Chip-based enrichment and NanoLC-MS/MS analysis of phosphopeptides from whole lysates

Journal of Proteome Research

Volumn 7, Issue 4, 2008, Pages 1565-1571

  Mohammed, Shabaz ^a   Kraiczek, Karsten ^b   Pinkse, Martijn W H ^a,c   Lemeer, Simone ^a   Benschop, Joris J ^a,d   Heck, Albert J R ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b AGILENT TECHNOLOGIES   (Germany)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Automated; Chip; Phosphopeptide enrichment; Tio2

Indexed keywords

PHOSPHOPEPTIDE; TITANIUM DIOXIDE; BOVINE SERUM ALBUMIN; CASEIN; HEMOGLOBIN; TITANIUM; TRYPSIN;

ARTICLE; CELL LYSATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MICROCHIP ANALYSIS; MICROFLUIDIC ANALYSIS; NANOANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; CELL LINE; CHEMISTRY; INSTRUMENTATION; ION EXCHANGE CHROMATOGRAPHY; METHODOLOGY; TANDEM MASS SPECTROMETRY;

CASEINS; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, ION EXCHANGE; HEMOGLOBINS; HUMANS; MICROFLUIDIC ANALYTICAL TECHNIQUES; PHOSPHOPEPTIDES; SERUM ALBUMIN, BOVINE; TANDEM MASS SPECTROMETRY; TITANIUM; TRYPSIN;

EID: 45549083940     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr700635a     Document Type: Article

References (45)

