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Sci. Signal., 12 January 2010
Vol. 3, Issue 104, p. ra3
[DOI: 10.1126/scisignal.2000475]


Quantitative Phosphoproteomics Reveals Widespread Full Phosphorylation Site Occupancy During Mitosis

Jesper V. Olsen1,2*, Michiel Vermeulen1,3*, Anna Santamaria4*, Chanchal Kumar1,5*, Martin L. Miller2,6, Lars J. Jensen2, Florian Gnad1, Jürgen Cox1, Thomas S. Jensen7, Erich A. Nigg4, Søren Brunak2,7, and Matthias Mann1,2{dagger}

1 Department of Proteomics and Signal Transduction, Max-Planck-Institute for Biochemistry, Am Klopferspitz 18, D-82152 Martinsried near Munich, Germany.
2 Novo Nordisk Foundation Center for Protein Research, Faculty of Health Sciences, University of Copenhagen, Blegdamsvej 3, DK-2200 Copenhagen, Denmark.
3 Department of Physiological Chemistry and Cancer Genomics Centre, University Medical Centre Utrecht, 3584 CG Utrecht, the Netherlands.
4 Biozentrum, Universität Basel, Klingelbergstrasse 50/70, CH-4056 Basel, Switzerland.
5 Lilly Singapore Centre for Drug Discovery, 8A Biomedical Grove #02-05, Immunos, Biopolis, Singapore 138648, Singapore.
6 Computational Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA.
7 Center for Biological Sequence Analysis, Technical University of Denmark, Kemitorvet, Building 208, DK-2800 Lyngby, Denmark.

* These authors contributed equally to this work.

Abstract: Eukaryotic cells replicate by a complex series of evolutionarily conserved events that are tightly regulated at defined stages of the cell division cycle. Progression through this cycle involves a large number of dedicated protein complexes and signaling pathways, and deregulation of this process is implicated in tumorigenesis. We applied high-resolution mass spectrometry–based proteomics to investigate the proteome and phosphoproteome of the human cell cycle on a global scale and quantified 6027 proteins and 20,443 unique phosphorylation sites and their dynamics. Co-regulated proteins and phosphorylation sites were grouped according to their cell cycle kinetics and compared to publicly available messenger RNA microarray data. Most detected phosphorylation sites and more than 20% of all quantified proteins showed substantial regulation, mainly in mitotic cells. Kinase-motif analysis revealed global activation during S phase of the DNA damage response network, which was mediated by phosphorylation by ATM or ATR or DNA-dependent protein kinases. We determined site-specific stoichiometry of more than 5000 sites and found that most of the up-regulated sites phosphorylated by cyclin-dependent kinase 1 (CDK1) or CDK2 were almost fully phosphorylated in mitotic cells. In particular, nuclear proteins and proteins involved in regulating metabolic processes have high phosphorylation site occupancy in mitosis. This suggests that these proteins may be inactivated by phosphorylation in mitotic cells.

{dagger} To whom correspondence should be addressed. E-mail: mmann{at}

Citation: J. V. Olsen, M. Vermeulen, A. Santamaria, C. Kumar, M. L. Miller, L. J. Jensen, F. Gnad, J. Cox, T. S. Jensen, E. A. Nigg, S. Brunak, M. Mann, Quantitative Phosphoproteomics Reveals Widespread Full Phosphorylation Site Occupancy During Mitosis. Sci. Signal. 3, ra3 (2010).

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A. Pines, C. D. Kelstrup, M. G. Vrouwe, J. C. Puigvert, D. Typas, B. Misovic, A. de Groot, L. von Stechow, B. van de Water, E. H. J. Danen, et al. (2011)
Mol. Cell. Biol. 31, 4964-4977
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Interaction of Sororin Protein with Polo-like Kinase 1 Mediates Resolution of Chromosomal Arm Cohesion.
N. Zhang, A. K. Panigrahi, Q. Mao, and D. Pati (2011)
J. Biol. Chem. 286, 41826-41837
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Delineation of key regulatory elements identifies points of vulnerability in the mitogen-activated signaling network.
N. Jailkhani, S. Ravichandran, S. R. Hegde, Z. Siddiqui, S. C. Mande, and K. V. S. Rao (2011)
Genome Res. 21, 2067-2081
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Two Ancient Bacterial-like PPP Family Phosphatases from Arabidopsis Are Highly Conserved Plant Proteins That Possess Unique Properties.
R. G. Uhrig and G. B. Moorhead (2011)
Plant Physiology 157, 1778-1792
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Systematic Phosphorylation Analysis of Human Mitotic Protein Complexes.
B. Hegemann, J. R. A. Hutchins, O. Hudecz, M. Novatchkova, J. Rameseder, M. M. Sykora, S. Liu, M. Mazanek, P. Lenart, J.-K. Heriche, et al. (2011)
Science Signaling 4, rs12
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Online Nanoflow Multidimensional Fractionation for High Efficiency Phosphopeptide Analysis.
S. B. Ficarro, Y. Zhang, M. J. Carrasco-Alfonso, B. Garg, G. Adelmant, J. T. Webber, C. J. Luckey, and J. A. Marto (2011)
Mol. Cell. Proteomics 10, O111.011064
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KIBRA Protein Phosphorylation Is Regulated by Mitotic Kinase Aurora and Protein Phosphatase 1.
L. Xiao, Y. Chen, M. Ji, D. J. Volle, R. E. Lewis, M.-Y. Tsai, and J. Dong (2011)
J. Biol. Chem. 286, 36304-36315
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Phosphoproteomic Analysis of Salmonella-Infected Cells Identifies Key Kinase Regulators and SopB-Dependent Host Phosphorylation Events.
L. D. Rogers, N. F. Brown, Y. Fang, S. Pelech, and L. J. Foster (2011)
Science Signaling 4, rs9
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Correct Interpretation of Comprehensive Phosphorylation Dynamics Requires Normalization by Protein Expression Changes.
R. Wu, N. Dephoure, W. Haas, E. L. Huttlin, B. Zhai, M. E. Sowa, and S. P. Gygi (2011)
Mol. Cell. Proteomics 10, M111.009654
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