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Protein Peroxidation: The Covalent Modification of Protein Induced Through Reactive Oxygen Species (ROS) and With Secondary By-products of Oxidative Stress.
Abstract
The abundance in biological system and high reaction rate constant are making the proteins as major targets for radicals and two-electron oxidants in biological systems. The multiple side-chain and backbone sites are susceptible for highly reactive radical damage. Less reactive species exhibit greater selectivity with reference to the residues targeted and their spatial location. Modified structure may result in the increased side-chain hydrophilicity, side-chain fragmentation and backbone fragmentation, aggregation through covalent cross-linking or hydrophobic interactions, unfolding of protein and altered conformation, altered interactions with biological partners and modified turnover. In the presence of oxygen, high yields of peroxyl radicals and peroxides of protein (through peroxidation) are formed. The peroxides of protein account for up to 70 % of the initial oxidant flux. The peroxides of protein deserve capability to oxidize both proteins and other target compounds.
Key words: Oxidation of amino acids; Hydroperoxide; Peroxidatio;, Peroxides
References
Halliwell, B. and Gutteridge, J.M.C. (2015) Free Radicals in Biology & Medicine, Oxford University Press, Oxford.
Hammer, T. and Bode, R. (1992) Enzymatic production of α-aminoadipate-δ-semialdehyde and related compounds by lysine ϵ-dehydrogenase from Candida albicans. Zentralbl. Mikrobiol. 147, 65–70.
Winterbourn, C.C. (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4, 278–286.
Ferrer-Sueta, G. and Radi, R. (2009) Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem. Biol. 4, 161–177.
Carballal, S., Radi, R., Kirk, M.C., Barnes, S., Freeman, B.A. and Alvarez, B. (2003) Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitrite. Biochemistry 42, 9906–9914.
Ogusucu, R., Rettori, D., Munhoz, D.C., Netto, L.E. and Augusto, O. (2007) Reactions of yeast thioredoxin peroxidases I and II with hydrogen peroxide and peroxynitrite: rate constants by competitive kinetics. Free Radic. Biol. Med. 42, 326–334.
Peskin, A.V., Low, F.M., Paton, L.N., Maghzal, G.J., Hampton, M.B. and Winterbourn, C.C. (2007) The high reactivity of peroxiredoxin 2 with H2O2 is not reflected in its reaction with other oxidants and thiol reagents. J. Biol. Chem. 282, 11885–11892.
Davies, M.J. (2004) Reactive species formed on proteins exposed to singlet oxygen. Photochem. Photobiol. Sci. 3, 17–25.
JM Protein hydroperoxides as new reactive oxygen species. RedoxRep. 1997;3: 99-110 p.
Davies, M.J. (2005) The oxidative environment and protein damage. Biochim. Biophys. Acta 1703, 93–109.
Dalle-Donne, I., Scaloni, A., Giustarini, D., Cavarra, E., Tell, G., Lungarella, G., Colombo, R., Rossi, R. and Milzani, A. (2005). Proteins as biomarkers of oxidative/nitrosative stress in diseases: the contribution of redox proteomics. Mass Spectrom. Rev. 24, 55–99.
Kopoldova, J., Liebster, J. and Babicky, A. (1963) .. Int. J. App. Radiat Isotop 14, 493–498.
Kopoldova, J., Liebster, J. and Babicky, A. (1963) The mechanism of the radiation chemical degradation of amino acids–IV. Radiolysis of valine in aqueous oxygenated and oxygen-free solutions. Int. J. App. Radiat Isotop. 14, 489–492.
Hawkins, C.L. and Davies, M.J. (1998) EPR studies on the selectivity of hydroxyl radical attack on amino acids and peptides. J. Chem. Soc. Perkin Trans. 2, 2617–2622.
Hawkins, C.L. and Davies, M.J. (1998) Hypochlorite-induced damage to proteins: formation of nitrogen-centred radicals from lysine residues and their role in protein fragmentation. Biochem. J. 332, 617–625.
Hawkins, C.L. and Davies, M.J. (1998) Reaction of HOCl with amino acids and peptides: EPR evidence for rapid rearrangement and fragmentation reactions of nitrogen-centered radicals. J. Chem. Soc. Perkin Trans. 2, 1937–1945.
Watts, Z.I. and Easton, C.J. (2009) Peculiar stability of amino acids and peptides from a radical perspective. J. Am. Chem. Soc. 131, 11323–11325.
Kollonitsch, J., Rosegay, A. and Doldouras, G. (1964) Reactions in strong acids. II. New concept in amino acid chemistry: C-derivatization of amino acids. J. Am. Chem. Soc. 86, 1857–1858.