1. Jensen, O. N. Interpreting the protein language using proteomics. Nat. Rev. Mol. Cell Biol. 2006, 7(6), 391-403.
2. Manning, G.; Whyte, D. B.; Martinez, R.; Hunter, T.; Sudarsanam, S. The protein kinase complement of the human genome. Science 2002, 298 (5600), 1912.
3. Mann, M.; Jensen, O. N. Proteomic analysis of post-translational modifications. Nat. Biotechnol. 2003, 21 (3), 255-261.
4. Linding, R.; Jensen, L. J.; Ostheimer, G. J.; van Vugt, M.; Jorgensen, C.; Miron, I. M.; Diella, F.; Colwill, K.; Taylor, L.; Elder, K.; Metalnikov, P.; Nguyen, V.; Pasculescu, A.; Jin, J.; Park, J. G.; Samson, L. D.; Woodgett, J. R.; Russell, R. B.; Bork, P.; Yaffe, M. B.; Pawson, T. Systematic discovery of in vivo phosphorylation networks. Cell 2007, 129 (7), 1415-1426.
5. 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.
6. Pandey, A.; Podtelejnikov, A. V.; Blagoev, B.; Bustelo, X. R.; Mann, M.; Lodish, H. F. Analysis of receptor signaling pathways by mass spectrometry: Identification of Vav-2 as a substrate of the epidermal and platelet-derived growth factor receptors. Proc. Natl. Acad. Sc. U.S.A. 2000, 97 (1), 179-184.
7. Gronborg, M.; Kristiansen, T. Z.; Stensballe, A.; Andersen, J. S.; Ohara, O.; Mann, M.; Jensen, O. N.; Pandey, A. 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 (7), 517-527.
8. Zheng, H. Y.; Hu, P.; Quinn, D. F.; Wang, Y. K. Phosphotyrosine proteomic study of interferon alpha signaling pathway using a combination of immunoprecipitation and immobilized metal affinity chromatography. Mol. Cell. Proteomics 2005, 4 (6), 721- 730.
9. Posewitz, M. C.; Tempst, P. Immobilized gallium(III) affinity chromatography of phoshopetides. Anal. Chem. 1999, 71 (14), 2883-2892.
10. Stensballe, A.; Andersen, S.; Jensen, O. N. Characterization of phosphoproteinhs from electrophoretic gels by nanoscale Fe(III) affinity chromatography with off-line mass spectrometry analysis. Proteomics 2001, 1 (2), 207-222.
11. Ficarro, S. B.; McCleland, M. L.; Stukenberg, P. T.; Burke, D. J.; Ross, M. M.; Shabanowitz, J.; Hunt, D. F.; White, F. M. Phosphop- roteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 2002, 20 (3), 301-305.
12. Kweon, H. K.; Hakansson, K. Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Anal. Chem. 2006, 78 (6), 1743-1749.
13. Chen, C. T.; Chen, W. Y.; Tsai, P. J.; Chien, K. Y.; Yu, J. S.; Chen, Y. C. Rapid enrichment of phosphopeptides and phosphoproteins from complex samples using magnetic particles coated with alumina as the concentrating probes for MALDI MS analysis. J. Proteome Res. 2007, 6 (1), 316-325.
14. 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.
15. Larsen, M. R.; Thingholm, T. E.; Jensen, O. N.; Roepstorff, P.; Jorgensen, T. J. D. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 2005, 4 (7), 873-886.
16. Benschop, J. J.; Mohammed, S.; O'Flaherty, M. C.; Heck, A. J. R.; Slijper, M.; Menke, F. L. H. Quantitative phospho-proteomics of early elicitor signalling in Arabidopsis. Mol. Cell. Proteomics 2007, 6(7), 1198-1214.
17. Ishihama, Y.; Wei, F. Y.; Aoshima, K.; Sato, T.; Kuromitsu, J.; Oda, Y. Enhancement of the efficiency of phosphoproteomic identification by removing phosphates after phosphopeptide enrichment. J. Proteome Res. 2007, 6 (3), 1139-1144.
18. Beausoleil, S. A.; Jedrychowski, M.; Schwartz, D.; Elias, J. E.; Villen, I.; Li, J. X.; Cohn, M. A.; Cantley, L. C.; Gygi, S. P. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. U.S.A 2004, 101 (33), 12130-12135.
19. Nuhse, T. S.; Stensballe, A.; Jensen, O. N.; Peck, S. C. Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry. Mol. Cell. Proteomics 2003, 2 (11), 1234-1243.
20. Dai, J.; Jin, W. FL; 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.
21. Pinkse, M. W. H.; Heck, A. J. R. Essential enrichment strategies in phosphoproteomics. Drug Discovery Today: Technol. 2006, 3, 331- 337.
22. Zahedi, R. P.; Begonja, A. J.; Gambaryan, S.; Sickmann, A. Phosphoproteomics of human platelets: A quest for novel activation pathways. Biochim. Biophys. Acta 2006, 1764 (12), 1963-1976.
23. Carr, S. A.; Huddleston, M. J.; Annan, R. S. Selective detection and sequencing of phosphopeptides at the femtomole level by mass spectrometry. Anal. Biochem. 1996, 239 (2), 180-192.
