Mass Spectrometry in the Analysis of DNA, Protein, Peptide, and Lipid Biomarkers of Oxidative Stress
Stacy L. Gelhaus
Centers for Cancer Pharmacology and Excellence in Environmental Toxicology, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Search for more papers by this authorIan A. Blair
Centers for Cancer Pharmacology and Excellence in Environmental Toxicology, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Search for more papers by this authorStacy L. Gelhaus
Centers for Cancer Pharmacology and Excellence in Environmental Toxicology, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Search for more papers by this authorIan A. Blair
Centers for Cancer Pharmacology and Excellence in Environmental Toxicology, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Search for more papers by this authorMingshe Zhu
Department of Biotransformation, Bristol-Myers Squibb Research and Development, Princeton, New Jersey, USA
Search for more papers by this authorSummary
This chapter contains sections titled:
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Introduction
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DNA Biomarkers of Oxidative Stress
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Protein and Peptide Biomarkers of Oxidative Stress
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Lipid Biomarkers of Oxidative Stress
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Creatinine: The Common Denominator
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Summary and Conclusions
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Acknowledgments
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References
REFERENCES
- Akman SA, Doroshow JH, Burke TG, Dizdaroglu M. DNA base modifications induced in isolated human chromatin by NADH dehydrogenase-catalyzed reduction of doxorubicin. Biochemistry 1992; 31: 3500–3506.
- Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 1993; 90: 7915–7922.
- Annangudi SP, Deng Y, Gu X, Zhang W, Crabb JW, Salomon RG. Low-density lipoprotein has an enormous capacity to bind (E)-4-hydroxynon-2-enal (HNE): Detection and characterization of lysyl and histidyl adducts containing multiple molecules of HNE. Chem Res Toxicol 2008; 21: 1384–1395.
- Armitage B. Photocleavage of nucleic acids. Chem Rev 1998; 98: 1171–1200.
- Aruoma OI, Halliwell B, Dizdaroglu M. Iron ion-dependent modification of bases in DNA by the superoxide radical-generating system hypoxanthine/xanthine oxidase. J Biol Chem 1989a: 264: 13024–13028.
- Aruoma Ol, Halliwell B, Gajewski E, Dizdaroglu M. Damage to the bases in DNA induced by hydrogen peroxide and ferric ion chelates. J Biol Chem 1989b: 264: 20509–20512.
- Atwood CS, Scarpa RC, Huang X, Moir RD, Jones WD, Fairlie DP, Tanzi RE, Bush AI. Characterization of copper interactions with alzheimer amyloid beta peptides: Identification of an attomolar-affinity copper binding site on amyloid beta1-42. J. Neurochem 2000; 75: 1219–1233.
- Baillie TA. Future of toxicology-metabolic activation and drug Design: Challenges and opportunities in chemical toxicology. Chem Res Toxicol 2006; 19: 889–893.
- Baillie TA, Davis MR. Mass spectrometry in the analysis of glutathione conjugates. Biol Mass Spectrom 1993; 22: 319–325.
- Barbin A, Bartsch H. Mutagenic and promutagenic properties of DNA adducts formed by vinyl chloride metabolites. IARC Sci Publ 1986; 70: 345–358.
- Barnham KJ, Haeffner F, Ciccotosto GD, Curtain CC, Tew D., Mavros C, Beyreuther K, Carrington D, Masters CL, Cherny, RA, Cappai R, Bush AI. Tyrosine gated electron transfer is key to the toxic mechanism of Alzheimer's disease beta-amyloid. FASEB J 2004; 18: 1427–1429.
- Birincioglu M, Jaruga P, Chowdhury G, Rodriguez H, Dizdaroglu M, Gates KS. DNA base damage by the antitumor agent 3-amino-1,2,4-benzotriazine 1,4-dioxide (tirapazamine). J Am Chem Soc 2003; 125: 11607–11615.
- Blair IA. The role of oxidative stress in cancer and toxicology. In: Encyclopedia of Mass Spectrometry, Caprioli RM, Gross ML Eds., Elsevier, New York, 2005, pp. 283–307.
- Blair IA. DNA adducts with lipid peroxidation products. J Biol Chem 2008; 283: 15545–15549.
- Blakely WF, Fuciarelli, AF, Wegher, BJ, Dizdaroglu, M. Hydrogen peroxide–induced base damage in deoxyribonucleic acid. Radiat Res 1990; 121: 338–343.
- Boiteux S, Gajewski E, Laval J, Dizdaroglu M. Substrate specificity of theEscherichia coliFpg protein (formamidopyrimidine-DNA glycosylase): Excision of purine lesions in DNA produced by ionizing radiation or photosensitization. Biochemistry 1992; 31: 106–110.
- Brigelius-Flohe R. Tissue-specific functions of individual glutathione peroxidases. Free Radic Biol Med 1999; 27: 951–965.
- Burcham PC, Fontaine FR, Petersen DR, Pyke SM. Reactivity with Tris(hydroxymethyl)aminomethane confounds immunodetection of acrolein-adducted proteins. Chem Res Toxicol 2003; 16: 1196–1201.
- Burrows CJ, Muller JG. Oxidative nucleobase modifications leading to strand scission. Chem Rev 1998; 98: 1109–1152.
- Bush AI. The metallobiology of Alzheimer's disease. Trends Neurosci 2003; 26: 207–214.
