Stabilising cysteinyl thiol oxidation and nitrosation for proteomic analysis

Journal of Proteomics

Volumn 92, Issue , 2013, Pages 160-170

  Ratnayake, Shibani ^a   Dias, Irundika H K ^a   Lattman, Eric ^a   Griffiths, Helen R ^a  

^a ASTON UNIVERSITY   (United Kingdom)

Author keywords

Dimedone; Gel electrophoresis; ICAT; Nitrosothiol; Sulfenic acid

Indexed keywords

BIOTIN; CERAMIDE; CYSTEINE; DISULFIDE; GLUTAREDOXIN; POLYUNSATURATED FATTY ACID; S NITROSOGLUTATHIONE; S NITROSOTHIOL; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; THIOL; THIOREDOXIN;

CATALYSIS; DISULFIDE BOND; ELECTROPHILICITY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HYDROLYSIS; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; ISOELECTRIC FOCUSING; LIPID PEROXIDATION; MASS SPECTROMETRY; NITROSATION; NONHUMAN; NUCLEOPHILICITY; OXIDATION; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEOMICS; REVIEW;

3-(2,4-DIOXOCYCLOHEXYL)PROPYL; BIOTIN SWITCH TECHNIQUE; BSO; BST; BUTHIONINE SULFOXIMINE; CYS-SOH; CYSTEINE SULPHENIC ACID; DCP; DIMEDONE; DITHIONITROBISBENZOIC ACID; DITHIOTHREITOL; DTNB; DTT; GEL ELECTROPHORESIS; GLUTAREDOXIN; GLUTATHIONE; GLUTATHIONE DISULPHIDE; GLUTATHIONE REDUCTASE; GRX; GSH; GSR; GSSG; HNE; HYDROXYNONENAL; IAA; IAM; ICAT; IEF; IODOACETAMIDE; IODOACETIC ACID; ISOELECTRIC FOCUSSING; ISOTOPE-CODED AFFINITY TAG; N-ETHYL MALEIMIDE; NEM; NITRIC OXIDE; NITROSOTHIOL; NO; PEG; POLYETHYLENE GLYCOL; REACTIVE OXYGEN SPECIES; ROS; SMASE; SNO; SPHINGOMYELINASE; SULFENIC ACID; THIOREDOXIN; THIOREDOXIN REDUCTASE; TRX; TRXR;

ANIMALS; CYSTEINE; HUMANS; MASS SPECTROMETRY; NITROSO COMPOUNDS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; SULFHYDRYL COMPOUNDS;

EID: 84886949676     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.06.019     Document Type: Review

References (88)

