Oxidative damage to DNA during aging: 8-hydroxy-2'-deoxyguanosine in rat organ DNA and urine. Proc Natl Acad Sci USA 87: 4533-4537.
• Franks LM, Teich NM (1997) Introduction to the cellular and molecular biology of cancer. 3rd edn. Oxford University Press, Oxford, New York, Tokyo.
• Fritz G, Grosch S, Tomicic M, Kaina B (2003) APE/Ref-1 and the mammalian response to genotoxic stress. Toxicology 193: 67-78.
• Fujimoto H, Ando Y, Yamashita T, Terazaki H, Tanaka Y, Sasaki J, Matsumoto M, Suga M, Ando M (1997) Nitric oxide synthase activity in human lung cancer. Jpn J Cancer Res 88: 1190-1198.
• Gackowski D, Kruszewski M, Jawien A, Ciecierski M, Olinski R (2001) Further evidence that oxidative stress may be a risk factor responsible for the development of atherosclerosis. Free Radic Biol Med 31: 542-547.
• Gackowski D, Kruszewski M, Bartlomiejczyk T, Jawien A, Ciecierski M, Olinski R (2002) The level of 8-oxo-7,8-dihydro-2'-deoxyguanosine is positively correlated with the size of the labile iron pool in human lymphocytes. J Biol Inorg Chem 7: 548-550.
• Gackowski D, Speina E, Zielinska M, Kowalewski J, Rozalski R, Siomek A, Paciorek T, Tudek B, Olinski R (2003) Products of oxidative DNA damage and repair as possible biomarkers of susceptibility to lung cancer. Cancer Res 63: 4899-4902.
• Goode EL, Ulrich CM, Potter JD (2002) Polymorphisms in DNA repair genes and associations with cancer risk. Cancer Epidemiol Biomarkers Prev 11: 1513-1530.
• Goukassian D, Gad F, Yaar M, Eller MS, Nehal US, Gilchrest BA (2000) Mechanisms and implications of the age-associated decrease in DNA repair capacity. FASEB J 14: 1325-1334.
• Graziewicz M, Wink DA, Laval F (1996) Nitric oxide inhibits DNA ligase activity: potential mechanisms for NO-mediated DNA damage. Carcinogenesis 17: 2501-2505.
• Habib SL, Phan MN, Patel SK, Li D, Monks TJ, Lau SS (2003) Reduced constitutive 8-oxoguanine-DNA glycosylase expression and impaired induction following oxidative DNA damage in the tuberin deficient Eker rat. Carcinogenesis 24: 573-582.
• Halliwell B, Gutteridge JM (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, Oxford, New York.
• Hamilton ML, Guo Z, Fuller CD, Van Remmen H, Ward WF, Austad SN, Troyer DA, Thompson I, Richardson A (2001a) A reliable assessment of 8-oxo-2-deoxyguanosine levels in nuclear and mitochondrial DNA using the sodium iodide method to isolate DNA. Nucleic Acids Res 29: 2117-2126.
• Hamilton ML, Van Remmen H, Drake JA, Yang H, Guo ZM, Kewitt K, Walter CA, Richardson A (2001b) Does oxidative damage to DNA increase with age? Proc Natl Acad Sci USA 98: 10469-10474.
• Hardie LJ, Briggs JA, Davidson LA, Allan JM, King RF, Williams GI, Wild CP (2000) The effect of hOGG1 and glutathione peroxidase I genotypes and 3p chromosomal loss on 8-hydroxydeoxyguanosine levels in lung cancer. Carcinogenesis 21: 167-172.
• Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11: 298-300.
• Hart RW, Setlow RB (1974) Correlation between deoxyribonucleic acid excision-repair and life-span in a number of mammalian species. Proc Natl Acad Sci USA 71: 2169-2173.
• Hazra TK, Izumi T, Maidt L, Floyd RA, Mitra S (1998) The presence of two distinct 8-oxoguanine repair enzymes in human cells: their potential complementary roles in preventing mutation. Nucleic Acids Res 26: 5116-5122.
• Hazra TK, Izumi T, Venkataraman R, Kow YW, Dizdaroglu M, Mitra S (2000) Characterization of a novel 8-oxoguanine-DNA glycosylase activity in Escherichia coli and identification of the enzyme as endonuclease VIII. J Biol Chem 275: 27762-27767.
• Hazra TK, Hill JW, Izumi T, Mitra S (2001) Multiple DNA glycosylases for repair of 8-oxoguanine and their potential in vivo functions. Prog Nucleic Acid Res Mol Biol 68: 193-205.
