586
Views
2
CrossRef citations to date
0
Altmetric
Review

Identification and characterization of protein cross-links induced by oxidative reactions

, &
Pages 665-681 | Received 11 May 2018, Accepted 06 Aug 2018, Published online: 27 Aug 2018

References

  • Wedemeyer WJ, Welker E, Narayan M, et al. Disulfide bonds and protein folding. Biochemistry. 2000;39:4207–4216.
  • Thornton JM. Disulphide bridges in globular proteins. J Mol Biol. 1981;151:261–287.
  • Kagan HM. Lysyl oxidase: mechanism, regulation and relationship to liver fibrosis. Pathol Res Pract. 1994;190:910–919.
  • López B, González A, Hermida N, et al. Role of lysyl oxidase in myocardial fibrosis: from basic science to clinical aspects. Am J Physiol. Heart Circ Physiol. 2010;299:H1–9.
  • Trackman PC. Lysyl oxidase isoforms and potential therapeutic opportunities for fibrosis and cancer. Expert Opin Ther Targets. 2016;20:935–945.
  • McCall AS, Cummings CF, Bhave G, et al. Bromine is an essential trace element for assembly of collagen IV scaffolds in tissue development and architecture. Cell. 2014;157:1380–1392.
  • Bhave G, Cummings CF, Vanacore RM, et al. Peroxidasin forms sulfilimine chemical bonds using hypohalous acids in tissue genesis. Nat Chem Biol. 2012;8:784–790.
  • Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol. 2003;4:140–156.
  • Heck T, Faccio G, Richter M, et al. Enzyme-catalyzed protein crosslinking. Appl Microbiol Biotechnol. 2013;97:461–475.
  • Wang D-S, Dickson DW, Malter JS. Tissue transglutaminase, protein cross-linking and Alzheimer’s disease: review and views. Int J Clin Exp Pathol. 2008;1:5–18.
  • Westermann S, Weber K. Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol. 2003;4:938–947.
  • Kerscher O, Felberbaum R, Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol. 2006;22:159–180.
  • Monnier VM, Mustata GT, Biemel KL, et al. Cross-linking of the extracellular matrix by the maillard reaction in aging and diabetes: an update on “a puzzle nearing resolution”. Ann N Y Acad Sci. 2005;1043:533–544.
  • Ajith TA, Vinodkumar P. Advanced glycation end products: association with the pathogenesis of diseases and the current therapeutic advances. Curr Clin Pharmacol. 2016;11:118–127.
  • Oryan A, Kamali A, Moshiri A, et al. Chemical crosslinking of biopolymeric scaffolds: current knowledge and future directions of crosslinked engineered bone scaffolds. Int J Biol Macromol. 2018;107:678–688.
  • Klaips CL, Jayaraj GG, Hartl FU. Pathways of cellular proteostasis in aging and disease. J Cell Biol. 2018;217:51–63.
  • Carver JA, Ecroyd H, Truscott RJW, et al. Proteostasis and the regulation of intra- and extracellular protein aggregation by ATP-independent molecular chaperones: lens alpha-crystallins and milk caseins. Acc Chem Res. 2018;51:745–752.
  • van Witteloostuijn SB, Pedersen SL, Jensen KJ. Half-life extension of biopharmaceuticals using chemical methods: alternatives to PEGylation. ChemMedChem. 2016;11:2474–2495.
  • Sies H, Berndt C, Jones DP. Oxidative stress. Annu Rev Biochem. 2017;86:715–748.
  • Davies MJ. Protein oxidation and peroxidation. Biochem J. 2016;473:805–825.
  • Halliwell B, Gutteridge JMC. Free radicals in biology & medicine. Oxford: Oxford University Press; 2015.
  • Misra HP, Fridovich I. The generation of superoxide radical during the autoxidation of hemoglobin. J Biol Chem. 1972;247:6960–6962.
  • Mittal M, Siddiqui MR, Tran K, et al. Reactive oxygen species in inflammation and tissue injury. Antiox Redox Signal. 2014;20:1126–1167.
  • Robinson JM. Reactive oxygen species in phagocytic leukocytes. Histochem Cell Biol. 2008;130:281–297.