1. Winterbourn C.C., Hampton M.B. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 2008, 45(5):549-561.
2. Dormeyer W., Dorr A., Ott M., Schnolzer M. Acetylation of the HIV-1 Tat protein: an in vitro study. Anal Bioanal Chem 2003, 376(7):994-1005.
3. Nagy P., Ashby M.T. Reactive sulfur species: kinetics and mechanisms of the oxidation of cysteine by hypohalous acid to give cysteine sulfenic acid. J Am Chem Soc 2007, 129(45):14082-14091.
4. Jaffrey S.R., Erdjument-Bromage H., Ferris C.D., Tempst P., Snyder S.H. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 2001, 3(2):193-197.
5. Mallis R.J., Hamann M.J., Zhao W., Zhang T., Hendrich S., Thomas J.A. Irreversible thiol oxidation in carbonic anhydrase III: protection by S-glutathiolation and detection in aging rats. Biol Chem 2002, 383(3-4):649-662.
6. Vila A., Tallman K.A., Jacobs A.T., Liebler D.C., Porter N.A., Marnett L.J. Identification of protein targets of 4-hydroxynonenal using click chemistry for ex vivo biotinylation of azido and alkynyl derivatives. Chem Res Toxicol 2008, 21(2):432-444.
7. Pace N.J., Weerapana E. Diverse functional roles of reactive cysteines. ACS Chem Biol 2012, 8(2):283-296.
8. Wu H., Ma B.G., Zhao J.T., Zhang H.Y. How similar are amino acid mutations in human genetic diseases and evolution. Biochem Biophys Res Commun 2007, 362(2):233-237.
9. Wang W., Ballatori N. Endogenous glutathione conjugates: occurrence and biological functions. Pharmacol Rev 1998, 50(3):335-355.
10. Griffiths H., Mistry P., Herbert K., Lunec J. Molecular and cellular effects of ultraviolet light-induced genotoxicity. Crit Rev Clin Lab Sci 1998, 35(3):189-237.
11. Cesaratto L., Vascotto C., Calligaris S., Tell G. The importance of redox state in liver damage. Ann Hepatol 2004, 3:86-92.
12. Hancock J.T., Desikan R., Neill S.J. Cytochrome c, glutathione, and the possible role of redox potentials in apoptosis. Ann N Y Acad Sci 2003, 1010:446-448. [Apoptosis from Signaling Pathways to Therapeutic Tools].
13. Kemp M., Go Y.-M., Jones D.P. Non-equilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology. Free Radic Biol Med 2008, 44(6):921-937.
14. Samiec P., Drews-Botsch C., Flagg E., Kurtz J., Sternberg P.J., Reed R., et al. Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic Biol Med 1998, 24(5):699-704.
15. Hansen J.M., Watson W.H., Jones D.P. Compartmentation of Nrf-2 redox control: regulation of cytoplasmic activation by glutathione and DNA binding by thioredoxin-1. Toxicol Sci 2004, 82(1):308-317.
16. Hancock J.T., Desikan R., Neill S.J., Cross A.R. New equations for redox and nano-signal transduction. J Theor Biol 2004, 226(1):65-68.
17. Poole L.B., Karplus P.A., Claiborne A. Protein sulfenic acids in redox signaling. Annu Rev Pharmacol Toxicol 2004, 44:325-347.
18. Jacob C., Holme A.L., Fry F.H. The sulfinic acid switch in proteins. Org Biomol Chem 2004, 2:1953-1956.
19. Sekhar K.R., Rachakonda G., Freeman M.L. Cysteine-based regulation of the CUL3 adaptor protein Keap1. Toxicol Appl Pharmacol 2010, 244(1):21-26.
20. Hess, Douglas T., Matsumoto A., Kim S.-O., Marshall H.E., Stamler J.S. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 2005, 6(2):150-166.
21. Leonard S.E., Carroll K.S. Chemical 'omics' approaches for understanding protein cysteine oxidation in biology. Curr Opin Chem Biol 2011, 15(1):88-102.
22. Schissel S.L., Keesler G.A., Schuchman E.H., Williams K.J., Tabas I. The cellular trafficking and zinc dependence of secretory and lysosomal sphingomyelinase, two products of the acid sphingomyelinase gene. J Biol Chem 1998, 273(29):18250-18259.
23. Holopainen J.M., Subramanian M., Kinnunen P.K.J. Sphingomyelinase induces lipid microdomain formation in a fluid phosphatidylcholine/sphingomyelin membrane. Biochem 1998, 37:17562-17570.
