Chasing cysteine oxidative modifications: Proteomic tools for characterizing cysteine redox status

Circulation: Cardiovascular Genetics

Volumn 5, Issue 5, 2012, Pages

  Murray, Christopher I ^a   Van Eyk, Jennifer E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biotin switch assay; Cysteine modification; Mass spectrometry; Redox proteomics

Indexed keywords

BIOTIN; CYSTEINE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SULFINIC ACID DERIVATIVE; SULFONIC ACID DERIVATIVE; GLUTATHIONE; THIOL DERIVATIVE;

ACYLATION; ARTICLE; DISULFIDE BOND; GLUTATHIONYLATION; HEART FAILURE; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; MASS SPECTROMETRY; NITROSYLATION; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEOMICS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SULFENYLATION; SULFHYDRATION; CHEMISTRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; TANDEM MASS SPECTROMETRY;

ACYLATION; BIOTIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYSTEINE; GLUTATHIONE; HUMANS; OXIDATION-REDUCTION; PROTEOMICS; REACTIVE OXYGEN SPECIES; SULFHYDRYL COMPOUNDS; SULFINIC ACIDS; SULFONIC ACIDS; TANDEM MASS SPECTROMETRY;

EID: 84868622900     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.111.961425     Document Type: Article

References (134)

1. Forman HJ, Fukuto JM, Torres M. Redox signaling: thiol chemistry de-fnes which reactive oxygen and nitrogen species can act as second messengers. Am J Physiol, Cell Physiol. 2004;287:C246-C256. (Pubitemid 38955213)
2. Santos CX, Anilkumar N, Zhang M, Brewer AC, Shah AM. Redox signaling in cardiac myocytes. Free Radic Biol Med. 2011;50:777-793.
3. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J. 2009;417:1-13.
4. Brandes RP, Weissmann N, Schröder K. NADPH oxidases in cardiovascular disease. Free Radic Biol Med. 2010;49:687-706.
5. Seddon M, Shah AM, Casadei B. Cardiomyocytes as effectors of nitric oxide signalling. Cardiovasc Res. 2007;75:315-326. (Pubitemid 46961933)
6. Shao D, Oka S, Brady CD, Haendeler J, Eaton P, Sadoshima J. Redox modification of cell signaling in the cardiovascular system. J Mol Cell Cardiol. 2012;52:550-558.
7. Buchanan BB, Balmer Y. Redox regulation: a broadening horizon. Annu Rev Plant Biol. 2005;56:187-220. (Pubitemid 40802408)
8. Winterbourn CC, Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med. 2008;45:549-561.
9. Paulsen CE, Carroll KS. Orchestrating redox signaling networks through regulatory cysteine switches. ACS Chem Biol. 2010;5:47-62.
10. Georgiou G. How to fip the (redox) switch. Cell. 2002;111:607-610.
11. Hancock JT. The role of redox mechanisms in cell signalling. Mol Biotechnol. 2009;43:162-166.
12. Forrester MT, Stamler JS. A classification scheme for redox-based modi-fications of proteins. Am J Respir Cell Mol Biol. 2007;36:135-137.
13. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol. 2005;6:150-166. (Pubitemid 40215810)
14. Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol. 2008;4:278-286. (Pubitemid 351550893)
15. Whalen EJ, Foster MW, Matsumoto A, Ozawa K, Violin JD, Que LG, Nelson CD, Benhar M, Keys JR, Rockman HA, Koch WJ, Daaka Y, Lefkowitz RJ, Stamler JS. Regulation of beta-adrenergic receptor signaling by S-nitrosylation of G-protein-coupled receptor kinase 2. Cell. 2007;129:511-522. (Pubitemid 46660966)
16. Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD, Vatner SF, Sadoshima J. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell. 2008;133:978-993. (Pubitemid 351787743)
17. Chouchani ET, James AM, Fearnley IM, Lilley KS, Murphy MP. Pro-teomic approaches to the characterization of protein thiol modification. Curr Opin Chem Biol. 2011;15:120-128.
