Highly robust, automated, and sensitive online TiO2-based phosphoproteomics applied to study endogenous phosphorylation in Drosophila melanogaster

Journal of Proteome Research

Volumn 7, Issue 2, 2008, Pages 687-697

  Pinkse, Martijn W H ^a,b   Mohammed, Shabaz ^a   Gouw, Joost W ^a   Van Breukelen, Bas ^a   Vos, Harmjan R ^a   Heck, Albert J R ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Automated, Large Scale; Phosphopeptide iso electric point; Phosphoproteomics; TiO2 phosphopeptide enrichment

Indexed keywords

CATION; PEPTIDE; PHOSPHOPEPTIDE; TITANIUM DIOXIDE;

ARTICLE; AUTOMATION; CELL LYSATE; CHROMATOGRAPHY; DROSOPHILA MELANOGASTER; EVALUATION; ION EXCHANGE CHROMATOGRAPHY; NONHUMAN; PHOSPHOPROTEOMIC; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHROMATOGRAPHY, ION EXCHANGE; CHROMATOGRAPHY, LIQUID; DROSOPHILA MELANOGASTER; MOLECULAR SEQUENCE DATA; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TITANIUM;

DROSOPHILA MELANOGASTER;

EID: 39749186759     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr700605z     Document Type: Article

References (36)

1. Morandell, S.; Stasyk, T.; Grosstessner-Hain, K.; Roitinger, E.; Mechtler, K.; Bonn, G. K.; Huber, L. A. Phosphoproteomics strategies for the functional analysis of signal transduction. Proteomics 2006, 6 (14), 4047-4056.
2. Pinkse, M. W. H.; Heck, A. J. R. Essential enrichment strategies in phosphoproteomics. Drug Discovery Today: Technol. 2006, 3 (3), 331-337.
3. Reinders, J.; Sickmann, A. State-of-the-art in phosphoproteomics. Proteomics 2005, 5 (16), 4052-4061.
4. Garcia, B. A.; Shabanowitz, J.; Hunt, D. F. Analysis of protein phosphorylation by mass spectrometry. Methods 2005, 35 (3), 256-264.
5. Jensen, O. N. Interpreting the protein language using proteomics. Nat. Rev. Mol. Cell Biol. 2006, 7 (6), 391-403.
6. Mann, M.; Jensen, O. N. Proteomic analysis of post-translational modifications. Nat. Biotechnol. 2003, 21 (3), 255-261.
7. Posewitz, M. C.; Tempst, P. Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal. Chem. 1999, 71 (14), 2883-2892.
8. Ficarro, S. B.; McCleland, M. L.; Stukenberg, P. T.; Burke, D. J.; Ross, M. M.; Shabanowitz, J.; Hunt, D. F.; White, F. M. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 2002, 20 (3), 301-305.
9. Pinkse, M. W.; Uitto, P. M.; Hilhorst, M. J.; Ooms, B.; Heck, A. J. 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.
10. Kuroda, I.; Shintani, Y.; Motokawa, M.; Abe, S.; Furuno, M. Phosphopeptide-selective column-switching RP-HPLC with a titania precolumn. Anal. Sci. 2004, 20 (9), 1313-1319.
11. 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.
12. Stensballe, A.; Andersen, S.; Jensen, O. N. Characterization of phosphoproteins from electrophoretic gels by nanoscale Fe(III) affinity chromatography with off-line mass spectrometry analysis. Proteomics 2001, 1 (2), 207-222.
13. Thingholm, T. E.; Jorgensen, T. J. D.; Jensen, O. N.; Larsen, M. R. Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nat. Protocols 2006, 1 (4), 1929-1935.
14. Kweon, H. K.; Hakansson, K. Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Anal. Chem. 2006, 78 (6), 1743-1749.
15. Mazanek, M.; Mitulovi, Ã. G.; Herzog, F.; Stingl, C.; Hutchins, J. R. A.; Peters, J.-M.; Mechtler, K. Titanium dioxide as a chemoaffinity solid phase in offline phosphopeptide chromatography prior to HPLC-MS/MS analysis. Nat. Protocols 2006, 1 (4), 1977-1987.
16. Ficarro, S. B.; Salomon, A. R.; Brill, L. M.; Mason, D. E.; Stettler-Gill, M.; Brock, A.; Peters, E. C. Automated immobilized metal affinity chromatography/nano-liquid chromatography/electrospray ionization mass spectrometry platform for profiling protein phosphorylation sites. Rapid Commun. Mass Spectrom. 2005, 19 (1), 57-71.
17. Wang, J.; Zhang, Y.; Jiang, H.; Cai, Y.; Qian, X. Phosphopeptide detection using automated online IMAC-capillary LC-ESI-MS/MS. Proteomics 2006, 6 (2), 404-411.
18. Beausoleil, S. A.; Jedrychowski, M.; Schwartz, D.; Elias, J. E.; Villen, J.; Li, J.; 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. 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.
20. 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.
21. Benschop, J. J.; Mohammed, S.; O'Flaherty, M.; Heck, A. J.; Slijper, M.; Menke, F. L. Quantitative phospho-proteomics of early elicitor signalling in Arabidopsis. Mol. Cell. Proteomics 2007, 6, 1198-1214.
22. Rappsilber, J.; Ishihama, Y.; Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 2003, 75 (3), 663-670.
23. Elias, J. E.; Haas, W.; Faherty, B. K.; Gygi, S. P. Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2005, 2 (9), 667-75.
24. Bjellqvist, B.; Basse, B.; Olsen, E.; Celis, J. E. Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 1994, 15 (3-4), 529-539.
25. Bjellqvist, B.; Hughes, G. J.; Pasquali, C.; Paquet, N.; Ravier, F.; Sanchez, J. C.; Frutiger, S.; Hochstrasser, D. The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 1993, 14 (10), 1023-1031.
26. Kumar, Y.; Khachane, A.; Belwal, M.; Das, S.; Somsundaram, K.; Tatu, U. ProteoMod: A new tool to quantitate protein posttranslational modifications. Proteomics 2004, 4 (6), 1672-1683.
27. 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.
28. 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.
29. 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.
30. Sugiyama, N.; Masuda, T.; Shinoda, K.; Nakamura, A.; Tomita, M.; Ishihama, Y. Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for NanoLC-MS/MS in proteomics applications. Mol. Cell. Proteomics 2007, 6, 1103-1109.
31. 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.
32. Klemm, 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.
33. 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.
34. 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.
35. Krijgsveld, J.; Gauci, S.; Dormeyer, W.; Heck, A. J. In-gel isoelectric focusing of peptides as a tool for improved protein identification. J. Proteome Res. 2006, 5 (7), 1721-1730.
36. Jones, D. R.; Bultsma, Y.; Keune, W. J.; Halstead, J. R.; Elouarrat, D.; Mohammed, S.; Heck, A. J.; D'Santos, C. S.; Divecha, N. Nuclear PtdIns5P as a transducer of stress signaling: an in vivo role for PIP4Kbeta. Mol. Cell 2006, 23 (5), 685-695.