Quantitative site-specific phosphorylation dynamics of human protein kinases during mitotic progression

Molecular and Cellular Proteomics

Volumn 9, Issue 6, 2010, Pages 1167-1181

  Dulla, Kalyan ^a   Daub, Henrik ^a   Hornberger, Renate ^a   Nigg, Erich A ^a,b   Körner, Roman ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; MITOGEN ACTIVATED PROTEIN KINASE;

ARTICLE; DOWN REGULATION; DYNAMICS; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; INTROSPECTION; MASS SPECTROMETRY; MITOSIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; UPREGULATION;

AMINO ACID SEQUENCE; ENZYME ACTIVATION; HELA CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOSIS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 77953158465     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900335-MCP200     Document Type: Article

References (70)

1. Cohen, P. (2002) The origins of protein phosphorylation. Nat. Cell Biol. 4, E127-E130
2. Pawson, T., and Scott, J. D. (2005) Protein phosphorylation in signaling-50 years and counting. Trends Biochem. Sci. 30, 286-290 (Pubitemid 40799044)
3. Graves, J. D., and Krebs, E. G. (1999) Protein phosphorylation and signal transduction. Pharmacol. Ther. 82, 111-121
4. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912-1934 (Pubitemid 35425239)
5. Draviam, V. M., Orrechia, S., Lowe, M., Pardi, R., and Pines, J. (2001) The localization of human cyclins B1 and B2 determines CDK1 substrate specificity and neither enzyme requires MEK to disassemble the Golgi apparatus. J. Cell Biol. 152, 945-958
6. Bischoff, J. R., Anderson, L., Zhu, Y., Mossie, K., Ng, L., Souza, B., Schryver, B., Flanagan, P., Clairvoyant, F., Ginther, C., Chan, C. S., Novotny, M., Slamon, D. J., and Plowman, G. D. (1998) A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J. 17, 3052-3065 (Pubitemid 28254378)
7. Mundt, K. E., Golsteyn, R. M., Lane, H. A., and Nigg, E. A. (1997) On the regulation and function of human polo-like kinase 1 (PLK1): effects of overexpression on cell cycle progression. Biochem. Biophys. Res. Commun. 239, 377-385
8. Ubersax, J. A., and Ferrell, J. E., Jr. (2007) Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell Biol. 8, 530-541
9. Nolen, B., Taylor, S., and Ghosh, G. (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell 15, 661-675 (Pubitemid 39194898)
10. Jang, Y. J., Ma, S., Terada, Y., and Erikson, R. L. (2002) Phosphorylation of threonine 210 and the role of serine 137 in the regulation of mammalian polo-like kinase. J. Biol. Chem. 277, 44115-44120 (Pubitemid 36157840)
11. Krek, W., and Nigg, E. A. (1992) Cell cycle regulation of vertebrate p34cdc2 activity: identification of Thr161 as an essential in vivo phosphorylation site. New Biol. 4, 323-329
12. Krek, W., and Nigg, E. A. (1991) Differential phosphorylation of vertebrate p34cdc2 kinase at the G1/S and G2/M transitions of the cell cycle: identification of major phosphorylation sites. EMBO J. 10, 305-316 (Pubitemid 21905480)
13. Elia, A. E., Cantley, L. C., and Yaffe, M. B. (2003) Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299, 1228-1231
14. Qi, W., Tang, Z., and Yu, H. (2006) Phosphorylation- and polo-box-dependent binding of Plk1 to Bub1 is required for the kinetochore localization of Plk1. Mol. Biol. Cell 17, 3705-3716 (Pubitemid 44156460)
15. Saurin, A. T., Durgan, J., Cameron, A. J., Faisal, A., Marber, M. S., and Parker, P. J. (2008) The regulated assembly of a PKCepsilon complex controls the completion of cytokinesis. Nat. Cell Biol. 10, 891-901
16. Biondi, R. M., Komander, D., Thomas, C. C., Lizcano, J. M., Deak, M., Alessi, D. R., and van Aalten, D. M. (2002) High resolution crystal structure of the human PDK1 catalytic domain defines the regulatory phosphopeptide docking site. EMBO J. 21, 4219-4228
17. Watanabe, N., Arai, H., Nishihara, Y., Taniguchi, M., Watanabe, N., Hunter, T., and Osada, H. (2004) M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP. Proc. Natl. Acad. Sci. U.S.A. 101, 4419-4424 (Pubitemid 38437427)