Faulstich, H., D¨olling, J., Michl, K. and Wieland, T. (1973) Synthese von α-amino-γ -hydroxyauren durch photochorierung. Justus Liebigs Ann. Chem. 560–565.
Fu, S., Gebicki, S., Jessup, W., Gebicki, J.M. and Dean, R.T. (1995) Biological fate of amino acid, peptide and protein hydroperoxides. Biochem. J. 311, 821–827.
Fu, S., Hick, L.A., Sheil, M.M. and Dean, R.T. (1995) Structural identification of valine hydroperoxides and hydroxides on radical-damaged amino acid, peptide, and protein molecules. Free Radic. Biol. Med. 19, 281–292.
Hawkins, C.L. and Davies, M.J. (2001) Generation and propagation of radical reactions on proteins. Biochim. Biophys. Acta 1504, 196–219.
Hawkins, C.L. and Davies, M.J. (1997) Oxidative damage to collagen and related substrates by metal ion/hydrogen peroxide systems: random attack or site-specific damage ? Biochim. Biophys. Acta. 1360, 84–96.
Wheeler, O.H. and Montalvo, R. (1969) Radiolysis of phenylalanine and tyrosine and aqueous solution. Radiat Res. 40, 1–10.
Dizdaroglu, M. and Simic, M.G. (1980) Radiation induced conversion of phenylalanine to tyrosines. Radiat Res. 83, 437.
Davies, M.J., Fu, S., Wang, H. and Dean, R.T. (1999) Stable markers of oxidant damage to proteins and their application in the study of human disease. Free Radic. Biol. Med. 27, 1151–1163.
Houee-Levin, C., Bobrowski, K., Horakova, L., Karademir, B., Schoneich, C., Davies, M.J. and Spickett, C.M. (2015) Exploring oxidative modifications of tyrosine: an update on mechanisms of formation, advances in analysis and biological consequences. Free Radic Res. 49, 347–373.
Ehrenshaft, M., Deterding, L.J. and Mason, R.P. (2015) Tripping up Trp: Modification of protein tryptophan residues by reactive oxygen species, modes of detection, and biological consequences. Free Radic. Biol. Med. 89, 220–228.
von Sonntag, C. (1987) The Chemical Basis of Radiation Biology, Taylor and Francis, London 1987.
Armstrong, D.A. (1990) Applications of pulse radiolysis for the study of short-lived sulphur species. In Sulfur-Centered Reactive Intermediates in Chemistry and Biology (Chatgilialoglu, C. and Asmus, K.D., eds), pp. 121–134, Plenum Press, New York
von Sonntag, C. (1990) Free-Radical Reactions Involving Thiols and Disulphides. In Sulfur-Centered Reactive Intermediates in Chemistry and Biology (Chatgilialoglu, C. and Asmus, K.-D., eds), pp. 359–366, Plenum Press, New York.
Wardman, P. and von Sonntag, C. (1995) Kinetic factors that control the fate of thiyl radicals in cells. Meth. Enzymol. 251, 31–45.
Trujillo, M., Alvarez, B. and Radi, R. (2016) One- and two-electron oxidation of thiols: mechanisms, kinetics and biological fates. Free Radic Res., From: https://www.tandfonline.com/doi/abs/10.3109/10715762.2015.1089988?src=recsys&journalCode=ifra20
Schoneich, C. (2008) Mechanisms of protein damage induced by cysteine thiyl radical formation. Chem. Res. Toxicol. 21, 1175–1179.
Schoneich, C. (2016) Thiyl radicals and induction of protein degradation. Free Radic. Res., https://www.ncbi.nlm.nih.gov/pubmed/26212409
Asmus, K.-D., G¨obl, M., Hiller, K.-O., Mahling, S. and M¨onig, J. (1985) S∴N and S∴O three-electron-bonded radicals and radical cations in aqueous solutions. J. Chem. Soc. Perkin. Trans. 2, 641–646.
Hiller, K.O. and Asmus, K.D. (1981) Oxidation of methionine by X2.- in aqueous solution and characterization of some S . . . X three-electron bonded intermediates. A pulse radiolysis study. Int. J. Radiat Biol. 40, 583–595.
Hiller, K.-O., Masloch, B., Gobl, M. and Asmus, K.-D. (1981) Mechanism of the OH. radical induced oxidation of methionine in aqueous solution. J. Am. Chem. Soc. 103, 2734–2743.
Schoneich, C. and Yang, J. (1996) Oxidation of methionine peptides by Fenton systems: the importance of peptide sequence, neighbouring groups and EDTA. J. Chem. Soc. Perkin Trans. 2, 915–924.
