The oxidized thiol proteome in fission yeast-Optimization of an ICAT-based method to identify H 2O 2-oxidized proteins

Journal of Proteomics

Volumn 74, Issue 11, 2011, Pages 2476-2486

  García Santamarina, Sarela ^a   Boronat, Susanna ^a   Espadas, Guadalupe ^b   Ayté, José ^a   Molina, Henrik ^b   Hidalgo, Elena ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

Dimethyl labeling; Disulfides; H 2O 2; ICAT; Pap1; Peroxiredoxin; Pombe

Indexed keywords

ACID; ANTIOXIDANT; CHAPERONE; CYSTEINE; DISULFIDE; ENZYME; FUNGAL PROTEIN; HYDROGEN PEROXIDE; IODOACETAMIDE; ISOTOPE; PEROXIREDOXIN; PROTEIN TPX1; PROTEOME; REDOX EFFECTOR FACTOR 1; THIOL; THIOL GROUP; THIOL REAGENT; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAP1; UNCLASSIFIED DRUG;

AFFINITY LABELING; ARTICLE; CHEMICAL LABELING; CONCENTRATION (PARAMETERS); CYTOLYSIS; DISULFIDE BOND; FREEZING; GEL ELECTROPHORESIS; IN VIVO STUDY; ISOTOPE LABELING; KINETICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; PROTEIN TARGETING; REDOX STRESS; SCHIZOSACCHAROMYCES POMBE; TOXICITY; YEAST;

AMINO ACIDS, SULFUR; CALIBRATION; CHROMATOGRAPHY, LIQUID; HYDROGEN PEROXIDE; ISOTOPE LABELING; MASS SPECTROMETRY; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; REACTIVE OXYGEN SPECIES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SULFHYDRYL COMPOUNDS;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 80054858298     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.05.030     Document Type: Article

References (47)

