Phosphoproteomics: Searching for a needle in a haystack

Journal of Proteomics

Volumn 74, Issue 12, 2011, Pages 2786-2797

  Tichy, Ales ^a   Salovska, Barbora ^a   Rehulka, Pavel ^b   Klimentova, Jana ^b   Vavrova, Jirina ^a   Stulik, Jiri ^b   Hernychova, Lenka ^b  

^a UNIVERSITY OF DEFENCE   (Czech Republic)

^b UNIVERSITY OF DEFENCE   (Czech Republic)

Author keywords

MS MS; Phosphopeptide enrichment; Quantitative phosphoproteomics

Indexed keywords

AMINO ACID; CALCIUM PHOSPHATE; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; PHOSPHOPROTEOME; PROTEOME; TITANIUM DIOXIDE; TYROSINE; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; BINDING AFFINITY; BIOINFORMATICS; ELECTRON CAPTURE DETECTION; ELECTROSPRAY MASS SPECTROMETRY; HIGH THROUGHPUT SCREENING; HUMAN; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IMMUNOPRECIPITATION; LIMIT OF DETECTION; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METAL OXIDE AFFINITY CHROMATOGRAPHY; MOLECULE; PHOSPHOPROTEOMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEOMICS; QUANTITATIVE ANALYSIS; REVIEW; SENSITIVITY AND SPECIFICITY; STOICHIOMETRY; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL DIVISION; GENE EXPRESSION REGULATION; HUMANS; MASS SPECTROMETRY; PEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS;

EID: 81055140468     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.07.018     Document Type: Review

References (100)

