Recent advances and special considerations for the analysis of phosphorylated peptides by LC-ESI-MS/MS

Current Analytical Chemistry

Volumn 8, Issue 1, 2012, Pages 35-42

  Liu, Suya ^a   Hughes, Chris ^a   Lajoie, Gilles A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Liquid chromatography; Phosphopeptides; Phosphoproteomics; Tandem mass spectrometry

Indexed keywords

LIQUID CHROMATOGRAPHY; METAL IONS; MOLECULAR BIOLOGY; PEPTIDES; PHOSPHORYLATION;

ELECTROSPRAY TANDEM MASS SPECTROMETRY; ESI MASS SPECTROMETRY; LIQUID CHROMATOGRAPHY ELECTROSPRAY; PHOSPHOPEPTIDES; PHOSPHOPROTEOMICS; PHOSPHORYLATED PEPTIDES; PROTEOMICS; SAMPLE ANALYSIS; TANDEM MASS SPECTROMETRY; TANDEM-MASS SPECTROMETRY;

MASS SPECTROMETRY;

EID: 84855263935     PISSN: 15734110     EISSN: None     Source Type: Journal    
DOI: 10.2174/157341112798472215     Document Type: Article

References (70)

1. Domon, B.; Aebersold, R. Mass spectrometry and protein analysis. Science, 2006, 312(5771), 212-217.
2. Yates, J.R.; Ruse, C.I.; Nakorchevsky, A. Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng., 2009, 11, 49-79.
3. Delahunty, C.; Yates, J.R. Protein identification using 2D-LCMS/ MS. Methods, 2005, 35(3), 248-255.
4. Steen, H.; Mann, M. The ABC's (and XYZ's) of peptide sequencing. Nat. Rev. Mol. Cell Biol., 2004, 5(9), 699-711.
5. Hayes, R.N.; Gross, M.L. Collision-induced dissociation. Methods Enzymol., 1990, 193, 237-263.
6. Appella, E.; Anderson, C.W. New prospects for proteomics-electroncapture (ECD) and electron-transfer dissociation (ETD) fragmentation techniques and combined fractional diagonal chromatography (COFRADIC). FEBS J., 2007, 274(24), 6255.
7. Christin, C.; Bischoff, R.; Horvatovich, P. Data processing pipelines for comprehensive profiling of proteomics samples by label-free LCMS for biomarker discovery. Talanta, 2011, 83(4), 1209-1224.
8. Li, M.; Zhou, Z.; Nie, H.; Bai, Y.; Liu, H. Recent advances of chromatography and mass spectrometry in lipidomics. Anal. Bioanal. Chem., 2011, 399(1), 243-249.
9. Ning, Z.; Zhou, H.; Wang, F.; Abu-Farha, M.; Figeys, D. Analytical Aspects of proteomics: 2009-2010. Anal. Chem., 2011, 83, 4407-4426.
10. Hunter, T. Signaling-2000 and beyond. Cell, 2000, 100(1), 113-127.
11. Pawson, T.; Nash, P. Assembly of cell regulatory systems through protein interaction domains. Science, 2003, 300(5618), 445-452.
12. McLachlin, D.T.; Chait, B.T. Analysis of phosphorylated proteins and peptides by mass spectrometry. Curr. Opin. Chem. Biol., 2001, 5(5), 591-602.
13. Rush, J.; Moritz, A.; Lee, K.A.; Guo, A.; Goss, V.L.; Spek, E.J.; Zhang, H.; Zha, X.M.; Polakiewicz, R.D.; Comb, M.J. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol., 2005, 23(1), 94-101.
14. Prat, M.; Di Renzo, M.F.; Gaudino, G.; Ponzetto, C.; Comoglio, P.M. Phosphotyrosine antibodies as probes for activated oncogene products endowed with tyrosine kinase activity. Ann. Ist Super Sanita, 1991, 27(1), 175-181.
15. Wang, J.Y. Antibodies for phosphotyrosine: analytical and preparative tool for tyrosyl-phosphorylated proteins. Anal. Biochem., 1988, 172(1), 1-7.
16. Andersson, L.; Porath, J. Isolation of phosphoproteins by immobilized metal (Fe-3+) affinity-chromatography. Anal. Biochem., 1986, 154(1), 250-254.
17. Thingholm, T.E.; Jensen, O.N. Enrichment and characterization of phosphopeptides by immobilized metal affinity chromatography (IMAC) and mass spectrometry. Methods Mol. Biol., 2009, 527, 47-56, xi.
18. Thingholm, T.E.; Jensen, O.N.; Larsen, M.R. Enrichment and separation of mono- and multiply phosphorylated peptides using sequential elution from IMAC prior to mass spectrometric analysis. Methods Mol. Biol., 2009, 527, 67-78, xi.