18. Hunter, T. (2007) The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 28, 730-738
19. Nigg, E. A. (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2, 21-32
20. Musacchio, A., and Salmon, E. D. (2007) The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379-393
21. Li, J. J., and Li, S. A. (2006) Mitotic kinases: the key to duplication, segregation, and cytokinesis errors, chromosomal instability, and oncogenesis. Pharmacol. Ther. 111, 974-984
22. Barr, F. A., Silljé, H. H., and Nigg, E. A. (2004) Polo-like kinases and the orchestration of cell division. Nat. Rev. Mol. Cell Biol. 5, 429-440
23. Marumoto, T., Zhang, D., and Saya, H. (2005) Aurora-A - a guardian of poles. Nat. Rev. Cancer 5, 42-50
24. Meraldi, P., Honda, R., and Nigg, E. A. (2004) Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr. Opin. Genet. Dev. 14, 29-36 (Pubitemid 38167474)
25. Morgan, D. (2007) The Cell Cycle: Principles of Control, 1st Ed., New Science Press Ltd., London
26. Tang, J., Yang, X., and Liu, X. (2008) Phosphorylation of Plk1 at Ser326 regulates its functions during mitotic progression. Oncogene 27, 6635-6645
27. Kittler, R., Pelletier, L., Heninger, A. K., Slabicki, M., Theis, M., Miroslaw, L., Poser, I., Lawo, S., Grabner, H., Kozak, K., Wagner, J., Surendranath, V., Richter, C., Bowen, W., Jackson, A. L., Habermann, B., Hyman, A. A., and Buchholz, F. (2007) Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat. Cell Biol. 9, 1401-1412 (Pubitemid 350201753)
28. Johnson, S. A., and Hunter, T. (2005) Kinomics: methods for deciphering the kinome. Nat. Methods 2, 17-25
29. Sugiyama, N., Masuda, T., Shinoda, K., Nakamura, A., Tomita, M., and Ishihama, Y. (2007) Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications. Mol. Cell. Proteomics 6, 1103-1109 (Pubitemid 47019410)
30. Schreiber, T. B., Mäusbacher, N., Breitkopf, S. B., Grundner-Culemann, K., and Daub, H. (2008) Quantitative phosphoproteomics - an emerging key technology in signal-transduction research. Proteomics 8, 4416-4432
31. Daub, H., Olsen, J. V., Bairlein, M., Gnad, F., Oppermann, F. S., Körner, R., Greff, Z., Kéri, G., Stemmann, O., and Mann, M. (2008) Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 31, 438-448
32. Bantscheff, M., Eberhard, D., Abraham, Y., Bastuck, S., Boesche, M., Hobson, S., Mathieson, T., Perrin, J., Raida, M., Rau, C., Reader, V., Sweetman, G., Bauer, A., Bouwmeester, T., Hopf, C., Kruse, U., Neubauer, G., Ramsden, N., Rick, J., Kuster, B., and Drewes, G. (2007) Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat. Biotechnol. 25, 1035-1044 (Pubitemid 47517638)
33. Elowe, S., Hümmer, S., Uldschmid, A., Li, X., and Nigg, E. A. (2007) Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev. 21, 2205-2219 (Pubitemid 47360842)
34. Brehmer, D., Greff, Z., Godl, K., Blencke, S., Kurtenbach, A., Weber, M., Müller, S., Klebl, B., Cotten, M., Kéri, G., Wissing, J., and Daub, H. (2005) Cellular targets of gefitinib. Cancer Res. 65, 379-382
35. Godl, K., Gruss, O. J., Eickhoff, J., Wissing, J., Blencke, S., Weber, M., Degen, H., Brehmer, D., Orfi, L., Horváth, Z., Kéri, G., Müller, S., Cotten, M., Ullrich, A., and Daub, H. (2005) Proteomic characterization of the angiogenesis inhibitor SU6668 reveals multiple impacts on cellular kinase signaling. Cancer Res. 65, 6919-6926 (Pubitemid 41060731)
36. Wissing, J., Jänsch, L., Nimtz, M., Dieterich, G., Hornberger, R., Kéri, G., Wehland, J., and Daub, H. (2007) Proteomics analysis of protein kinases by target class-selective prefractionation and tandem mass spectrometry. Mol. Cell. Proteomics 6, 537-547 (Pubitemid 46554547)
37. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (Pubitemid 26101214)
38. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670 (Pubitemid 36176744)
