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Originally published In Press as doi:10.1074/mcp.M400219-MCP200 on January 22, 2005.
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Molecular & Cellular Proteomics 4:310-327, 2005.
© 2005 by The American Society for Biochemistry and Molecular Biology, Inc.

Research

Quantitative Phosphoproteomics Applied to the Yeast Pheromone Signaling Pathway*,S

Albrecht Gruhler{ddagger}, Jesper V. Olsen{ddagger}, Shabaz Mohammed, Peter Mortensen, Nils J. Færgeman, Matthias Mann§ and Ole N. Jensen

From the Protein Research Group, Lipid/Hormone Group and Center for Experimental Bioinformatics (CEBI), Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Campusvej 55, DK-5230 Odense M, Denmark

Cellular processes such as proliferation, differentiation, and adaptation to environmental changes are regulated by protein phosphorylation. Development of sensitive and comprehensive analytical methods for determination of protein phosphorylation is therefore a necessity in the pursuit of a detailed molecular view of complex biological processes. We present a quantitative modification-specific proteomic approach that combines stable isotope labeling by amino acids in cell culture (SILAC) for quantitation with IMAC for phosphopeptide enrichment and three stages of mass spectrometry (MS/MS/MS) for identification. This integrated phosphoproteomic technology identified and quantified phosphorylation in key regulator and effector proteins of a prototypical G-protein-coupled receptor signaling pathway, the yeast pheromone response. SILAC encoding of yeast proteomes was achieved by incorporation of [13C6]arginine and [13C6]lysine in a double auxotroph yeast strain. Pheromone-treated yeast cells were mixed with SILAC-encoded cells as the control and lysed, and extracted proteins were digested with trypsin. Phosphopeptides were enriched by a combination of strong cation exchange chromatography and IMAC. Phosphopeptide fractions were analyzed by LC-MS using a linear ion trap-Fourier transform ion cyclotron resonance mass spectrometer. MS/MS and neutral loss-directed MS/MS/MS analysis allowed detection and sequencing of phosphopeptides with exceptional accuracy and specificity. Of more than 700 identified phosphopeptides, 139 were differentially regulated at least 2-fold in response to mating pheromone. Among these regulated proteins were components belonging to the mitogen-activated protein kinase signaling pathway and to downstream processes including transcriptional regulation, the establishment of polarized growth, and the regulation of the cell cycle.

§ To whom correspondence may be addressed. E-mail: mann{at}bmb.sdu.dk

To whom correspondence may be addressed. E-mail: jenseno{at}bmb.sdu.dk


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M. R. Larsen, T. E. Thingholm, O. N. Jensen, P. Roepstorff, and T. J. D. Jorgensen
Highly Selective Enrichment of Phosphorylated Peptides from Peptide Mixtures Using Titanium Dioxide Microcolumns
Mol. Cell. Proteomics, July 1, 2005; 4(7): 873 - 886.
[Abstract] [Full Text] [PDF]

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T. Sparre, M. R. Larsen, P. E. Heding, A. E. Karlsen, O. N. Jensen, and F. Pociot
Unraveling the Pathogenesis of Type 1 Diabetes with Proteomics: Present And Future Directions
Mol. Cell. Proteomics, April 1, 2005; 4(4): 441 - 457.
[Abstract] [Full Text] [PDF]


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