19. Pinkse, M.W.H.; Uitto, P.M.; Hilhorst, M.J.; Ooms, B.; Heck, A.J.R. 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(14), 3935-3943.
20. Thingholm, T.E.; Larsen, M.R. The use of titanium dioxide microcolumns to selectively isolate phosphopeptides from proteolytic digests. Methods Mol. Biol., 2009, 527, 57-66, xi.
21. Larsen, M.R.; Thingholm, T.E.; Jensen, O.N.; Roepstorff, P.; Jorgensen, T.J. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics, 2005, 4(7), 873-886.
22. Pinkse, M.W.; Mohammed, S.; Gouw, J.W.; van Breukelen, B.; Vos, H.R.; Heck, A.J. Highly robust, automated, and sensitive online TiO2-based phosphoproteomics applied to study endogenous phosphorylation in Drosophila melanogaster. J. Proteome Res., 2008, 7(2), 687-697.
23. Haydon, C.E.; Eyers, P.A.; Aveline-Wolf, L.D.; Resing, K.A.; Maller, J.L.; Ahn, N.G. Identification of novel phosphorylation sites on Xenopus laevis Aurora A and analysis of phosphopeptide enrichment by immobilized metal-affinity chromatography. Mol. Cell. Proteomics, 2003, 2(10), 1055-1067.
24. Porath, J. Immobilized metal-ion affinity-chromatography. Protein Expr. Purif., 1992, 3(4), 263-281.
25. Porath, J.; Olin, B. Immobilized metal-ion affinity adsorption and immobilized metal-ion affinity-chromatography of biomaterials - serum-protein affinities for gel-immobilized iron and nickel ions. Biochem., 1983, 22(7), 1621-1630.
26. Schlosser, A.; Bodem, J.; Bossemeyer, D.; Grummt, I.; Lehmann, W.D. Identification of protein phosphorylation sites by combination of elastase digestion, immobilized metal affinity chromatography, and quadrupole-time of flight tandem mass spectrometry. Proteomics, 2002, 2(7), 911-918.
27. Gilar, M.; Olivova, P.; Daly, A.E.; Gebler, J.C. Orthogonality of separation in two-dimensional liquid chromatography. Anal. Chem., 2005, 77(19), 6426-6434.
28. Washburn, M.P.; Wolters, D.; Yates, J.R. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol., 2001, 19(3), 242-247.
29. Beausoleil, S.A.; Jedrychowski, M.; Schwartz, D.; Elias, J.E.; Villen, J.; Li, J.; Cohn, M.A.; Cantley, L.C.; Gygi, S.P. Largescale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. U. S. A., 2004, 101(33), 12130-12135.
30. Rigbolt, K.T.; Prokhorova, T.A.; Akimov, V.; Henningsen, J.; Johansen, P.T.; Kratchmarova, I.; Kassem, M.; Mann, M.; Olsen, J.V.; Blagoev, B. System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci. Signal., 2011, 4(164), rs3, DOI: 10.1126/scisignal.2001570; [E-pub ahead of print].
31. Van Hoof, D.; Munoz, J.; Braam, S.R.; Pinkse, M.W.; Linding, R.; Heck, A.J.; Mummery, C.L.; Krijgsveld, J. Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell, 2009, 5(2), 214-226.
32. Swaney, D.L.; McAlister, G.C.; Coon, J.J. Decision tree-driven tandem mass spectrometry for shotgun proteomics. Nat. Methods, 2008, 5(11), 959-964.
33. Dai, J.; Jin, W.H.; Sheng, Q.H.; Shieh, C.H.; Wu, J.R.; Zeng, R. Protein phosphorylation and expression profiling by Yin-yang multidimensional liquid chromatography (Yin-yang MDLC) mass spectrometry. J. Proteome Res., 2007, 6(1), 250-262.
34. Han, G.; Ye, M.; Zhou, H.; Jiang, X.; Feng, S.; Tian, R.; Wan, D.; Zou, H.; Gu, J. Large-scale phosphoproteome analysis of human liver tissue by enrichment and fractionation of phosphopeptides with strong anion exchange chromatography. Proteomics, 2008, 8(7), 1346-1361.
35. Motoyama, A.; Xu, T.; Ruse, C.I.; Wohlschlegel, J.A.; Yates, J.R. Anion and cation mixed-bed ion exchange for enhanced multidimensional separations of peptides and phosphopeptides. Anal. Chem., 2007, 79(10), 3623-3634.