Schoneich, C., Pogocki, D., Hug, G.L. and Bobrowski, K. (2003) Free radical reactions of methionine in peptides: mechanisms relevant to beta-amyloid oxidation and Alzheimer’s disease. J. Am. Chem. Soc. 125, 13700–13713.
Jonsson, M. and Kraatz, H.-B. (1997) Redox chemistry of carbon-centred α-amino acid radicals. J. Chem. Soc. Perkin Trans. 2, 2673–2676.
Welle, F.M., Beckhaus, H.-D. and Ruchardt, C. (1997) Thermochemical stability of α-amino-α-carbonylmethyl radicals and their resonance as measured by ESR. J. Org. Chem. 62, 552–558.
Easton, C.J. (1991) α-Carbon-centred radicals from amino acids and their derivatives. In Advances in Detailed Reaction Mechanisms (Coxon, J.M., ed.), pp. 83–126, JAI Press, Greenwich, Connecticut
Sperling, J. and Elad, D. (1971) Photochemical modification of glycine containing polypeptides. J. Am. Chem. Soc. 93, 967–971.
Schwarzberg, M., Sperling, J. and Elad, D. (1973) Photoalkylation of peptides. Visible light-induced conversion of glycine residues into branched α-amino acids. J. Am. Chem. Soc. 95, 6418–6426.
Easton, C.J. and Hay, M.P. (1986) Preferential reactivity of glycine residues in free radical reactions of amino acid derivatives. J. Chem. Soc. Chem. Commun. 55–57.
Burgess, V.A., Easton, C.J. and Hay, M.P. (1989) Selective reaction of glycine residues in hydrogen atom transfer from amino acid derivatives. J. Am. Chem. Soc. 111, 1047–1052.
Rauk, A. and Armstrong, D.A. (2000) Influence of β-sheet structure on the susceptibility of proteins to backbone oxidative damage: preference for αc-centered radical formation at glycine residues of antiparallele β-sheets. J. Am. Chem. Soc. 122, 4185–4192.
Rauk, A., Yu, D. and Armstrong, D.A. (1997) Toward site specificity of oxidative damage in proteins: C-H and C-C bond dissociation energies and reduction potentials of the radicals of alanine, serine and threonine residues – an ab initio study. J. Am. Chem. Soc. 119, 208–217.
Rauk, A., Yu, D., Taylor, J., Shustov, G.V., Block, D.A. and Armstrong, D.A. (1999) Effects of structure on alpha C-H bond enthalpies of amino acid residues: relevance to H transfers in enzyme mechanisms and in protein oxidation. Biochemistry 38, 9089–9096.
Stadtman, E.R. (1993) Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Ann. Rev. Biochem. 62, 797–821
Orr, C.W. (1967) Studies on ascorbic acid. I. Factors influencing the ascorbate-mediated inhibition of catalase. Biochemistry 6, 2995–3000.
Orr, C.W. (1967) Studies on ascorbic acid. II. Physical changes in catalase following incubation with ascorbate or ascorbate and copper (II). Biochemistry 6, 3000–3006
Marx, G. and Chevion, M. (1986) Site-specific modification of albumin by free radicals. Reaction with copper(II) and ascorbate. Biochem. J. 236, 397–400.
Bateman, R.C. Jr., Youngblood, W.W., Busby, W.H. Jr. and Kizer, J.S. (1985). Nonenzymatic peptide alpha-amidation. Implications for a novel enzyme mechanism. J. Biol. Chem. 260, 9088–9090.
Levine, R.L. (1983) Oxidative modification of glutamine synthetase. I. Inactivation is due to loss of one histidine residue. J. Biol. Chem. 258, 11823–11827.
Rivett, A.J. and Levine, R.L. (1990) Metal-catalyzed oxidation of Escherichia coli glutamine synthetase: correlation of structural and functional changes. Arch. Biochem. Biophys. 278, 26–34.
Zhao, F., Ghezzo Schoneich, E., Aced, G.I., Hong, J., Milby, T. and Schoneich, C. (1997) Metal-catalyzed oxidation of histidine in human growth hormone. Mechanism, isotope effects, and inhibition by a mild denaturing alcohol. J. Biol. Chem. 272, 9019–9029
Li, S., Schoneich, C. and Borchardt, R.T. (1995) Chemical pathways of peptide degradation. VIII. Oxidation of methionine in small model peptides by prooxidant/transition metal ion systems: influence of selective scavengers for reactive oxygen intermediates. Pharm. Res. 12, 348–355.
Itakura, K., Uchida, K. and Kawakishi, S. (1994) Selective formation of oxindole- and formylkynurenine-type products from tryptophan and its peptides treated with a superoxide-generating system in the presence of iron(III)-EDTA: a possible involvement with iron-oxygen complex. Chem. Res. Toxicol. 7, 185–190.