24. Martin S.F., Sawai H., Villalba J.M., Hannun Y.A. Redox regulation of neutral sphingomyelinase-1 activity in HEK293 cells through a GSH-dependent mechanism. Arch Biochem Biophys 2007, 459:295-300.
25. Li P., Zhang Y., Yi F. Lipid raft redox signaling platforms in endothelial dysfunction. Antiox Redox 2007, 9(9):1457-1470.
26. Zhang A., Yi F., Jin S., Xia M., Chen Q., Gulbins E., et al. Acid sphingomyelinase and its redox amplification in formation of lipid raft redox signaling platforms in endothelial cells. Antioxid Redox Signal 2007, 9(7):817-828.
27. Qiu H., Edmunds T., Baker-Malcolm J., Karey K.P., Estes S., Schwarz C., et al. Activation of human acid sphingomyelinase through modification or deletion of C-terminal cysteine. J Biol Chem 2003, 278(35):32744-32752.
28. Leonarduzzi G., Sottero B., Testa G., Biasi F., Poli G. New insights into redox-modulated cell signaling. Curr Pharm Des 2011, 17(36):3994-4006.
29. Grassme H., Jendrossek V., Riehle A., Kurthy G.v., Berger J., Schwarz H., et al. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Medicine 2003, 9:322-330.
30. Megha E. London Ceramide selectively displaces cholesterol from ordered lipid domains (rafts): implications for lipid raft structure and function. J Biol Chem 2004, 279(11):9997-10004.
31. Liu P., Anderson R.G.W. Compartmentalized production of ceramide at the cell surface. J Biol Chem 1995, 270(45):27179-27185.
32. Charollais J., Van Der Goot F.G. Palmitoylation of membrane proteins (review). Mol Membr Biol 2009, 26(1):55-66.
33. Bulaj G., Kortemme T., Goldenberg D.P. Ionization-reactivity relationships for cysteine thiols in polypeptides. Biochemistry 1998, 37(25):8965-8972.
34. Harris T.K., Turner G.J. Structural basis of perturbed pKa values of catalytic groups in enzyme active sites. IUBMB Life 2002, 53(2):85-98.
35. Poole L.B., Nelson K.J. Discovering mechanisms of signaling-mediated cysteine oxidation. Curr Opin Chem Biol 2008, 12(1):18-24.
36. Reddie K., Carroll K. Expanding the functional diversity of proteins through cysteine oxidation. Curr Opin Chem Biol 2008, 12(6):746-754.
37. Reddie K.G., Seo Y.H., Muse W.B.I.ii, Leonard S.E., Carroll K.S. A chemical approach for detecting sulfenic acid-modified proteins in living cells. Mol Biosyst 2008, 4(6):521-531.
38. Reddie K.G., Carroll K.S. Expanding the functional diversity of proteins through cysteine oxidation. Curr Opin Chem Biol 2008, 12(6):746-754.
39. Jacob C., Giles G.I., Giles N., Sies H. Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Ed 2003, 42:4742-4758.
40. Woo H.A., Won Kang S., Kim H.K., Yang K.-S., Chae H.Z., Rhee S.G. Reversible oxidation of the active site cysteine of peroxiredoxins to cysteine sulfinic acid: immunoblot detection with antibodies specific for the hyperoxidized cysteine-containing sequence. J Biol Chem 2003, 278(48):47361-47364.
41. Denu J.H., Tanner K.G. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochem 1998, 37:5633-5642.
42. Di Stefano A., et al. GSH depletion, protein S-glutathionylation and mitochondrial transmembrane potential hyperpolarization are early events in initiation of cell death induced by a mixture of isothiazolinones in HL60 cells. Biochimica et Biophysica Acta (BBA) - Mol Cell Res 2006, 1763(2):214-225.
43. Brennan J.P., Miller J.I., Fuller W., Wait R., Begum S., Dunn M.J., et al. The utility of N, N-biotinyl glutathione disulfide in the study of protein S-glutathiolation. Mol Cell Proteomics 2006, 5(2):215-225.
44. Phillips D.C., Dias H.K., Kitas G.D., Griffiths H.R. Aberrant reactive oxygen and nitrogen species generation in rheumatoid arthritis (RA): causes and consequences for immune function, cell survival and therapeutic intervention. Antioxid Redox Signal 2009, [mauscript submitted].