18. Murphy E, Kohr M, Sun J, Nguyen T, Steenbergen C. S-nitrosylation: a radical way to protect the heart. J Mol Cell Cardiol. 2012;52:568-577
19. Martínez-Ruiz A, Cadenas S, Lamas S. Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic Biol Med. 2011;51:17-29.
20. Lima B, Forrester MT, Hess DT, Stamler JS. S-nitrosylation in cardiovascular signaling. Circ Res. 2010;106:633-646.
21. Sun J, Morgan M, Shen RF, Steenbergen C, Murphy E. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res. 2007;101:1155-1163. (Pubitemid 350146442)
22. Lima B, Lam GK, Xie L, Diesen DL, Villamizar N, Nienaber J, Messina E, Bowles D, Kontos CD, Hare JM, Stamler JS, Rockman HA. Endogenous S-nitrosothiols protect against myocardial injury. Proc Natl Acad Sci USA. 2009;106:6297-6302.
23. Shiva S, Sack MN, Greer JJ, Duranski M, Ringwood LA, Burwell L, Wang X, MacArthur PH, Shoja A, Raghavachari N, Calvert JW, Brookes PS, Lefer DJ, Gladwin MT. Nitrite augments tolerance to ischemia/reper-fusion injury via the modulation of mitochondrial electron transfer. J Exp Med. 2007;204:2089-2102. (Pubitemid 47360871)
24. Nadtochiy SM, Burwell LS, Brookes PS. Cardioprotection and mito-chondrial S-nitrosation: effects of S-nitroso-2-mercaptopropionyl gly-cine (SNO-MPG) in cardiac ischemia-reperfusion injury. J Mol Cell Cardiol. 2007;42:812-825. (Pubitemid 46527599)
25. Prime TA, Blaikie FH, Evans C, Nadtochiy SM, James AM, Dahm CC, Vitturi DA, Patel RP, Hiley CR, Abakumova I, Requejo R, Chouchani ET, Hurd TR, Garvey JF, Taylor CT, Brookes PS, Smith RA, Murphy M P. A mitochondria-targeted S-nitrosothiol modulates respiration, nitro-sates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci USA. 2009;106:10764-10769.
26. Foster MW. Methodologies for the characterization, identification and quantification of S-nitrosylated proteins. Biochim Biophys Acta. 2012;1820:675-683.
27. Jaffrey SR, Snyder SH. The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE. 2001;2001:p11.
28. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol. 2001;3:193-197. (Pubitemid 32118373)
29. Hao G, Derakhshan B, Shi L, Campagne F, Gross SS. SNOSID, a pro-teomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures. Proc Natl Acad Sci USA. 2006;103:1012-1017. (Pubitemid 43212213)
30. Derakhshan B, Wille PC, Gross SS. Unbiased identification of cysteine S-nitrosylation sites on proteins. Nat Protoc. 2007;2:1685-1691.
31. Forrester MT, Thompson JW, Foster MW, Nogueira L, Moseley MA, Stamler JS. Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture. Nat Biotechnol. 2009;27:557-559.
32. Paige JS, Xu G, Stancevic B, Jaffrey SR. Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability. Chem Biol. 2008;15:1307-1316. (Pubitemid 352841468)
33. Huang B, Chen C. Detection of protein S-nitrosation using irreversible biotinylation procedures (IBP). Free Radic Biol Med. 2010;49:447-456.
34. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics. 2004;3:1154-1169.
35. Ong SE, Kratchmarova I, Mann M. Properties of 13C-substituted argi-nine in stable isotope labeling by amino acids in cell culture (SILAC). J Proteome Res. 2003;2:173-181. (Pubitemid 37099053)
36. Ong SE, Mann M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc. 2006;1:2650-2660.
37. Zhou X, Han P, Li J, Zhang X, Huang B, Ruan HQ, Chen C. ESNOQ, proteomic quantification of endogenous S-nitrosation. PLoS ONE. 2010;5:e10015.
38. Kohr MJ, Aponte AM, Sun J, Wang G, Murphy E, Gucek M, Steenbergen C. Characterization of potential S-nitrosylation sites in the myocardium. Am J Physiol Heart Circ Physiol. 2011;300:H1327-H1335.
39. Kohr MJ, Sun J, Aponte A, Wang G, Gucek M, Murphy E, Steenbergen C. Simultaneous measurement of protein oxidation and S-nitrosylation during preconditioning and ischemia/reperfusion injury with resin-assisted capture. Circ Res. 2011;108:418-426.
40. Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R. Quantitative analysis of complex protein mixtures using isotope-coded affnity tags. Nat Biotechnol. 1999;17:994-999. (Pubitemid 29474856)
41. Zhang X, Huang B, Zhou X, Chen C. Quantitative proteomic analysis of S-nitrosated proteins in diabetic mouse liver with ICAT switch method. Protein Cell. 2010;1:675-687.