  • Babior BM. The respiratory burst oxidase. TIBS. 1987;12:241–243.
  • Koppenol WH. The centennial of the Fenton reaction. Free Radic Biol Med. 1993;15:645–651.
  • Valko M, Morris H, Cronin M. Metals, toxicity and oxidative stress. Curr Med Chem. 2005;12:1161–1208.
  • Sies H. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress. Redox Biol. 2017;11:613–619.
  • Butterfield DA, Perluigi M, Reed T, et al. Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications. Antiox Redox Signal. 2012;17:1610–1655.
  • Davies MJ. The oxidative environment and protein damage. Biochim Biophys Acta. 2005;1703(2):93–109.
  • Davies MJ, Hawkins CL, Pattison DI, et al. Mammalian heme peroxidases: from molecular mechanisms to health implications. Antioxid Redox Signal. 2008;10:1199–1234.
  • Pattison DI, Davies MJ. Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds. Chem Res Toxicol. 2001;14:1453–1464.
  • Pattison DI, Davies MJ, Hawkins CL. Reactions and reactivity of myeloperoxidase-derived oxidants: differential biological effects of hypochlorous and hypothiocyanous acids. Free Radic Res. 2012;46:975–995.
  • Ronsein GE, Winterbourn CC, Di Mascio P, et al. Cross-linking methionine and amine residues with reactive halogen species. Free Radic Biol Med. 2014;70:278–287.
  • Davies MJ. Protein and peptide alkoxyl radicals can give rise to C-terminal decarboxylation and backbone cleavage. Arch Biochem Biophys. 1996;336:163–172.
  • Morgan PE, Pattison DI, Davies MJ. Quantification of hydroxyl radical-derived oxidation products in peptides containing glycine, alanine, valine, and proline. Free Radic Biol Med. 2012;52:328–339.
  • Ferrer-Sueta G, Manta B, Botti H, et al. Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem Res Toxicol. 2011;24:434–450.
  • Criado S, Soltermann AT, Marioli JM, et al. Sensitized photooxidation of di- and tripeptides of tyrosine. Photochem Photobiol. 1998;68:453–458.
  • Butler J, Land EJ, Prutz WA, et al. Charge transfer between tryptophan and tyrosine in proteins. Biochim Biophys Acta. 1982;705:150–162.
  • Prutz WA, Butler J, Land EJ, et al. The role of sulphur peptide functions in free radical transfer: a pulse radiolysis study. Int J Radiat Biol. 1989;55:539–556.
  • Prutz WA, Land EJ. Charge transfer in peptides. Pulse radiolysis investigation of one-electron reactions in dipeptides of tryptophan and tyrosine. Int J Radiat Biol. 1979;36:513–520.
  • Prutz WA, Siebert F, Butler J, et al. Charge transfer in peptides. Intramolecular radical transformations involving methionine, tryptophan and tyrosine. Biochim Biophys Acta. 1982;705:139–149.
  • Aubert C, Vos MH, Mathis P, et al. Intraprotein radical transfer during photoactivation of DNA photolyase. Nature. 2000;405:586–590.
  • Barry BA, Chen J, Keough J, et al. Proton coupled electron transfer and redox active tyrosines: structure and function of the tyrosyl radicals in ribonucleotide reductase and photosystem II. J Phys Chem Lett. 2012;3:543–554.
  • Winkler JR, Gray HB. Electron flow through biological molecules: does hole hopping protect proteins from oxidative damage? Q Rev Biophys. 2015;48:411–420.
  • Warren JJ, Ener ME, Vlcek A Jr., et al. Electron hopping through proteins. Coord Chem Rev. 2012;256:2478–2487.
  • Zhang L, Am E, Dl B, et al. Analysis of monoclonal antibody sequence and post-translational modifications by time-controlled proteolysis and tandem mass spectrometry. Mol Cell Proteomics. 2016;15:1479–1488.
  • Ferrer-Sueta G, Campolo N, Trujillo M, et al. Biochemistry of peroxynitrite and protein tyrosine nitration. Chem Rev. 2018;118:1338–1408.
