Oxidative damage to nucleic acids m evans, m cooke (springer, 2007)

MOLECUlAR BIOWGY INTELLIGENCE UNIT Oxidative Damage to Nucleic Acids Mark D Evans, B.Sc., Ph.D Radiation and Oxidative Stress Group Department of Cancer Studies and Molecular Medicine RKCSB, Leicester Royal Infirmary University of Leicester Leicester, U K Marcus S Cooke, B.Sc., M.Sc., Ph.D Department of Cancer Studies and Molecular Medicine and Department of Genetics University of Leicester Leicester, U.K ! ANDES BIOSCIENCE AUSTIN, TEXAS U.S.A SPRINGER SCIENCE+BuSINESS MEDIA NEW YORK, NEW YORK U.S.A OXIDATIVE DAMAGE TO NUCLEIC ACIDS Molecular Biology Intelligence Unit Landes Bioscience Springer Science-Business Media, LLC ISBN: 978-0-387-72973-2 Printed on acid-free paper Copyright ©2007 Landes Bioscience and Springer Science-Business Media, LLC All rights reserved This work may not be translated or copied in whole or in part without the written permission of the publisher, except for brief excerpts in connection with reviews or scholarly analysis Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden The use in the publication of trade names, trademarks, service marks and similar terms even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights While the authors, editors and publisher believe that drug selection and dosage and the specifications and usage of equipment and devices, as set forth in this book, are in accord with current recommendations and practice at the time of publication, they make no warranty, expressed or implied, with respect to material described in this book In view of the ongoing research, equipment development, changes in governmental regulations and the rapid accumulation of information relating to the biomedical sciences, the reader is urged to carefully review and evaluate the information provided herein Springer Science-Business Media, LLC, 233 Spring Street, New York, New York 10013, U.S.A http://www.springer.com Please address all inquiries to the Publishers: Landes Bioscience, 1002 West Avenue, 2nd Floor, Austin, Texas 78701, U.S.A Phone: 512/6376050; FAX: 512/6376079 http://www.1andesbioscience.com Printed in the United States of America 876 321 Library of Congress Cataloging-ia-Pubilcation Data Oxidative damage to nucleic acids [edited by] Mark D Evans, Marcus S Cooke p ; em (Molecular biology intelligence unit) Includes bibliographical references and index ISBN-13: 978-0-387-72973-2 (a1k paper) Nucleic acids-Oxidation DNA repair Chemical mutagenesis I Evans, Mark D (Mark Dennis), 1962- II Cooke, Marcus S III Series: Molecular biology intelligence unit (Unnumbered) [DNLM: DNA Damage Oxidative Stress Antioxidants-vtherapeutic use DNA Repair Enzymes DNA Repair QU 477 098 2007] QP620.095 2007 611'.01816 dc22 2007024908 About the Editors MARK D EVANS is a non-clinical lecturer in the Department of Cancer Studies and Molecular Medicine at the University of Leicester, U.K His main research interests are in the areas of DNA oxidation and repair and the pathological roles of DNA oxidation in malignant and non-malignant disease He obtained his B.Sc (Hons) in Applied Biochemistry from Brunei University, Uxbridge U.K He graduated with a Ph.D., in the area of cigarette smoke-induced protein damage and emphysema, from Louisiana State University, Baton Rouge working in The Biodynamics Institute and Department of Biochemistry under the guidanceof ProfessorWilliam A Pryor MARCUS S COOKE is a senior lecturer with a joint appointment between the Department of Cancer Studies and Molecular Medicine and the Department of Genetics, at the University of Leicester The role of genotoxicology in the pathogenesis of disease is the central theme in his research program, focussed primarily upon free radical mechanisms of cellular damage, particular oxidative DNA damage and repair He obtained his B.Sc (Hons) in Biomedical Sciences at Liverpool Polytechnic, before moving to the University of Leicester for his M.Sc in Molecular Pathology and Toxicology, and then his Ph.D in ultra-violet radiation and free radical biochemistry He was appointed a Fellowof the Institute of Biomedical Science in 1997, and in 2004 became a Chartered Scientist MDE would like to dedicate this book to hisfamily, relations andfriends ofthe family-past, present andfUture MSC would like to dedicate this book to Emily and Evie r.