42. Wu C, Parrott AM, Liu T, Jain MR, Yang Y, Sadoshima J, Li H. Distinction of thioredoxin transnitrosylation and denitrosylation target proteins by the ICAT quantitative approach. J Proteomics. 2011;74:2498-2509.
43. Borisov OV, Goshe MB, Conrads TP, Rakov VS, Veenstra TD, Smith RD. Low-energy collision-induced dissociation fragmentation analysis of cysteinyl-modifed peptides. Anal Chem. 2002;74:2284-2292. (Pubitemid 34526034)
44. Zhou H, Ranish JA, Watts JD, Aebersold R. Quantitative proteome analysis by solid-phase isotope tagging and mass spectrometry. Nat Biotechnol. 2002;20:512-515. (Pubitemid 34495941)
45. Hansen KC, Schmitt-Ulms G, Chalkley RJ, Hirsch J, Baldwin MA, Bur-lingame AL. Mass spectrometric analysis of protein mixtures at low levels using cleavable 13C-isotope-coded affnity tag and multidimensional chromatography. Mol Cell Proteomics. 2003;2:299-314.
46. Thompson A, Schäfer J, Kuhn K, Kienle S, Schwarz J, Schmidt G, Neumann T, Johnstone R, Mohammed AK, Hamon C. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem. 2003;75:1895-1904. (Pubitemid 36438013)
47. Murray CI, Uhrigshardt H, O'Meally RN, Cole RN, Van Eyk JE. Identi-fication and quantification of S-nitrosylation by cysteine reactive tandem mass tag switch assay. Mol Cell Proteomics. 2012;11:M111.013441.
48. Landino LM, Koumas MT, Mason CE, Alston JA. Ascorbic acid reduction of microtubule protein disulfdes and its relevance to protein S-nitro-sylation assays. Biochem Biophys Res Commun. 2006;340:347-352. (Pubitemid 43021755)
49. Huang B, Chen C. An ascorbate-dependent artifact that interferes with the interpretation of the biotin switch assay. Free Radic Biol Med. 2006;41:562-567. (Pubitemid 44080503)
50. Kallakunta VM, Staruch A, Mutus B. Sinapinic acid can replace ascor-bate in the biotin switch assay. Biochim Biophys Acta. 2010;1800:23-30.
51. Forrester MT, Foster MW, Benhar M, Stamler JS. Detection of protein S-nitrosylation with the biotin-switch technique. Free Radic Biol Med. 2009;46:119-126.
52. Forrester MT, Foster MW, Stamler JS. Assessment and application of the biotin switch technique for examining protein S-nitrosylation under conditions of pharmacologically induced oxidative stress. J Biol Chem. 2007;282:13977- 13983. (Pubitemid 47100466)
53. Doulias PT, Greene JL, Greco TM, Tenopoulou M, Seeholzer SH, Dunbrack RL, Ischiropoulos H. Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc Natl Acad Sci USA. 2010;107:16958-16963.
54. Zhang Y, Keszler A, Broniowska KA, Hogg N. Characterization and application of the biotin-switch assay for the identification of S-nitrosated proteins. Free Radic Biol Med. 2005;38:874-881. (Pubitemid 40321079)
55. Kettenhofen NJ, Wood MJ. Formation, reactivity, and detection of protein sulfenic acids. Chem Res Toxicol. 2010;23:1633-1646.
56. Sethuraman M, McComb ME, Heibeck T, Costello CE, Cohen RA. Isotope-coded affnity tag approach to identify and quantify oxidant-sensitive protein thiols. Mol Cell Proteomics. 2004;3:273-278. (Pubitemid 38714283)
57. Sethuraman M, McComb ME, Huang H, Huang S, Heibeck T, Costello CE, Cohen RA. Isotope-coded affnity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures. J Proteome Res. 2004;3:1228-1233. (Pubitemid 40040377)
58. Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, Strahler JR, Andrews PC, Jakob U. Quantifying changes in the thiol re-dox proteome upon oxidative stress in vivo. Proc Natl Acad Sci USA. 2008;105:8197-8202. (Pubitemid 351904734)
59. Sethuraman M, Clavreul N, Huang H, McComb ME, Costello CE, Cohen RA. Quantification of oxidative posttranslational modifications of cysteine thiols of p21ras associated with redox modulation of activity using isotope-coded affnity tags and mass spectrometry. Free Radic Biol Med. 2007;42:823-829. (Pubitemid 46274168)
60. Burgoyne JR, Eaton P. A rapid approach for the detection, quantification, and discovery of novel sulfenic acid or S-nitrosothiol modifed proteins using a biotin-switch method. Meth Enzymol. 2010;473:281-303.