  • Dizdaroglu M, Simic MG. Isolation and characterization of radiation-induced aliphatic peptide dimers. Int J Radiati Biol. 1983;44:231–239.
  • Schoneich C. Thiyl radicals and induction of protein degradation. Free Radic Res. 2016;50:143–149.
  • Fang X, Jin F, Jin H, et al. Reaction of the superoxide radical with the N-centred radical derived from N-acetyltryptophan methyl ester. J Chem Soc, Perkin Trans. 1998;2:259–263.
  • Hunter EP, Desrosiers MF, Simic MG. The effect of oxygen, antioxidants, and superoxide radical on tyrosine phenoxyl radical dimerization. Free Radic Biol Med. 1989;6:581–585.
  • Pattison DI, Rahmanto AS, Davies MJ. Photo-oxidation of proteins. Photochem Photobiol Sci. 2012;11:38–53.
  • Skjoldager N, Blanner Bang M, Rykær M, et al. The structure of Lactococcus lactis thioredoxin reductase reveals molecular features of photo-oxidative damage. Scientific Rep. 2017;7: 46282.
  • Bjornberg O, Viennet T, Skjoldager N, et al. Lactococcus lactis thioredoxin reductase is sensitive to light inactivation. Biochemistry. 2015;54:1628–1637.
  • Siodlak D. alpha,beta-Dehydroamino acids in naturally occurring peptides. Amino Acids. 2015;47:1–17.
  • Friedman M. Chemistry, biochemistry, nutrition, and microbiology of lysinoalanine, lanthionine, and histidinoalanine in food and other proteins. J Agric Food Chem. 1999;47:1295–1319.
  • Steinmann D, Mozziconacci O, Bommana R, et al. Photodegradation pathways of protein disulfides: human growth hormone. Pharm Res. 2017;34:2756–2778.
  • Agon VV, Bubb WA, Wright A, et al. Sensitizer-mediated photooxidation of histidine residues: evidence for the formation of reactive side-chain peroxides. Free Radic Biol Med. 2006;40:698–710.
  • Wright A, Bubb WA, Hawkins CL, et al. Singlet oxygen-mediated protein oxidation: evidence for the formation of reactive side chain peroxides on tyrosine residues. Photochem Photobiol. 2002;76:35–46.
  • Gracanin M, Hawkins CL, Pattison DI, et al. Singlet oxygen-mediated amino acid and protein oxidation: formation of tryptophan peroxides and decomposition products. Free Radic Biol Med. 2009;47:92–102.
  • Karam LR, Dizdaroglu M, Simic MG. OH radical-induced products of tyrosine peptides. Int J Radiat Biol. 1984;46:715–724.
  • Rzepecki LM, Nagafuchi T, Waite JH. alpha,beta-dehydro-3,4-dihydroxyphenylalanine derivatives: potential schlerotization intermediates in natural composite materials. Arch Biochem Biophys. 1991;285:17–26.
  • Torosantucci R, Sharov VS, Van Beers M, et al. Identification of oxidation sites and covalent cross-links in metal catalyzed oxidized interferon beta-1a: potential implications for protein aggregation and immunogenicity. Molec Pharmac. 2013;10:2311–2322.
  • Suzuki YJ, Carini M, Butterfield DA. Protein carbonylation. Antioxid Redox Signal. 2010;12:323–325.
  • Aquilina JA, Truscott RJ. Cysteine is the initial site of modification of a-crystallin by kynurenine. Biochem Biophys Res Commun. 2000;276:216–223.
  • Harwood DT, Kettle AJ, Winterbourn CC. Production of glutathione sulfonamide and dehydroglutathione from GSH by myeloperoxidase-derived oxidants and detection using a novel LC-MS/MS method. Biochem J. 2006;399:161–168.
  • Fu X, Mueller DM, Heinecke JW. Generation of intramolecular and intermolecular sulfenamides, sulfinamides, and sulfonamides by hypochlorous acid: a potential pathway for oxidative cross-linking of low-density lipoprotein by myeloperoxidase. Biochemistry. 2002;41:1293–1301.