======CONTENTS================:::::;l Preface Oxidatively Generated Damage to Cellular DNA: Mechanistic Aspects xv Jean Cadet, Thierry Douki, Carine Badouard, Alain Favier andJean-LucRavanat Hydroxyl Radical-Mediated Oxidation of Thymine Degradation Pathways of Purine Basesby 'OH Radical Singlet Oxygen Oxidation of Guanine Halogenation Reactions of Nucleobases by HOCI Secondary Radical Oxidation Reactions of 8-oxo-7,8-dihydroguanine Chlorination and Nitration of DNA and Nucleic Acid Components Clare L Hawkins, David I Pattison, Matthew Whiteman and Michael j Davies Chlorination Nitration 14 16 21 Prevention of the Mutagenicity and Cytotoxicity of Oxidized Purine Nucleotides 40 Yusaku Nakabeppu, Mehrdad Behmanesb, Hiroo Yamaguchi, Daisuke Yoshimura and Kunihiko Sakumi Oxidation of Free Nucleotides and Their Mutability Removal of Oxidized Nucleotides by Sanitization of Nucleotide Pools Mutagenesis and Carcinogenesis Caused by the Accumulation of Oxidized Nucleotides and Prevention by MTHI Cellular Dysfunction Caused by the Accumulation of Oxidized Nucleotides and Its Prevention by MTH1 Neuronal Accumulation of Oxidized Nucleotides Causes Neurodegeneration, Suppression by MTHI Oxidative Deamination of Nucleotides and Its Biological Consequences Nucleotide Incision Repair: An Alternative and Ubiquitous Pathway to Handle Oxidative DNA Damage 40 42 46 46 48 48 54 Sophie Couoe-Prioat, Alexander A Isbcbenko, Jacques Laval and Murat Saparbaev Free Radical Species and Oxidative Damage of DNA AP Endonucleases Involved in the Nucleotide Incision Repair Pathway Substrate Specificity ofNIR Endonucleases and Their Physiological Relevance Structure and 3'-5' Exonuclease Activity of AP Endonucleases 56 56 58 60 OGG1: From Structural Analysis to the Knockout Mouse Arne Klungland, Jon K Laerdahl and Torbjem Rognes Cloning of OGG1 '" Substrate Specificity of OGG OGG Structure , OGG Catalytic Mechanism OGGI Mutants Backup Activities for OGG OGG Orthologs 67 68 70 70 73 74 76 76 Processing of 3' -End Modified DNA Strand Breaks Induced by Oxidative Damage Jason L Parsons, Emma Boswell and Grigory L Dianov Formation of "Damaged" DNA 3'-Ends Repair of DNA Single Strand Breaks Induced by the Base Excision Repair Pathway AP Endonuclease (APEI) Polynucleotide Kinase (PNK) Tyrosyl-DNA Phosphodiesterase (TdpI) Aprataxin Polymorphisms of Proteins Involved in the Processing of 3'-End Modified DNA Strand Breaks 86 Oxidative Damage and Promoter Function 91 81 82 82 84 85 85 86 David Mitchell and Rita Ghosh Nonrandom Induction of Oxidative Damage in Promoter Regions Cis Effects of Oxidative Damage on Promoter Function Trans Effects of Oxidative Damage on Promoter Function Oxidative DNA Damage and Telomere Shortening 92 93 95 100 Torsten Richter and Thomas vonZglinicki Telomere Structure Telomeres and DNA Repair Telomere Shortening and DNA Damage Telomeres Are Vulnerable to Oxidative Stress-Induced Single-Strand Breaks Telomere-Specific Deficiency ofSSB Repair Possible Mechanisms ofStress-Dependent Telomere Shortening Oxidative Damage and Repair in the Mitochondrial Genome 100 102 102 103 105 106 109 LeneJuel Rasmussen and Keshav K Singh Repair of Oxidatively-Damaged DNA in the Nucleus Repair of Oxidatively-Modified DNA in Mitochondria Imbalanced Repair in Mitochondria Mitochondria-Mediated Mutagenesis Mitochondrial Dysfunction and Human Disease 110 114 117 117 117 10 The Role of Oxidative Damage to Nucleic Acids in the Pathogenesis of Neurological Disease 123 V Prakash Reddy, Ayse Beyaz, George Perry, Marcus S Cooke, Lawrence M Sayre and Mark A Smith Oxidative Stress and Free Radical