909
Views
44
CrossRef citations to date
0
Altmetric
Review Article

Analysis of protein carbonylation — pitfalls and promise in commonly used methods

, , , &
Pages 1145-1162 | Received 25 Feb 2014, Accepted 10 Jul 2014, Published online: 11 Aug 2014

References

  • Dean RT, Fu S, Stocker R, Davies MJ. Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 1997;324:1–18.
  • Berlett BS, Stadtman ER. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 1997;272:20313–20316.
  • Grune T. Oxidants and antioxidative defense. Hum Exp Toxicol 2002;21:61–62.
  • Grimm S, Hohn A, Grune T. Oxidative protein damage and the proteasome. Amino Acids 2012;42:23–38.
  • Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury: present concepts. J Gastroenterol Hepatol 2011;26:173–179.
  • Breusing N, Grune T. Biomarkers of protein oxidation from a chemical, biological and medical point of view. Exp Gerontol 2010;45:733–737.
  • Robinson MA, Baumgardner JE, Otto CM. Oxygen- dependent regulation of nitric oxide production by inducible nitric oxide synthase. Free Radic Biol Med 2011;51: 1952–1965.
  • Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002;82:47–95.
  • Polidori MC, Griffiths HR, Mariani E, Mecocci P. Hallmarks of protein oxidative damage in neurodegenerative diseases: focus on Alzheimer’s disease. Amino Acids 2007;32: 553–559.
  • Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39:44–84.
  • Traber MG, Stevens JF. Vitamins C and E: beneficial effects from a mechanistic perspective.. Free Radic Biol Med 2011;51:1000–1013.
  • Sueishi Y, Hori M, Kita M, Kotake Y. Nitric oxide (NO) scavenging capacity of natural antioxidants. Food chemistry 2011;129:866–870.
  • Gerard-Monnier D, Chaudiere J. [Metabolism and antioxidant function of glutathione]. Pathol Biol (Paris) 1996;44: 77–85.
  • Barelli S, Canellini G, Thadikkaran L, Crettaz D, Quadroni M, Rossier JS, et al. Oxidation of proteins: basic principles and perspectives for blood proteomics. Proteomics Clin Appl 2008;2:142–157.
  • Nystrom T. Role of oxidative carbonylation in protein quality control and senescence. EMBO J 2005;24:1311–1317.
  • Catalgol B, Grune T. Turnover of oxidatively modified proteins: the usage of in vitro and metabolic labeling. Free Radic Biol Med 2009;46:8–13.
  • Griffiths HR. Is the generation of neo-antigenic determinants by free radicals central to the development of autoimmune rheumatoid disease? Autoimmun Rev. 2008;7:544–549.
  • Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 2003;329:23–38.
  • Luo S, Wehr NB. Protein carbonylation: avoiding pitfalls in the 2,4-dinitrophenylhydrazine assay. Redox Rep 2009;14: 159–166.
  • Tarentino AL, Gomez CM, Plummer TH, Jr. Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F. Biochemistry 1985;24:4665–4671.
  • Moller IM, Rogowska-Wrzesinska A, Rao RS. Protein carbonylation and metal-catalyzed protein oxidation in a cellular perspective. J Proteomics 2011.2228–2242.
  • Held JM, Gibson BW. Regulatory control or oxidative damage? proteomic approaches to interrogate the role of cysteine oxidation status in biological processes. Mol Cell Proteomics 2012;11:R111 013037.
  • Wong CM, Cheema AK, Zhang L, Suzuki YJ. Protein carbonylation as a novel mechanism in redox signaling. Circ Res 2008;102:310–318.
  • Wang P, Powell SR. Decreased sensitivity associated with an altered formulation of a commercially available kit for detection of protein carbonyls. Free Radic Biol Med 2010;49:119–121.
  • Dybkaer R. Metrological traceability in laboratory medicine. Accred Qual Assur 2003;8:46–52.
  • Panteghini M. Traceability, reference systems and result comparability. Clin Biochem Rev 2007;28:97–104.
  • Armbruster D. Measurement traceability and US IVD manufacturers: the impact of metrology. Accred Qual Assur 2009;14:393–398.
  • Buss H, Chan TP, Sluis KB, Domigan NM, Winterbourn CC. Protein carbonyl measurement by a sensitive ELISA method. Free Radic Biol Med 1997;23:361–366.