- Butterfield DA, Kanski J. Methionine residue 35 is critical for the oxidative stress and neurotoxic properties of Alzheimer's amyloid beta-peptide 1-42. Peptides 2002; 23: 1299–1309.
- Carbone DL, Doorn JA, Kiebler Z, Ickes B.R, Petersen DR. Modification of heat shock protein 90 by 4-hydroxynonenal in a rat model of chronic alcoholic liver disease. J Pharmacol Exp Ther 2005; 315: 8–15.
- Carbone DL, Doorn JA, Kiebler Z, Sampey BP, Petersen DR. Inhibition of Hsp72-mediated protein refolding by 4-hydroxy-2-nonenal. Chem Res Toxicol 2004; 17: 1459–1467.
- Carini M, Aldini, G, Facino, R.M. Mass spectrometry for detection of 4-hydroxy-trans-2-nonenal (HNE) adducts with peptides and proteins. Mass Spectrom Rev 2004; 23: 281–305.
- Castellani RJ, Honda K, Zhu X, Cash AD, Nunomura A, Perry G, Smith MA. Contribution of redox-active iron and copper to oxidative damage in Alzheimer disease. Ageing Res Rev 2004; 3: 319–326.
- Chaitidis P, Schewe T, Sutherland M, Kuhn H, Nigam S. 15-Lipoxygenation of phospholipids may precede the sn-2 cleavage by phospholipases A2: Reaction specificities of secretory and cytosolic phospholipases A2 towards native and 15-lipoxygenated arachidonoyl phospholipids. FEBS Lett. 1998; 434: 437–441.
- Chaudhary AK, Nokubo M, Reddy GR, Yeola SN, Morrow JD, Blair IA, Marnett LJ. Detection of endogenous malondialdehyde-deoxyguanosine adducts in human liver. Science 1994; 265: 1580–1582.
- Ciccimaro E, Hanks SK, Yu KH, Blair IA. Absolute quantification of phosphorylation on the kinase activation loop of cellular focal adhesion kinase by stable isotope dilution liquid chromatography/mass spectrometry. Anal Chem 2009; 81: 3304–3313.
- Citardi MJ, Song W, Batra PS, Lanza DC, Hazen SL. Characterization of oxidative pathways in chronic rhinosinusitis and sinonasal polyposis. Am J Rhinol 2006; 20: 353–359.
- Codreanu SG, Zhang B, Sobecki SM, Billheimer DD, Liebler DC. Global analysis of protein damage by the lipid electrophile 4-hydroxy-2-nonenal. Mol Cell Proteomics 2009; 8: 670–680.
- Cohen G, Hochstein P Glutathione peroxidase: The primary agent for the elimination of hydrogen peroxide in erythrocytes. Biochemistry 1963; 2: 1420–1428.
- Cook JA, Gius D, Wink DA, Krishna MC, Russo A, Mitchell JB. Oxidative stress, redox, and the tumor microenvironment. Semin Radiat Oncol 2004; 14: 259–266.
- Dennehy MK, Richards KA, Wernke GR, Shyr Y, Liebler DC. Cytosolic and nuclear protein targets of thiol-reactive electrophiles. Chem Res Toxicol 2006; 19: 20–29.
- Dickinson DA, Forman HJ. Cellular glutathione and thiols metabolism. Biochem Pharm 2002; 64: 1019–1026.
- Dieckhaus CM, Fernandez-Metzler CL, King R, Krolikowski PH, Baillie TA. Negative ion tandem mass spectrometry for the detection of glutathione conjugates. Chem Res Toxicol 2005; 18: 630–638.
- Dizdaroglu M, Kirkali G, Jaruga P. Formamidopyrimidines in DNA: Mechanisms of formation, repair, and biological effects. Free Radic Biol Med 2008; 45: 1610–1621.
- Dizdaroglu M, Rao G, Halliwell B, Gajewski E. Damage to the DNA bases in mammalian chromatin by hydrogen peroxide in the presence of ferric and cupric ions. Arch Biochem Biophys 1991; 285: 317–324.
- Ehrenberg L, Hiesche KD, Osterman-Golkar S, Wenneberg I. Evaluation of genetic risks of alkylating agents: Tissue doses in the mouse from air contaminated with ethylene oxide. Mutat Res 1974; 24: 83–103.
- England TG, Jenner A, Aruoma OI, Halliwell B. Determination of oxidative DNA base damage by gas chromatography–mass spectrometry. Effect of derivatization conditions on artifactual formation of certain base oxidation products. Free Radic Res 1998; 29: 321–330.
- Evans DC, Baillie TA. Minimizing the potential for metabolic activation as an integral part of drug design. Curr Opin Drug Discov Devel 2005; 8: 44–50.
- Evans DC, Watt AP, Nicoll-Griffith DA, Baillie TA. Drug-protein adducts: An industry perspective on minimizing the potential for drug bioactivation in drug discovery and development. Chem Res Toxicol 2004; 17: 3–16.
- Farmer PB, Bailey E, Lamb JH, Connors TA. Approach to the quantitation of alkylated amino acids in haemoglobin by gas chromatography mass spectrometry. Biomed Mass Spectrom 1980; 7: 41–46.
- Farooqui AA, Yi OW, Lu XR, Halliwell B, Horrocks LA. Neurochemical consequences of kainate-induced toxicity in brain: Involvement of arachidonic acid release and prevention of toxicity by phospholipase A(2) inhibitors. Brain Res Brain Res Rev 2001; 38: 61–78.