Species Oxidative Stress Involving Advanced Glycation End Products (AGEs) and Advanced Lipid Peroxidation End Products (ALEs) Markers of Nucleic Acid Damage in AD Mitochondrial DNA Damage DNA Repair in AD 11 Nucleic Acid Oxidation and the Pathogenesis of Cardiovascular Diseases 124 128 132 134 134 141 Maria Grazia Andreassi Pathogenesis ofAtherosclerosis 142 Genetic Instability and Oxidatively Damaged DNA in Atherosclerosis 145 12 Oxidative DNA Damage and Carcinogenesis 153 Ryszard Glinski, Marek Foksinski and Barbara Tudek Accumulation of 8-0HGua in Cancer Patients Oxidative DNA Damage Repair, Mutagenesis and Carcinogenesis Aging, Cancer and Oxidative DNA Damage Role ofInflammation in ROS Generation and Oxidative DNA Damage-Association with Cancer Development 13 The Physiological and Pathological Roles of Oxidative Damage to DNA in Relation to Life Stage 154 156 160 161 167 Alberto Izzotti Early Life Stages: Intrauterine Life The Foetus-Newborn Transition Intermediate Life Stages Late Life Stages 169 171 173 174 14 Analysis of8-Hydroxy-2'-Deoxyguanosine as a Marker of Oxidatively Damaged DNA in Relation to Carcinogenesis and Aging 178 H Kasai, T Hirano, K Kawai, Y Tsurudome, H Itoh, D Himeji and T Horiuchi Methods for Measuring 8-0H-dG in DNA Formation of 8-0H-dG in DNA of Animal Organ or Cultured Cell DNA during Aging and by Treatment with Oxidative Stress-Inducing Carcinogens Clinical Analysisof 8-0H-dG in Human DNA Analysisof the 8-0H-dG Repair System Analysis of Urinary 8-0H-dG Urinary 8-0H-dG Levels in Cancer Patients and Cancer High-Risk Groups 179 180 180 180 181 184 15 Oxidatively Damaged DNA and Inflammation 188 Peter C Dedon and Marita C Barth Chemical Mediators ofInflammation Nitrosative Deamination of DNA Oxidation of DNA by Peroxynitrite and Nitrosoperoxycarbonate Reactions of DNA with Endogenous Electrophiles Arising from Oxidation Oxidative DNA Damage as a Source of DNA Adduct-Forming Electrophiles Putting It All Together: DNA Biomarkers of Inflammation in Vivo 16 The Role ofAntioxidants in the Prevention of Oxidative Damage to Nucleic Acids 189 190 192 197 198 200 207 Peter Metler and Steffen Loft Evaluation ofAntioxidant Intervention Studies Effect of Antioxidant Supplementation on Oxidative DNA Damage in WBC Effect of Antioxidant Supplementation on 8-0HdG Levelsin Urine Index 209 210 214 225 r;:=::============== EDITORS =================:::;-] Mark D Evans Radiation and Oxidative Stress Group Department of Cancer Studies and Molecular Medicine RKCSB, Leicester Royal Infirmary University of Leicester Leicester, U.K Email: mde2@leicester.ac.uk Preface Marcus S Cooke Department of Cancer Studies and Molecular Medicine and Department of Genetics University of Leicester Leicester, U.K Email: msc5@le.ac.uk Preface, Chapter 10 ~~~=CONTroBUTORS~~~~ Maria Grazia Andreassi CNR Institute of Clinical Physiology G Pasquinucci Hospital Massa, Italy Email: andreas@ifc.cnr.it Chapter 11 Mehrdad Behmanesh Department of Genetics School of Sciences Tarbiat Modarres University Tehran, Iran Chapter Carine Badouard Departement de Recherche Fondamentale sur la Matere Condensee Laboratoire "Lesions des Acides Nucleiques" Grenoble, France Chapter Ayse Beyaz Department of Chemistry University of Missouri-Rolla Rolla, Missouri, U.S.A Chapter 10 Marita C Barth Biological Engineering Division and Center for Environmental Health Sciences Massachusetts Institute of Technology Cambridge, Massachusetts, U.S.A Chapter 15 Emma Boswell Medical Research Council Radiation and Genome Stability Unit Harwell, Oxfordshire, U.K Chapter 19-52 33 ± 11 27 ± 21-45 26-54 57 MF (6S) 22 M (S) 43 MF (NS) 18 MF (NR) 14 MF (NS) Parallel study of blackcurrant juice, anthocyanine drink or placebo (475-1000 rnl) for wk Vegetablelfruit (500 g) in crossover design for wk with wk washout Vegetable/fruit (600 g), tablets with the same concentration of antioxidants/minerals, or placebo for 24 days Cruciferous and legume sprouts (113 g) or placebo for wk