45. Matthews J.R., Wakasugi N., Virelizier J.L., Yodoi J., Hay R.T. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 2008, 10(11):1941-1988.
46. Seth D., Stamler J.S. The SNO-proteome: causation and classifications. Curr Opin Chem Biol 2011, 15(1):129-136.
47. Liu L., Hausladen A., Zeng M., Que L., Heitman J., Stamler J.S. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 2001, 410(6827):490-494.
48. Eaton P. Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radic Biol Med 2006, 40(11):1889-1899.
49. Hill B.G., Reily C., Oh J.Y., Johnson M.S., Landar A. Methods for the determination and quantification of the reactive thiol proteome. Free Radic Biol Med 2009, 47(6):675-683.
50. Rogers L.K., Leinweber B.L., Smith C.V. Detection of reversible protein thiol modifications in tissues. Anal Biochem 2006, 358(2):171-184.
51. Sethuraman M., Clavreul N., Huang H., McComb M.E., Costello C.E., Cohen R.A. Quantification of oxidative posttranslational modifications of cysteine thiols of p21ras associated with redox modulation of activity using isotope-coded affinity tags and mass spectrometry. Free Radic Biol Med 2007, 42(6):823-829.
52. Sethuraman M., McComb M.E., Huang H., Huang S., Heibeck T., Costello C.E., et al. Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures. J Proteome Res 2004, 3(6):1228-1233.
53. Ellman G.L. Tissue sulfhydryl groups. Arch Biochem Biophys 1959, 82(1):70-77.
54. Leichert L.I., Gehrke F., Gudiseva H.V., Blackwell T., Ilbert M., Walker A.K., et al. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci USA 2008, 105(24):8197-8202.
55. Jaffrey S.R., Snyder S.H. The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE 2001, 2001(86):pl1.
56. Leonard S.E., Reddie K.G., Carroll K.S. Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. ACS Chem Biol 2009, 4(9):783-799.
57. Brennan J.P., Miller J.I., Fuller W., Wait R., Begum S., Dunn M.J., et al. The utility of N, N-biotinyl glutathione disulfide in the study of protein S-glutathiolation. Mol Cell Proteomics 2006, 5(2):215-225.
58. Chiappetta G., Ndiaye S., Igbaria A., Kumar C., Vinh J., Toledano M.B. Proteome screens for Cys residues oxidation: the redoxome. Methods Enzymol 2010, 473:199-216.
59. Sinha V., Wijewickrama G.T., Chandrasena R.E., Xu H., Edirisinghe P.D., Schiefer I.T., et al. Proteomic and mass spectroscopic quantitation of protein S-nitrosation differentiates NO-donors. ACS Chem Biol 2010, 5(7):667-680.
60. Forrester M.T., Thompson J.W., Foster M.W., Nogueira L., Moseley M.A., Stamler J.S. Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture. Nat Biotechnol 2009, 27(6):557-559.
61. Zhou X., Han P., Li J., Zhang X., Huang B., Ruan H.Q., Chen C. ESNOQ, proteomic quantification of endogenous S-nitrosation. PLoS One 2010, 5(4):e10015.
62. Zhang X., Huang B., Chen C. SNO spectral counting (SNOSC), a label-free proteomic method for quantification of changes in levels of protein S-nitrosation. Free Radic Res 2012, 46(8):1044-1050.
63. Benitez L.V., Allison W.S. The inactivation of the acyl phosphatase activity catalyzed by the sulfenic acid form of glyceraldehyde 3-phosphate dehydrogenase by dimedone and olefins. J Biol Chem 1974, 249(19):6234-6243.
64. Ellis H.R., Poole L.B. Novel application of 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole to identify cysteine sulfenic acid in the AhpC component of alkyl hydroperoxide reductase. Biochemistry 1997, 36(48):15013-15018.
65. Birkett D.J., et al. The reactivity of SH groups with a fluorogenic reagent. FEBS Lett 1970, 6(4):346-348.
66. Poole L.B., Klomsiri C., Knaggs S.A., Furdui C.M., Nelson K.J., Thomas M.J., et al. Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins. Bioconjug Chem 2007, 18(6):2004-2017.