- Farrow B, Evers BM. Inflammation and the development of pancreatic cancer. Surg Oncol 2002; 10: 153–169.
- Feng Z, Hu W, Hu Y, Tang MS. Acrolein is a major cigarette-related lung cancer agent: Preferential binding at p53 mutational hotspots and inhibition of DNA repair. Proc Natl Acad Sci USA 2006; 103: 15404–15409.
- Fernandes AP, Holmgren A. Glutaredoxins: Glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal 2004; 6: 63–74.
- Frelon S, Douki, T, Favier, A, Cadet, J. Hydroxyl radical is not the main reactive species involved in the degradation of DNA bases by copper in the presence of hydrogen peroxide. Chem Res Toxicol 2003; 16: 191–197.
- Gedik CM, Collins A Establishing the background level of base oxidation in human lymphocyteDNA:Resultsofaninterlaboratoryvalidationstudy. FASEBJ 2005; 19: 82–84.
- Green LC, Skipper PL, Turesky RJ, Bryant MS, Tannenbaum SR. In vivo dosimetry of 4-aminobiphenyl in rats via a cysteine adduct in hemoglobin. Cancer Res 1984; 44: 4254–4259.
- Heinecke JW. Oxidized amino acids: Culprits in human atherosclerosis and indicators of oxidative stress. Free Radic Biol Med 2002; 32: 1090–1101.
- Hensley K, Maidt ML, Yu Z, Sang H, Markesbery WR, Floyd RA. Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer brain indicates region-specific accumulation. J Neurosci 1998; 18: 8126–8132.
- Hoberg AM, Otteneder M, Marnett LJ, Poulsen HE. Measurement of the malondialdehyde-2'-deoxyguanosine adduct in human urine by immuno-extraction and liquid chromatography/atmospheric pressure chemical ionization tandem mass spectrometry. J Mass Spectrom 2004; 39: 38–42.
- Homolya L, Varadi A, Sarkadi B. Multidrug resistance-associated proteins: Export pumps for conjugates with glutathione, glucuronate or sulfate. Biofactors 2003; 17: 103–114.
- Huang X, Cuajungco MP, Atwood CS, Hartshorn MA, Tyndall JD, Hanson GR, Stokes KC, Leopold M, Multhaup G, Goldstein LE, Scarpa RC, Saunders AJ, Lim J, Moir RD, Glabe C, Bowden EF, Masters CL, Fairlie DP, Tanzi RE, Bush AI. Cu (II) potentiation of alzheimer abeta neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction. J Biol Chem 1999; 274: 37111–37116.
- Huang X, Cuajungco MP, Atwood CS, Moir RD, Tanzi RE, Bush AI. Alzheimer's disease, beta-amyloid protein and zinc. J Nutr 2000; 130: 1488S-1492S.
- Inoue K, Garner C, Ackermann BL, Oe T, Blair IA. Liquid chromatography/tandem mass spectrometry characterization of oxidized amyloid beta peptides as potential biomarkers of Alzheimer's disease. Rapid Commun Mass Spectrom 2006; 20: 911–918.
- Jang JH, Surh YJ. Beta-amyloid-induced apoptosis is associated with cyclooxygenase-2 up-regulation via the mitogen-activated protein kinase-NF-kappaB signaling pathway. Free Radic Biol Med 2005; 38: 1604–1613.
- Jaruga P, Kirkali G, Dizdaroglu M. Measurement of formamidopyrimidines in DNA. Free Radic Biol Med 2008; 45: 1601–1609.
- Jian W, Arora JS, Oe T, Shuvaev VV, Blair IA. Induction of endothelial cell apoptosis by lipid hydroperoxide-derived bifunctional electrophiles. Free Radic Biol Med 2005a: 39: 1162–1176.
- Jian W, Lee SH, Arora JS, Silva Elipe MV, Blair IA. Unexpected formation of etheno-2′-deoxyguanosine adducts from 5(S)-hydroperoxyeicosatetraenoic acid: Evidence for a bis-hydroperoxide intermediate. Chem Res Toxicol 2005b: 18: 599–610.
- Jian W, Lee SH, Mesaros C, Oe T, Elipe MV, Blair IA. A novel 4-oxo-2(E)nonenal-derived endogenous thiadiazabicyclo glutathione adduct formed during cellular oxidative stress. Chem Res Toxicol 2007; 20: 1008–1018.
- Kadiiska MB, Gladen BC, Baird DD, Germolec D, Graham LB, Parker CE, Nyska A, Wachsman JT, Ames BN, Basu S, Brot N, FitzGerald GA, Floyd RA, George M, Heinecke JW, Hatch GE, Hensley K, Lawson JA, Marnett LJ, Morrow JD, Murray DM, Plastaras J, Roberts LJ, Rokach J, Shigenaga MK, Sohal RS, Sun J, Tice RR, Van Thiel DH, Wellner D, Walter PB, Tomer KB, Mason RP, Barrett JC. Biomarkers of oxidative stress study II: are oxidation products of lipids, proteins, and DNA markers of CCl4 poisoning? Free Radic Biol Med 2005a: 38: 698–710.