Kiwi fruit (1-3 pieces) crossover for wk with wk washout between supplement Comet Comet Comet Comet Comet Method Effect on Yes No effect Yes Yes Yes Antioxidants" Decreased ENDOIII and FPG sites, but without dose-effect relationship No effect on FPG sites No effect on ENDOIII and FPG sites No effect on ENDOIII sites No effect on ENDOII' and FPG sites Effect 29 40 42 38 37 Ref a Number of subjects indicated as males (M) and females (F).Smokers(S) and nonsmokers (NS) are indicated in brackets b Age is shown asrange or mean ± standard deviation C The effect of the antioxidants in plasma or WBC may increase or decrease depending on the type of study This effect is considered successful (yes) if the study reported statistically significant (a < 0.05) alterations of at least one antioxidant concentration compared to baseline or placebo groups d The two juices contain a mixture of apple, mango, and orange juice as basis ingredients; one juice contained aronia, blue-berries, and boysenberries (anthocyanine-rich fruits), whereas the other juice contained green tea, apricot, and lime (flavanol-rlch substances) Age (Yr)b Subjects" Supplement per Day Table Continued \.>.> w "~ ~ " ;; ~ ~ :! ~ "l:t ~ ::to ~ ~ S' ~ ;:s s~~ s " , :so !:t ~ il ::to ;:s ::.,: ~ ~ " ;;i 214 Oxidative Damage to Nucleic Acids Antioxidant Rich Foods Eight studies on antioxidant-rich foods met the criteria to be included in the analysis Ingestion of a diet rich in flavonols (including quercetin) and cruciferous and legume sprouts (113 g/day for wk) did not alter the level of ENDOIII and FPG sites, respectively.36,40 Ingestion of rye crisp bread (76.5 mg/d for wk) as a source oflignans was not associated with increased plasma enterolactone concentration, and had no effect on ENDOIII sites.35The null effect finding of lignans in WBC is probably reasonable considering the low bioavailability of the active substances in rye crisp bread, whereas the effects in the gastrointestinal tract are easier to comprehend Drinking blackcurrant juice or anthocyanine drinks (475-1000 mllday for wk) also had no beneficial effect on ENDOIII and FPG sensitive sites; in fact there was a tendency that the level of FPG sites increased in the group of subjects drinking blackcurrant juice 37 Anthocyanines have low bioavailability and the dose was rather high; it may be speculated that the subjects unintentionally suffered from slight intoxication of the gastrointestinal tract (e.g., some of the subjects in the active groups complained of nausea) Two studies investigated the effect of vegetables and fruits; a cross-over study with male smokers showed no effect on ENDOIII sites after ingesting 500 g/day for wk,38 whereas a placebo-controlled parallel study of 600 g/day for 24 days among nonsmoking subjects of both sexeswas negative with respect to ENDOIII and FPG sites.42 The quality of these studies is high and the null effects are quite robust Drinking soy milk (1000 mllday for wk) as a source of phytoestrogens increased plasma levels of genistein and daidzein, but not enterolactone; assessment of DNA damage revealed lower levelsof ENDOIII.28 The only study showing consistent effect by more than one endpoint is a study of kiwi fruit supplementation (1-3 kiwi fruits/day for wk), which showed lower levelsof EN DOIII and FPG sensitive sites.29 An overall summary of the studies shows that six investigations reported a beneficial effect of antioxidant supplementation, whereas 12 studies reported a null effect Studies usually set the significance level at 5%; this implies that one out of 20 studies should show a statistical significance by chance even if there is no biological effect This means that the distribution observed here indicates that there is an over-representation of studies showing a beneficial effect of dietary antioxidants in terms of oxidative DNA damage in WBC However, it is difficult to explain why some studies show beneficial effects and other null findings We