67. Seo Y.H., Carroll K.S. Facile synthesis and biological evaluation of a cell-permeable probe to detect redox-regulated proteins. Bioorg Med Chem Lett 2009, 19(2):356-359.
68. Paulsen C.E., Truong T.H., Garcia F.J., Homann A., Gupta V., Leonard S.E., et al. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat Chem Biol 2012, 8(1):57-64.
69. Palace V., Kumar D., Hill M.F., Khaper N., Singal P.K. Regional differences in non-enzymatic antioxidants in the heart under control and oxidative stress conditions. J Mol Cell Cardiol 1999, 31(1):193-202.
70. Brennan J.P., Wait R., Begum S., Bell J.R., Dunn M.J., Eaton P. Detection and mapping of widespread intermolecular protein disulfide formation during cardiac oxidative stress using proteomics with diagonal electrophoresis. J Biol Chem 2004, 279(40):41352-41360.
71. Forrester M.T., Hess D.T., Thompson J.W., Hultman R., Moseley M.A., Stamler J.S., et al. Site-specific analysis of protein S-acylation by resin-assisted capture. J Lipid Res 2011, 52(2):393-398.
72. Makmura L., Hamann M., Areopagita A., Furuta S., Munoz A., Momand J. Development of a sensitive assay to detect reversibly oxidized protein cysteine sulfhydryl groups. Antioxid Redox Signal 2001, 3(6):1105-1118.
73. Ungerstedt J., Du Y., Zhang H., Nair D., Holmgren A. In vivo redox state of Human thioredoxin and redox shift by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA). Free Radic Biol Med 2012, 53(11):2002-2007.
74. Cumming R.C. Analysis of global and specific changes in the disulfide proteome using redox two-dimensional polyacrylamide gel electrophoresis. Methods Mol Biol 2008, 476:165-179.
75. Lindahl M., Mata-Cabana A., Kieselbach T. The disulfide proteome and other reactive cysteine proteomes: analysis and functional significance. Antioxid Redox Signal 2011, 14(12):2581-2642.
76. Dormeyer W., Ott M., Schnölzer M. Probing lysine acetylation in proteins. Mol Cell Proteomics 2005, 4(9):1226-1239.
77. Lee T.Y., Chen Y.J., Lu C.T., Ching W.C., Teng Y.C., Huang H.D. dbSNO: a database of cysteine S-nitrosylation. Bioinformatics 2012, 28(17):2293-2295.
78. Sun M.A., Wang Y., Cheng H., Zhang Q., Ge W., Guo D. RedoxDB - a curated database for experimentally verified protein oxidative modification. Bioinformatics 2012, 28(19):2551-2552.
79. Thelen J.J., Miernyk J.A. The proteomic future: where mass spectrometry should be taking us. Biochem J 2012, 444(2):169-181.
80. Zhang D.D., Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 2003, 23:8137-8151.
81. Hirota K., Minoru M., Satoshi I., Akira N., Kenjiro M., Junji Y. AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc Natl Acad Sci USA 1997, 94:3633.
82. Matthews J.R., Wakasugi N., Virelizier J.L., Yodoi J., Hay R.T. Thioredoxin regulates the DNA binding activity of NF-κB by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 1992, 20:3821.
83. Gulshan K., Lee S.S., Moye-Rowley W.S. Differential oxidant tolerance determined by the key transcription factor Yap1 is controlled by levels of the Yap1-binding protein, Ybp1. J Biol Chem 2011, 286(39):34071-34081.
84. 2 receptor and redox-transducer in gene activation. Cell 2002, 111:471-481.
85. Hofmann B., Hecht H.-J., Flohe L. Peroxiredoxins. Biol Chem 2002, 383:347-364.
86. Lee W., Choi K.S., Riddell J., Ip C., Ghosh D., Park J.H., et al. Human peroxiredoxin 1 and 2 are not duplicate proteins: the unique presence of CYS83 in Prx1 underscores the structural and functional differences between Prx1 and Prx2. J Biol Chem 2007, 282:22011-22022.
87. Rainwater R., Parks D., Anderson M.E., Tegtmeyer P., Mann K. Role of cysteine residues in regulation of p53 function. Mol Cell Biol 1995, 15:3892-3903.
88. Shackelford R.E., Heinloth A.N., Heard S.C., Paules R.S. Cellular and molecular targets of protein S-glutathiolation. Antioxid Redox Signal 2005, 7:940-950.