- Kadiiska MB, Gladen BC, Baird DD, Graham LB, Parker CE, Ames BN, Basu S, FitzGerald GA, Lawson JA, Marnett LJ, Morrow JD, Murray DM, Plastaras J, Roberts LJ, Rokach J, Shigenaga MK, Sun J, Walter PB, Tomer KB, Barrett JC, Mason RP. Biomarkers of oxidative stress study III. Effects of the nonsteroidal anti-inflammatory agents indomethacin and meclofenamic acid on measurements of oxidative products of lipids in CCl4 poisoning. Free Radic Biol Med 2005b; 38: 711–718.
- Kapphahn RJ, Giwa BM, Berg KM, Roehrich H, Feng X, Olsen TW, Ferrington DA. Retinal proteins modified by 4-hydroxynonenal: Identification of molecular targets. Exp Eye Res 2006; 83: 165–175.
- Kato Y, Wu X, Naito M, Nomura H, Kitamoto N, Osawa T. Immunochemical detection of protein dityrosine in atherosclerotic lesion of apo-E-deficient mice using a novel monoclonal antibody. Biochem Biophys Res Commun 2000; 275: 11–15.
- Kawai Y, Uchida K, Osawa T. 2′-deoxycytidine in free nucleosides and double-stranded DNA as the major target of lipid peroxidation products. Free Radic Biol Med 2004; 36: 529–541.
- Ketterer B. Protective role of glutathione and glutathione transferases in mutagenesis and carcinogenesis. Mutat Res 1988; 202: 343–361.
- Knutson CG, Skipper PL, Liberman RG, Tannenbaum SR, Marnett LJ. Monitoring in vivo metabolism and elimination of the endogenous DNA adduct, M1dG {3-(2-deoxy-beta-D-erythro-pentofuranosyl)pyrimido[1,2-alpha]purin-10(3H)-one}, by accelerator mass spectrometry. Chem Res Toxicol 2008; 21: 1290–1294.
- Kolb HC, Sharpless KB. The growing impact of click chemistry on drug discovery. Drug Discov Today 2003; 8: 1128–1137.
- Kolman A, Chovanec M, Osterman-Golkar S. Genotoxic effects of ethylene oxide, propylene oxide and epichlorohydrin in humans: Update review (1990–2001). Mutat Res 2002; 512: 173–194.
- Krishnamurthy N, Haraguchi K, Greenberg MM, David SS. Efficient removal of formamidopyrimidines by 8-oxoguanine glycosylases. Biochemistry 2008; 47: 1043–1050.
- Lam BK, Austen KF. Leukotriene C4 synthase: a pivotal enzyme in cellular biosynthesis of the cysteinyl leukotrienes. Prostaglandins Other Lipid Mediat. 2002; 68–69: 511–520.
- Lawson JA, Li H, Rokach J, Adiyaman M, Hwang SW, Khanapure SP, FitzGerald GA. Identification of two major F2 isoprostanes, 8,12-iso- and 5-epi-8, 12-iso-isoprostane F2alpha-VI, in human urine. J Biol Chem 1998; 273: 29295–29301.
- Lee SH, Blair IA. Characterization of 4-oxo-2-nonenal as a novel product of lipid peroxidation. Chem Res Toxicol 2000; 13: 698–702.
- Lee SH, Blair IA. Oxidative DNA damage and cardiovascular disease. Trends Cardiovasc. Med 2001a: 11: 148–155.
- Lee SH, Blair IA. Targeted chiral lipidomics analysis by liquid chromatography electron capture atmospheric pressure chemical ionization mass spectrometry (LC-ECAPCI/ MS). Methods Enzymol 2007; 433: 159–174.
- Lee SH, Elipe MVS, Arora JS, Blair IA. Dioxododecenoic acid: A lipid hydroperoxide-derived bifunctional electrophile responsible for etheno DNA adduct formation. Chem Res Toxicol 2005a: 18: 566–578.
- Lee SH, Oe T, Arora JS, Blair IA. Analysis of Fe-II-mediated decomposition of a linoleic acid-derived lipid hydroperoxide by liquid chromatography/mass spectrometry. J Mass Spectrom. 2005b: 40: 661–668.
- Lee SH, Oe T, Blair IA. Vitamin C-induced decomposition of lipid hydroperoxides to endogenous genotoxins. Science 2001; 292: 2083–2086.
- Lee SH, Williams MV, Blair IA. Targeted chiral lipidomics analysis. Prostaglandins Other Lipid Mediat 2005c: 77: 141–157.
- Lee SH, Williams MV, Dubois RN, Blair IA. Cyclooxygenase-2-mediated DNA damage. J Biol Chem 2005d: 280: 28337–28346.
- Leeuwenburgh C, Hansen PA, Holloszy JO, Heinecke JW. Hydroxyl radical generation during exercise increases mitochondrial protein oxidation and levels of urinary dityrosine. Free Radic Biol Med 1999a: 27: 186–192.
- Leeuwenburgh C, Hansen PA, Holloszy JO, Heinecke JW. Oxidized amino acids in the urine of aging rats: potential markers for assessing oxidative stress in vivo. Am J Physiol 1999b: 276: R128–R135.
- Leeuwenburgh C, Rasmussen JE, Hsu FF, Mueller DM, Pennathur S, Heinecke JW. Mass spectrometric quantification of markers for protein oxidation by tyrosyl radical, copper, and hydroxyl radical in low density lipoprotein isolated from human atherosclerotic plaques. J Biol Chem 1997; 272: 3520–3526.