  • Raftery MJ, Yang Z, Valenzuela SM, et al. Novel intra- and inter-molecular sulfinamide bonds in S100A8 produced by hypochlorite oxidation. J Biol Chem. 2001;276:33393–33401.
  • Gross AJ, Sizer IW. The oxidation of tyramine, tyrosine, and related compounds by peroxidase. J Biol Chem. 1959;234:1611–1614.
  • Heinecke JW, Shapiro BM. Respiratory burst oxidase of fertilization. Proc Natl Acad Sci U S A. 1989;86:1259–1263.
  • Aeschbach R, Amado R, Neukom H. Formation of dityrosine cross-links in proteins by oxidation of tyrosine residues. Biochim Biophys Acta. 1976;439:292–301.
  • Heinecke JW, Li W, Francis GA, et al. Tyrosyl radical generated by myeloperoxidase catalyzes the oxidative cross-linking of proteins. J Clin Invest. 1993;91:2866–2872.
  • Jacob JS, Cistola DP, Hsu FF, et al. Human phagocytes employ the myeloperoxidase-hydrogen peroxide system to synthesize dityrosine, trityrosine, pulcherosine, and isodityrosine by a tyrosyl radical-dependent pathway. J Biol Chem. 1996;271:19950–19956..
  • Giulivi C, Traaseth NJ, Davies KJ. Tyrosine oxidation products: analysis and biological relevance. Amino Acids. 2003;25(3–4):227–232.
  • Ziouzenkova O, Asatryan L, Akmal M, et al. Oxidative cross-linking of ApoB100 and hemoglobin results in low density lipoprotein modification in blood. Relevance to atherogenesis caused by hemodialysis. J Biol Chem. 1999;274:18916–18924.
  • Francis GA, Mendez AJ, Bierman EL, et al. Oxidative tyrosylation of high density lipoprotein by peroxidase enhances cholesterol removal from cultured fibroblasts and macrophage foam cells. Proc Natl Acad Sci U S A. 1993;90:6631–6635.
  • Leeuwenburgh C, Rasmussen JE, Hsu FF, et al. 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.
  • Leinisch F, Mariotti M, Rykaer M, et al. Peroxyl radical- and photo-oxidation of glucose 6-phosphate dehydrogenase generates cross-links and functional changes via oxidation of tyrosine and tryptophan residues. Free Radic Biol Med. 2017;112:240–252.
  • Leinisch F, Mariotti M, Hägglund P, et al. Structural and functional changes in RNAse A originating from tyrosine and histidine cross-linking and oxidation. Free Radic Biol Med. 2018;126:73–86.
  • Degendorfer G, Chuang CY, Kawasaki H, et al. Peroxynitrite-mediated oxidation of plasma fibronectin. Free Radic Biol Med. 2016;97:602–615.
  • Degendorfer G, Chuang CY, Hammer A, et al. Peroxynitrous acid induces structural and functional modifications to basement membranes and its key component, laminin. Free Radic Biol Med. 2015;89:721–733.
  • Malencik DA, Anderson SR. Dityrosine formation in calmodulin: cross-linking and polymerization catalyzed by Arthromyces peroxidase. Biochemistry. 1996;35:4375–4386.
  • Paviani V, Queiroz RF, Marques EF, et al. Production of lysozyme and lysozyme-superoxide dismutase dimers bound by a ditryptophan cross-link in carbonate radical-treated lysozyme. Free Radic Biol Med. 2015;89:72–82.
  • Arenas A, López-Alarcón C, Kogan M, et al. Chemical modification of lysozyme, glucose 6-phosphate dehydrogenase, and bovine eye lens proteins induced by peroxyl radicals: role of oxidizable amino acid residues. Chem Res Toxicol. 2013;26:67–77.
  • Tew D, Ortiz de Montellano PR. The myoglobin protein radical. Coupling of Tyr-103 to Tyr-151 in the H2O2-mediated cross-linking of sperm whale myoglobin. J Biol Chem. 1988;263:17880–17886.
  • Das AB, Nagy P, Abbott HF, et al. Reactions of superoxide with the myoglobin tyrosyl radical. Free Radic Biol Med. 2010;48:1540–1547.
