Proteomic identification and quantification of S-glutathionylation in mouse macrophages using resin-assisted enrichment and isobaric labeling

Bachi, 2013, Redox proteomics: chemical principles, methodological approaches and biological/biomedical promises, Chem. Rev., 113, 596, 10.1021/cr300073p Finkel, 2011, Signal transduction by reactive oxygen species, J. Cell Biol., 194, 7, 10.1083/jcb.201102095 Janssen-Heininger, 2008, Redox-based regulation of signal transduction: principles, pitfalls, and promises, Free Radic. Biol. Med., 45, 1, 10.1016/j.freeradbiomed.2008.03.011 Winterbourn, 2008, Thiol chemistry and specificity in redox signaling, Free Radic. Biol. Med., 45, 549, 10.1016/j.freeradbiomed.2008.05.004 Held, 2012, Regulatory control or oxidative damage? Proteomic approaches to interrogate the role of cysteine oxidation status in biological processes, Mol. Cell. Proteomics, 11, 013037 Pastore, 2012, S-Glutathionylation signaling in cell biology: progress and prospects, Eur. J. Pharm. Sci., 46, 279, 10.1016/j.ejps.2012.03.010 Dalle-Donne, 2009, Protein S-glutathionylation: a regulatory device from bacteria to humans, Trends Biochem. Sci., 34, 85, 10.1016/j.tibs.2008.11.002 Mieyal, 2008, Molecular mechanisms and clinical implications of reversible protein S-glutathionylation, Antioxid. Redox Signal., 10, 1941, 10.1089/ars.2008.2089 Shelton, 2008, Regulation by reversible S-glutathionylation: molecular targets implicated in inflammatory diseases, Mol. Cells, 25, 332 Gallogly, 2007, Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress, Curr. Opin. Pharmacol., 7, 381, 10.1016/j.coph.2007.06.003 Dalle-Donne, 2007, S-glutathionylation in protein redox regulation, Free Radic. Biol. Med., 43, 883, 10.1016/j.freeradbiomed.2007.06.014 Mohr, 1999, Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase, J. Biol. Chem., 274, 9427, 10.1074/jbc.274.14.9427 Pan, 2007, Glutathiolation regulates tumor necrosis factor-alpha-induced caspase-3 cleavage and apoptosis: key role for glutaredoxin in the death pathway, Circ. Res., 100, 213, 10.1161/01.RES.0000256089.30318.20 Humphries, 2002, Regulation of cAMP-dependent protein kinase activity by glutathionylation, J. Biol. Chem., 277, 43505, 10.1074/jbc.M207088200 Ward, 2000, Oxidant-induced S-glutathiolation inactivates protein kinase C-alpha (PKC-alpha): a potential mechanism of PKC isozyme regulation, Biochemistry, 39, 10319, 10.1021/bi000781g Reynaert, 2006, Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta, Proc. Natl. Acad. Sci. USA, 103, 13086, 10.1073/pnas.0603290103 Pineda-Molina, 2001, Glutathionylation of the p50 subunit of NF-kappaB: a mechanism for redox-induced inhibition of DNA binding, Biochemistry, 40, 14134, 10.1021/bi011459o Klatt, 1999, Redox regulation of c-Jun DNA binding by reversible S-glutathiolation, FASEB J., 13, 1481, 10.1096/fasebj.13.12.1481 Lancel, 2009, Nitroxyl activates SERCA in cardiac myocytes via glutathiolation of cysteine 674, Circ. Res., 104, 720, 10.1161/CIRCRESAHA.108.188441 Adachi, 2004, S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide, Nat. Med., 10, 1200, 10.1038/nm1119 Anathy, 2009, Redox amplification of apoptosis by caspase-dependent cleavage of glutaredoxin 1 and S-glutathionylation of Fas, J. Cell Biol., 184, 241, 10.1083/jcb.200807019 Casagrande, 2002, Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems, Proc. Natl. Acad. Sci. USA, 99, 9745, 10.1073/pnas.152168599 Fratelli, 2003, Identification of proteins undergoing glutathionylation in oxidatively stressed hepatocytes and hepatoma cells, Proteomics, 3, 1154, 10.1002/pmic.200300436 Gao, 2009, Methods for analysis of protein glutathionylation and their application to photosynthetic organisms, Mol. Plant, 2, 218, 10.1093/mp/ssn072 Fratelli, 2004, Redox proteomics: identification and functional role of glutathionylated proteins, Expert Rev. Proteomics, 1, 365, 10.1586/14789450.1.3.365 Cheng, 2005, Detection of S-glutathionylated proteins by glutathione S-transferase overlay, Arch. Biochem. Biophys., 435, 42, 10.1016/j.abb.2004.12.016 Brennan, 2006, The utility of N,N-biotinyl glutathione disulfide in the study of protein S-glutathiolation, Mol. Cell. Proteomics, 5, 215, 10.1074/mcp.M500212-MCP200 Zaffagnini, 2012, Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey, Mol. Cell.Proteomics, 11, 014142 Chiang, 2012, In vivo tagging and characterization of S-glutathionylated proteins by a chemoenzymatic method, Angew. Chem. Int. Ed. Engl., 51, 5871, 10.1002/anie.201200321 Lind, 2002, Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis, Arch. Biochem. Biophys., 406, 229, 10.1016/S0003-9861(02)00468-X Su, 2013, Quantitative site-specific reactivity profiling of S-nitrosylation in mouse skeletal muscle using cysteinyl peptide enrichment coupled with mass spectrometry, Free Radic. Biol. Med., 57, 68, 10.1016/j.freeradbiomed.2012.12.010 Forrester, 