Artifactual sulfation of silver-stained proteins: Implications for the assignment of phosphorylation and sulfation sites

Molecular and Cellular Proteomics

Volumn 8, Issue 3, 2009, Pages 506-518

  Gharib, Marlene ^a,b   Marcantonio, Maria ^a,b   Lehmann, Sylvia G ^a   Courcelles, Mathieu ^a,b   Meloche, Sylvain ^a,b   Verreault, Alain ^a,b   Thibault, Pierre ^a,b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANAZOLENE SODIUM; SERINE; SODIUM THIOSULFATE; THREONINE; TYROSINE;

ARTICLE; ARTIFACT; BACTERIAL CELL; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; SILVER STAINING; SULFATION;

AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; ARTIFACTS; BACTERIAL PROTEINS; CRICETINAE; ESCHERICHIA COLI; HUMANS; HYDROXYLATION; MITOGEN-ACTIVATED PROTEIN KINASE 3; MOLECULAR SEQUENCE DATA; PEPTIDES; PHOSPHOPYRUVATE HYDRATASE; PHOSPHORYLATION; PROTEINS; SACCHAROMYCES CEREVISIAE; SILVER STAINING; SULFATES; THIOSULFATES;

ESCHERICHIA COLI;

EID: 63049086405     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M800327-MCP200     Document Type: Article

References (50)

1. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site,specific phosphorylation dynamics in signaling networks. Cell 127, 635-648
2. Rikova, K., Guo, A., Zeng, Q., Possemato, A., Yu, J., Haack, H., Nardone, J., Lee, K., Reeves, C., Li, Y., Hu, Y., Tan, Z., Stokes, M., Sullivan, L., Mitchell, J., Wetzel, R., Macneill, J., Ren, J. M., Yuan, J., Bakalarski, C. E., Villen, J., Komhauser, J. M., Smith, B., Li, D., Zhou, X., Gygi, S. P., Gu, T. L., Polakiewicz, R. D., Rush,J., and Comb, M. J. (2007) Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131, 1190-1203
3. Villen, J., Beausoleil, S. A., Gerber, S. A., and Gygi, S. P. (2007) Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. U. S. A. 104, 1488-1493
4. Walsh, C. T. (2006) Posttranslational Modification of Proteins: Expanding Nature's Inventory, p. 33, Roberts and Co. Publishers, Greenwood Village, CO
5. Zolnierowicz, S., and Bollen, M. (2000) Protein phosphorylation and protein phosphatases. De Panne, Belgium, September 19-24, 1999. EMBO J. 19, 483-488
6. Mann, M., Ong, S. E., Gronborg, M., Steen, H., Jensen, O. N., and Pandey, A. (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 20, 261-268
7. Bonenfant, D., Schmelzle, T., Jacinto, E., Crespo, J. L., Mini, T., Hall, M. N., and Jenoe, P. (2003) Quantitation of changes in protein phosphorylation: a simple method based on stable isotope labeling and mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 100, 880-885
8. McLachlin, D. T., and Chait, B. T. (2001) Analysis of phosphorylated proteins and peptides by mass spectrometry. Curr. Opin. Chem. Biol. 5, 591-602
9. Hunter, T. (2000) Signaling - 2000 and beyond. Cell 100, 113-127
10. Strott, C. A. (2002) Sulfonation and molecular action. Endocr. Rev. 23, 703-732
11. Moore, K. L. (2003) The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278, 24243-24246
12. Monigatti, F., Hekking, B., and Steen, H. (2006) Protein sulfation analysis - a primer. Biochim. Biophys. Acta 1764, 1904-1913
13. Yu, Y., Hoffhines, A. J., Moore, K. L., and Leary, J. A. (2007) Determination of the sites of tyrosine O-sulfation in peptides and proteins. Nat. Methods 4, 583-588
14. Kehoe, J. W., and Bertozzi, C. R. (2000) Tyrosine sulfation: a modulator of extracellular protein-protein interactions. Chem. Biol. 7, R57-R61
15. Medzihradszky, K. F., Darula, Z., Perison, E., Fainzilber, M., Chalkley, R. J., Ball, H., Greenbaum, D., Bogyo, M., Tyson, D. R., Bradshaw, R. A., and Burlingame, A. L. (2004) 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 3, 429-440
16. Witze, E. S., Old, W. M., Resing, K. A., and Ahn, N. G. (2007) Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 4, 798-806
17. Baldwin, M. A. (2004) Protein identification by mass spectrometry: issues to be considered. Mol. Cell. Proteomics 3, 1-9
18. Mann, M., and Jensen, O. N. (2003) Proteomic analysis of post-translational modifications. Nat. Biotechnol. 211, 255-261
19. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860
20. Graham, D. R., Elliott, S. T., and Van Eyk, J. E. (2005) Broad-based proteomic strategies: a practical guide to proteomics and functional screening. J. Physiol. 563, 1-9
21. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
22. Richert, S., Luche, S., Chevallet, M., Van Dorsselaer, A., Leize-Wagner, E., and Rabilloud, T. (2004) About the mechanism of interference of silver staining with peptide mass spectrometry. Proteomics 4, 909-916
23. Metz, B., Kersten, G. F., Baart, G. J., & Jong, A., Meiring, H., ten Hove, J., van Steenbergen, M. J., Hennink, W. E., Crommelin, D. J., and Jiskoot, W. (2006) Identification of formaldehyde-induced modifications in proteins: reactions with insulin. Bioconjug. Chem. 17, 815-822
24. Oses-Prieto, J. A., Zhang, X., and Burlingame, A. L. (2007) Formation of ε-formyllysine on silver-stained proteins: implications for assignment of isobaric dimethylation sites by tandem mass spectrometry. Mol. Cell. Proteomics 6, 181-192
25. Jaitly, G., Bonneil, E., Jaitly, N., Eng, K., Pomiès, C., and Thibault, P. (2007) Comprehensive profiling of unlabeled peptide ions from large-scale proteomics experiments using one and two dimensional nanoLC-MS/MS, in Proceedings of the 55th ASMS Conference on Mass Spectrometry, Indianapolis, June 3-7, 2007, Indianapolis, IN
26. Oda, Y., Nagasu, T., and Chait, B. T. (2001) Enrichment analysis of phosphorylated proteins as a tool for probing the phosphoproteome. Nat. Biotechnol. 19, 379-382
27. Thompson, A. J., Hart, S. R., Franz, C., Bamouin, K, Ridley, A., and Cramer, R. (2003) Characterization of protein phosphorylation by mass spectrometry using immobilized metal ion affinity chromatography with on-resin β-elimination and Michael addition. Anal. Chem. 75, 3232-3243
28. Greis, K. D., Hayes, B. K., Comer, F. I., Kirk, M., Barnes, S., Lowery, T. L., and Hart, G. W. (1996) Selective detection and site-analysis of O-GIc-NAc-modified glycopeptides by beta-elimination and tandem electrospray mass spectrometry. Anal. Biochem. 234, 38-49
29. Wells, L., Vosseller, K., Cole, R. N., Cronshaw, J. M., Matunis, M. J., and Hart, G. W. (2002) Mapping sites of O-GIcNAc: modification using affinity tags for serine and threonine post-translational modifications. Mol. Cell. Proteomics 1, 791-804
30. Chalmers, M. J., Kolch, W., Emmett, M. R., Marshall, A. G., and Mischak, H. (2004) Identification and analysis of phosphopeptides. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 803, 111-120
31. 2+ ions for their detection during peptide microsequencing. Biochem. J. 280, 261-265
32. Li, W., Backlund, P. S., Boykins, R. A., Wang, G., and Chen, H. C. (2003) Susceptibility of the hydroxyl groups in serine and threonine to β-elimination/Michael addition under commonly used moderately high-temperature conditions. Anal. Biochem. 323, 94-102
33. Chevallet, M., Luche, S., and Rabilloud, T. (2006) Silver staining of proteins in polyacrylamide gels. Nat. Protoc. 1, 1852-1858
34. Roux, P. P., and Blenis, J. (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68, 320-344
35. Butch, E. R., and Guan, K. L. (1996) Characterization of ERK1 activation site mutants and the effect on recognition by MEK1 and MEK2. J. Biol. Chem. 271, 4230-4235
36. Ballif, B. A., Roux, P. P., Gerber, S. A., MacKeigan, J. P., Blenis, J., and Gygi, S. P. (2005) Quantitative phosphorylation profiling of the ERK/ p90 ribosomal S6 kinase-signaling cassette and its targets, the tuberous sclerosis tumor suppressors. Proc. Natl. Acad. Sci. U. S. A. 102, 667-672
37. Lippmann, C., Lindschau, C., Vijgenboom, E., Schroder, W., Bosch, L., and Erdmann, V. A. (1993) Prokaryotic elongation factor Tu is phosphorylated in vivo. J. Biol. Chem. 268, 601-607
38. Gharahdaghi, F., Weinberg, C. R., Meagher, D. A., Imai, B. S., and Mische, S. M. (1999) Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 20, 601-605
39. Rabilloud, T. (1990) Mechanisms of protein silver staining in polyacrylamide gels: a 10-year synthesis. Electrophoresis 11, 785-794
40. Granvogl, B., Ploscher, M., and Eichacker, L. A. (2007) Sample preparation by in-gel digestion for mass spectrometry-based proteomics. Anal. Bioanal. Chem. 389, 991-1002
41. Patras, G., Qiao, G. G., and Solomon, D. H. (1999) On the mechanism of background silver staining during sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Electrophoresis 20, 2039-2045
42. Herrmann, W. A. (1986). Multiple bonds between transition metals and "bare" main group elements: links between inorganic solid state chemistry and organometallic chemistry. Angew. Chem. Int. Ed. Engl. 25, 56-76
43. Zhang, M., and Vogel, H. J. (1993) Determination of the side chain pKa values of the lysine residues in calmodulin. J. Biol. Chem. 268, 22420-22428
44. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190
45. Marcantonio, M., Trost, M., Courcelles, M., Desjardins, M., and Thibault, P. (2008) Combined enzymatic and data mining approaches for comprehensive phosphoproteome analyses: application to cell signaling events of interferon-γ-stimulated macrophages. Mol. Cell. Proteomics 7, 645-660
46. Reinders, J., and Sickmann, A. (2005) State-of-the-art in phosphoproteomics. Proteomics 5, 4052-4061
47. DeGnore, J. P., and Qin, J. (1998) Fragmentation of phosphopeptides in an ion trap mass spectrometer. J. Am. Soc. Mass Spectrom. 9, 1175-1188
48. Medzihradszky, K. F., Guan, S., Maltby, D. A., and Burlingame, A. L. (2007) Sulfopeptide fragmentation in electron-capture and electron-transfer dissociation. J. Am. Soc. Mass Spectrom. 18, 1617-1624
49. Nemeth-Cawley, J. F., Kamik, S., and Rouse, J. C. (2001) Analysis of sulfated peptides using positive electrospray ionization tandem mass spectrometry. J. Mass Spectrom. 36, 1301-1311
50. Syka, J. E., Coon, J. J., Schroeder, M. J., Shabanowitz, J., and Hunt, D. F. (2004) Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 101, 9528-9533