  • Torosantucci R, Mozziconacci O, Sharov V, et al. Chemical modifications in aggregates of recombinant human insulin induced by metal-catalyzed oxidation: covalent cross-linking via michael addition to tyrosine oxidation products. Pharmaceut Res. 2012;29:2276–2293.
  • Das AB, Nauser T, Koppenol WH, et al. Rapid reaction of superoxide with insulin-tyrosyl radicals to generate a hydroperoxide with subsequent glutathione addition. Free Radic Biol Med. 2014;70:86–95.
  • Giulivi C, Davies KJA. Dityrosine and tyrosine oxidation products are endogenous markers for the selective proteolysis of oxidatively modified red blood cell hemoglobin by (the 19 S) proteasome. J Biol Chem. 1993;268:8752–8759.
  • Truscott RJW, Friedrich MG. The etiology of human age-related cataract. Proteins don’t last forever. Biochim Biophys Acta. 2016;1860:192–198.
  • Serpell LC, Williams TL, Stewart-Parker M, et al. A central role for dityrosine crosslinking of amyloid-β in Alzheimer’s disease. Acta Neuropathol Commun. 2013;1:83.
  • Tiwari MK, Leinisch F, Sahin C, et al. Early events in copper-ion catalyzed oxidation of α-synuclein. Free Radic Biol Med. 2018;121:38–50.
  • Pennathur S, Jackson-Lewis V, Przedborski S, et al. Mass spectrometric quantification of 3-nitrotyrosine, ortho-tyrosine, and o,o’-dityrosine in brain tissue of 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-treated mice, a model of oxidative stress in Parkinson’s disease. J Biol Chem. 1999;274:34621–34628.
  • Mukherjee S, Kapp EA, Lothian A, et al. Characterization and identification of dityrosine cross-linked peptides using tandem mass spectrometry. Anal Chem. 2017;89:6136–6145.
  • Kato Y, Maruyama W, Naoi M, et al. Immunohistochemical detection of dityrosine in lipofuscin pigments in the aged human brain. FEBS Lett. 1998;439:231–234.
  • Kato Y, Dozaki N, Nakamura T, et al. Quantification of modified tyrosines in healthy and diabetic human urine using liquid chromatography/tandem mass spectrometry. J Clin Biochem Nutr. 2009;44:67–78.
  • Wu GR, Cheserek M, Shi YH, et al. Elevated plasma dityrosine in patients with hyperlipidemia compared to healthy individuals. Ann Nutr Metab. 2014;66:44–50.
  • Heinecke JW, Shapiro BM. Superoxide peroxidase activity of ovoperoxidase, the cross-linking enzyme of fertilization. J Biol Chem. 1990;265:9241–9246.
  • Schaefer J, Kramer KJ, Garbow JR, et al. Aromatic cross-links in insect cuticle: detection by solid-state 13C and 15N NMR. Science. 1987;235(4793):1200–1204.
  • Mai K, Smith NC, Feng ZP, et al. Peroxidase catalysed cross-linking of an intrinsically unstructured protein via dityrosine bonds in the oocyst wall of the apicomplexan parasite, Eimeria maxima. Int J Parasitol. 2011;41:1157–1164.
  • Medinas DB, Gozzo FC, Santos LFA, et al. A ditryptophan cross-link is responsible for the covalent dimerization of human superoxide dismutase 1 during its bicarbonate-dependent peroxidase activity. Free Radic Biol Med. 2010;49:1046–1053.
  • Carroll L, Pattison DI, Davies JB, et al. Formation and detection of oxidant-generated tryptophan dimers in peptides and proteins. Free Radic Biol Med. 2017;113:132–142.
  • Sherin PS, Zelentsova EA, Sormacheva ED, et al. Aggregation of α-crystallins in kynurenic acid-sensitized UVA photolysis under anaerobic conditions. Phys Chem Chem Phys. 2016;18:8827–8839.
  • Bhaskar B, Immoos CE, Shimizu H, et al. A novel heme and peroxide-dependent tryptophan-tyrosine cross-link in a mutant of cytochrome c peroxidase. J Mol Biol. 2003;328:157–166.