  • Oikawa S, Yamada T, Minohata T, Kobayashi H, Furukawa A, Tada-Oikawa S, et al. Proteomic identification of carbonylated proteins in the monkey hippocampus after ischemia-reperfusion. Free Radic Biol Med 2009;46:1472–1477.
  • Fields R, Dixon HB. Micro method for determination of reactive carbonyl groups in proteins and peptides, using 2,4-dinitrophenylhydrazine. Biochem J 1971;121:587–589.
  • Stadtman ER. Protein oxidation and aging. Free Radic Res 2006;40:1250–1258.
  • Arnold AR, Staples R. The determination of carbonyls as their 2,4-dinitrophenylhydrazine (DNPH) derivatives in peroxide-containing polymers. Polymer 1992;33:1739–1741.
  • Dalle-Donne I, Carini M, Orioli M, Vistoli G, Regazzoni L, Colombo G, et al. Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids. Free Radic Biol Med 2009;46:1411–1419.
  • Fagan JM, Sleczka BG, Sohar I. Quantitation of oxidative damage to tissue proteins. Int J Biochem Cell Biol 1999; 31:751–757.
  • Mesquita CS, Oliveira R, Bento F, Geraldo D, Rodrigues J, Marcos JC. Simplified 2,4 dinitrophenylhydrazine spectrophotometric assay for quantification of carbonyls in oxidized proteins. Anal Biochem 2014.
  • Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A. Protein carbonylation in human diseases. Trends Mol Med 2003;9:169–176.
  • Hart FD. The use of psychotropic drugs in rheumatology. J Int Med Res 1976;4:15–19.
  • Lenz AG, Costabel U, Shaltiel S, Levine RL. Determination of carbonyl groups in oxidatively modified proteins by reduction with tritiated sodium borohydride. Anal Biochem 1989;177:419–425.
  • Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 1990;186: 464–478.
  • Robinson CE, Keshavarzian A, Pasco DS, Frommel TO, Winship DH, Holmes EW. Determination of protein carbonyl groups by immunoblotting. Anal Biochem 1999;266:48–57.
  • Alamdari DH, Kostidou E, Paletas K, Sarigianni M, Konstas AG, Karapiperidou A, Koliakos G. High sensitivity enzyme-linked immunosorbent assay (ELISA) method for measuring protein carbonyl in samples with low amounts of protein. Free Radic Biol Med 2005;39:1362–1367.
  • Cao G, Cutler RG. Protein oxidation and aging. I. difficulties in measuring reactive protein carbonyls in tissues using 2,4-dinitrophenylhydrazine. Arch Biochem Biophys 1995; 320:106–114.
  • Matthijssens F, Braeckman BP, Vanfleteren JV. Evaluation of Different Methods for Assaying Protein Carbonylation. Curr Anal Chem. 2007;3:93–102.
  • Mohanty JG, Bhamidipaty S, Evans MK, Rifkind JM. A fluorimetric semi-microplate format assay of protein carbonyls in blood plasma. Anal Biochem 2010;400: 289–294.
  • Reznick AZ, Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 1994;233:357–363.
  • Shacter E, Williams JA, Lim M, Levine RL. Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay. Free Radic Biol Med 1994;17:429–437.
  • Sultana R, Newman SF, Huang Q, Butterfield DA. Detection of carbonylated proteins in two-dimensional sodium dodecyl sulfate polyacrylamide gel electrophoresis separations. Methods Mol Biol 2008;476:153–163.
  • Choi J, Malakowsky CA, Talent JM, Conrad CC, Gracy RW. Identification of oxidized plasma proteins in Alzheimer’s disease. Biochem Biophys Res Commun 2002;293:1566–1570.
  • Conrad CC, Choi J, Malakowsky CA, Talent JM, Dai R, Marshall P, Gracy RW. Identification of protein carbonyls after two-dimensional electrophoresis. Proteomics 2001; 1:829–834.
  • Conrad CC, Talent JM, Malakowsky CA, Gracy RW. Post-electrophoretic identification of oxidized proteins. Biol Proced Online 2000;2:39–45.
  • Baraibar MA, Hyzewicz J, Rogowska-Wrzesinska A, Ladouce R, Roepstorff P, Mouly V, Friguet B. Oxidative stress-induced proteome alterations target different cellular pathways in human myoblasts. Free Radic Biol Med 2011;51:1522–1532.