61. Saurin AT, Neubert H, Brennan JP, Eaton P. Widespread sulfenic acid formation in tissues in response to hydrogen peroxide. Proc Natl Acad Sci USA. 2004;101:17982-17987. (Pubitemid 40054061)
62. Charles RL, Schröder E, May G, Free P, Gaffney PR, Wait R, Begum S, Heads RJ, Eaton P. Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol Cell Proteomics. 2007;6:1473-1484. (Pubitemid 47506161)
63. Leonard SE, Reddie KG, Carroll KS. Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. ACS Chem Biol. 2009;4:783-799.
64. Seo YH, Carroll KS. Quantification of protein sulfenic acid modifica-tions using isotope-coded dimedone and iododimedone. Angew Chem Int Ed Engl. 2011;50:1342-1345.
65. Truong TH, Garcia FJ, Seo YH, Carroll KS. Isotope-coded chemical reporter and acid-cleavable affnity reagents for monitoring protein sulfen-ic acids. Bioorg Med Chem Lett. 2011;21:5015-5020.
66. Paulsen CE, Truong TH, Garcia FJ, Homann A, Gupta V, Leonard SE, Carroll KS. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat Chem Biol. 2012;8:57-64.
67. Giustarini D, Rossi R, Milzani A, Colombo R, Dalle-Donne I. S-glutathi-onylation: from redox regulation of protein functions to human diseases. J Cell Mol Med. 2004;8:201-212. (Pubitemid 44145509)
68. Adachi T, Weisbrod RM, Pimentel DR, Ying J, Sharov VS, Schöneich C, Cohen RA. S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med. 2004;10:1200-1207. (Pubitemid 39540436)
69. Chen CA, Wang TY, Varadharaj S, Reyes LA, Hemann C, Taluk-der MA, Chen YR, Druhan LJ, Zweier JL. S-glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature. 2010;468:1115-1118.
70. Hill BG, Bhatnagar A. Protein S-glutathiolation: redox-sensitive regulation of protein function. J Mol Cell Cardiol. 2012;52:559-567.
71. Lind C, Gerdes R, Hamnell Y, Schuppe-Koistinen I, Von Löwenhielm HB, Holmgren A, Cotgreave IA. Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affnity purification and proteomic analysis. Arch Biochem Biophys. 2002;406:229-240. (Pubitemid 35216349)
72. Reynaert NL, Ckless K, Guala AS, Wouters EF, Van Der Vliet A, Janssen-Heininger YM. In situ detection of S-glutathionylated proteins following glutaredoxin-1 catalyzed cysteine derivatization. Biochim Biophys Acta. 2006;1760:380-387.
73. Aesif SW, Anathy V, Havermans M, Guala AS, Ckless K, Taatjes DJ, Janssen-Heininger YM. In situ analysis of protein S-glutathionylation in lung tissue using glutaredoxin-1-catalyzed cysteine derivatization. Am J Pathol. 2009;175:36-45.
74. Aesif SW, Janssen-Heininger YM, Reynaert NL. Protocols for the detection of s-glutathionylated and s-nitrosylated proteins in situ. Meth Enzymol. 2010;474:289-296.
75. Gravina SA, Mieyal JJ. Thioltransferase is a specific glutathionyl mixed disulfde oxidoreductase. Biochemistry. 1993;32:3368-3376. (Pubitemid 23126904)
76. Brennan JP, Miller JI, Fuller W, Wait R, Begum S, Dunn MJ, Eaton P. The utility of N, N-biotinyl glutathione disulfde in the study of protein S-glutathiolation. Mol Cell Proteomics. 2006;5:215-225. (Pubitemid 43329300)
77. Sullivan DM, Levine RL, Finkel T. Detection and affnity purification of oxidant-sensitive proteins using biotinylated glutathione ethyl ester. Meth Enzymol. 2002;353:101-113. (Pubitemid 34625584)
78. Sullivan DM, Wehr NB, Fergusson MM, Levine RL, Finkel T. Identifica-tion of oxidant-sensitive proteins: TNF-alpha induces protein glutathio-lation. Biochemistry. 2000;39:11121-11128.