Easton, C.J., Eichinger, S.K. and Pitt, M.J. (1997) Glycine-selective α-carbon-nitrogen bond cleavage of dipeptides by nickel peroxide. Tetrahedron 53, 5609–5616 CrossRef
Easton, C.J., Kelly, J.B. and Ward, C.M. (1997) Regioselective hydrogen atom transfer from triglycine. J. Chem. Res. 470–471.
Gill, G., Richter Rusli, A.A., Ghosh, M., Burrows, C.J. and Rokita, S.E. (1997) Nickel-dependent oxidative cross-linking of a protein. Chem. Res. Toxicol. 10, 302–309.
Platis, I.E., Ermacora, M.R. and Fox, R.O. (1993) Oxidative polypeptide cleavage mediated by EDTA-Fe covalently linked to cysteine residues. Biochemistry 32, 12761–12767.
Tullius, T.D. and Dombroski, B.A. (1986) Hydroxyl radical “footprinting”: high-resolution information about DNA-protein contacts and application to lambda repressor and Cro protein. Proc. Natl. Acad. Sci. U.S.A. 83, 5469–5473.
Rana, T.M. and Meares, C.F. (1990) Specific cleavage of a protein by an attached iron chelate. J. Am. Chem. Soc. 112, 2457–2458.
Ermacora, M.R., Delfino, J.M., Cuenoud, B., Schepartz, A. and Fox, R.O. (1992) Conformation-dependent cleavage of staphylococcal nuclease with a disulfide-linked iron chelate. Proc. Natl. Acad. Sci. U.S.A. 89, 6383–6387.
Mustaev, A., Kozlov, M., Markovtsov, V., Zaychikov, E., Denissova, L. and Goldfarb, A. (1997) Modular organization of the catalytic center of RNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 94, 6641–6645.
Fu, S., Dean, R., Southan, M. and Truscott, R. (1998) The hydroxyl radical in lens nuclear cataractogenesis. J. Biol. Chem. 273, 28603–28609.
Fu, S., Fu, M.-X., Baynes, J.W., Thorpe, S.R. and Dean, R.T. (1998) Presence of dopa and amino acid hydroperoxides in proteins modified with advanced glycation end products: amino acid oxidation products as possible source of oxidative stress induced by age proteins. Biochem. J. 330, 233–239.
Wolff, S.P. and Dean, R.T. (1987) Glucose autoxidation and protein modification. The potential role of ‘autoxidative glycosylation’ in diabetes. Biochem. J. 245, 243–250.
Wolff, S.P. and Dean, R.T. (1988) Aldehydes and dicarbonyls in non-enzymic glycosylation of proteins. Biochem. J. 249, 618–619.
Wolff, S.P., Jiang, Z.Y. and Hunt, J.V. (1991) Protein glycation and oxidative stress in diabetes mellitus and ageing. Free Radic. Biol. Med. 10, 339–352.
Wells-Knecht, M.C., Lyons, T.J., McCance, D.R., Thorpe, S.R. and Baynes, J.W. (1997) Age-dependent increase in ortho-tyrosine and methionine sulfoxide in human skin collagen is not accelerated in diabetes. Evidence against a generalized increase in oxidative stress in diabetes. J. Clin. Invest. 100, 839–846.
Berdnikov, V.M., Bazhin, N.M., Federov, V.K. and Polyakov, O.V. (1972) Isomerization of the ethoxyl radical to the α-hydroxyethyl radical in aqueous solution. Kinet Catal. (Engl. Trans.) 13, 986–998.
Gilbert, B.C., Holmes, R.G.G., Laue, H.A.H. and Norman, R.O.C. (1976) Electron spin resonance studies. Part L. Reactions of alkoxyl radicals generated from hydroperoxides and titanium(III) ion in aqueous solution. J. Chem. Soc. Perkin Trans. 2, 1047–1052.
Davies, M.J. and Gilbert, B.C. (1991) Free radical reactions. Fragmentation and rearrangements in aqueous solution. Adv. Detailed Reaction Mechanisms. 1, 35–81.
Alfassi, Z. (1997) In Peroxyl Radicals, John Wiley and Sons, Chichester. 1997.
Nauser, T., Casi, G., Koppenol, W.H. and Schoneich, C. (2008) Reversible intramolecular hydrogen transfer between cysteine thiyl radicals and glycine and alanine in model peptides: absolute rate constants derived from pulse radiolysis and laser flash photolysis. J. Phys. Chem. B. 112, 15034–15044.
Dizdaroglu, M. and Simic, M.G. (1983) Isolation and characterization of radiation-induced aliphatic peptide dimers. Int. J. Radiat Biol. 44, 231–239.