36. Kong, R.P.; Siu, S.O.; Lee, S.S.; Lo, C.; Chu, I.K. Development of online high-/low-pH reversed-phase-reversed-phase twodimensional liquid chromatography for shotgun proteomics: a reversed-phase-strong cation exchange-reversed-phase approach. J. Chromatogr. A, 2011, 1218(23), 3681-3688.
37. Song, C.; Ye, M.; Han, G.; Jiang, X.; Wang, F.; Yu, Z.; Chen, R.; Zou, H. Reversed-phase-reversed-phase liquid chromatography approach with high orthogonality for multidimensional separation of phosphopeptides. Anal. Chem., 2010, 82(1), 53-56.
38. Dephoure, N.; Gygi, S.P. A solid phase extraction-based platform for rapid phosphoproteomic analysis. Methods, 2011, 54(4), 379-386.
39. Gruhler, A.; Olsen, J.V.; Mohammed, S.; Mortensen, P.; Faergeman, N.J.; Mann, M.; Jensen, O.N. Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol. Cell Proteomics, 2005, 4(3), 310-327.
40. Olsen, J.V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell, 2006, 127(3), 635-648.
41. Villen, J.; Beausoleil, S.A.; Gerber, S.A.; Gygi, S.P. Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. U. S. A., 2007, 104(5), 1488-1493.
42. Trinidad, J.C.; Specht, C.G.; Thalhammer, A.; Schoepfer, R.; Burlingame, A.L. Comprehensive identification of phosphorylation sites in postsynaptic density preparations. Mol. Cell Proteomics, 2006, 5(5), 914-922.
43. McNulty, D.E.; Annan, R.S. Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol. Cell Proteomics, 2008, 7(5), 971-980.
44. Gan, C.S.; Guo, T.; Zhang, H.; Lim, S.K.; Sze, S.K. A comparative study of electrostatic repulsion-hydrophilic interaction chromatography (ERLIC) versus SCX-IMAC-based methods for phosphopeptide isolation/enrichment. J. Proteome Res., 2008, 7(11), 4869-4877.
45. Hao, P.; Guo, T.; Sze, S.K. Simultaneous analysis of proteome, phospho- and glycoproteome of rat kidney tissue with electrostatic repulsion hydrophilic interaction chromatography. PLoS One, 2011, 6(2), e16884.
46. Dorsey, J.G.; Dill, K.A. The molecular mechanism of retention in reversed-phase liquid-chromatography. Chem. Rev., 1989, 89(2), 331-346.
47. Kaliszan, R.; van Straten, M.A.; Markuszewski, M.; Cramers, C.A.; Claessens, H.A. Molecular mechanism of retention in reversed-phase high-performance liquid chromatography and classification of modern stationary phases by using quantitative structure-retention relationships. J. Chromatogr. A, 1999, 855(2), 455-486.
48. Rafferty, J.L.; Zhang, L.; Siepmann, J.I.; Schure, M.R. Retention mechanism in reversed-phase liquid chromatography: A molecular perspective. Anal. Chem., 2007, 79(17), 6551-6558.
49. MacNair, J.E.; Lewis, K.C.; Jorgenson, J.W. Ultrahigh pressure reversed-phase liquid chromatography in packed capillary columns. Anal. Chem., 1997, 69(6), 983-989.
50. Marcantonio, M.; Trost, M.; Courcelles, M.; Desjardins, M.; Thibault, P. Combined enzymatic and data mining approaches for comprehensive phosphoproteome analyses: application to cell signaling events of interferon-gamma-stimulated macrophages. Mol. Cell. Proteomics, 2008, 7(4), 645-660.
51. Kim, J.; Camp, D.G., 2nd; Smith, R.D. Improved detection of multiphosphorylated peptides in the presence of phosphoric acid in liquid chromatography/mass spectrometry. J. Mass Spectrom., 2004, 39(2), 208-215.
52. Rogers, L.D.; Foster, L.J. Phosphoproteomics-finally fulfilling the promise? Mol. Biosyst., 2009, 5(10), 1122-1129.
53. Eyrich, B.; Sickmann, A.; Zahedi, R.P. Catch me if you can: mass spectrometry-based phosphoproteomics and quantification strategies. Proteomics, 2011, 11(4), 554-570.
54. Steen, H.; Jebanathirajah, J.A.; Rush, J.; Morrice, N.; Kirschner, M.W. Phosphorylation analysis by mass spectrometry: myths, facts, and the consequences for qualitative and quantitative measurements. Mol. Cell Proteomics, 2006, 5(1), 172-181.
