Site-specific mapping and quantification of protein S-sulphenylation in cells

Nature Communications

Volumn 5, Issue , 2014, Pages

  Yang, Jing ^a,b   Gupta, Vinayak ^c   Carroll, Kate S ^c   Liebler, Daniel C ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; EPIDERMAL GROWTH FACTOR; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN; SIRTUIN 6; SOLVENT; THIOL; HIF1A PROTEIN, HUMAN; SIRT6 PROTEIN, HUMAN; SIRTUIN; SULFENIC ACID DERIVATIVE;

HYDROGEN PEROXIDE; MAPPING; PROTEIN; PROTEOMICS; REDOX CONDITIONS;

ARTICLE; BIOINFORMATICS; CELL LINE; CHEMICAL MODIFICATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; OXIDATION REDUCTION REACTION; PEPTIDE MAPPING; PROTEIN ACETYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SULFENYLATION; UBIQUITINATION; WORKFLOW; ACETYLATION; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN PROCESSING; TUMOR CELL LINE;

ACETYLATION; CELL LINE, TUMOR; CYSTEINE; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; HYDROGEN PEROXIDE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MOLECULAR SEQUENCE ANNOTATION; OXIDATION-REDUCTION; PEPTIDE MAPPING; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIRTUINS; SULFENIC ACIDS; UBIQUITINATION;

EID: 84907339922     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5776     Document Type: Article

References (54)