Easton, C.J. (1997) Free-radical reactions in the synthesis of alpha-amino acids and derivatives. Chem. Rev. 97, 53–82.
Karam, L.R., Dizdaroglu, M. and Simic, M.G. (1984) OH radical-induced products of tyrosine peptides. Int. J. Radiat. Biol. 46, 715–724.
Simic, M.G., Gajewski, E. and Dizdaroglu, M. (1985) Kinetics and mechanisms of hydroxyl radical-induced crosslinks between phenylalanine peptides. Radiat Phys. Chem. 24, 465–473.
Jin, F., Leitich, J. and von Sonntag, C. (1993) The superoxide radical reacts with tyrosine-derived phenoxyl radicals by addition rather than by electron transfer. J. Chem. Soc. Perkin Trans. 2, 1583–1588.
Vanhooren, A., Devreese, B., Vanhee, K., Van Beeumen, J. and Hanssens, I. (2002) Photoexcitation of tryptophan groups induces reduction of two disulfide bonds in goat alpha-lactalbumin. Biochemistry 41, 11035–11043.
Medinas, D.B., Gozzo, F.C., Santos, L.F., Iglesias, A.H. and Augusto, O. (2010) 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. 49, 1046–1053.
Zhang, H., Andrekopoulos, C., Joseph, J., Chandran, K., Karoui, H., Crow, J.P. and Kalyanaraman, B. (2003) Bicarbonate-dependent peroxidase activity of human Cu,Zn-superoxide dismutase induces covalent aggregation of protein: intermediacy of tryptophan-derived oxidation products. J. Biol. Chem. 278, 24078–24089
Nagy, P., Kettle, A.J. and Winterbourn, C.C. (2010) Neutrophil-mediated oxidation of enkephalins via myeloperoxidase-dependent addition of superoxide. Free Radic. Biol. Med. 49, 792–799.
Paviani, V. n., Queiroz, R.F., Marques, E.F., Di Mascio, P. and Augusto, O. (2015). Production of lysozyme and lysozyme-superoxide dismutase dimers bound by a ditryptophan cross-link in carbonate radical-treated lysozyme. Free Radic. Biol. Med. 89, 72–82.
Torosantucci, R., Mozziconacci, O., Sharov, V., Schoneich, C. and Jiskoot, W. (2012). Chemical modifications in aggregates of recombinant human insulin induced by metal-catalyzed oxidation: covalent cross-linking via michael addition to tyrosine oxidation products. Pharm. Res. 29, 2276–2293.
Torosantucci, R., Sharov, V.S., van Beers, M., Brinks, V., Schoneich, C. and Jiskoot, W. (2013) Identification of oxidation sites and covalent cross-links in metal catalyzed oxidized interferon Beta-1a: potential implications for protein aggregation and immunogenicity. Mol. Pharm. 10, 2311–2322.
Mozziconacci, O. and Schoneich, C. (2014) Sequence-specific formation of D-amino acids in a monoclonal antibody during light exposure. Mol. Pharm. 11, 4291–4297.
Fradkin, A.H., Mozziconacci, O., Schoneich, C., Carpenter, J.F. and Randolph, T.W. (2014) UV photodegradation of murine growth hormone: chemical analysis and immunogenicity consequences. Eur. J. Pharm. Biopharm. 87, 395–402.
Jiskoot, W., Randolph, T.W., Volkin, D.B., Middaugh, C.R., Schoneich, C., Winter, G., Friess, W., Crommelin, D.J. and Carpenter, J.F. (2012) Protein instability and immunogenicity: roadblocks to clinical application of injectable protein delivery systems for sustained release. J. Pharm. Sci. 101, 946–954.
Mozziconacci, O., Kerwin, B.A. and Schoneich, C. (2010) Photolysis of an intrachain peptide disulfide bond: primary and secondary processes, formation of H2S, and hydrogen transfer reactions. J. Phys. Chem. B. 114, 3668–3688.
Mozziconacci, O., Kerwin, B.A. and Schoneich, C. (2010) Reversible hydrogen transfer between cysteine thiyl radical and glycine and alanine in model peptides: covalent H/D exchange, radical-radical reactions, and L- to D-Ala conversion. J. Phys. Chem. B 114, 6751–6762.
Mozziconacci, O., Sharov, V., Williams, T.D., Kerwin, B.A. and Schoneich, C. (2008). Peptide cysteine thiyl radicals abstract hydrogen atoms from surrounding amino acids: the photolysis of a cystine containing model peptide. J. Phys. Chem. B. 112, 9250–9257.
Behrens, G. and Koltzenburg, G. (1985) Elimination of ammonium ion from the α-hydroxyalkyl radicals of serine and threonine in aqueous solution and the difference in the reaction mechanism. Z. Naturforsch. 40c, 785–797.