55. Kebarle, P. A brief overview of the present status of the mechanisms involved in electrospray mass spectrometry. J. Mass Spectrom., 2000, 35(7), 804-817.
56. Eyrich, B.; Sickmann, A.; Zahedi, R.P. Catch me if you can: mass spectrometry-based phosphoproteomics and quantification strategies. Proteomics, 2011, 11(4), 554-570.
57. Piggee, C. Phosphoproteomics: miles to go before it's routine. Anal. Chem., 2009, 81(7), 2418-2420.
58. Larsen, M.R.; Cordwell, S.J.; Roepstorff, P. Graphite powder as an alternative or supplement to reversed-phase material for desalting and concentration of peptide mixtures prior to matrix-assisted laser desorption/ionization-mass spectrometry. Proteomics, 2002, 2(9), 1277-1287.
59. Larsen, M.R.; Graham, M.E.; Robinson, P.J.; Roepstorff, P. Improved detection of hydrophilic phosphopeptides using graphite powder microcolumns and mass spectrometry: evidence for in vivo doubly phosphorylated dynamin I and dynamin III. Mol. Cell Proteomics, 2004, 3(5), 456-65.
60. Nuwaysir, L.M.; Stults, J.T. Electrospray ionization mass spectrometry of phosphopeptides isolated by on-line immobilized metal-ion affinity chromatography J. Am. Soc. Mass Spectrom., 1993, 4(8), 662-669.
61. Kim, J.; Petritis, K.; Shen, Y.; Camp, D.G. 2nd; Moore, R.J.; Smith, R.D. Phosphopeptide elution times in reversed-phase liquid chromatography. J. Chromatogr. A, 2007, 1172(1), 9-18.
62. Liu, S.; Zhang, C.; Campbell, J.L.; Zhang, H.; Yeung, K.K.; Han, V.K.; Lajoie, G.A. Formation of phosphopeptide-metal ion complexes in liquid chromatography/electrospray mass spectrometry and their influence on phosphopeptide detection. Rapid Commun. Mass Spectrom., 2005, 19(19), 2747-2756.
63. Nakamura, T.; Myint, K.T.; Oda, Y. Ethylenediaminetetraacetic acid increases identification rate of phosphoproteomics in real biological samples. J. Proteome Res., 2009, 9(3), 1385-1391.
64. Winter, D.; Seidler, J.; Ziv, Y.; Shiloh, Y.; Lehmann, W.D. Citrate boosts the performance of phosphopeptide analysis by UPLC-ESIMS/ MS. J. Proteome Res., 2009, 8(1), 418-424.
65. Seidler, J.; Zinn, N.; Haaf, E.; Boehm, M.E.; Winter, D.; Schlosser, A.; Lehmann, W.D. Metal ion-mobilizing additives for comprehensive detection of femtomole amounts of phosphopeptides by reversed phase LC-MS. Amino Acids, 2011, 41(2), 311-320.
66. Zhang, C.; Liu, S.; Lenehan, J.; Litchfield, D.W.; Lajoie, G.A. In: Global Phosphoproteome Analysis by Combining Highly Selective TiO2 Enrichment and EDTA-Enhanced Detection by LC-MS, The 54th ASMS Conference on Mass Spectrometry and Allied Topics, Seattle, WA, USA, May 28 - June 1; 2006.
67. Zhao, R.; Ding, S.J.; Shen, Y.; Camp, D.G. 2nd; Livesay, E.A.; Udseth, H.; Smith, R.D. Automated metal-free multiple-column nanoLC for improved phosphopeptide analysis sensitivity and throughput. J. Chromatogr. B, Anal. Technol. Biomed. Life Sci., 2009, 877(8-9), 663-670.
68. Yang, F.; Waters, K.M.; Miller, J.H.; Gritsenko, M.A.; Zhao, R.; Du, X.; Livesay, E.A.; Purvine, S.O.; Monroe, M.E.; Wang, Y.; Camp, D.G. 2nd; Smith, R.D. Stenoien, D.L. Phosphoproteomics profiling of human skin fibroblast cells reveals pathways and proteins affected by low doses of ionizing radiation. PLoS One, 5(11), e14152.
69. th ASMS Conference on Mass Spectrometry and Allied Topics, Seattle, WA, USA, May 28 - June 1; 2006.
70. Tian, R.; Wang, S.; Elisma, F.; Li, L.; Zhou, H.; Wang, L.; Figeys, D. Rare cell proteomic reactor applied to stable isotope labeling by amino acids in cell culture (SILAC)-based quantitative proteomics study of human embryonic stem cell differentiation. Mol. Cell Proteomics, 2011, 10(2), M110 000679; [E-pub ahead of print].