79. Clavreul N, Bachschmid MM, Hou X, Shi C, Idrizovic A, Ido Y, Pimentel D, Cohen RA. S-glutathiolation of p21ras by peroxynitrite mediates en-dothelial insulin resistance caused by oxidized low-density lipoprotein. Arterioscler Thromb Vasc Biol. 2006;26:2454-2461. (Pubitemid 44607465)
80. West MB, Hill BG, Xuan YT, Bhatnagar A. Protein glutathiolation by nitric oxide: an intracellular mechanism regulating redox protein modif-cation. FASEB J. 2006;20:1715-1717.
81. Wang SB, Foster DB, Rucker J, O'Rourke B, Kass DA, Van Eyk JE. Re-dox regulation of mitochondrial ATP synthase: implications for cardiac resynchronization therapy. Circ Res. 2011;109:750-757.
82. Lindahl M, Mata-Cabana A, Kieselbach T. The disulfde proteome and other reactive cysteine proteomes: analysis and functional significance. Antioxid Redox Signal. 2011;14:2581-2642.
83. Cumming RC, Andon NL, Haynes PA, Park M, Fischer WH, Schubert D. Protein disulfde bond formation in the cytoplasm during oxidative stress. J Biol Chem. 2004;279:21749-21758. (Pubitemid 38679361)
84. Linke K, Jakob U. Not every disulfde lasts forever: disulfde bond formation as a redox switch. Antioxid Redox Signal. 2003;5:425-434. (Pubitemid 37087402)
85. Brennan JP, Wait R, Begum S, Bell JR, Dunn MJ, Eaton P. Detection and mapping of widespread intermolecular protein disulfde formation during cardiac oxidative stress using proteomics with diagonal electro-phoresis. J Biol Chem. 2004;279:41352-41360. (Pubitemid 39313574)
86. Brown JR, Hartley BS. Location of disulphide bridges by diagonal paper electrophoresis. The disulphide bridges of bovine chymotrypsinogen A. Biochem J. 1966;101:214-228.
87. Sommer A, Traut RR. Diagonal polyacrylamide-dodecyl sulfate gel electrophoresis for the identification of ribosomal proteins cross-linked with methyl-4-mercaptobutyrimidate. Proc Natl Acad Sci USA. 1974;71:3946-3950.
88. Cumming RC. Analysis of global and specific changes in the disulfde proteome using redox two-dimensional polyacrylamide gel electropho-resis. Methods Mol Biol. 2009;476:160-174.
89. McDonagh B. Diagonal electrophoresis for detection of protein disul-phide bridges. Methods Mol Biol. 2009;519:305-310.
90. Fedorova M, Kuleva N, Hoffmann R. Reversible and irreversible modi-fications of skeletal muscle proteins in a rat model of acute oxidative stress. Biochim Biophys Acta. 2009;1792:1185-1193.
91. Winger AM, Taylor NL, Heazlewood JL, Day DA, Millar AH. Identi-fication of intra-and intermolecular disulphide bonding in the plant mitochondrial proteome by diagonal gel electrophoresis. Proteomics. 2007;7:4158-4170. (Pubitemid 350190287)
92. Burgoyne JR, Madhani M, Cuello F, Charles RL, Brennan JP, Schröder E, Browning DD, Eaton P. Cysteine redox sensor in PKGIa enables oxi-dant-induced activation. Science. 2007;317:1393-1397. (Pubitemid 47417480)
93. Lee K, Lee J, Kim Y, Bae D, Kang KY, Yoon SC, Lim D. Defning the plant disulfde proteome. Electrophoresis. 2004;25:532-541.
94. Hu W, Tedesco S, McDonagh B, Bárcena JA, Keane C, Sheehan D. Selection of thiol-and disulfde-containing proteins of Escherichia coli on activated thiol-Sepharose. Anal Biochem. 2010;398:245-253.
95. Fu C, Hu J, Liu T, Ago T, Sadoshima J, Li H. Quantitative analysis of redox-sensitive proteome with DIGE and ICAT. J Proteome Res. 2008;7:3789-3802.
96. Hägglund P, Bunkenborg J, Maeda K, Svensson B. Identification of thio-redoxin disulfde targets using a quantitative proteomics approach based on isotope-coded affnity tags. J Proteome Res. 2008;7:5270-5276.