  • Leo G, Altucci C, Bourgoin-Voillard S, et al. Ultraviolet laser-induced cross-linking in peptides. Rapid Commun Mass Spectrom. 2013;27:1660–1668.
  • Mariotti M, Leinisch F, Leeming DJ, et al. Mass-spectrometry-based identification of cross-links in proteins exposed to photo-oxidation and peroxyl radicals using 18O labeling and optimized tandem mass spectrometry fragmentation. J Proteome Res. 2018;17:2017–2027.
  • Bailey AJ. The chemistry of natural enzyme-induced cross-links of proteins. Amino Acids. 1991;1:293–306.
  • Burzio LA, Waite JH. Cross-linking in adhesive proteins: studies with model decapeptides. Biochemistry. 2000;39:11147–11153.
  • Rzepecki LM, Waite JH. Wresting the muscle from mussel beards: research and applications. Mol Mar Biol Biotechnol. 1995;4:313–322.
  • Taylor SW, Ross MM, Waite JH. Novel 3,4-di- and 3,4,5-trihydroxyphenylalanine-containing polypeptides from the blood cells of the ascidians Ascidia ceratodes and Molgula manhattensis. Arch Biochem Biophys. 1995;324(2):228–240.
  • Winterbourn CC, Parsons-Mair HN, Gebicki S, et al. Requirements for superoxide-dependent tyrosine hydroperoxide formation in peptides. Biochem J. 2004;381:241–248.
  • Tweeddale HJ, Hawkins CL, Jamie JF, et al. Cross-linking of lens crystallin proteins induced by tryptophan metabolites and metal ions: implications for cataract development. Free Radic Res. 2016;50:1116–1130.
  • Truscott RJ. Age-related nuclear cataract-oxidation is the key. Exp Eye Res. 2005;80:709–725.
  • Davies MJ, Truscott RJW. Photo-oxidation of proteins and its role in cataractogenesis. J Photochem Photobiol B. 2001;63:114–125.
  • Liu M, Zhang Z, Cheetham J, et al. Discovery and characterization of a photo-oxidative histidine-histidine cross-link in IgG1 antibody utilizing 18O-labeling and mass spectrometry. Anal Chem. 2014;86:4940–4948.
  • Xu CF, Chen Y, Yi L, et al. Discovery and characterization of histidine oxidation initiated cross-links in an IgG1 monoclonal antibody. Anal Chem. 2017;89:7915–7923.
  • Shen H-R, Spikes JD, Smith CJ, et al. Photodynamic cross-linking of proteins: IV. Nature of the His-His bond(s) formed in the rose bengal-photosensitized cross-linking of N-benzoyl-L-histidine. J Photochem Photobiol A. 2000;130:1–6.
  • Barata-Vallejo S, Ferreri C, Zhang T, et al. Radiation chemical studies of Gly-Met-Gly in aqueous solution. Free Radic Res. 2016;50(Sup1):S24–S39.
  • Weder JKP, Belitz H-D. Proteins: interactions and reactions involved in food processing. In: Encyclopedia of Food Science and Nutrition, 2nd Edition). Caballero B. Ed, Academic Press, 2003;4841–4847
  • Linetsky M, Hill JM, LeGrand RD, et al. Dehydroalanine crosslinks in human lens. Exp Eye Res. 2004;79(4):499–512.
  • Reiser K, McCormick RJ, Rucker RB. Enzymatic and nonenzymatic cross-linking of collagen and elastin. FASEB J. 1992;6:2439–2449.
  • Eyre DR, Weis MA, Wu JJ. Advances in collagen cross-link analysis. Methods. 2008;45:65–74.
  • Pisano JJ, Finlayson JS, Peyton MP. Cross-link in fibrin polymerized by factor 13: epsilon-(gamma-glutamyl)lysine. Science. 1968;160(3830):892–893.
  • Wilhelmus MMM, Grunberg SCS, Jgjm B, et al. Transglutaminases and transglutaminase-catalyzed cross-links colocalize with the pathological lesions in Alzheimer’s disease brain. Brain Pathol. 2009;19:612–622.
  • Komander D, Rape M. The ubiquitin code. Annu Rev Biochem. 2012;81:203–229.