1. Paulsen, C. E. & Carroll, K. S. Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem. Rev. 113, 4633-4679 (2013).
2. Leonard, S. E. & Carroll, K. S. Chemical 'omics' approaches for understanding protein cysteine oxidation in biology. Curr. Opin. Chem. Biol. 15, 88-102 (2011).
3. Paulsen, C. E. et al. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat. Chem. Biol. 8, 57-64 (2012).
4. Kulathu, Y. et al. Regulation of A20 and other OTU deubiquitinases by reversible oxidation. Nat. Commun. 4, 1569 (2013).
5. 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. 4, 783-799 (2009).
6. Kim, H. Y., Tallman, K. A., Liebler, D. C. & Porter, N. A. An azido-biotin reagent for use in the isolation of protein adducts of lipid-derived electrophiles by streptavidin catch and photorelease. Mol. Cell. Proteomics 8, 2080-2089 (2009).
7. Weerapana, E. et al. Quantitative reactivity profiling predicts functional cysteines in proteomes. Nature 468, 790-795 (2010).
8. Wang, C., Weerapana, E., Blewett, M. M. & Cravatt, B. F. A chemoproteomic platform to quantitatively map targets of lipid-derived electrophiles. Nat. Methods 11, 79-85 (2014).
9. Szychowski, J. et al. Cleavable biotin probes for labeling of biomolecules via azide-alkyne cycloaddition. J. Am. Chem. Soc. 132, 18351-18360 (2010).
10. Qian, Y. et al. An isotopically tagged azobenzene-based cleavable linker for quantitative proteomics. Chembiochem 14, 1410-1414 (2013).
11. Zheng, T., Jiang, H. & Wu, P. Single-stranded DNA as a cleavable linker for bioorthogonal click chemistry-based proteomics. Bioconjug. Chem. 24, 859-864 (2013).
12. Presolski, S. I., Hong, V., Cho, S. H. & Finn, M. G. Tailored ligand acceleration of the Cu-catalyzed azide-alkyne cycloaddition reaction: practical and mechanistic implications. J. Am. Chem. Soc. 132, 14570-14576 (2010).
13. Olsen, J. V. et al. Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 4, 709-712 (2007).
14. Levsen, K. et al. Structure elucidation of phase II metabolites by tandem mass spectrometry: an overview. J. Chromatogr. A 1067, 55-72 (2005).
15. Schilling, B. et al. Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in skyline: application to protein acetylation and phosphorylation. Mol. Cell. Proteomics 11, 202-214 (2012).
16. Veal, E. A., Day, A. M. & Morgan, B. A. Hydrogen peroxide sensing and signaling. Mol. Cell 26, 1-14 (2007).
17. Hohoff, C., Borchers, T., Rustow, B., Spener, F. & van Tilbeurgh, H. Expression, purification, and crystal structure determination of recombinant human epidermal-type fatty acid binding protein. Biochemistry 38, 12229-12239 (1999).
18. Mostoslavsky, R. et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124, 315-329 (2006).
19. Sebastian, C. et al. The histone deacetylase SIRT6 is a tumor suppressor that controls cancer metabolism. Cell 151, 1185-1199 (2012).
20. Toiber, D. et al. SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling. Mol. Cell 51, 454-468 (2013).
21. Kugel, S. & Mostoslavsky, R. Chromatin and beyond: the multitasking roles for SIRT6. Trends Biochem. Sci. 39, 72-81 (2014).
22. Zhong, L. et al. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 140, 280-293 (2010).
23. Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
24. Ushio-Fukai, M. Localizing NADPH oxidase-derived ROS. Sci. STKE 2006, re8 (2006).
25. Delaunay, A., Pflieger, D., Barrault, M. B., Vinh, J. & Toledano, M. B. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111, 471-481 (2002).
26. Lee, J. G., Baek, K., Soetandyo, N. & Ye, Y. Reversible inactivation of deubiquitinases by reactive oxygen species in vitro and in cells. Nat. Commun. 4, 1568 (2013).
27. Anastasiou, D. et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 334, 1278-1283 (2011).
28. Pappenberger, G. et al. Structure of the human fatty acid synthase KS-MAT didomain as a framework for inhibitor design. J. Mol. Biol. 397, 508-519 (2010).
29. Petersen, B., Petersen, T. N., Andersen, P., Nielsen, M. & Lundegaard, C. A generic method for assignment of reliability scores applied to solvent accessibility predictions. BMC Struct. Biol. 9, 51 (2009).
30. Seo, Y. H. & Carroll, K. S. Quantification of protein sulfenic acid modifications using isotope-coded dimedone and iododimedone. Angew. Chem. Int. Ed. Engl. 50, 1342-1345 (2011).
31. Doulias, P. T., Tenopoulou, M., Greene, J. L., Raju, K. & Ischiropoulos, H. Nitric oxide regulates mitochondrial fatty acid metabolism through reversible protein S-nitrosylation. Sci. Signal. 6, rs1 (2013).
32. Witt, A. C. et al. Cysteine pKa depression by a protonated glutamic acid in human DJ-1. Biochemistry 47, 7430-7440 (2008).
33. Gupta, V. & Carroll, K. S. Sulfenic acid chemistry, detection and cellular lifetime. Biochim. Biophys. Acta 1840, 847-875 (2014).
34. van Montfort, R. L., Congreve, M., Tisi, D., Carr, R. & Jhoti, H. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423, 773-777 (2003).
35. Rosenwasser, S. et al. Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment. Proc. Natl Acad. Sci. USA 111, 2740-2745 (2014).
36. Brandes, N. et al. Time line of redox events in aging postmitotic cells. Elife (Cambridge) 2, e00306 (2013).
37. Su, D. et al. Proteomic identification and quantification of S-glutathionylation in mouse macrophages using resin-assisted enrichment and isobaric labeling. Free. Radic. Biol. Med. 67, 460-470 (2014).
38. Klamt, F. et al. Oxidant-induced apoptosis is mediated by oxidation of the actin-regulatory protein cofilin. Nat. Cell Biol. 11, 1241-1246 (2009).
39. Juarez, J. C. et al. Superoxide dismutase 1 (SOD1) is essential for H2O2-mediated oxidation and inactivation of phosphatases in growth factor signaling. Proc. Natl Acad. Sci. USA 105, 7147-7152 (2008).
40. Woo, H. A. et al. Inactivation of peroxiredoxin I by phosphorylation allows localized H(2)O(2) accumulation for cell signaling. Cell 140, 517-528 (2010).
41. Hwang, J. W., Yao, H., Caito, S., Sundar, I. K. & Rahman, I. Redox regulation of SIRT1 in inflammation and cellular senescence. Free. Radic. Biol. Med. 61C, 95-110 (2013).
42. Cotto-Rios, X. M., Bekes, M., Chapman, J., Ueberheide, B. & Huang, T. T. Deubiquitinases as a signaling target of oxidative stress. Cell Rep. 2, 1475-1484 (2012).
43. Simon, G. M., Niphakis, M. J. & Cravatt, B. F. Determining target engagement in living systems. Nat. Chem. Biol. 9, 200-205 (2013).
44. Truong, T. H. & Carroll, K. S. Bioorthogonal chemical reporters for analyzing protein sulfenylation in cells. Curr. Protoc. Chem. Biol. 4, 101-122 (2012).
45. Depuydt, M. et al. A periplasmic reducing system protects single cysteine residues from oxidation. Science 326, 1109-1111 (2009).
46. Reddie, K. G., Seo, Y. H., Muse Iii, W. B., Leonard, S. E. & Carroll, K. S. A chemical approach for detecting sulfenic acid-modified proteins in living cells. Mol. Biosyst. 4, 521-531 (2008).
47. Hulce, J. J., Cognetta, A. B., Niphakis, M. J., Tully, S. E. & Cravatt, B. F. Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells. Nat. Methods 10, 259-264 (2013).
48. Alfaro, J. F. et al. Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc. Natl Acad. Sci. USA 109, 7280-7285 (2012).
49. Dasari, S. et al. TagRecon: high-throughput mutation identification through sequence tagging. J. Proteome Res. 9, 1716-1726 (2010).
50. Ma, Z. Q. et al. IDPicker 2.0: Improved protein assembly with high discrimination peptide identification filtering. J. Proteome Res. 8, 3872-3881 (2009).
51. Tabb, D. L., Friedman, D. B. & Ham, A. J. Verification of automated peptide identifications from proteomic tandem mass spectra. Nat. Protoc. 1, 2213-2222 (2006).
52. MacLean, B. et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968 (2010).
53. Chambers, M. C. et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 30, 918-920 (2012).
54. O'Shea, J. P. et al. pLogo: a probabilistic approach to visualizing sequence motifs. Nat. Methods 10, 1211-1212 (2013).