1. Nystrom T. Role of oxidative carbonylation in protein quality control and senescence. EMBO J 2005, 24:1311-1317.
2. Madian AG, Regnier FE. Proteomic identification of carbonylated proteins and their oxidation sites. J Proteome Res.9:3766-80.
3. Souza J.M., Peluffo G., Radi R. Protein tyrosine nitration-functional alteration or just a biomarker?. Free Radic Biol Med 2008, 45:357-366.
4. Butterfield D.A., Sultana R. Identification of 3-nitrotyrosine-modified brain proteins by redox proteomics. Methods Enzymol 2008, 440:295-308.
5. Veal E.A., Day A.M., Morgan B.A. Hydrogen peroxide sensing and signaling. Mol Cell 2007, 26:1-14.
6. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol 2003, 15:247-254.
7. Winterbourn C.C. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 2008, 4:278-286.
8. Paget M.S., Buttner M.J. Thiol-based regulatory switches. Annu Rev Genet 2003, 37:91-121.
9. Winterbourn C.C., Hampton M.B. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 2008, 45:549-561.
10. Janssen-Heininger Y.M., Mossman B.T., Heintz N.H., Forman H.J., Kalyanaraman B., Finkel T., et al. Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic Biol Med 2008, 45:1-17.
11. Ma L.H., Takanishi C.L., Wood M.J. Molecular mechanism of oxidative stress perception by the Orp1 protein. J Biol Chem 2007, 282:31429-31436.
12. Choi H., Kim S., Mukhopadhyay P., Cho S., Woo J., Storz G., et al. Structural basis of the redox switch in the OxyR transcription factor. Cell 2001, 105:103-113.
13. Gladysheva T., Liu J., Rosen B.P. His-8 lowers the pKa of the essential Cys-12 residue of the ArsC arsenate reductase of plasmid R773. J Biol Chem 1996, 271:33256-33260.
14. Klomsiri C, Karplus PA, Poole LB. Cysteine-based redox switches in enzymes. Antioxid Redox Signal.14:1065-77.
15. Schafer F.Q., Buettner G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 2001, 30:1191-1212.
16. Ritz D., Beckwith J. Roles of thiol-redox pathways in bacteria. Annu Rev Microbiol 2001, 55:21-48.
17. Kemp M., Go Y.M., Jones D.P. Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology. Free Radic Biol Med 2008, 44:921-937.
18. Berndt C., Lillig C.H., Holmgren A. Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am J Physiol Heart Circ Physiol 2007, 292:H1227-H1236.
19. Carmel-Harel O., Storz G. Roles of The Glutath. Annu Rev Microbiol 2000, 54:439-461.
20. Holmgren A., Lu J. Thioredoxin and thioredoxin reductase: current research with special reference to human disease. Biochem Biophys Res Commun 2010, 396:120-124.
21. Meyer Y., Buchanan B.B., Vignols F., Reichheld J.P. Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 2009, 43:335-367.
22. Baty J.W., Hampton M.B., Winterbourn C.C. Proteomic detection of hydrogen peroxide-sensitive thiol proteins in Jurkat cells. Biochem J 2005, 389:785-795.
23. Le Moan N., Clement G., Le Maout S., Tacnet F., Toledano M.B. The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. J Biol Chem 2006, 281:10420-10430.
24. Ghezzi P., Bonetto V. Redox proteomics: identification of oxidatively modified proteins. Proteomics 2003, 3:1145-1153.
25. Le Moan N., Tacnet F., Toledano M.B. Protein-thiol oxidation, from single proteins to proteome-wide analyses. Methods Mol Biol 2009, 476:175-192.
26. Chiappetta G, Ndiaye S, Igbaria A, Kumar C, Vinh J, Toledano MB. Proteome screens for Cys residues oxidation: the redoxome. Methods Enzymol.473:199-216.
27. Törnvall U. Pinpointing oxidative modifications in proteins-recent advances in analytical methods. Anal Methods 2010, 2:1638-1650.
28. 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, 3:1228-1233.
29. 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.
30. Hagglund P., Bunkenborg J., Maeda K., Svensson B. Identification of thioredoxin disulfide targets using a quantitative proteomics approach based on isotope-coded affinity tags. J Proteome Res 2008, 7:5270-5276.
31. Fu C., Wu C., Liu T., Ago T., Zhai P., Sadoshima J., et al. Elucidation of thioredoxin target protein networks in mouse. Mol Cell Proteomics 2009, 8:1674-1687.
32. Vivancos A.P., Jara M., Zuin A., Sanso M., Hidalgo E. Oxidative stress in Schizosaccharomyces pombe: different H2O2 levels, different response pathways. Mol Genet Genomics 2006, 276:495-502.
33. Veal E.A., Findlay V.J., Day A.M., Bozonet S.M., Evans J.M., Quinn J., et al. A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase. Mol Cell 2004, 15:129-139.
34. Vivancos A.P., Castillo E.A., Biteau B., Nicot C., Ayte J., Toledano M.B., et al. A cysteine-sulfinic acid in peroxiredoxin regulates H2O2-sensing by the antioxidant Pap1 pathway. Proc Natl Acad Sci U S A 2005, 102:8875-8880.
35. Bozonet S.M., Findlay V.J., Day A.M., Cameron J., Veal E.A., Morgan B.A. Oxidation of a eukaryotic 2-Cys peroxiredoxin is a molecular switch controlling the transcriptional response to increasing levels of hydrogen peroxide. J Biol Chem 2005, 280:23319-23327.
36. Kudo N., Taoka H., Toda T., Yoshida M., Horinouchi S. A novel nuclear export signal sensitive to oxidative stress in the fission yeast transcription factor Pap1. J Biol Chem 1999, 274:15151-15158.
37. Castillo E.A., Ayte J., Chiva C., Moldon A., Carrascal M., Abian J., et al. Diethylmaleate activates the transcription factor Pap1 by covalent modification of critical cysteine residues. Mol Microbiol 2002, 45:243-254.
38. Castillo E.A., Vivancos A.P., Jones N., Ayte J., Hidalgo E. Schizosaccharomyces pombe cells lacking the Ran-binding protein Hba1 show a multidrug resistance phenotype due to constitutive nuclear accumulation of Pap1. J Biol Chem 2003, 278:40565-40572.
39. Moreno S., Klar A., Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 1991, 194:795-823.
40. Jara M., Vivancos A.P., Calvo I.A., Moldon A., Sanso M., Hidalgo E. The peroxiredoxin Tpx1 is essential as a H2O2 scavenger during aerobic growth in fission yeast. Mol Biol Cell 2007, 18:2288-2295.
41. Olsen J.V., de Godoy L.M., Li G., Macek B., Mortensen P., Pesch R., et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 2005, 4:2010-2021.
42. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008, 26:1367-1372.
43. Hsu J.L., Huang S.Y., Chow N.H., Chen S.H. Stable-isotope dimethyl labeling for quantitative proteomics. Anal Chem 2003, 75:6843-6852.
44. Boersema P.J., Raijmakers R., Lemeer S., Mohammed S., Heck A.J. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 2009, 4:484-494.
45. Rappsilber J., Mann M., Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2007, 2:1896-1906.
46. Wisniewski J.R., Zougman A., Mann M. Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J Proteome Res 2009, 8:5674-5678.
47. Vivancos A.P., Castillo E.A., Jones N., Ayte J., Hidalgo E. Activation of the redox sensor Pap1 by hydrogen peroxide requires modulation of the intracellular oxidant concentration. Mol Microbiol 2004, 52:1427-1435.