  • Ahmed EK, Rogowska-Wrzesinska A, Roepstorff P, Bulteau AL, Friguet B. Protein modification and replicative senescence of WI-38 human embryonic fibroblasts. Aging Cell 2010;9:252–272.
  • Poon HF, Abdullah L, Reed J, Doore SM, Laird C, Mathura V, et al. Improving image analysis in 2DGE-based redox proteomics by labeling protein carbonyl with fluorescent hydroxylamine. Biol Proced Online 2007;9:65–72.
  • Chaudhuri AR, de Waal EM, Pierce A, Van Remmen H, Ward WF, Richardson A. Detection of protein carbonyls in aging liver tissue: a fluorescence-based proteomic approach. Mech Ageing Dev 2006;127:849–861.
  • Yoo BS, Regnier FE. Proteomic analysis of carbonylated proteins in two-dimensional gel electrophoresis using avidin-fluorescein affinity staining. Electrophoresis 2004;25: 1334–1341.
  • Wehr NB, Levine RL. Quantitation of protein carbonylation by dot blot. Anal Biochem 2012;423:241–245.
  • Wehr NB, Levine RL. Quantification of protein carbonylation. Methods Mol Biol 2013;965:265–281.
  • Yan LJ, Forster MJ. Chemical probes for analysis of carbonylated proteins: a review. J Chromatogr B Analyt Technol Biomed Life Sci 2011;879:1308–1315.
  • Ahn B, Rhee SG, Stadtman ER. Use of fluorescein hydrazide and fluorescein thiosemicarbazide reagents for the fluorometric determination of protein carbonyl groups and for the detection of oxidized protein on polyacrylamide gels. Anal Biochem 1987;161:245–257.
  • Tamarit J, de Hoogh A, Obis E, Alsina D, Cabiscol E, Ros J. Analysis of oxidative stress-induced protein carbonylation using fluorescent hydrazides. J Proteomics 2012; 75:3778–3788.
  • Baraibar MA, Ladouce R, Friguet B. Proteomic quantification and identification of carbonylated proteins upon oxidative stress and during cellular aging. J Proteomics 2013;92:63–70.
  • Pazos M, da Rocha AP, Roepstorff P, Rogowska-Wrzesinska A. Fish proteins as targets of ferrous-catalyzed oxidation: identification of protein carbonyls by fluorescent labeling on two-dimensional gels and MALDI-TOF/TOF mass spectrometry. J Agric Food Chem 2011;59:7962–7977.
  • Levine RL, Williams JA, Stadtman ER, Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 1994;233:346–357.
  • Headlam HA, Davies MJ. Markers of protein oxidation: different oxidants give rise to variable yields of bound and released carbonyl products. Free Radic Biol Med 2004;36: 1175–1184.
  • Dalsgaard TK, Otzen D, Nielsen JH, Larsen LB. Changes in structures of milk proteins upon photo-oxidation. J Agric Food Chem 2007;55:10968–10976.
  • Requena JR, Chao CC, Levine RL, Stadtman ER. Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc Natl Acad Sci U S A 2001;98:69–74.
  • Akagawa M, Sasaki D, Ishii Y, Kurota Y, Yotsu-Yamashita M, Uchida K, Suyama K. New method for the quantitative determination of major protein carbonyls, alpha-aminoadipic and gamma-glutamic semialdehydes: investigation of the formation mechanism and chemical nature in vitro and in vivo. Chem Res Toxicol 2006;19:1059–1065.
  • Estevez M, Ollilainen V, Heinonen M. Analysis of protein oxidation markers alpha-aminoadipic and gamma-glutamic semialdehydes in food proteins using liquid chromatography (LC)-electrospray ionization (ESI)-multistage tandem mass spectrometry (MS). J Agric Food Chem 2009;57:3901–3910.
  • Amici A, Levine RL, Tsai L, Stadtman ER. Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions. J Biol Chem 1989;264:3341–3346.
  • Ayala A, Cutler RG. The utilization of 5-hydroxyl-2-amino valeric acid as a specific marker of oxidized arginine and proline residues in proteins. Free Radic Biol Med 1996;21: 65–80.