1. Halada P. Metodické přístupy současné fosfoproteomoé analýzy. Chem Listy 2005, 99:922-929.
2. Graves J.D., Krebs E.G. Protein phosphorylation and signal transduction. Pharmacol Ther 1999, 82:111-121.
3. Manning G., Whyte D.B., Martinez R., et al. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
4. Venter J.C., Adams M.D., Myers E.W., et al. The sequence of the human genome. Science 2001, 9:1304-1351.
5. Reinders J., Sickmann A. State-of-the-art in phosphoproteomics. Proteomics 2005, 5:4052-4061.
6. Kaufmann H., Bailey J.E., Fussenegger M. Use of antibodies for detection of phosphorylated proteins separated by two-dimensional gel electrophoresis. Proteomics 2001, 1:194-199.
7. Clarke S.J., Khaliulin I., Das M., Parker J.E., et al. Inhibition of mitochondrial permeability transition pore opening by ischemic preconditioning is probably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation. Circ Res 2008, 102:1082-1090.
8. Eymann C., Becher D., Bernhardt J., Gronau K., et al. Dynamics of protein phosphorylation on Ser/Thr/Tyr in Bacillus subtilis. Proteomics 2007, 7:3509-3526.
9. Nakanishi T., Ando E., Furuta M., Kinoshita E., Kinoshita-Kikuta E., Koike T., et al. Identification on membrane and characterization of phosphoproteins using an alkoxide-bridged dinuclear metal complex as a phosphate-binding tag molecule. J Biomol Tech 2007, 18:278-286.
10. Su H.C., Hutchison C.A., Giddings M.C. Mapping phosphoproteins in Mycoplasma genitalium and Mycoplasma pneumonia. BMC Microbiol 2007, 7:63.
11. Rush J., Moritz A., Lee K.A. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat Biotechnol 2005, 23:94-101.
12. Steen H., Kuster B., Fernandez M., et al. Tyrosine phosphorylation mapping of the epidermal growth factor receptor signaling pathway. J Biol Chem 2002, 277:1031-1039.
13. Villén J., Beausoleil S.A., Gerber S.A., et al. Large-scale phosphorylation analysis of mouse liver. Proc Natl Acad Sci USA 2007, 104:1488-1493.
14. Grønborg M., Kristiansen T.Z., Stensballe A., Andersen J.S., Ohara O., Mann M., et al. A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies - identification of a novel protein, Frigg, as a protein kinase a substrate. Mol Cell Proteomics 2002, 1:517-527.
15. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
16. Zhang H., Zha X., Tan Y., et al. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J Biol Chem 2002, 277:39379-39387.
17. Dunn J.D., Reid G.E., Bruening M.L. Techniques for phosphopeptide enrichment prior to analysis by mass spectrometry. Mass Spectrom Rev 2010, 29:29-54.
18. 2 enrichment in combination with MALDI TOF/TOF MS. Proteomics 2008, 8:4577-4592.
19. Ikeguchi Y., Nakamura H. Determination of organic phosphates by column-switching high performance anion exchange chromatography using on-line preconcentration on titania. Anal Sci 1997, 13:479-483.
20. Pinkse M.W., Uitto P.M., Hilhorst M.J., et al. Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns. Anal Chem 2004, 76:3935-3943.
21. Koizumi Y., Taya M. Kinetic evaluation of biocidal activity of titanium dioxide against phage MS2 considering interaction between the vage and photocatalyst particles. Biochem Eng J 2002, 12:107-116.
22. Larsen M.R., Thingholm T.E., Jensen O.N., et al. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titaniumdioxide microcolumns. Mol Cell Proteomics 2005, 4:873-886.
23. Jensen S.S., Larsen M.R. Evaluation of the impact of some experimental procedures on different phosphopeptides enrichment techniques. Rapid Comm Mass Spectrom 2007, 21:3635-3645.
24. Thingholm T.E., Jorgensen T.J., Jensen O.N., et al. Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nat Protoc 2006, 1:1929-1935.
25. Blackwell J.A., Carr P.W. Fluoride-modified zirconium-oxide as a biocompatible stationary phase for high-performance liquid-chromatography. J Chromatogr 1991, 549:59-75.
26. Kweon H.K., Håkansson K. Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Anal Chem 2006, 78:1743-1749.
27. Gates M.B., Tomer K.B., Deterding L.J. Comparison of metal and metal oxide media for phosphopeptide enrichment prior to mass spectrometric analyses. J Am Soc Mass Spectrom 2010, 21:1649-1659.
28. Sun X., Chiu J.F., He Q.Y. Application of immobilized metal affinity chromatography in proteomics. Expert Rev Proteom 2005, 2:649-657.
29. Thingholm T.E., Jensen O.N., Larsen R. Analytical strategies for phosphoproteomics. Proteomics 2009, 9:1451-1468.
30. Lindeberg G., Bennich H., Engström A. Purification of synthetic peptides. Immobilized metal ion affinity chromatography (IMAC). Int J Pept Protein Res 1991, 38:253-259.
31. Andersson L., Porath J. Isolation of phosphoproteins by immobilized metal (Fe3+) affinity chromatography. Anal Biochem 1986, 154:250-254.
32. Ficarro S.B., McCleland M.L., Stukenberg P.T., Burke D.J., et al. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 2002, 20:301-305.
33. Brill L.M., Salomon A.R., Ficarro S.B., Mukherji M., Stettler-Gill M., Peters E.C. Robust phosphoproteomic profiling of tyrosine phosphorylation sites from human T cells using immobilized metal affinity chromatography and tandem mass spectrometry. Anal Chem 2004, 76:2763-2772.