- Levsen K, Schiebel HM, Behnke B, Dotzer R, Dreher W, Elend M, Thiele H. Structure elucidation of phase II metabolites by tandem mass spectrometry: An overview. J Chromatogr A 2005; 1067: 55–72.
- Li H, Lawson JA, Reilly M, Adiyaman M, Hwang SW, Rokach J, FitzGerald GA. Quantitative high performance liquid chromatography/tandem mass spectrometric analysis of the four classes of F(2)-isoprostanes in human urine. Proc Natl Acad Sci USA 1999; 96: 13381–13386.
- Liebler DC. Protein damage by reactive electrophiles: targets and consequences. Chem Res Toxicol 2008; 21: 117–128.
- Little JM, Kurkela M, Sonka J, Jantti S, Ketola R, Bratton S, Finel M, RadominskaPandya A. Glucuronidation of oxidized fatty acids and prostaglandins B1 and E2 by human hepatic and recombinant UDP-glucuronosyltransferases. J Lipid Res. 2004; 45: 1694–1703.
- Liu X, Lovell MA, Lynn BC. Development of a method for quantification of acroleindeoxyguanosine adducts in DNA using isotope dilution-capillary LC/MS/MS and its application to human brain tissue. Anal Chem 2005; 77: 5982–5989.
- Lu SC. Regulation of glutathione synthesis. Curr Top Cell Regul 2000; 36: 95–116.
- Mangal D, Vudathala D, Park JH, Lee SH, Penning TM, Blair IA. Analysis of 7,8-dihydro-8-oxo-2′-deoxyguanosine in cellular DNA during oxidative stress. Chem Res Toxicol 2009: 22(5): 788–97.
- Mason DE, Liebler DC. Quantitative analysis of modified proteins by LC-MS/MS of peptides labeled with phenyl isocyanate. J Proteome Res 2003; 2: 265–272.
- McGiff JC, Quilley J. 20-Hydroxyeicosatetraenoic acid and epoxyeicosatrienoic acids and blood pressure. Curr Opin Nephrol Hypertens 2001; 10: 231–237.
- Meier BW, Gomez JD, Kirichenko OV, Thompson JA. Mechanistic basis for inflammation and tumor promotion in lungs of 2,6-di-tert-butyl-4-methylphenol-treated mice: Electrophilic metabolites alkylate and inactivate antioxidant enzymes. Chem Res Toxicol 2007; 20: 199–207.
- Meier BW, Gomez JD, Zhou A, Thompson JA. Immunochemical and proteomic analysis of covalent adducts formed by quinone methide tumor promoters in mouse lung epithelial cell lines. Chem Res Toxicol 2005; 18: 1575–1585.
- Mesaros C, Lee SH, Blair IA. Targeted quantitative analysis of eicosanoid lipids in biological samples using liquid chromatography–tandem mass spectrometry. J Chromatogr B 2009; 877: 2736–2745.
- Miller EC, Miller JA. The presence and significance of bound aminoazo dyes in the livers of rats fed para-dimethylaminoazobenzene. Cancer Res 1947; 7: 468–480.
- Milne GL, Yin H, Morrow JD. Human biochemistry of the isoprostane pathway. J Biol Chem 2008; 283: 15533–15537.
- Morrow JD, Awad JA, Boss HJ, Blair IA, Roberts LJ. Non-cyclooxygenase-derived prostanoids (F2-isoprostanes) are formed in situ on phospholipids. Proc Natl Acad Sci USA 1992; 89: 10721–10725.
- Morrow JD, Harris TM, Roberts LJ. Noncyclooxygenase oxidative formation of a series of novel prostaglandins: analytical ramifications for measurement of eicosanoids. Anal. Biochem 1990; 184: 1–10.
- Morrow JD, Minton TA, Mukundan CR, Campbell MD, Zackert WE, Daniel VC, Badr KF, Blair IA, Roberts LJ. Free radical-induced generation of isoprostanes in vivo. Evidence for the formation of D-ring and E-ring isoprostanes. J Biol Chem 1994; 269: 4317–4326.
- Multhaup G, Scheuermann S, Schlicksupp A, Simons A, Strauss M, Kemmling A, Oehler C, Cappai R, Pipkorn R, Bayer TA. Possible mechanisms of APP-mediated oxidative stress in Alzheimer's disease. Free Radic Biol Med 2002; 33: 45–51.
- Murphy RC, Zarini S. Glutathione adducts of oxyeicosanoids. Prostaglandins Other Lipid Mediat 2002; 68-69: 471–482.
- Nackerdien Z, Kasprzak KS, Rao G, Halliwell B, Dizdaroglu M. Nickel(II)- and cobalt (II)-dependent damage by hydrogen peroxide to the DNA bases in isolated human chromatin. Cancer Res 1991; 51: 5837–5842.
- Nath RG, Chung FL. Detection of exocyclic 1,N2-propanodeoxyguanosine adducts as common DNA lesions in rodents and humans. Proc Natl Acad Sci USA 1994; 91: 7491–7495.
- Nath RG, Ocando JE, Chung FL. Detection of 1,N2-propanodeoxyguanosine adducts as potential endogenous DNA lesions in rodent and human tissues. Cancer Res 1996; 56: 452–456.
- Nath RG, Ocando JE, Guttenplan JB, Chung FL. 1,N2-Propanodeoxyguanosine adducts: Potential New Biomarkers of smoking-induced DNA damage in human oral tissue. Cancer Res 1998; 58: 581–584.