Hunter, E.P., Desrosiers, M.F. and Simic, M.G. (1989) The effect of oxygen, antioxidants, and superoxide radical on tyrosine phenoxyl radical dimerization. Free Radic. Biol. Med. 6, 581–585.
Davies, M.J., Fu, S. and Dean, R.T. (1995) Protein hydroperoxides can give rise to reactive free radicals. Biochem. J. 305, 643–649.
Adamic, K., Howard, J.A. and Ingold, K.U. (1969) Absolute rate constants for hydrocarbon autoxidation. XVI. Reactions of peroxy radicals at low temperatures. Can. J. Chem. 47, 3803–3808.
Bartlett, P.D. and Guaraldi, G. (1967) Di-t-butyl trioxide and di-t-butyl tetroxide. J. Am. Chem. Soc. 1967, 4799–4801.
Bennett, J.E. (1990) Kinetic electron paramagnetic resonance study of the reactions of t-butylperoxyl radicals in aqueous solution. J. Chem. Soc. Faraday Trans. 86, 3247–3252.
Bennett, J.E., Brown, D.M. and Mile, B. (1970) Studies by electron spin resonance of the reactions of alkylperoxy radicals. Part 2. Equilibrium between alkylperoxy radicals and tetroxide molecules. Trans. Faraday Soc. 66, 397–405.
Howard, J.A. (1972) Absolute rate constants for reactions of oxyl radicals. Adv. Free Rad. Chem. 4, 49–173.
Dalle-Donne, I., Aldini, G., Carini, M., Colombo, R., Rossi, R. and Milzani, A. (2006). Protein carbonylation, cellular dysfunction, and disease progression. J. Cell. Molec. Med. 10, 389–406.
Dalle-Donne, I., Aldini, G., Carini, M., Colombo, R., Rossi, R. and Milzani, A. (2006). Protein carbonylation, cellular dysfunction, and disease progression. J. Cell. Molec. Med. 10, 389–406.
Dalle-Donne, I., Giustarini, D., Colombo, R., Rossi, R. and Milzani, A. (2003) Protein carbonylation in human diseases. Trends Molec. Med. 9, 169–176.
Dalle-Donne, I., Rossi, R., Colombo, R., Giustarini, D. and Milzani, A. (2006) Biomarkers of oxidative damage in human disease. Clin. Chem. 52, 601–623.
Pan, X.-M., Schuchmann, M.N. and von Sonntag, C. (1993) Oxidation of benzene by the OH radical. A product and pulse radiolysis study in oxygenated aqueous solution. J. Chem. Soc. Perkin Trans. 2, 289–297.
Latarjet, R. and Loiseleur, J. (1942) Modalit´es de la Fixation de L’Oxyg`ene en Radiobiologie. Soc. Biologie Comptes Rendue 136, 60–63.
Simpson, J.A., Narita, S., Gieseg, S., Gebicki, S., Gebicki, J.M. and Dean, R.T. (1992). Long-lived reactive species on free-radical-damaged proteins. Biochem. J. 282, 621–624.
Davies, M.J. (2003) Singlet oxygen-mediated damage to proteins and its consequences. Biochem. Biophys. Res. Commun. 305, 761–770.
Garrison, W.M. (1972) Radiation-induced reactions of amino acids and peptides. Radiat Res. Rev. 3, 305–326.
Gebicki, S. and Gebicki, J.M. (1993) Formation of peroxides in amino acids and proteins exposed to oxygen free radicals. Biochem. J. 289, 743–749.
Gebicki, S. and Gebicki, J.M. (1999) Crosslinking of DNA and proteins induced by protein hydroperoxides. Biochem. J. 338, 629–636.
Gebicki, S., Bartosz, G. and Gebicki, J.M. (1995) The action of iron on amino acid and protein peroxides. Biochem. Soc. Trans. 23, 2495.
Gebicki, S., Dean, R.T. and Gebicki, J.M. (1996) Inactivation of glutathione reductase by protein and amino acid peroxides. In Oxidative Stress and Redox Regulation: Cellular Signalling, AIDS, Cancer and Other Diseases, p. 139, Institute Pasteur, Paris.
Gebicki, S., Gill, K.H., Dean, R.T. and Gebicki, J.M. (2002) Action of peroxidases on protein hydroperoxides. Redox. Rep. 7, 235–242.
Robinson, S., Bevan, R., Lunec, J. and Griffiths, H. (1998) Chemiluminescence determination of hydroperoxides following radiolysis and photolysis of free amino acids. FEBS Lett. 430, 297–300.
