Site-Specific Proteomic Mapping Identifies Selectively Modified Regulatory Cysteine Residues in Functionally Distinct Protein Networks

Chemistry and Biology

Volumn 22, Issue 7, 2015, Pages 965-975

  Gould, Neal S ^a   Evans, Perry ^a   Martínez Acedo, Pablo ^b   Marino, Stefano M ^c   Gladyshev, Vadim N ^d   Carroll, Kate S ^b   Ischiropoulos, Harry ^a,e  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c AKDENIZ UNIVERSITY   (Turkey)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; PROTEOME;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MOUSE; NITROSYLATION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEOMICS; REDUCTION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; HUMAN; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; PEPTIDE MAPPING; PROCEDURES; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; ANIMALS; CYSTEINE; HUMANS; MASS SPECTROMETRY; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE MAPPING; PROTEIN INTERACTION MAPS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS;

EID: 84937731185     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2015.06.010     Document Type: Article

References (44)

1. J. Alegre-Cebollada, P. Kosuri, D. Giganti, E. Eckels, J.A. Rivas-Pardo, N. Hamdani, C.M. Warren, R.J. Solaro, W.A. Linke, and J.M. Fernández S-glutathionylation of cryptic cysteines enhances titin elasticity by blocking protein folding Cell 156 2014 1235 1246
2. M. Benhar, J.W. Thompson, M.A. Moseley, and J.S. Stamler Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach Biochemistry 49 2010 6963 6969
3. N. Brandes, S. Schmitt, and U. Jakob Thiol-based redox switches in eukaryotic proteins Antioxid. Redox Signal. 11 2009 997 1014
4. P.J. Britto, L. Knipling, and J. Wolff The local electrostatic environment determines cysteine reactivity of tubulin J. Biol. Chem. 277 2002 29018 29027
5. E.T. Chouchani, C. Methner, S.M. Nadtochiy, A. Logan, V.R. Pell, S. Ding, A.M. James, H.M. Cochemé, J. Reinhold, K.S. Lilley, and et al. Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I Nat. Med. 19 2013 753 759
6. M.E. Conway, L.B. Poole, and S.M. Hutson Roles for cysteine residues in the regulatory CXXC motif of human mitochondrial branched chain aminotransferase enzyme Biochemistry 43 2004 7356 7364
7. I. Dalle-Donne, R. Rossi, D. Giustarini, R. Colombo, and A. Milzani S-glutathionylation in protein redox regulation Free Radic. Biol. Med. 43 2007 883 898
8. J.M. Denu, and K.G. Tanner Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation Biochemistry 37 1998 5633 5642
9. P.-T. Doulias, J.L. Greene, T.M. Greco, M. Tenopoulou, S.H. Seeholzer, R.L. Dunbrack, and H. Ischiropoulos Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation Proc. Natl. Acad. Sci. USA 107 2010 16958 16963
10. P.T. Doulias, K. Raju, J.L. Greene, M. Tenopoulou, and H. Ischiropoulos Mass spectrometry-based identification of S-nitrosocysteine in vivo using organic mercury assisted enrichment Methods 62 2013 165 170
11. P.T. Doulias, M. Tenopoulou, J.L. Greene, K. Raju, and H. Ischiropoulos Nitric oxide regulates mitochondrial fatty acid metabolism through reversible protein S-nitrosylation Sci. Signal. 6 2013 rs1
12. T. Finkel Signal transduction by reactive oxygen species J. Cell Biol. 194 2011 7 15
13. B. Groitl, and U. Jakob Thiol-based redox switches Biochim. Biophys. Acta 1844 2014 1335 1343
14. M. Hagel, D. Niu, T. St Martin, M.P. Sheets, L. Qiao, H. Bernard, R.M. Karp, Z. Zhu, M.T. Labenski, P. Chaturvedi, and et al. Selective irreversible inhibition of a protease by targeting a noncatalytic cysteine Nat. Chem. Biol. 7 2011 22 24
15. Y. Hamnell-Pamment, C. Lind, C. Palmberg, T. Bergman, and I.A. Cotgreave Determination of site-specificity of S-glutathionylated cellular proteins Biochem. Biophys. Res. Commun. 332 2005 362 369
16. R.E. Hansen, D. Roth, and J.R. Winther Quantifying the global cellular thiol-disulfide status Proc. Natl. Acad. Sci. USA 106 2009 422 427
17. E.L. Huttlin, M.P. Jedrychowski, J.E. Elias, T. Goswami, R. Rad, S.A. Beausoleil, J. Villen, W. Haas, M.E. Sowa, and S.P. Gygi A tissue-specific atlas of mouse protein phosphorylation and expression Cell 143 2010 1174 1189
18. R. Karisch, M. Fernandez, P. Taylor, C. Virtanen, J.R. St-Germain, L.L. Jin, I.S. Harris, J. Mori, T.W. Mak, Y.A. Senis, and et al. Global proteomic assessment of the classical protein-tyrosine phosphatome and "Redoxome" Cell 146 2011 826 840