  • Griffin M, Casadio R, Bergamini CM. Transglutaminases: nature’s biological glues. Biochem J. 2002;368:377–396.
  • Hawkins CL, Morgan PE, Davies MJ. Quantification of protein modification by oxidants. Free Radic Biol Med. 2009;46:965–988.
  • Davies MJ, Fu S, Wang H, et al. Stable markers of oxidant damage to proteins and their application in the study of human disease. Free Radic Biol Med. 1999;27:1151–1163.
  • Kato Y, Wu X, Naito M, et al. 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.
  • Al-Hilaly YK, Biasetti L, Blakeman BJF, et al. The involvement of dityrosine crosslinking in α-synuclein assembly and deposition in Lewy Bodies in Parkinson’s disease. Sci Rep. 2016;6:39171.
  • Degendorfer G, Chuang CY, Mariotti M, et al. Exposure of tropoelastin to peroxynitrous acid gives high yields of nitrated tyrosine residues, di-tyrosine cross-links and altered protein structure and function. Free Radic Biol Med. 2017;115:219–231.
  • Fuentes-Lemus E, Silva E, Leinisch F, et al. alpha- and beta-casein aggregation induced by riboflavin-sensitized photo-oxidation occurs via di-tyrosine cross-links and is oxygen concentration dependent. Food Chem. 2018;256:119–128.
  • Abdelrahim M, Morris E, Carver J, et al. Liquid chromatographic assay of dityrosine in human cerebrospinal fluid. J Chromatog B. 1997;696:175–182.
  • DiMarco T, Giulivi C. Current analytical methods for the detection of dityrosine, a biomarker of oxidative stress, in biological samples. Mass Spectrometry Rev. 2007;26:108–120.
  • Giulivi C, Davies KJ. Mechanism of the formation and proteolytic release of H2O2-induced dityrosine and tyrosine oxidation products in hemoglobin and red blood cells. J Biol Chem. 2001;276:24129–24136.
  • Marvin LF, Delatour T, Tavazzi I, et al. Quantification of o,o’-dityrosine, o-nitrotyrosine, and o-tyrosine in cat urine samples by LC/electrospray ionization-MS/MS using isotope dilution. Anal Chem. 2003;75:261–267.
  • Wells-Knecht MC, Huggins TG, Dyer DG, et al. Oxidized amino acids in lens protein with age. Measurement of o-tyrosine and dityrosine in the aging human lens. J Biol Chem. 1993;268:12348–12352.
  • Toby TK, Fornelli L, Kelleher NL. Progress in top-down proteomics and the analysis of proteoforms. Ann Rev Anal Chem. 2016;9:499–519.
  • Aebersold R, Mann M. Mass-spectrometric exploration of proteome structure and function. Nature. 2016;537:347–355.
  • Sinz A. Cross-linking/mass spectrometry for studying protein structures and protein-protein interactions: where are we now and where should we go from here? Angew Chem Int Ed Engl. 2018;57:6390–6396.
  • Fritzsche R, Ihling CH, Götze M, et al. Optimizing the enrichment of cross-linked products for mass spectrometric protein analysis. Rapid Commun Mass Spectrom. 2012;26:653–658.
  • Toste RA, Holding AN, Kent H, et al. Architecture of the Pol III-clamp-exonuclease complex reveals key roles of the exonuclease subunit in processive DNA synthesis and repair. EMBO J. 2013;32:1334–1343.
  • Schmidt R, Sinz A. Improved single-step enrichment methods of cross-linked products for protein structure analysis and protein interaction mapping. Anal Bioanal Chem. 2017;409:2393–2400.
  • Tinnefeld V, Venne AS, Sickmann A, et al. Enrichment of cross-linked peptides using charge-based fractional diagonal chromatography (ChaFRADIC). J Proteome Res. 2017;16:459–469.
  • Rose K, Savoy LA, Simona MG, et al. C-terminal peptide identification by fast atom bombardment mass spectrometry. Biochem J. 1988;250:253–259.