- Nikolic D, Fan PW, Bolton JL, van Breemen RB. Screening for xenobiotic electrophilic metabolites using pulsed ultrafiltration–mass spectrometry. Comb Chem High Throughput Screen 1999; 2: 165–175.
- Oe T, Lee SH, Arora JS, Blair IA. Reactivity and selectivity of lipid hydroperoxide-derived modifications to peptides. Abstr Pap Am Chem Soc 2004; 228: U391.
- Orhan H, Coolen S, Meerman JH. Quantification of urinary o,o′-dityrosine, a biomarker for oxidative damage to proteins, by high performance liquid chromatography with triple quadrupole tandem mass spectrometry. A comparison with ion-trap tandem mass spectrometry. J Chromatogr B 2005; 827: 104–108.
- Orioli M, Aldini G, Benfatto MC, Facino RM, Carini M. HNE Michael adducts to histidine and histidine-containing peptides as biomarkers of lipid-derived carbonyl stress in urines: LC-MS/MS profiling in Zucker obese rats. Anal Chem 2007; 79: 9174–9184.
- Orioli M, Aldini G, Beretta G, Facino RM, Carini M LC-ESI-MS/MS determination of 4-hydroxy-trans-2-nonenal Michael adducts with cysteine and histidine-containing peptides as early markers of oxidative stress in excitable tissues. J Chromatogr B 2005; 827: 109–118.
- Orton CR, Liebler DC. Analysis of protein adduction kinetics by quantitative mass spectrometry: competing adduction reactions of glutathione-S-transferase P1-1 with electrophiles. Chem Biol Interact 2007; 168: 117–127.
- Parastatidis I, Thomson L, Burke A, Chernysh I, Nagaswami C, Visser J, Stamer S, Liebler DC, Koliakos G, Heijnen HF, FitzGerald GA, Weisel JW, Ischiropoulos H. Fibrinogen beta-chain tyrosine nitration is a prothrombotic risk factor. J Biol. Chem 2008; 283: 33846–33853.
- Parastatidis I, Thomson L, Fries DM, Moore RE, Tohyama J, Fu X, Hazen SL, Heijnen HF, Dennehy MK, Liebler DC, Rader DJ, Ischiropoulos H. Increased protein nitration burden in the atherosclerotic lesions and plasma of apolipoprotein A-I deficient mice. Circ Res 2007; 101: 368–376.
- Phinney SD, Odin RS, Johnson SB, Holman RT. Reduced arachidonate in serum phospholipids and cholesteryl esters associated with vegetarian diets in humans. Am J Clin Nutr 1990; 51: 385–392.
- Potter WZ, Davis DC, Mitchell JR, Jollow DJ, Gillette JR, Brodie BB. Acetaminophen-induced hepatic necrosis. 3. Cytochrome P-450-mediated covalent binding in vitro. J Pharmacol Exp Ther 1973; 187: 203–210.
- Prakash C, Zhang JY, Falck JR, Chauhan K, Blair IA. 20-Hydroxyeicosatetraenoic acid is excreted as a glucuronide conjugate in human urine. Biochem Biophys Res Commun 1992; 185: 728–733.
- Rahman I, Marwick J, Kirkham P. Redox modulation of chromatin remodeling: Impact on histone acetylation and deacetylation, NF-kappaB and pro-inflammatory gene expression. Biochem Pharm 2004; 68: 1255–1267.
- Rivera J, Ward N, Hodgson J, Puddey IB, Falck JR, Croft KD. Measurement of 20-hydroxyeicosatetraenoic acid in human urine by gas chromatography-mass spectrometry. Clin Chem 2004; 50: 224–226.
- Roberts LJ, Moore KP, Zackert WE, Oates JA, Morrow JD. Identification of the major urinary metabolite of the F2-isoprostane 8-iso-prostaglandin F2alpha in humans. J Biol Chem 1996; 271: 20617–20620.
- Roberts SA, Price VF, Jollow DJ. Acetaminophen structure-toxicity studies: In vivo covalent binding of a nonhepatotoxic analog, 3-hydroxyacetanilide. Toxicol Appl Pharmacol 1990; 105: 195–208.
- Rock CL, Lampe JW, Patterson RE. Nutrition, genetics, and risks of cancer. Annu Rev Public Health 2000; 21: 47–64.
- Rokach J, Khanapure SP, Hwang SW, Adiyaman M, Lawson JA, FitzGerald GA. Nomenclature of isoprostanes: A proposal. Prostaglandins 1997; 54: 853–873.
- Rouzer CA, Chaudhary AK, Nokubo M, Ferguson DM, Reddy GR, Blair IA, Marnett LJ. Analysis of the malondialdehyde-2'-deoxyguanosine adduct pyrimidopurinone in human leukocyte DNA by gas chromatography/electron capture/negative chemical ionization/mass spectrometry. Chem Res Toxicol 1997; 10: 181–188.
- Sacerdoti D, Balazy M, Angeli P, Gatta A, McGiff JC. Eicosanoid excretion in hepatic cirrhosis. Predominance of 20-HETE. J Clin Invest 1997; 100: 1264–1270.
- Sasaki DM, Yuan Y, Gikas K, Kanai K, Taber D, Morrow JD, Roberts LJ, Callewaert DM. Enzyme immunoassays for 15-F2T isoprostane-M, an urinary biomarker for oxidant stress. Adv Exp Med Biol 2002; 507: 537–541.