19. T. Kislinger, B. Cox, A. Kannan, C. Chung, P. Hu, A. Ignatchenko, M.S. Scott, A.O. Gramolini, Q. Morris, M.T. Hallett, and et al. Global survey of organ and organelle protein expression in mouse: combined proteomic and transcriptomic profiling Cell 125 2006 173 186
20. P. Klatt, E.P. Molina, and S. Lamas Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation J. Biol. Chem. 274 1999 15857 15864
21. M. Kruger, M. Moser, S. Ussar, I. Thievessen, C.A. Luber, F. Forner, S. Schmidt, S. Zanivan, R. Fassler, and M. Mann SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function Cell 134 2008 353 364
22. J.C. Lim, J.M. Gruschus, G. Kim, B.S. Berlett, N. Tjandra, and R.L. Levine A low pKa cysteine at the active site of mouse methionine sulfoxide reductase A J. Biol. Chem. 287 2012 25596 25601
23. M.E. Linder, and R.J. Deschenes New insights into the mechanisms of protein palmitoylation Biochemistry 42 2003 4311 4320
24. S.M. Marino, and V.N. Gladyshev Cysteine function governs its conservation and degeneration and restricts its utilization on protein surfaces J. Mol. Biol. 404 2010 902 916
25. S.M. Marino, and V.N. Gladyshev Structural analysis of cysteine S-nitrosylation: a modified acid-based motif and the emerging role of trans-nitrosylation J. Mol. Biol. 395 2010 844 859
26. S.M. Marino, and V.N. Gladyshev Analysis and functional prediction of reactive cysteine residues J. Biol. Chem. 287 2012 4419 4425
27. B.R. Martin, C. Wang, A. Adibekian, S.E. Tully, and B.F. Cravatt Global profiling of dynamic protein palmitoylation Nat. Methods 9 2012 84 89
28. P. Martínez-Acedo, V. Gupta, and K.S. Carroll Proteomic analysis of peptides tagged with dimedone and related probes J. Mass Spectrom. 49 2014 257 265
29. A. Martínez-Ruiz, and S. Lamas Signalling by NO-induced protein S-nitrosylation and S-glutathionylation: convergences and divergences Cardiovasc. Res. 75 2007 220 228
30. P. Mertins, J.W. Qiao, J. Patel, N.D. Udeshi, K.R. Clauser, D.R. Mani, M.W. Burgess, M.A. Gillette, J.D. Jaffe, and S.A. Carr Integrated proteomic analysis of post-translational modifications by serial enrichment Nat. Methods 10 2013 634 637
31. D.A. Mitchell, and M.A. Marletta Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine Nat. Chem. Biol. 1 2005 154 158
32. N.J. Pace, and E. Weerapana Zinc-binding cysteines: diverse functions and structural motifs Biomolecules 4 2014 419 434
33. L.A. Passmore, and D. Barford Getting into position: the catalytic mechanisms of protein ubiquitylation Biochem. J. 379 2004 513 525
34. C.E. Paulsen, T.H. Truong, F.J. Garcia, A. Homann, V. Gupta, S.E. Leonard, and K.S. Carroll Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity Nat. Chem. Biol. 8 2012 57 64
35. F.R. Salsbury, S.T. Knutson, L.B. Poole, and J.S. Fetrow Functional site profiling and electrostatic analysis of cysteines modifiable to cysteine sulfenic acid Protein Sci. 17 2008 299 312
36. B. Schmidt, L. Ho, and P.J. Hogg Allosteric disulfide bonds Biochemistry 45 2006 7429 7433
37. N. Sen, B.D. Paul, M.M. Gadalla, A.K. Mustafa, T. Sen, R. Xu, S. Kim, and S.H. Snyder Hydrogen sulfide-linked sulfhydration of NF-kB mediates its antiapoptotic actions Mol. Cell 45 2012 13 24
38. D. Seth, A. Hausladen, Y.J. Wang, and J.S. Stamler Endogenous protein S-nitrosylation in E. coli: regulation by OxyR Science 336 2012 470 473
39. Y.Y. Shi, W. Tang, S.F. Hao, and C.C. Wang Contributions of cysteine residues in Zn2 to zinc fingers and thiol-disulfide oxidoreductase activities of chaperone DnaJ Biochemistry 44 2005 1683 1689
40. B.C. Smith, and M.A. Marletta Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling Curr. Opin. Chem. Biol. 16 2012 498 506
41. M.D. Stewart, and T.I. Igumenova Reactive cysteine in the structural Zn(2+) site of the C1B domain from PKCalpha Biochemistry 51 2012 7263 7277
42. D.M. Townsend, Y. Manevich, L. He, S. Hutchens, C.J. Pazoles, and K.D. Tew Novel role for glutathione S-transferase pi. Regulator of protein S-Glutathionylation following oxidative and nitrosative stress J. Biol. Chem. 284 2009 436 445
43. E. Weerapana, C. Wang, G.M. Simon, F. Richter, S. Khare, M.B. Dillon, D.A. Bachovchin, K. Mowen, D. Baker, and B.F. Cravatt Quantitative reactivity profiling predicts functional cysteines in proteomes Nature 468 2010 790 795
44. Z.A. Wood, E. Schröder, J. Robin Harris, and L.B. Poole Structure, mechanism and regulation of peroxiredoxins Trends Biochem. Sci. 28 2003 32 40