2009, Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture, Nat. Biotechnol., 27, 557, 10.1038/nbt.1545 Liu, 2004, High throughput comparative proteome analysis using a quantitative cysteinyl-peptide enrichment technology, Anal. Chem., 76, 5345, 10.1021/ac049485q Liu, 2010, Site-specific proteomics approach for study protein S-nitrosylation, Anal. Chem., 82, 7160, 10.1021/ac100569d Elias, 2007, Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry, Nat. Methods, 4, 207, 10.1038/nmeth1019 Qian, 2005, Probability-based evaluation of peptide and protein identifications from tandem mass spectrometry and sequest analysis: the human proteome, J. Proteome Res., 4, 53, 10.1021/pr0498638 Kim, 2008, Spectral probabilities and generating functions of tandem mass spectra: a strike against decoy databases, J. Proteome Res., 7, 3354, 10.1021/pr8001244 Thompson, 2003, Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS, Anal. Chem., 75, 1895, 10.1021/ac0262560 Zhang, 2010, Deuterium isobaric amine-reactive tags for quantitative proteomics, Anal. Chem., 82, 7588, 10.1021/ac101306x Gilge, 2008, The effect of oxidant and the non-oxidant alteration of cellular thiol concentration on the formation of protein mixed-disulfides in HEK 293 cells, PLoS One, 3, e4015, 10.1371/journal.pone.0004015 Nordstrand, 1999, NMR structure of Escherichia coli glutaredoxin 3-glutathione mixed disulfide complex: implications for the enzymatic mechanism, J. Mol. Biol., 286, 541, 10.1006/jmbi.1998.2444 Stone, 2006, Hydrogen peroxide: a signaling messenger, Antioxid. Redox Signal., 8, 243, 10.1089/ars.2006.8.243 Chae, 2012, Protein glutathionylation in the regulation of peroxiredoxins: a family of thiol-specific peroxidases that function as antioxidants, molecular chaperones, and signal modulators, Antioxid. Redox Signal., 16, 506, 10.1089/ars.2011.4260 Caplan, 2004, Regulation of annexin A2 by reversible glutathionylation, J. Biol. Chem., 279, 7740, 10.1074/jbc.M313049200 Tao, 2004, Protein S-glutathiolation triggered by decomposed S-nitrosoglutathione, Biochemistry, 43, 4028, 10.1021/bi035924o Chen, 2006, Decline of contractility during ischemia-reperfusion injury: actin glutathionylation and its effect on allosteric interaction with tropomyosin, Am. J. Physiol. Cell Physiol., 290, C719, 10.1152/ajpcell.00419.2005 Forman, 2001, Redox signaling in macrophages, Mol. Aspects Med., 22, 189, 10.1016/S0098-2997(01)00010-3 Anathy, 2012, Redox-based regulation of apoptosis: S-glutathionylation as a regulatory mechanism to control cell death, Antioxid. Redox Signal., 16, 496, 10.1089/ars.2011.4281 Mieyal, 2012, Posttranslational modification of cysteine in redox signaling and oxidative stress: focus on s-glutathionylation, Antioxid. Redox Signal., 16, 471, 10.1089/ars.2011.4454 Ghezzi, 2007, Glutathionylation pathways in drug response, Curr. Opin. Pharmacol., 7, 398, 10.1016/j.coph.2007.04.006 Zaffagnini, 2012, The emerging roles of protein glutathionylation in chloroplasts, Plant Sci., 185–186, 86, 10.1016/j.plantsci.2012.01.005 Yang, 1998, Reactivity of the human thioltransferase (glutaredoxin) C7S, C25S, C78S, C82S mutant and NMR solution structure of its glutathionyl mixed disulfide intermediate reflect catalytic specificity, Biochemistry, 37, 17145, 10.1021/bi9806504 Reynaert, 2006, In situ detection of S-glutathionylated proteins following glutaredoxin-1 catalyzed cysteine derivatization, Biochim. Biophys. Acta, 1760, 380, 10.1016/j.bbagen.2006.01.006 Hamnell-Pamment, 2005, Determination of site-specificity of S-glutathionylated cellular proteins, Biochem. Biophys. Res. Commun., 332, 362, 10.1016/j.bbrc.2005.04.130 Zhang, 2011, S-Glutathionyl quantification in the attomole range using glutaredoxin-3-catalyzed cysteine derivatization and capillary gel electrophoresis with laser-induced fluorescence detection, Anal. Bioanal. Chem., 401, 2165, 10.1007/s00216-011-5311-x Murray, 2012, Identification and quantification of S-nitrosylation by cysteine reactive tandem mass tag switch assay, Mol. Cell. Proteomics, 11, 013441 Tavakoli, 2012, Reactive oxygen species and thiol redox signaling in the macrophage biology of atherosclerosis, Antioxid. Redox Signal., 17, 1785, 10.1089/ars.2012.4638 Nicholls, 2012, GAPDH: a common enzyme with uncommon functions, Clin. Exp. Pharmacol. Physiol., 39, 674, 10.1111/j.1440-1681.2011.05599.x Butterfield, 2010, Oxidatively modified glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and Alzheimer's disease: many pathways to neurodegeneration, J. Alzheimer's Dis., 20, 369, 10.3233/JAD-2010-1375 Furukawa, 2008, Complete loss of post-translational modifications triggers fibrillar aggregation of SOD1 in the familial form of amyotrophic lateral sclerosis, J. Biol. Chem., 283, 24167, 10.1074/jbc.M802083200 Meissner, 2008, Superoxide dismutase 1 regulates caspase-1 and endotoxic shock, Nat. Immunol., 9, 866, 10.1038/ni.1633