• Hazra TK, Izumi T, Boldogh I, Imhoff B, Kow YW, Jaruga P, Dizdaroglu M, Mitra S (2002) Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc Natl Acad Sci USA 99: 3523-3528.
• Helbock HJ, Beckman KB, Shigenaga MK, Walter PB, Woodall AA, Yeo HC, Ames BN (1998) DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Natl Acad Sci USA 95: 288-293.
• Hill JW, Hazra TK, Izumi T, Mitra S (2001) Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res 29: 430-438.
• Hu W, Feng Z, Eveleigh J, Iyer G, Pan J, Amin S, Chung FL, Tang MS (2002) The major lipid peroxidation product, trans-4-hydroxy-2-nonenal, preferentially forms DNA adducts at codon 249 of human p53 gene, a unique mutational hotspot in hepatocellular carcinoma. Carcinogenesis 23: 1781-1789.
• Huang X, Moir RD, Tanzi RE, Bush AI, Rogers JT (2004) Redox-active metals, oxidative stress, and Alzheimer's disease pathology. Ann N Y Acad Sci 1012: 153-163.
• Hudson EK, Hogue BA, Souza-Pinto NC, Croteau DL, Anson RM, Bohr VA, Hansford RG (1998) Age-associated change in mitochondrial DNA damage. Free Radic Res 29: 573-579.
• Jackson AL, Loeb LA (2001) The contribution of endogenous sources of DNA damage to the multiple mutations in cancer. Mutat Res 477: 7-21.
• Jaiswal M, LaRusso NF, Nishioka N, Nakabeppu Y, Gores GJ (2001) Human Ogg1, a protein involved in the repair of 8-oxoguanine, is inhibited by nitric oxide. Cancer Res 61: 6388-6393.
• Kayanoki Y, Fujii J, Suzuki K, Kawata S, Matsuzawa Y, Taniguchi N (1994) Suppression of antioxidative enzyme expression by transforming growth factor-beta 1 in rat hepatocytes. J Biol Chem 269: 15488-15492.
• Kennedy CH, Cueto R, Belinsky SA, Lechner JF, Pryor WA (1998) Overexpression of hMTH1 mRNA: a molecular marker of oxidative stress in lung cancer cells. FEBS Lett 429: 17-20.
• Kennedy CH, Pass HI, Mitchell JB (2003) Expression of human MutT homologue (hMTH1) protein in primary non-small-cell lung carcinomas and histologically normal surrounding tissue. Free Radic Biol Med 34: 1447-1457.
• Kirkwood TB, Austad SN (2000) Why do we age? Nature 408: 233-238.
• Kleiber M (1961) The fire of life. John Wiley, New York.
• Klein JA, Longo-Guess CM, Rossmann MP, Seburn KL, Hurd RE, Frankel WN, Bronson RT, Ackerman SL (2002) The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419: 367-374.
• Kohno T, Shinmura K, Tosaka M, Tani M, Kim SR, Sugimura H, Nohmi T, Kasai H, Yokota J (1998) Genetic polymorphisms and alternative splicing of the hOGG1 gene, that is involved in the repair of 8-hydroxyguanine in damaged DNA. Oncogene 16: 3219-3225.
• Kopsidas G, Kovalenko SA, Kelso JM, Linnane AW (1998) An age-associated correlation between cellular bioenergy decline and mtDNA rearrangements in human skeletal muscle. Mutat Res 421: 27-36.
• Laval F, Wink DA (1994) Inhibition by nitric oxide of the repair protein, O6-methylguanine-DNA-methyltransferase. Carcinogenesis 15: 443-447.
• Lee SH, Blair IA (2001) Oxidative DNA damage and cardiovascular disease. Trends Cardiovasc Med 11: 148-155.
• Le Marchand L, Donlon T, Lum-Jones A, Seifried A, Wilkens LR (2002) Association of the hOGG1 Ser326Cys polymorphism with lung cancer risk. Cancer Epidemiol Biomarkers Prev 11: 409-412.
• Leutner S, Schindowski K, Frolich L, Maurer K, Kratzsch T, Eckert A, Muller WE (2005) Enhanced ROS-generation in lymphocytes from Alzheimer's patients. Pharmacopsychiatry 38: 312-315.
• Loeb LA (2001) A mutator phenotype in cancer. Cancer Res 61: 3230-3239.
• Loft S, Poulsen HE (1998) Estimation of oxidative DNA damage in man from urinary excretion of repair products. Acta Biochim Polon 45: 133-144.