  • Hajkova D, Sekhar Rao KC, Miyagi M. pH dependency of the carboxyl oxygen exchange reaction catalyzed by lysyl endopeptidase and trypsin. J Proteome Res. 2006;5:1667–1673.
  • Reynolds KJ, Yao X, Fenselau C. Proteolytic 18O labeling for comparative proteomics: evaluation of endoprotease Glu-C as the catalytic agent. J Proteome Res. 2002;1:27–33.
  • Wallis TP, Pitt JJ, Gorman JJ. Identification of disulfide-linked peptides by isotope profiles produced by peptic digestion of proteins in 50% (18)O water. Protein Sci. 2001;10:2251–2271.
  • Taverner T, Hall NE, O’Hair RAJ, et al. Characterization of an antagonist interleukin-6 dimer by stable isotope labeling, cross-linking, and mass spectrometry. J Biol Chem. 2002;277:46487–46492.
  • Roepstorff P, Fohlman J. Letter to the editors. Biol Mass Spectrom. 1984;11:601.
  • Trnka MJ, Baker PR, Robinson PJJ, et al. Matching cross-linked peptide spectra: only as good as the worse identification. Molec Cell Proteomics. 2014;13:420–434.
  • Gardner MW, Brodbelt JS. Impact of proline and aspartic acid residues on the dissociation of intermolecularly crosslinked peptides. J Am Soc Mass Spectrom. 2008;19(3):344–357.
  • Giese SH, Fischer L, Rappsilber JA. Study into the collision-induced dissociation (CID) behavior of cross-linked peptides. Molec Cell Proteomics. 2016;15:1094–1104.
  • Giese SH, Belsom A, Rappsilber J. Optimized fragmentation regime for diazirine photo-cross-linked peptides. Anal Chem. 2016;88:8239–8247.
  • Iacobucci C, Sinz A. To be or not to be? Five guidelines to avoid misassignments in cross-linking/mass spectrometry. Anal Chem. 2017;89:7832–7835.
  • Panchaud A, Singh P, Shaffer SA, et al. xComb: a cross-linked peptide database approach to protein-protein interaction analysis. J Proteome Res. 2010;9:2508–2515.
  • Soderberg CA, Lambert W, Kjellstrom S, et al. Detection of crosslinks within and between proteins by LC-MALDI-TOFTOF and the software FINDX to reduce the MSMS-data to acquire for validation. PLoS One. 2012;7:e38927.
  • Gotze M, Pettelkau J, Schaks S, et al. StavroX–a software for analyzing crosslinked products in protein interaction studies. J Am Soc Mass Spectrom. 2012;23:76–87.
  • Fan SB, Meng JM, Lu S, et al. Using pLink to analyze cross-linked peptides. Curr Protoc Bioinformatics. 2015;49:8 21 21–19.
  • Hoopmann MR, Zelter A, Johnson RS, et al. Kojak: efficient analysis of chemically cross-linked protein complexes. J Proteome Res. 2015;14:2190–2198.
  • Yu F, Li N, Yu W. ECL: an exhaustive search tool for the identification of cross-linked peptides using whole database. BMC Bioinformatics. 2016;17:217.
  • Yilmaz S, Drepper F, Hulstaert N, et al. Xilmass: A new approach toward the identification of cross-linked peptides. Anal Chem. 2016;88:9949–9957.
  • Chu F, Baker PR, Burlingame AL, et al. Finding chimeras: a bioinformatics strategy for identification of cross-linked peptides. Mol Cell Proteomics. 2010;9:25–31.
  • Singh P, Shaffer SA, Scherl A, et al. Characterization of protein cross-links via mass spectrometry and an open-modification search strategy. Anal Chem. 2008;80:8799–8806.
  • Rinner O, Seebacher J, Walzthoeni T, et al. Identification of cross-linked peptides from large sequence databases. Nat Methods. 2008;5:315–318.
  • Rasmussen MI, Refsgaard JC, Peng L, et al. CrossWork: software-assisted identification of cross-linked peptides. J Proteomics. 2011;74:1871–1883.
  • Gebicki JM, Nauser T, Domazou A, et al. Reduction of protein radicals by GSH and ascorbate: potential biological significance. Amino Acids. 2010;39:1131–1137.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.