  • Larsen MR, Trelle MB, Thingholm TE, Jensen ON. Analysis of posttranslational modifications of proteins by tandem mass spectrometry. Biotechniques 2006;40: 790–798.
  • Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nat Biotechnol 2003;21:255–261.
  • Jensen ON. Modification-specific proteomics: characterization of post-translational modifications by mass spectrometry. Curr Opin Chem Biol 2004;8:33–41.
  • Jensen ON. Interpreting the protein language using proteomics. Nat Rev Mol Cell Biol 2006;7:391–403.
  • Siuti N, Kelleher NL. Decoding protein modifications using top-down mass spectrometry. Nat Methods 2007;4: 817–821.
  • Chait BT. Chemistry. Mass spectrometry: bottom-up or top-down? Science 2006;314:65–66.
  • Han X, Aslanian A, Yates Iii JR. Mass spectrometry for proteomics. Curr Opin Chem Biol 2008;12:483–490.
  • de Godoy LM, Olsen JV, Cox J, Nielsen ML, Hubner NC, Frohlich F, et al. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008;455:1251–1254.
  • Picotti P, Bodenmiller B, Mueller LN, Domon B, Aebersold R. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 2009;138:795–806.
  • Mann M. Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 2006;7:952–958.
  • Ong S-E, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M. Stable isotope labeling by amino acids in cell culture, silac, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 2002;1:376–386.
  • Mirgorodskaya OA, Kozmin YP, Titov MI, Körner R, Sönksen CP, Roepstorff P. Quantitation of peptides and proteins by matrix-assisted laser desorption/ionization mass spectrometry using 18O-labeled internal standards. Rapid Commun Mass Spectrom 2000;14:1226–1232.
  • Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 2009;4: 484–494.
  • Hsu JL, Huang SY, Chow NH, Chen SH. Stable-isotope dimethyl labeling for quantitative proteomics. Anal Chem 2003;75:6843–6852.
  • Picotti P, Aebersold R. Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat Methods 2012;9:555–566.
  • Bantscheff M, Lemeer S, Savitski MM, Kuster B. Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal Bioanal Chem 2012; 404:939–965.
  • Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005;4:1265–1272.
  • Gerber SA, Rush J, Stemman O, Kirschner MW, Gygi SP. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc Natl Acad Sci U S A 2003;100:6940–6945.
  • Beynon RJ, Doherty MK, Pratt JM, Gaskell SJ. Multiplexed absolute quantification in proteomics using artificial QCAT proteins of concatenated signature peptides. Nat Methods 2005;2:587–589.
  • Hermjakob H. The HUPO proteomics standards initiative– overcoming the fragmentation of proteomics data. Proteomics 2006;6:34–38.
  • Lau KW, Jones AR, Swainston N, Siepen JA, Hubbard SJ. Capture and analysis of quantitative proteomic data. Proteomics 2007;7:2787–2799.
  • Miyagi M, Rao KCS. Proteolytic 18O-labeling strategies for quantitative proteomics. Mass Spectrom Rev 2007;26: 121–136.
  • Treumann A, Thiede B. Isobaric protein and peptide quantification: perspectives and issues. Expert Rev Proteomics 2011;7:647–653.
  • Madian AG, Regnier FE. Proteomic identification of carbonylated proteins and their oxidation sites. J Proteome Res 2010;9:3766–3780.
  • Yan LJ, Forster MJ. Chemical probes for analysis of carbonylated proteins: A review. J Chromatogr B Analyt Technol Biomed Life Sci 2010.
  • Mirzaei H, Regnier F. Affinity chromatographic selection of carbonylated proteins followed by identification of oxidation sites using tandem mass spectrometry. Anal Chem 2005; 77:2386–2392.
  • Mirzaei H, Regnier F. Enrichment of carbonylated peptides using Girard P reagent and strong cation exchange chromatography. Anal Chem 2006;78:770–778.
  • Roe MR, Xie H, Bandhakavi S, Griffin TJ. Proteomic mapping of 4-hydroxynonenal protein modification sites by solid-phase hydrazide chemistry and mass spectrometry. Anal Chem 2007;79:3747–3756.
  • Palmese A, De Rosa C, Chiappetta G, Marino G, Amoresano A. Novel method to investigate protein carbonylation by iTRAQ strategy. Anal Bioanal Chem 2012;404:1631–1635.