97. Hung CW, Schlosser A, Wei J, Lehmann WD. Collision-induced reporter fragmentations for identification of covalently modifed peptides. Anal Bioanal Chem. 2007;389:1003-1016. (Pubitemid 47482250)
98. Lioe H, O'Hair RA. Comparison of collision-induced dissociation and electron-induced dissociation of singly protonated aromatic amino acids, cystine and related simple peptides using a hybrid linear ion trap-FT-ICR mass spectrometer. Anal Bioanal Chem. 2007;389:1429-1437. (Pubitemid 350023667)
99. Choi S, Jeong J, Na S, Lee HS, Kim HY, Lee KJ, Paek E. New algorithm for the identification of intact disulfde linkages based on fragmentation characteristics in tandem mass spectra. J Proteome Res. 2010;9:626-635.
100. Mormann M, Eble J, Schwöppe C, Mesters RM, Berdel WE, Peter-Katalinic J, Pohlentz G. Fragmentation of intra-peptide and inter-peptide disulfde bonds of proteolytic peptides by nanoESI collision-induced dissociation. Anal Bioanal Chem. 2008;392:831-838.
101. Zhang Y, Dewald HD, Chen H. Online mass spectrometric analysis of proteins/peptides following electrolytic cleavage of disulfde bonds. J Proteome Res. 2011;10:1293-1304.
102. Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem. 1996;68:850-858.
103. Saito K, Yasuo I, Uchimura H, Koide-Yoshida S, Mizuguchi T, Kiso Y. Verification of protein disulfde bond arrangement by in-gel tryp-tic digestion under entirely neutral pH conditions. Proteomics. 2010;10:1505-1509.
104. Mauri P, Toppo S, De Palma A, Benazzi L, Maiorino M, Ursini F. Iden-tification by MS/MS of disulfdes produced by a functional redox transition. Meth Enzymol. 2010;473:217-225.
105. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, Wang R. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science. 2008;322:587-590.
106. Li L, Rose P, Moore PK. Hydrogen sulfde and cell signaling. Annu Rev Pharmacol Toxicol. 2011;51:169-187.
107. Li L, Bhatia M, Zhu YZ, Zhu YC, Ramnath RD, Wang ZJ, Anuar FB, Whiteman M, Salto-Tellez M, Moore PK. Hydrogen sulfde is a novel mediator of lipopolysaccharide-induced infilammation in the mouse. FASEB J. 2005;19:1196-1198. (Pubitemid 40946463)
108. Nicholson CK, Calvert JW. Hydrogen sulfde and ischemia-reperfusion injury. Pharmacol Res. 2010;62:289-297.
109. Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W, Gazi SK, Barrow RK, Yang G, Wang R, Snyder SH. H2S signals through protein S-sulfhydra-tion. Sci Signal. 2009;2:ra72.
110. Mustafa AK, Sikka G, Gazi SK, Steppan J, Jung SM, Bhunia AK, Barod-ka VM, Gazi FK, Barrow RK, Wang R, Amzel LM, Berkowitz DE, Sny-der SH. Hydrogen sulfde as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ Res. 2011;109:1259-1268.
111. Krishnan N, Fu C, Pappin DJ, Tonks NK. H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal. 2011;4:ra86.
112. Sen N, Paul BD, Gadalla MM, Mustafa AK, Sen T, Xu R, Kim S, Snyder SH. Hydrogen sulfde-linked sulfhydration of NF-?B mediates its anti-apoptotic actions. Mol Cell. 2012;45:13-24.
113. Iwanaga T, Tsutsumi R, Noritake J, Fukata Y, Fukata M. Dynamic protein palmitoylation in cellular signaling. Prog Lipid Res. 2009;48:117-127.
114. Linder ME, Deschenes RJ. Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol. 2007;8:74-84. (Pubitemid 46012016)
115. Dohlman HG, Song J, Apanovitch DM, Di Bello PR, Gillen KM. Regulation of G protein signalling in yeast. Semin Cell Dev Biol. 1998;9:135-141. (Pubitemid 128352264)
116. Yang W, Di Vizio D, Kirchner M, Steen H, Freeman MR. Proteome scale characterization of human S-acylated proteins in lipid raft-enriched and non-raft membranes. Mol Cell Proteomics. 2010;9:54-70.