Fu, S.L. and Dean, R.T. (1997) Structural characterization of the products of hydroxyl-radical damage to leucine and their detection on proteins. Biochem. J. 324, 41–48.
Moller, M.N., Hatch, D.M., Kim, H.Y. and Porter, N.A. (2012) Superoxide reaction with tyrosyl radicals generates para-hydroperoxy and para-hydroxy derivatives of tyrosine. J. Am. Chem. Soc. 134, 16773–16780.
Winterbourn, C.C., Parsons-Mair, H.N., Gebicki, S., Gebicki, J.M. and Davies, M.J. (2004). Requirements for superoxide-dependent tyrosine hydroperoxide formation in peptides. Biochem. J. 381, 241–248.
d’Alessandro, N., Bianchi, G., Fang, X., Jin, F., Schuchmann, H.-P. and von Sonntag, C. (2000) Reaction of superoxide with phenoxyl-type radicals. J. Chem. Soc. Perkin Trans. 2, 1862–1867.
Das, A.B., Nagy, P., Abbott, H.F., Winterbourn, C.C. and Kettle, A.J. (2010) Reactions of superoxide with the myoglobin tyrosyl radical. Free Radic. Biol. Med. 48, 1540–1547.
Das, A.B., Nauser, T., Koppenol, W.H., Kettle, A.J., Winterbourn, C.C. and Nagy, P. (2014) Rapid reaction of superoxide with insulin-tyrosyl radicals to generate a hydroperoxide with subsequent glutathione addition. Free Radic. Biol. Med. 70, 86–95
Nagy, P., Kettle, A.J. and Winterbourn, C.C. (2009) Superoxide-mediated formation of tyrosine hydroperoxides and methionine sulfoxide in peptides through radical addition and intramolecular oxygen transfer. J. Biol. Chem. 284, 14723–14733.
Pichorner, H., Metodiewa, D. and Winterbourn, C.C. (1995) Generation of superoxide and tyrosine peroxide as a result of tyrosyl radical scavenging by glutathione. Arch. Biochem. Biophys. 323, 429–437.
Pattison, D.I., Rahmanto, A.S. and Davies, M.J. (2012) Photo-oxidation of proteins. Photochem. Photobiol. Sci. 11, 38–53.
Redmond, R.W. and Gamlin, J.N. (1999) A compilation of singlet oxygen yields from biologically relevant molecules. Photochem. Photobiol. 70, 391–475.
Michaeli, A. and Feitelson, J. (1994) Reactivity of singlet oxygen toward amino acids and peptides. Photochem. Photobiol. 59, 284–289.
Michaeli, A. and Feitelson, J. (1995) Reactivity of singlet oxygen toward large peptides. Photochem. Photobiol. 61, 255–260.
Foote, C. S. and J. V. Peters. 1971. Chemistry of singlet oxygen 14. A reactive intermediate in sulfide photooxidation. J. Am. Chem. Soc. 93 (15):3795–3796.
Gu, C.L., Foote, C.S. and Kacher, M.L. (1981) Chemistry of singlet oxygen 35. Nature of intermediates in the photooxygenation of sulfides. J. Am. Chem. Soc. 1981, 5949–5951.
Sysak, P.K., Foote, C.S. and Ching, T.-Y. (1977) Chemistry of singlet oxygen - XXV. Photooxygenation of methionine. Photochem. Photobiol. 26, 19–27.
Fang, X., Jin, F., Jin, H. and von Sonntag, C. (1998) Reaction of the superoxide radical with the N-centred radical derived from N-acetyltryptophan methyl ester. J. Chem. Soc. Perkin. Trans. 2, 259–263.
Jin, F.M., Leitich, J. and von Sonntag, C. (1995) The photolysis (λ = 254 nm) of tyrosine in aqueous solutions in the absence and presence of oxygen – the reaction of tyrosine with singlet oxygen. J. Photochem. Photobiol. A: Chem. 92, 147–153
Agon, V.V., Bubb, W.A., Wright, A., Hawkins, C.L. and Davies, M.J. (2006) Sensitizer-mediated photooxidation of histidine residues: evidence for the formation of reactive side-chain peroxides. Free Radic. Biol. Med. 40, 698–710.
Gracanin, M., Hawkins, C.L., Pattison, D.I. and Davies, M.J. (2009) Singlet oxygen-mediated amino acid and protein oxidation: formation of tryptophan peroxides and decomposition products Free Radic. Biol. Med. 47, 92–102.
Ronsein, G.E., de Oliveira, M.C., de Medeiros, M.H. and Di Mascio, P. (2009). Characterization of O(2) ((1)delta(g))-derived oxidation products of tryptophan: a combination of tandem mass spectrometry analyses and isotopic labeling studies. J. Am. Soc. Mass. Spectrom. 20, 188–197.