24. Steen, H.; Kuster, B.; Mann, M. Quadrupole time-of-flight versus triple-quadrupole mass spectrometry for the determination of phosphopeptides by precursor ion scanning. J. Mass Spectrom. 2001, 36 (7), 782-790.
25. Covey, T.; Shushan, B.; Bonner, R.; Shroder, W.; Hucho, F.; Jornvall, H.; Hoog, J.-O.; Gustavsson, A.-M. Methods Protein Sequence Anal. 1991, 24, 9-256.
26. Unwin, R. D.; Griffiths, J. R.; Leverentz, M. K.; Grallert, A.; Hagan, I. M.; Whetton, A. D. Multiple reaction monitoring to identify sites of protein phosphorylation with high sensitivity. Mol. Cell. Proteomics 2005, 4 (8), 1134-1144.
27. 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.
28. Schroeder, M. J.; Shabanowitz, J.; Schwartz, J. C.; Hunt, D. F.; Coon, J. J. A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal. Chem. 2004, 76 (13), 3590-3598.
29. Chi, A.; Huttenhower, C.; Geer, L. Y.; Coon, J. J.; Syka, J. E. P.; Bai, D. L.; Shabanowitz, J.; Burke, D. J.; Troyanskaya, O. G.; Hunt, D. F. Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (7), 2193-2198.
30. Molina, H.; Horn, D. M.; Tang, N.; Mathivanan, S.; Pandey, A. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (7), 2199-2204.
31. 2-based phosphoproteomics applied to study endogenous phosphorylation in Drosophila melanogaster. J. Proteome Res. 2008, 7 (2), 687-697.
32. Bodenmiller, B.; Mueller, L. N.; Mueller, M.; Domon, B.; Aebersold, R. Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat. Methods 2007, 4 (3), 231-237.
33. Lazar, I. M.; Grym, J.; Foret, F. Microfabricated devices: A new sample introduction approach to mass spectrometry. Mass Spectrom. Rev. 2006, 25 (4), 573-594.
34. Yin, H.; Killeen, K.; Brennen, R.; Sobek, D.; Werlich, M.; van de Goor, T. Microfluidic chip for peptide analysis with an integrated HPLC column, sample enrichment column, and nanoelectrospray tip. Anal. Chem. 2005, 77 (2), 527-533.
35. Hardouin, J.; Joubert-Caron, R.; Caron, M. HPLC-chip-mass spectrometry for protein signature identifications. J. Sep. Sci. 2007, 30 (10), 1482-1487.
36. Vollmer, M.; Horth, P.; Rozing, G.; Coute, Y.; Grimm, R.; Hoch- strasser, D.; Sanchez, J. C. Multi-dimensional HPLC/MS of the nucleolar proteome using HPLC-chip/MS. J. Sep. Sci. 2006, 29 (4), 499-509.
37. Fortier, M. H.; Bonneil, E.; Goodley, P.; Thibault, P. Integrated microfluidic device for mass spectrometry-based proteomics and its application to biomarker discovery programs. Anal. Chem. 2005, 77 (6), 1631-1640.
38. Ghitun, M.; Bonneil, E.; Fortier, M. H.; Yin, H.; Killeen, K.; Thibault, P. Integrated microfluidic devices with enhanced separation performance: application to phosphoproteome analyses of differentiated cell model systems. J. Sep. Sci. 2006, 29 (11), 1539- 1549.
39. Ninonuevo, M.; An, H.; Yin, H.; Killeen, K.; Grimm, R.; Ward, R.; German, B.; Lebrilla, C. Nanoliquid chromatography-mass spectrometry of oligosaccharides employing graphitized carbon chromatography on microchip with a high-accuracy mass analyzer. Electrophoresis 2005, 26 (19), 3641-3649.
40. Ishihama, Y.; Rappsilber, J.; Mann, M. Modular stop and go extraction tips with stacked disks for parallel and multidimensional peptide fractionation in proteomics. J. Proteome Res. 2006, 5 (4), 988-994.
41. Lemeer, S.; Pinkse, M. W. H.; Mohammed, S.; van Breukelen, B.; den Hertog, J.; Slijper, M.; Heck, A. J. R. On-line automated in vivo zebrafish phosphoproteomics: From large-scale analysis down-to a single embryo. J. Proteome Res. 2008, 7, 1555-1564.
42. Schlosser, A.; Vanselow, J. T.; Kramer, A. Mapping of phosphorylation sites by a multi-protease approach with specific phosphopeptide enrichment and nanoLC-MS/MS analysis. Anal. Chem. 2005, 77 (16), 5243-5250.
43. Sugiyama, N.; Masuda, T.; Shlnoda, K.; Nakamura, A.; Tomita, M.; Ishihama, Y. Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications. Mol. Cell. Proteomics 2007, 6 (6), 1103- 1109.
44. 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.
45. Hemm, C.; Otto, S.; Wolf, C.; Haseloff, R. F.; Beyermann, M.; Krause, E. Evaluation of the titanium dioxide approach for MS analysis of phosphopeptides. J. Mass Spectrom. 2006, 41 (12), 1623-1632.