regard this as weak support for the notion that ingestion of antioxidant-rich foods is associated with lower spontaneous level of oxidative DNA damage in WBC than single antioxidants On the other hand, there is virtually no evidence suggesting that high intake of antioxidants or antioxidant-rich products are associated with adverse effectsin terms of increased generation of oxidative DNA damage Although this is reassuring, it is not a proof of a more-is-better notion because there is an insufficient number of high-quality studies to address this firmly in the high-dose range Effect of Antioxidant Supplementation on 8-0HdG Levels in Urine Measurement of urinary excretion of 8-0HdG in antioxidant intervention studies is based on the notion that it decreases following a steady state ingestion of antioxidants, because of a decreased rate of generation ofoxidatively damaged DNA in the body However, the effect may remain unaltered if the DNA repair system is upregulated in studies lasting less than 24h Excretion of 8-0HdG is thought to be the result of sanitisation of the nucleotide pool by MTHI directed j§athways and possibly so far unknown endonuclease and nucleotide excision repair pathways, ,44 whereas 8-0HGua is derived from excision of the lesions in the DNA by the 8-oxo-guanine glycosylase (OGGl) and other glycosylases This is illustrated in OGGI deficient mice that have unaltered excretion of 8-0HdG, whereas 8-0HGua is excreted in lesser amounts compared to repair-proficient mice, although the difference is only by 25% suggesting alternative base excision repair.45 So far, antioxidant intervention studies have mainly been performed with 8-0HdG as a urinary biomarker, whereas 8-0HGua and many other oxidized DNA bases in urine would also be interesting to study TheRol« ofAntioxidants in the Prevention ofOxidative Damage to Nucleic Acids 215 Table outlines the characteristics of 25 studies with controlled desi~n of the effect of antioxidant supplementation on urinary excretion of 8_0HdG 20,42 ,46-69 Four studies on single carotenoid supplementation showed no effect on urinary excretion of8_0HdG,2°,46.52,63 whereas a mixture of carotenoids (daily intake: a-carotene (1.4 mg), ~-carotene (6.0 rng), lycopene (4.5 mg), bixin (11.7 mg), lutein (4.4 mg), and paprika carotenoids (2.2 mg) revealed a statistically significant difference in delta values (i.e., the difference between data obtained at the end of the supplementation and baseline) between the active and placebo groups , but there was no difference relative to the baseline values.56 In fact, the statistically significant difference of the delta values was mainly caused by an increased 8-0HdG excretion in the placebo group and the excretion only decreased slightly in the group receiving mixed carotenoids Supplementation with single or combination of vitamin C and vitamin E had no effect in most smdies,46,47.51.55.67whereas one study reported a beneficial effect ofhigh dose supplementation with vitamin C (1000 mg/day) and vitamin E (600 mg/day) in HIV-infected patients who had been treated with zidovudine 65 Multi-vitamin tablet si:fplementation provided no beneficial effectin normal subjects,42,58,59subjects at high altitude and subjects undergoing cold-weather field training at moderate altitude 19,54 Investigations of natural food products show an equal distribution between the studies reporting beneficial and null effect Ingestion of olive oils with high content of phenolic compounds was associated with reduced urinary excretion of 8-0HdG 48 A number of studies supplied antioxidants as berries, fruits, tea, and vegetables Ingestion of capsules containing extracts of fruits and berries, and eating diets rich in carotenoids lowered the excretion of 8_0HdG.59 A third, but small, study that did not report changes in plasma antioxidant concentration, showed lower 8-0HdG concentration in the urine of subjects, enrolled in a soccer summer training camp, who drank a