34. Trinidad J.C., Specht C.G., Thalhammer A. Comprehensive identification of phosphorylation sites in postsynaptic density preparations. Mol Cell Proteomics 2006, 5:914-922.
35. Krijgsveld J., Gauci S., Dormeyer W., Heck A. In-gel isoelectric focusing of peptides as a tool for improved protein identification. J Prot Res 2006, 5:1721-1730.
36. Posewitz M.C., Tempst P. Immobilized gallium (III+) affinity chromatography of phosphopeptides. Anal Chem 1999, 71:2883-2892.
37. 2 surfaces used in the study of regulated, dynamic protein phosphorylation. J Am Soc Mass Spectrom 2007, 18:1932-1944.
38. http://www.piercenet.com/previews/vol14iss2/PreviewsV14Iss2Pg18-19.pdf.
39. Lin H.Y., Chen C.T., Chen Y.C. Detection of phosphopeptides by localized surface plasma resonance of titania-coated gold nanoparticles immobilized on glass substrates. Anal Chem 2006, 78:6873-6878.
40. Qiao L., Roussel, Wan J., et al. Specific on-plate enrichment of phosphorylated peptides for direct MALDI-TOF MS analysis. J Proteome Res 2007, 6:4763-4769.
41. Zhou H., Xu S., Ye M., et al. Zirconium phosphonate-modified porous silicon for highly specific capture of phosphopeptides and MALDI-TOF MS analysis. J Proteome Res 2006, 5:2431-2437.
42. Eriksson A., Bergquist J., Edwards K., Hagfeldt A., Malmström D., Agmo Hernández V. Optimized protocol for on-target phosphopeptide enrichment prior to matrix-assisted laser desorption-ionization mass spectrometry using mesoporous titanium dioxide. Anal Chem 2010, 82:4577-4583.
43. Wang W.H., Bruening M.L. Phosphopeptide enrichment on functionalized polymer microspots for MALDI-MS analysis. Analyst 2009, 134:512-518.
44. Arrigoni G., Resjö S., Levander F., et al. Chemical derivatization of phosphoserine and phosphothreonine containing peptides to increase sensitivity for MALDI-based analysis and for selectivity of MS/MS analysis. Proteomics 2006, 6:757-766.
45. Zhou H., Watts J.D., Aebersold R. A systematic approach to the analysis of protein phosphorylation. Nat Biotechnol 2001, 19:375-378.
46. Leitner A., Lindner W. Chemical tagging strategies for mass spectrometry-based phospho-proteomics. Methods Mol Biol 2009, 527:229-243.
47. Salih E. Phosphoproteomics by mass spectrometry and classical protein chemistry approaches. Mass Spectrom Rev 2005, 24:828-846.
48. Schmidt S.R., Schweikart F., Andersson M.E. Current methods for phosphoprotein isolation and enrichment. J Chromatogr B Analyt Technol Biomed Life Sci 2007, 849:154-162.
49. Bodenmiller B., Mueller L.N., Mueller M., Domon B., Aebersold R. Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat Methods 2007, 4:231-237.
50. Dunn J.D., Watson J.T., Bruening M.L. Detection of phosphopeptides using Fe(III)-nitrilotriacetate complexes immobilized on a MALDI plate. Anal Chem 2006, 78:1574-1580.
51. Yang X.F., Wu X.P., Kobayashi T. Enhanced ionization of phosphorylated peptides during MALDI TOF mass spectrometry. Anal Chem 2004, 76:1532-1536.
52. Kjellström S., Jensen O.N. Phosphoric acid as a matrix additive for MALDI MS analysis of phosphopeptides and phosphoproteins. Anal Chem 2004, 76:5109-5117.
53. Fenn J.B., Mann M., Meng C.K., et al. Electrospray ionization for mass spectrometry of large biomolecules. Science 1989, 246:64-71.
54. Roepstorff P., Fohlman J. Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed Mass Spectrom 1984, 11:601.
55. Makarov A. Electrostatic axially harmonic orbital trapping: a high performance technique of mass analysis. Anal Chem 2000, 72:1156-1162.
56. Hardman M., Makarov A. Interfacing the orbitrap mass analyzer to an electrospray ion source. Anal Chem 2003, 75:1699-1705.
57. Macek B., Waanders L.F., Olsen J.V., Mann M. Top-down protein sequencing and MS3 on a hybrid linear quadrupole ion trap-orbitrap mass spectrometer. Mol Cell Proteomics 2006, 5:949-958.
58. Steen H., Kuster B., Fernandez M., et al. Detection of tyrosine phosphorylated peptides by precursor ion scanning quadrupole TOF mass spectrometry in positive ion mode. Anal Chem 2001, 73:1440-1448.
59. Olsen J.V., Mann M. Improved peptide identification in proteomics by two consecutive stages of mass spectrometric fragmentation. Proc Natl Acad Sci USA 2004, 101:13417-13422.
60. Boersema P.J., Mohammed S., Heck A.J. Phosphopeptide fragmentation and analysis by mass spectrometry. J Mass Spectrom 2009, 44:861-878.
61. Schroeder M.J., Shabanowitz J., Schwartz J.C., et al. A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal Chem 2004, 76:3590-3598.
62. Nakayasu E.S., Gaynor M.R., Sobreira T.J., et al. Phosphoproteomic analysis of the human pathogen Trypanosoma cruzi at the epimastigote stage. Proteomics 2009, 9:3489-3506.
63. Papayannopoulos I.A. The interpretation of collision-induced dissociation tandem mass spectra of peptides. Mass Spec Rev 1995, 14:49-73.
64. Savitski M.M., Lemeer S., Boesche M., et al. Confident phosphorylation site localization using the Mascot Delta Score. Mol Cell Proteomics 2011, 10. M110.003830.
65. Gant-Branum R.L., Broussard J.A., Mahsut A., et al. Identification of phosphorylation sites within the signaling adaptor APPL1 by mass spectrometry. J Proteome Res 2010, 9:1541-1548.
66. Annan R.S., Carr S.A. Phosphopeptide analysis by matrix-assisted laser desorption time-of-flight mass spectrometry. Anal Chem 1996, 68:3413-3421.