• Loft S, Svoboda P, Kasai H, Tjonneland A, Vogel U, Moller P, Overvad K, Raaschou-Nielsen O (2006) Prospective study of 8-oxo-7,8-dihydro-2'-deoxyguanosine excretion and the risk of lung cancer. Carcinogenesis 27: 1245-1250.
• Markesbery WR, Carney JM (1999) Oxidative alterations in Alzheimer's disease. Brain Pathol 9: 133-146.
• Marsin S, Vidal AE, Sossou M, Menissier-de Murcia J, Le Page F, Boiteux S, de Murcia G, Radicella JP (2003) Role of XRCC1 in the coordination and stimulation of oxidative DNA damage repair initiated by the DNA glycosylase hOGG1. J Biol Chem 278: 44068-44074.
• Martin GM, Loeb LA (2004) Ageing: mice and mitochondria. Nature 429: 357-359.
• McCarroll SA, Murphy CT, Zou S, Pletcher SD, Chin CS, Jan YN, Kenyon C, Bargmann CI, Li H (2004) Comparing genomic expression patterns across species identifies shared transcriptional profile in aging. Nat Genet 36: 197-204.
• Michaels ML, Miller JH (1992) The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J Bacteriol 174: 6321-6325.
• Migliore L, Fontana I, Trippi F, Colognato R, Coppede F, Tognoni G, Nucciarone B, Siciliano G (2005) Oxidative DNA damage in peripheral leukocytes of mild cognitive impairment and AD patients. Neurobiol Aging 26: 567-573.
• Nelson RL, Davis FG, Sutter E, Sobin LH, Kikendall JW, Bowen P (1994) Body iron stores and risk of colonic neoplasia. J Natl Cancer Inst 86: 455-460.
• Ohba M, Shibanuma M, Kuroki T, Nose K (1994) Production of hydrogen peroxide by transforming growth factor-beta 1 and its involvement in induction of egr-1 in mouse osteoblastic cells. J Cell Biol 126: 1079-1088.
• Olinski R, Gackowski D, Foksinski M, Rozalski R, Roszkowski K, Jaruga P (2002) Oxidative DNA damage: assessment of the role in carcinogenesis, atherosclerosis, and acquired immunodeficiency syndrome. Free Radic Biol Med 33: 192-200.
• Paz-Elizur T, Krupsky M, Blumenstein S, Elinger D, Schechtman E, Livneh Z (2003) DNA repair activity for oxidative damage and risk of lung cancer. J Natl Cancer Inst 95: 1312-1319.
• Peddie CM, Wolf CR, McLellan LI, Collins AR, Bowen DT (1997) Oxidative DNA damage in CD34+myelodysplastic cells is associated with intracellular redox changes and elevated plasma tumor necrosis factor-alpha concentration. Br J Haematol 99: 625-631.
• Penn A, Garte SJ, Warren L, Nesta D, Mindich B (1986) Transforming gene in human atherosclerotic plaque DNA. Proc Natl Acad Sci USA 83: 7951-7955.
• Privezentzev CV, Saparbaev M, Laval J (2001) The HAP1 protein stimulates the turnover of human mismatch-specific thymine-DNA-glycosylase to process 3,N(4)-ethenocytosine residues. Mutat Res 480-481: 277-284.
• Radicella JP, Dherin C, Desmaze C, Fox MS, Boiteux S (1997) Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94: 8010-8015.
• Rajaee-Behbahani N, Schmezer P, Risch A, Rittgen W, Kayser KW, Dienemann H, Schulz V, Drings P, Thiel S, Bartsch H (2001) Altered DNA repair capacity and bleomycin sensitivity as risk markers for non-small cell lung cancer. Int J Cancer 95: 86-91.
• Ross R (1993) Rous-Whipple Award Lecture. Atherosclerosis: a defense mechanism gone awry. Am J Pathol 143: 987-1002.
• Rozalski R, Gackowski D, Roszkowski K, Foksinski M, Olinski R (2002) The level of 8-hydroxyguanine, a possible repair product of oxidative DNA damage, is higher in urine of cancer patients than in control subjects. Cancer Epidemiol Biomarkers Prev 11: 1072-1075.
• Russo MT, Blasi MF, Chiera F, Fortini P, Degan P, Macpherson P, Furuichi M, Nakabeppu Y, Karran P, Aquilina G, Bignami M (2004) The oxidized deoxynucleoside triphosphate pool is a significant contributor to genetic instability in mismatch repair-deficient cells. Mol Cell Biol 24: 465-474.
• Sakumi K, Tominaga Y, Furuichi M, Xu P, Tsuzuki T, Sekiguchi M, Nakbeppu Y (2003) Ogg1 knockout-associated lung tumorigenesis and its suppression by Mth1 gene disruption. Cancer Res. 63: 902-905.