  • Bollineni RC, Fedorova M, Hoffmann R. Qualitative and quantitative evaluation of derivatization reagents for different types of protein-bound carbonyl groups. Analyst 2013; 138:5081–5088.
  • Lee S, Young NL, Whetstone PA, Cheal SM, Benner WH, Lebrilla CB, Meares CF. Method to site-specifically identify and quantitate carbonyl end products of protein oxidation using oxidation-dependent element coded affinity tags (O-ECAT) and nanoliquid chromatography Fourier transform mass spectrometry. J Proteome Res 2006;5:539–547.
  • Mirzaei H, Regnier F. Identification of yeast oxidized proteins: chromatographic top-down approach for identification of carbonylated, fragmented and cross-linked proteins in yeast. J Chromatogr A 2007;1141:22–31.
  • Mirzaei H, Baena B, Barbas C, Regnier F. Identification of oxidized proteins in rat plasma using avidin chromatography and tandem mass spectrometry. Proteomics 2008;8:1516–1527.
  • Madian AG, Myracle AD, Diaz-Maldonado N, Rochelle NS, Janle EM, Regnier FE. Differential Carbonylation of Proteins as a Function of in vivo Oxidative Stress. J Proteome Res 2011;10:3959–3972.
  • Madian AG, Regnier FE. Profiling carbonylated proteins in human plasma. J Proteome Res 2010;9:1330–1343.
  • Madian AG, Diaz-Maldonado N, Gao Q, Regnier FE. Oxidative stress induced carbonylation in human plasma. J Proteomics 2011;74:2395–2416.
  • Kinumi T, Osaka I, Hayashi A, Kawai T, Matsumoto H, Tsujimoto K. Protein Carbonylation Detected with Light and Heavy Isotope-Labelled 2,4-Dinitrophenylhydrazine by Matrix-Assisted Lasre Desorption/Ionisation Time-of-Flight Mass Spectrometry. J Mass Spectrom Soc Jpn 2009;57: 371–377.
  • Mirzaei H, Regnier F. Identification and quantification of protein carbonylation using light and heavy isotope labeled Girard’s P reagent. J Chromatogr A 2006;1134:122–133.
  • Han B, Stevens JF, Maier CS. Design, synthesis, and application of a hydrazide-functionalized isotope-coded affinity tag for the quantification of oxylipid-protein conjugates. Anal Chem 2007;79:3342–3354.
  • Meany DL, Xie H, Thompson LV, Arriaga EA, Griffin TJ. Identification of carbonylated proteins from enriched rat skeletal muscle mitochondria using affinity chromatography-stable isotope labeling and tandem mass spectrometry. Proteomics 2007;7:1150–1163.
  • Kim JH, Sedlak M, Gao Q, Riley CP, Regnier FE, Adamec J. Dynamics of protein damage in yeast frataxin mutant exposed to oxidative stress. OMICS 2010;14:689–699.
  • Suman SP, Faustman C, Stamer SL, Liebler DC. Proteomics of lipid oxidation-induced oxidation of porcine and bovine oxymyoglobins. Proteomics 2007;7:628–640.
  • Roe MR, McGowan TF, Thompson LV, Griffin TJ. Targeted 18O-labeling for improved proteomic analysis of carbonylated peptides by mass spectrometry. J Am Soc Mass Spectrom 2010;21:1190–1203.
  • Chavez J, Wu J, Han B, Chung WG, Maier CS. New role for an old probe: affinity labeling of oxylipid protein conjugates by N’-aminooxymethylcarbonylhydrazino d-biotin. Anal Chem 2006;78:6847–6854.
  • Peng J, Schmidt B, von Figura K, Dierks T. Identification of formylglycine in sulfatases by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J Mass Spectrom 2003;38:80–86.
  • Fenaille F, Tabet JC, Guy PA. Identification of 4-hydroxy-2-nonenal-modified peptides within unfractionated digests using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal Chem 2004;76:867–873.
  • Fenaille F, Parisod V, Tabet JC, Guy PA. Carbonylation of milk powder proteins as a consequence of processing conditions. Proteomics 2005;5:3097–3104.
  • Bollineni RC, Hoffmann R, Fedorova M. Proteome-wide profiling of carbonylated proteins and carbonylation sites in HeLa cells under mild oxidative stress conditions. Free Radic Biol Med 2014;68:186–195.