- Saxon E, Armstrong JI, Bertozzi CR. A “traceless” Staudinger ligation for the chemoselective synthesis of amide bonds. Org Lett 2000; 2: 2141–2143.
- Schneider C, Boeglin WE, Prusakiewicz JJ, Rowlinson SW, Marnett LJ, Samel N, Brash AR. Control of prostaglandin stereochemistry at the 15-carbon by cyclooxygenases-1 and -2. A critical role for serine 530 and valine 349. J Biol Chem 2002; 277: 478–485.
- Schroder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res 2005; 569: 29–63.
- Shah SJ, Yu KH, Sangar V, Parry SI, Blair IA. Identification and quantification of preterm birth biomarkers in human cervicovaginal fluid by liquid chromatography/ tandem mass spectrometry. J Proteome Res 2009; 8: 2407–2417.
- Shao B, Bergt C, Fu X, Green P, Voss JC, Oda MN, Oram JF, Heinecke JW. Tyrosine 192 in apolipoprotein A-I is the major site of nitration and chlorination by myeloperoxidase, but only chlorination markedly impairs ABCA1-dependent cholesterol transport. J Biol Chem 2005; 280: 5983–5993.
- Sharma RA, Farmer PB. Biological relevance of adduct detection to the chemoprevention of cancer. Clin Cancer Res 2004; 10: 4901–4912.
- Shelton MD, Chock PB, Mieyal JJ. Glutaredoxin: Role in reversible protein sglutathionylation and regulation of redox signal transduction and protein translocation. Antioxid Redox Signal 2005; 7: 348–366.
- Shin NY, Liu Q, Stamer SL, Liebler DC. Protein targets of reactive electrophiles in human liver microsomes. Chem Res Toxicol 2007; 20: 859–867.
- Singh G, Gutierrez A, Xu K, Blair IA. Liquid chromatography/electron capture atmospheric pressure chemical ionization/mass spectrometry: Analysis of pentafluorobenzyl derivatives of biomolecules and drugs in the attomole range. Anal Chem 2000; 72: 3007–3013.
- Sircar D, Subbaiah PV. Isoprostane measurement in plasma and urine by liquid chromatography–mass spectrometry with one-step sample preparation. Clin Chem 2007; 53: 251–258.
- Soberman RJ, Christmas P. The organization and consequences of eicosanoid signaling. J Clin Invest 2003; 111: 1107–1113.
- Stafforini DM, Sheller JR, Blackwell TS, Sapirstein A, Yull FE, McIntyre TM, Bonventre JV, Prescott SM, Roberts LJ. Release of free F2-isoprostanes from esterified phospholipids is catalyzed by intracellular and plasma platelet-activating factor acetylhydrolases. J Biol Chem 2006; 281: 4616–4623.
- Streeter AJ, Bjorge SM, Axworthy DB, Nelson SD, Baillie TA. The microsomal metabolism and site of covalent binding to protein of 3′-hydroxyacetanilide, a nonhepatotoxic positional isomer of acetaminophen. Drug Metab Dispos 1984; 12: 565–576.
- Suzuki H, Sugiyama Y. Excretion of GSSG and glutathione conjugates mediated by MRP1 and cMOAT/MRP2. Semin Liver Dis 1998; 18: 359–376.
- Suzuki N, Hishinuma T, Saga T, Sato J, Toyota T, Goto J, Mizugaki M. Determination of urinary 12(S)-hydroxyeicosatetraenoic acid by liquid chromatography–tandem mass spectrometry with column-switching technique: Sex difference in healthy volunteers and patients with diabetes mellitus. J. Chromatogr B Analyt Technol Biomed Life Sci 2003; 783: 383–389.
- Swenberg JA, Bogdanffy MS, Ham A, Holt S, Kim A, Morinello EJ, Ranasinghe A, Scheller N, Upton PB. Formation and repair of DNA adducts in vinyl chloride- and vinyl fluoride-induced carcinogenesis. IARC Sci Publ 1999; 150: 29–43.
- Swenberg JA, Koc H, Upton PB, Georguieva N, Ranasinghe A, Walker VE, Henderson R. Using DNA and hemoglobin adducts to improve the risk assessment of butadiene. Chem Biol Interact 2001; 135–136: 387–403.
- Szapacs ME, Riggins JN, Zimmerman LJ, Liebler DC. Covalent adduction of human serum albumin by 4-hydroxy-2-nonenal: Kinetic analysis of competing alkylation reactions. Biochemistry 2006; 45: 10521–10528.
- Taber DF, Morrow JD, Roberts LJ. A nomenclature system for the isoprostanes. Prostaglandins 1997; 53: 63–67.
- Tanabe T, Tohnai N. Cyclooxygenase isozymes and their gene structures and expression. Prostaglandins Other Lipid Mediat 2002; 68-69: 95–114.
- Tselepis AD, John CM. Inflammation, bioactive lipids and atherosclerosis: Potential roles of a lipoprotein-associated phospholipase A2, platelet activating factor-acetylhydrolase. Atheroscler Suppl 2002; 3: 57–68.