• Saparbaev M, Laval J (1998) 3,N4-ethenocytosine, a highly mutagenic adduct, is a primary substrate for Escherichia coli double-stranded uracil-DNA glycosylase and human mismatch-specific thymine-DNA glycosylase. Proc Natl Acad Sci USA 95: 8508-8513.
• Saparbaev M, Kleibl K, Laval J (1995) Escherichia coli, Saccharomyces cerevisiae, rat and human 3-methyladenine DNA glycosylases repair 1,N6-ethenoadenine when present in DNA. Nucleic Acids Res 23: 3750-3755.
• Schmielau J, Finn OJ (2001) Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res 61: 4756-4760.
• Schwartz LB, Diamond MP, Schwartz PE (1993) Leiomyosarcomas: clinical presentation. Am J Obstet Gynecol 168: 180-183.
• Sharma MK, Buettner GR (1993) Interaction of vitamin C and vitamin E during free radical stress in plasma: an ESR study. Free Radic Biol Med 14: 649-653.
• Shigenaga MK, Gimeno CJ, Ames BN (1989) Urinary 8-hydroxy-2'-deoxyguanosine as a biological marker of in vivo oxidative DNA damage. Proc Natl Acad Sci USA 86: 9697-9701.
• Siomek A, Gackowski D, Rozalski R, Dziaman T, Szpila A, Guz J, Olinski R (2007) Higher leukocyte 8-oxo-7,8-dihydro-2'-deoxyguanosine and lower plasma ascorbate in aging humans? Antioxid Redox Signal 9: 143-150.
• Sohal RS (2002) Oxidative stress hypothesis of aging. Free Radic Biol Med 33: 573-574.
• Sohal RS, Mockett RJ, Orr WC (2002) Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Radic Biol Med 33: 575-586.
• Speina E, Zielinska M, Barbin A, Gackowski D, Kowalewski J, Graziewicz MA, Siedlecki JA, Olinski R, Tudek B (2003) Decreased repair activities of 1,N(6)-ethenoadenine and 3,N(4)-ethenocytosine in lung adenocarcinoma patients. Cancer Res 63: 4351-4357.
• Speina E, Arczewska KD, Gackowski D, Zielinska M, Siomek A, Kowalewski J, Olinski R, Tudek B, Kusmierek JT (2005) Contribution of hMTH1 to the maintenance of 8-oxoguanine levels in lung DNA of non-small-cell lung cancer patients. J Natl Cancer Inst 97: 384-395.
• Stevens RG, Graubard BI, Micozzi MS, Neriishi K, Blumberg BS (1994) Moderate elevation of body iron level and increased risk of cancer occurrence and death. Int J Cancer 56: 364-369.
• Sugimura H, Kohno T, Wakai K, Nagura K, Genka K, Igarashi H, Morris BJ, Baba S, Ohno Y, Gao C, et al. (1999) hOGG1 Ser326Cys polymorphism and lung cancer susceptibility. Cancer Epidemiol Biomarkers Prev 8: 669-674.
• Szatrowski TP, Nathan CF (1991) Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794-798.
• Takasawa M, Hayakawa M, Sugiyama S, Hattori K, Ito T, Ozawa T (1993) Age-associated damage in mitochondrial function in rat hearts. Exp Gerontol 28: 269-280.
• Toyokuni S, Okamoto K, Yodoi J, Hiai H (1995) Persistent oxidative stress in cancer. FEBS Lett 358: 1-3.
• Trosko JE, Chang CC (1980) An integrative hypothesis linking cancer, diabetes and atherosclerosis: the role of mutations and epigenetic changes. Med Hypotheses 6: 455-468.
• Vanderkooi JM, Erecinska M, Silver IA (1991) Oxygen in mammalian tissue: methods of measurement and affinities of various reactions. Am J Physiol 260: C1131-C1150.
• Wikman H, Risch A, Klimek F, Schmezer P, Spiegelhalder B, Dienemann H, Kayser K, Schulz V, Drings P, Bartsch H (2000) hOGG1 polymorphism and loss of heterozygosity (LOH): significance for lung cancer susceptibility in a caucasian population. Int J Cancer 88: 932-937.
• Wink DA, Laval J (1994) The Fpg protein, a DNA repair enzyme, is inhibited by the biomediator nitric oxide in vitro and in vivo. Carcinogenesis 15: 2125-2129.
• Yu D, Berlin JA, Penning TM, Field J (2002) Reactive oxygen species generated by PAH o-quinones cause change-in-function mutations in p53. Chem Res Toxicol 15: 832-842.