67. Liao P.C., Leykam J., Andrews P.C., Gage D.A., Allison J. An approach to locate phosphorylation sites in phosphoprotein: mass mapping by combining specific enzymatic degradation with matrix assisted laser desorption/ionization mass spectrometry. Anal Biochem 1994, 219:9-20.
68. Zubarev R.A., Kelleher N.L., McLafferty F.W. Electron capture dissociation of multiply charged protein cations. A nonergodic process. J Am Chem Soc 1998, 12013:3265-3266.
69. Liu H., Håkansson K. Abundant b-type ions produced in electron capture dissociation of peptides without basic amino acid residues. J Am Soc Mass Spectrom 2007, 18:2007-2013.
70. Ding L., Brancia F.L. Electron capture dissociation in a digital ion trap mass spectrometer. Anal Chem 2006, 78:1995-2000.
71. Sweet S.M., Bailey C.M., Cunningham D.L. Large scale localization of protein phosphorylation by use of electron capture dissociation mass spectrometry. Mol Cell Proteomics 2009, 8:904-912.
72. Syka J.E., Coon J.J., Schroeder M.J., et al. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc Natl Acad Sci USA 2004, 101:9528-9533.
73. Navajas R., Paradela A., Albar J.P. Immobilized metal affinity chromatography/reversed-phase enrichment of phosphopeptides and analysis by CID/ETD tandem mass spectrometry. Methods Mol Biol 2011, 681:337-348.
74. Chi A., Huttenhower C., Geer L.Y., Coon J.J., Syka J.E., Bai D.L., et al. Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proc Natl Acad Sci USA 2007, 104:2193-2198.
75. Mann M. Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 2006, 7:952-958.
76. Grimsrud P.A., Swaney D.L., Wenger C.D., et al. Phosphoproteomics for the masses. ACS Chem Biol 2010, 5:105-119.
77. Malik R., Lenobel R., Santamaria A., et al. Quantitative analysis of the human spindle phosphoproteome at distinct mitotic stages. J Proteome Res 2009, 8:4553-4563.
78. Knowlton M.L., Selfors L.M., Wrobel C.N., et al. Profiling Y561-dependent and -independent substrates of CSF-1R in epithelial cells. PLoS One Oct 26, 2010, 5(10):e13587.
79. Gu T.L., Nardone J., Wang Y., et al. Survey of activated FLT3 signaling in leukemia. PLoS One Apr 28, 2011, 6(4):e19169.
80. Ross P.L., Huang Y.N., Marchese J.N., et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 2004, 3:1154-1169.
81. Thompson A., Schäfer J., Kuhn K., et al. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 2003, 75:1895-1904.
82. Ross P.L., Huang Y.N., Marchese J.N., et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 2004, 3:1154-1169.
83. Shadforth I.P., Dunkley T.P., Lilley K.S., Bessant C. i-Tracker: for quantitative proteomics using iTRAQ. BMC Genomics Oct 20, 2005, 6:145.
84. Boja E.S., Phillips D., French S.A., et al. Quantitative mitochondrial phosphoproteomics using iTRAQ on an LTQ-Orbitrap with high energy collision dissociation. J Proteome Res 2009, 8:4665-4675.
85. Zhang Y., Ficarro S.B., Li S., et al. Optimized orbitrap HCD for quantitative analysis of phosphopeptides. J Am Soc Mass Spectrom 2009, 20:1425-1434.
86. Gygi S.P., Rist B., Gerber S.A., et al. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 1999, 17:994-999.
87. Zhang R., Regnier F.E. Minimizing resolution of isotopically coded peptides in comparative proteomics. J Prot Res 2002, 1:139-147.
88. Schneider L.V., Hall M.P. Stable isotope methods for high-precision proteomics. Drug Discov Today 2005, 10:353-363.
89. Gerber S.A., Rush J., Stemman O., et al. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc Natl Acad Sci USA 2003, 100:6940-6945.
90. Jin L.L., Tong J., Prakash A., Peterman S.M., et al. Measurement of protein phosphorylation stoichiometry by selected reaction monitoring mass spectrometry. J Proteome Res 2010, 9:2752-2761.
91. Traweger A., Wiggin G., Taylor L., et al. Protein phosphatase 1 regulates the phosphorylation state of the polarity scaffold Par-3. Proc Natl Acad Sci USA 2008, 105:10402-10407.
92. Bantscheff M., Schirle M., Sweetman G., Rick J., Kuster B. Quantitative mass spectrometry in proteomics: a critical review. Anal Bioanal Chem 2007, 389:1017-1031.
93. Asara J.M., Christofk H.R., Freimark L.M., et al. A label-free quantification method by MS/MS TIC compared to SILAC and spectral counting in a proteomics screen. Proteomics 2008, 8:994-999.
94. Eng J.K., McCormack A.L., Yates J.R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 1994, 5:976-989.
95. http://www.matrixscience.com.
96. Beausoleil S.A., Villén J., Gerber S.A., Rush J., Gygi S.P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 2006, 24:1285-1292.
97. Ruttenberg B.E., Pisitkun T., Knepper M.A., Hoffert J.D. PhosphoScore: an open-source phosphorylation site assignment tool for MSn data. J Proteome Res 2008, 7:3054-3059.
98. Gnad F., Gunawardena J., Mann M. PHOSIDA 2011: the posttranslational modification diabase. Nucleic Acids Res 2011, 39:D253-D260.
99. Dinkel H., Chica C., Via A. Phospho.ELM: a database of phosphorylation sites-update 2011. Nucleic Acids Res 2011, 39:D261-D267.
100. Kokubu M., Ishihama Y., Sato T., Nagasu T., Oda Y. Specificity of immobilized metal affinity-based IMAC/C18 tip enrichment of phosphopeptides for protein phosphorylation analysis. Anal Chem 2005, 77:5144-5154.