Ronsein, G.E., Oliveira, M.C., Miyamoto, S., Medeiros, M.H. and Di Mascio, P. (2008). Tryptophan oxidation by singlet molecular oxygen [O2(1Deltag)]: mechanistic studies using 18O-labeled hydroperoxides, mass spectrometry, and light emission measurements. Chem. Res. Toxicol. 21, 1271–1283.
Wright, A., Bubb, W.A., Hawkins, C.L. and Davies, M.J. (2002) Singlet oxygen-mediated protein oxidation: evidence for the formation of reactive side-chain peroxides on tyrosine residues. Photochem. Photobiol. 76, 35–46.
Wright, A., Hawkins, C.L. and Davies, M.J. (2000) Singlet oxygen-mediated protein oxidation: evidence for the formation of reactive peroxides. Redox. Rep. 5, 159–161.
Saito, I., Matsuura, T., Nakagawa, M. and Hino, T. (1977) Peroxidic intermediates in photosensitized oxygenation of tryptophan derivatives. Acc. Chem. Res. 10, 346–352.
Santus, R., Patterson, L.K., Hug, G.L., Bazin, M., Maziere, J.C. and Morliere, P. (2000). Interactions of superoxide anion with enzyme radicals: kinetics of reaction with lysozyme tryptophan radicals and corresponding effects on tyrosine electron transfer. Free Radic. Res. 33, 383–391.
Davies, M.J. (1996) Protein and peptide alkoxyl radicals can give rise to C-terminal decarboxylation and backbone cleavage. Arch. Biochem. Biophys. 336, 163–172.
DeGray, J.A., Gunther, M.R., Tschirret-Guth, R., Ortiz de Montellano, P.R. and Mason, R.P. (1997) Peroxidation of a specific tryptophan of metmyoglobin by hydrogen peroxide. J. Biol. Chem. 272, 2359–2362.
Gunther, M.R., Kelman, D.J., Corbett, J.T. and Mason, R.P. (1995) Self-peroxidation of metmyoglobin results in formation of an oxygen-reactive tryptophan-centered radical. J. Biol. Chem. 270, 16075–16081.
Gunther, M.R., Tschirret-Guth, R.A., Lardinois, O.M. and Ortiz de Montellano, P.R. (2003) Tryptophan-14 is the preferred site of DBNBS spin trapping in the self-peroxidation reaction of sperm whale metmyoglobin with a single equivalent of hydrogen peroxide. Chem. Res. Toxicol. 16, 652–660.
Candeias, L.P., Wardman, P. and Mason, R.P. (1997) The reaction of oxygen with radicals from oxidation of tryptophan and indole-3-acetic acid. Biophys. J. 67, 229–237.
Stubbe, J.-A. (2003) Radicals with a controlled lifestyle. Chem. Commun. 20, 2511–2513.
Wolff, S.P. (1994) Ferrous ion oxidation in the presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Meth. Enzymol. 233, 182–189.
Gay, C., Collins, J. and Gebicki, J.M. (1999) Hydroperoxide assay with the ferric-xylenol orange complex. Anal. Biochem. 273, 149–155.
Gay, C. and Gebicki, J.M. (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal. Biochem. 284, 217–220.
Gay, A.C. and Gebicki, J.M. (2002) Perchloric acid enhances sensitivity and reproducibility of the ferric-xylenol orange peroxide assay. Anal. Biochem. 304, 42–46.
Gay, C.A. and Gebicki, J.M. (2003) Measurement of protein and lipid hydroperoxides in biological systems by the ferric-xylenol orange method. Anal. Biochem. 315, 29–35.
Hawkins, C.L., Morgan, P.E. and Davies, M.J. (2009) Quantification of protein modification by oxidants. Free Radic. Biol. Med. 46, 965–988.
Morgan, P.E., Pattison, D.I., Hawkins, C.L. and Davies, M.J. (2008) Separation, detection and quantification of hydroperoxides formed at side-chain and backbone sites on amino acids, peptides and proteins. Free Radic. Biol. Med. 45, 1279–1289.
Morin, B., Bubb, W.A., Davies, M.J., Dean, R.T. and Fu, S. (1998) 3-hydroxylysine, a potential marker for studying radical-induced protein oxidation. Chem. Res. Toxicol. 11, 1265–1273.
Michalski, R., Zielonka, J., Gapys, E., Marcinek, A., Joseph, J. and Kalyanaraman, B. (2014) Real-time measurements of amino acid and protein hydroperoxides using coumarin boronic acid. J. Biol. Chem. 289, 22536–22553.
DOI: https://doi.org/10.37628/jcst.v5i2.864
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