117. Wilson JP, Raghavan AS, Yang YY, Charron G, Hang HC. Proteomic analysis of fatty-acylated proteins in mammalian cells with chemical reporters reveals S-acylation of histone H3 variants. Mol Cell Proteomics. 2011;10:M110.001198.
118. Rousso I, Mixon MB, Chen BK, Kim PS. Palmitoylation of the HIV-1 envelope glycoprotein is critical for viral infectivity. Proc Natl Acad Sci USA. 2000;97:13523-13525.
119. Drisdel RC, Green WN. Labeling and quantifying sites of protein palmi-toylation. Bio Techniques. 2004;36:276-285. (Pubitemid 38174735)
120. Wan J, Roth AF, Bailey AO, Davis NG. Palmitoylated proteins: purifica-tion and identification. Nat Protoc. 2007;2:1573-1584.
121. Roth AF, Wan J, Bailey AO, Sun B, Kuchar JA, Green WN, Phinney BS, Yates JR 3rd, Davis NG. Global analysis of protein palmitoylation in yeast. Cell. 2006;125:1003-1013. (Pubitemid 43795188)
122. Forrester MT, Hess DT, Thompson JW, Hultman R, Moseley MA, Stam-ler JS, Casey PJ. Site-specific analysis of protein S-acylation by resin-assisted capture. J Lipid Res. 2011;52:393-398.
123. Zhang L, Foster K, Li Q, Martens JR. S-acylation regulates Kv1.5 channel surface expression. Am J Physiol, Cell Physiol. 2007;293:C152-C161. (Pubitemid 47105043)
124. Liang X, Nazarian A, Erdjument-Bromage H, Bornmann W, Tempst P, Resh MD. Heterogeneous fatty acylation of Src family kinases with poly-unsaturated fatty acids regulates raft localization and signal transduction. J Biol Chem. 2001;276:30987-30994.
125. Takeishi Y, Huang Q, Abe J, Glassman M, Che W, Lee JD, Kawakatsu H, Lawrence EG, Hoit BD, Berk BC, Walsh RA. Src and multiple MAP ki-nase activation in cardiac hypertrophy and congestive heart failure under chronic pressure-overload: comparison with acute mechanical stretch. J Mol Cell Cardiol. 2001;33:1637-1648. (Pubitemid 32844222)
126. Biteau B, Labarre J, Toledano MB. ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature. 2003;425:980-984. (Pubitemid 37376931)
127. Woo HA, Chae HZ, Hwang SC, Yang KS, Kang SW, Kim K, Rhee SG. Reversing the inactivation of peroxiredoxins caused by cysteine sulfnic acid formation. Science. 2003;300:653-656. (Pubitemid 36520592)
128. Budanov AV, Sablina AA, Feinstein E, Koonin EV, Chumakov PM. Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science. 2004;304:596-600. (Pubitemid 38541920)
129. Reddie KG, Carroll KS. Expanding the functional diversity of proteins through cysteine oxidation. Curr Opin Chem Biol. 2008;12:746-754.
130. Chang YC, Huang CN, Lin CH, Chang HC, Wu CC. Mapping protein cysteine sulfonic acid modifications with specific enrichment and mass spectrometry: an integrated approach to explore the cysteine oxidation. Proteomics. 2010;10:2961-2971.
131. Lo Conte M, Carroll KS. Chemoselective ligation of sulfnic acids with aryl-nitroso compounds. Angew Chem Int Ed Engl. 2012;51:6502-6505.
132. Kinumi T, Shimomae Y, Arakawa R, Tatsu Y, Shigeri Y, Yumoto N, Niki E. Effective detection of peptides containing cysteine sulfonic acid using matrix-assisted laser desorption/ionization and laser desorp-tion/ionization on porous silicon mass spectrometry. J Mass Spectrom. 2006;41:103-112. (Pubitemid 43164841)
133. Medzihradszky KF, Darula Z, Perlson E, Fainzilber M, Chalkley RJ, Ball H, Greenbaum D, Bogyo M, Tyson DR, Bradshaw RA, Burlingame AL. O-sulfonation of serine and threonine: mass spectrometric detection and characterization of a new posttranslational modification in diverse proteins throughout the eukaryotes. Mol Cell Proteomics. 2004;3:429-440.
134. Medzihradszky KF, Guan S, Maltby DA, Burlingame AL. Sulfopeptide fragmentation in electron-capture and electron-transfer dissociation. J Am Soc Mass Spectrom. 2007;18:1617-1624. (Pubitemid 47302322)