  • Bollineni R, Hoffmann R, Fedorova M. Identification of protein carbonylation sites by two-dimensional liquid chromatography in combination with MALDI- and ESI-MS. J Proteomics 2011;74:2338–2350.
  • Madian AG, Diaz-Maldonado N, Gao Q, Regnier FE. Oxidative stress induced carbonylation in human plasma. J Proteomics 2011;74:2395–2416.
  • Thermo Scientific Carbonyl-reactive, 6-plex aminoxyTMT Reagents http://www.piercenet.com/product/carbonyl-reactive-6-plex-tandem-mass-tag-reagents (accessed 12 June 2014).
  • Pan KT, Chen YY, Pu TH, Chao YS, Yang CY, Bomgarden RD, et al. Mass spectrometry-based quantitative proteomics for dissecting multiplexed redox cysteine modifications in nitric oxide-protected cardiomyocyte under hypoxia. Antioxid Redox Signal 2014;20:1365–1381.
  • Friedman DB, Andacht TM, Bunger MK, Chien AS, Hawke DH, Krijgsveld J, et al. The ABRF Proteomics Research Group studies: educational exercises for qualitative and quantitative proteomic analyses. Proteomics 2011; 11:1371–1381.
  • Maisonneuve E, Ducret A, Khoueiry P, Lignon S, Longhi S, Talla E, Dukan S. Rules governing selective protein carbonylation. PLoS One 2009;4:e7269.
  • Zhang D, Jiang D, Yanney M, Zou S, Sygula A. Ratiometric Raman spectroscopy for quantification of protein oxidative damage. Anal Biochem 2009;391:121–126.
  • Capeillere-Blandin C, Gausson V, Descamps-Latscha B, Witko-Sarsat V. Biochemical and spectrophotometric significance of advanced oxidized protein products. Biochim Biophys Acta 2004;1689:91–102.
  • Gracanin M, Hawkins CL, Pattison DI, Davies MJ. Singlet-oxygen-mediated amino acid and protein oxidation: formation of tryptophan peroxides and decomposition products. Free Radic Biol Med 2009;47:92–102.
  • Tomida H, Fujii T, Furutani N, Michihara A, Yasufuku T, Akasaki K, et al. Antioxidant properties of some different molecular weight chitosans. Carbohydr Res 2009;344: 1690–1696.
  • Wang C, Chen Y, Hu M, Ding J, Xu C, Wang R. In vitro antioxidant activities of the polysaccharides from Tricholoma lobayense. Int J Biol Macromol 2012;50: 534–539.
  • Bobrowski K, Wierzchowski KL, Holcman J, Ciurak M. Pulse radiolysis studies of intramolecular electron transfer in model peptides and proteins. IV. Met/S:.Br–> Tyr/O. radical transformation in aqueous solution of H-Tyr-(Pro)n-Met-OH peptides. Int J Radiat Biol 1 992;62:507–516.
  • Morgan PE, Pattison DI, Hawkins CL, Davies MJ. Separation, detection, and quantification of hydroperoxides formed at side-chain and backbone sites on amino acids, peptides, and proteins. Free Radic Biol Med 2008;45: 1279–1289.
  • Collin F, Hindo J, Therond P, Couturier M, Cosson C, Jore D, Gardes-Albert M. Experimental evidence of the reciprocal oxidation of bovine serum albumin and linoleate in aqueous solution, initiated by HO* free radicals. Biochimie 2010;92:1130–1137.
  • Patterson LK, Maziere JC, Bartels DM, Hug GL, Santus R, Morliere P. Evidence for a slow and oxygen-insensitive intra-molecular long range electron transfer from tyrosine residues to the semi-oxidized tryptophan 214 in human serum albumin: its inhibition by bound copper (II). Amino Acids 2012;42:1269–1275.
  • Bose B, Dube A. Interaction of chlorin p6 with bovine serum albumin and photodynamic oxidation of protein. J Photochem Photobiol B 2006;85:49–55.
  • Agon VV, Bubb WA, Wright A, Hawkins CL, Davies MJ. Sensitizer-mediated photooxidation of histidine residues: evidence for the formation of reactive side-chain peroxides. Free Radic Biol Med 2006;40:698–710.

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.