commercial vegetable juice 60 On the other hand, neither eating 600 g of fruit and vegetables, nor the corresponding amount of minerals and vitamins in tablet form, were associated with lower urinary excretion of 8-0HdG relative to the placebo group, whereas there was a pronounced decline in the urinary excretion of8-0HdG during the study in all the groups (i.e., a period effect).42 Ingestion of capsules containing juices and powder of fruits (apple, orange, pineapple, papaya, cranberry, and peach) and vegetables (carrot, parsley, beet, broccoli, kale, cabbage, spinach, and tomato) had no effect on 8-0HdG excretion in urine 66 Supplementation with Brussels sprouts (300 glday) was investigated in two studies with mixed outcome.61,64 The first study that included male subjects, concluded that Brusselssprouts lowered urinary excretion of8-0HdG 64 In the subsequent study of sexes, the effect was less clear; there was a tendency that only the males benefited from ingestion of Brussels sprouts, but the results were not firm because of the low number of subjects and one of the male subjects had unrealistically high urin~ 8-0HdG excretion 61 Three studies have investigated the effect of drinking green tea.? 53,57,69 In one study there was a beneficial effect of drinking 300 rnI/day for one week,5o whereas there was no effect of ingesting green tea extract in meat patties for wk 53 The unadjusted data of the third study did not indicate a beneficial effect of drinking green tea; however adjustment of the data for a number ofvariables, including baseline 8-0HdG levels, revealed a statistically significant effect of drinking green tea for months 57.69 Lastly, drinking soya hypocotyl tea was associated with lower urinary excretion of 8_0HdG 62 It should be emphasized that the fate of the antioxidants in these investigations was inconclusive because (1) the plasma concentration of carotenoids decreased; (2) the putative active constituents (isoflavones) were not measured in the plasma and the alterations in the urinary concentration could not be assessed due to insufficient information 62 An overallassessmentofthe antioxidant intervention studies on urinary excretion of8-0HdG not outline overt differences between studies reporting beneficial and null findings related to the duration of the intervention period, number of subjects, or the power to detect a 50% difference There was an equal number of studies reporting beneficial and null effects that investigated 8-0HdG in urine by HPLC and ELISA The collection period of urine differed 2x2 parall el study of vi tam in C (500 mg) and vit amin E (400 IU) 30 13 M (N R) mo 184 MF (NS) 58 30-65 116 M (5) mo mo 24- 75 15 F (NS) 6wk Vit amin C (500 mg) to patients with systemic lup us erythematosus Six groups receiving co mbinations of vita m ins" Vitamin C (1 g) and vitamin E(0.6 g) 17-49 30 MF (N S) ± ± NR 17.8 ng/mg creati ni ne 14 42.4 nmol 9.0 prnol/urn ol creatinine 9.3 prnol/urn ol creatin ine NR 21.6 ng/mg creatini ne 86.3 ng/mg creatinine 1.8 mmol/mmol creat inine Baseline DNA Damage 11 wk Vi tamin C (500 mg) ± 39 32 122 M (5) 32 M F (N S) 14wk 3wk fl-carote ne (20 mg) Caroteno ids" Age b 18-48 19-22 wk mo Rutin (500 mg) s-carotene (30 mg) Subjects" 16F(NR) 14 M (NS) Duration Supplement per Day Table Urinary excretion of 8-0HdG in antioxidant supplementation studies ELISA (24 h) HPLC (24 h) HPLC (24 h) ELISA (spot) ELISA (spot) HPLC (24 h) ELISA (spot) Yes NR Yes Yes Yes Yes Yes Yes Yes ELISA (spot) H PLC (24 h) Effect on Antioxidants'' Assay (Collection Period) 51 65 46 67 47,71 63 56 20 52 Ref continued on next page Low er 8-0HdG in the active group of HIV -infected patients receiving zid ovudine therapy No effect No effect No effect No effect before or after an exercise test No effect No effect versus baselin e, but decreased 8-oxodG in active group post-supplementatio n No effect due to vit amin C, but increased excretio n in wa shout period No effect Effect "~ ~ ~ ~ ~ :!l ~ "