- Tsikas D, Schwedhelm E, Suchy MT, Niemann J, Gutzki FM, Erpenbeck VJ, Hohlfeld JM, Surdacki A, Frolich JC. Divergence in urinary 8-iso-PGF(2alpha) (iPF(2alpha)-III, 15-F(2t)-IsoP) levels from gas chromatography-tandem mass spectrometry quantification after thin-layer chromatography and immunoaffinity column chromatography reveals heterogeneity of 8-iso-PGF(2alpha). Possible methodological, mechanistic and clinical implications. J Chromatogr B 2003; 794: 237–255.
- Turesky RJ. The role of genetic polymorphisms in metabolism of carcinogenic hetero-cyclic aromatic amines. Curr Drug Metab. 2004; 5: 169–180.
- Uchida K. 4-Hydroxy-2-nonenal: A product and mediator of oxidative stress. Prog Lipid Res 2003; 42: 318–343.
- Wang W, Ballatori N. Endogenous glutathione conjugates: Occurrence and biological functions. Pharmacol Rev 1998; 50: 335–356.
- Ward NC, Tsai IJ, Barden A, van Bockxmeer FM, Puddey IB, Hodgson JM, Croft KD. A single nucleotide polymorphism in the CYP4F2 but not CYP4A11 gene is associated with increased 20-HETE excretion and blood pressure. Hypertension 2008; 51: 1393–1398.
- Watzer B, Reinalter S, Seyberth HW, Schweer H. Determination of free and glucuronide conjugated 20-hydroxyarachidonic acid (20-HETE) in urine by gas chromatography/ negative ion chemical ionization mass spectrometry. Prostaglandins Leukot. Essent. Fatty Acids 2000; 62: 175–181.
- Williams CS, Luongo C, Radhika A, Zhang T, Lamps LW, Nanney LB, Beauchamp RD, Dubois RN. Elevated cyclooxygenase-2 levels in Min mouse adenomas. Gastroenterology 1996; 111: 1134–1140.
- Williams KE, Carver TA, Miranda JJ, Kautiainen A, Vogel JS, Dingley K, Baldwin MA, Turteltaub KW, Burlingame AL. Attomole detection of in vivo protein targets of benzene in mice: Evidence for a highly reactive metabolite. Mol Cell Proteomics 2002; 1: 885–895.
- Williams MV, Lee SH, Blair IA. Liquid chromatography/mass spectrometry analysis of bifunctional electrophiles and DNA adducts from vitamin C mediated decomposition of 15-hydroperoxyeicosatetraenoic acid. Rapid Commun Mass Spectrom 2005; 19: 849–858.
- Williams MV, Lee SH, Pollack M, Blair IA. Endogenous lipid hydroperoxide-mediated DNA-adduct formation in Min mice. J Biol Chem 2006; 281: 10127–10133.
- Winnik WM, Kitchin KT. Measurement of oxidative stress parameters using liquid chromatography–tandem mass spectroscopy (LC-MS/MS). Toxicol Appl Pharmacol 2008; 233: 100–106.
- Wong HL, Liebler DC. Mitochondrial protein targets of thiol-reactive electrophiles. Chem Res Toxicol. 2008; 21: 796–804.
- Wu G, Fang YZ, Yang S, Lupton JR, Turner ND. Glutathione metabolism and its implications for health. J Nutr 2004; 134: 489–492.
- Wu, K.K. Control of cyclooxygenase-2 transcriptional activation by pro-inflammatory mediators. Prostaglandins Leukot Essent Fatty Acids 2005; 72: 89–93.
- Yan W, Byrd GD, Ogden MW. Quantitation of isoprostane isomers in human urine from smokers and nonsmokers by LC-MS/MS. J Lipid Res 2007; 48: 1607–1617.
- Yan Y, Weaver VM, Blair IA. Analysis of protein expression during oxidative stress in breast epithelial cells using a stable isotope labeled proteome internal standard. J. Proteome Res 2005; 4: 2007–2014.
- Yocum AK, Yu K, Oe T, Blair IA. Effect of immunoaffinity depletion of human serum during proteomic investigations. J Proteome Res 2005; 4: 1722–1731.
- Zastawny TH, Doetsch PW, Dizdaroglu M. A novel activity of E. coli uracil DNA N-glycosylase excision of isodialuric acid (5,6-dihydroxyuracil), a major product of oxidative DNA damage, from DNA. FEBS Lett 1995; 364: 255–258.
- Zhang S, Villalta PW, Wang M, Hecht SS. Detection and quantitation of acrolein-derived 1,N2-propanodeoxyguanosine adducts in human lung by liquid chromatography–electrospray ionization–tandem mass spectrometry. Chem Res Toxicol 2007; 20: 565–571.
- Zhou L, Nilsson A. Sources of eicosanoid precursor fatty acid pools in tissues. J Lipid Res 2001; 42: 1521–1542.
- Zhou X, Taghizadeh K, Dedon PC. Chemical and biological evidence for base propenals as the major source of the endogenous M1dG adduct in cellular DNA. J Biol Chem 2005a: 280: 25377–25382.
- Zhou X, Taghizadeh K, Dedon PC. Chemical and biological evidence for base propenals as the major source of the endogenous M1dG adduct in cellular DNA. J Biol Chem 2005b: 280: 25377–25382.
- Zhu P, Oe T, Blair IA. Determination of cellular redox status by stable isotope dilution liquid chromatography/mass spectrometry analysis of glutathione and glutathione disulfide. Rapid Commun. Mass Spectrom 2008; 22: 432–440.