39. Olsen, J. V., de Godoy, L. M., Li, G., Macek, B., Mortensen, P., Pesch, R., Makarov, A., Lange, O., Horning, S., and Mann, M. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010-2021 (Pubitemid 41830195)
40. Schroeder, M. J., Shabanowitz, J., Schwartz, J. C., Hunt, D. F., and Coon, J. J. (2004) A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal. Chem. 76, 3590-3598 (Pubitemid 38868819)
41. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
42. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567
43. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214
44. Choi, H., and Nesvizhskii, A. I. (2008) False discovery rates and related statistical concepts in mass spectrometry-based proteomics. J. Proteome Res. 7, 47-50 (Pubitemid 351171114)
45. Nesvizhskii, A. I., and Aebersold, R. (2005) Interpretation of shotgun proteomic data: the protein inference problem. Mol. Cell. Proteomics 4, 1419-1440
46. Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., Doerks, T., Julien, P., Roth, A., Simonovic, M., Bork, P., and von Mering, C. (2009) STRING 8 - a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412-D416
47. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (Pubitemid 37428274)
48. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
49. Mann, M. (2006) Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 7, 952-958
50. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
51. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J., and Gygi, S. P. (2008) A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 105, 10762-10767
52. Wang, B., Malik, R., Nigg, E. A., and Körner, R. (2008) Evaluation of the low-specificity protease elastase for large-scale phosphoproteome analysis. Anal. Chem. 80, 9526-9533
53. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (Pubitemid 44647421)
54. Vulsteke, V., Beullens, M., Boudrez, A., Keppens, S., Van Eynde, A., Rider, M. H., Stalmans, W., and Bollen, M. (2004) Inhibition of spliceosome assembly by the cell cycle-regulated protein kinase MELK and involvement of splicing factor NIPP1. J. Biol. Chem. 279, 8642-8647 (Pubitemid 38295919)
55. Ma, W., Koch, J. A., and Viveiros, M. M. (2008) Protein kinase C delta (PKCdelta) interacts with microtubule organizing center (MTOC)-associated proteins and participates in meiotic spindle organization. Dev. Biol. 320, 414-425
56. Sturgill, T. W. (2008) MAP kinase: it's been longer than fifteen minutes. Biochem. Biophys. Res. Commun. 371, 1-4
57. Willard, F. S., and Crouch, M. F. (2001) MEK, ERK, and p90RSK are present on mitotic tubulin in Swiss 3T3 cells: a role for the MAP kinase pathway in regulating mitotic exit. Cell. Signal. 13, 653-664
58. Shinohara, M., Mikhailov, A. V., Aguirre-Ghiso, J. A., and Rieder, C. L. (2006) Extracellular signal-regulated kinase 1/2 activity is not required in mammalian cells during late G2 for timely entry into or exit from mitosis. Mol. Biol. Cell 17, 5227-5240 (Pubitemid 44907364)
59. Cha, H., Wang, X., Li, H., and Fornace, A. J., Jr. (2007) A functional role for p38 MAPK in modulating mitotic transit in the absence of stress. J. Biol. Chem. 282, 22984-22992 (Pubitemid 47267360)
60. Campos, C. B., Bédard, P. A., and Linden, R. (2002) Activation of p38 mitogen-activated protein kinase during normal mitosis in the developing retina. Neuroscience 112, 583-591 (Pubitemid 34634152)
61. Mikhailov, A., Shinohara, M., and Rieder, C. L. (2004) Topoisomerase II and histone deacetylase inhibitors delay the G2/M transition by triggering the p38 MAPK checkpoint pathway. J. Cell Biol. 166, 517-526 (Pubitemid 39097171)
62. Kauffman, S., and Wille, J. J. (1975) The mitotic oscillator in Physarum polycephalum. J. Theor. Biol. 55, 47-93
63. Murray, A. W., Solomon, M. J., and Kirschner, M. W. (1989) The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339, 280-286
64. Oppermann, F. S., Gnad, F., Olsen, J. V., Hornberger, R., Greff, Z., Kéri, G., Mann, M., and Daub, H. (2009) Large-scale proteomics analysis of the human kinome. Mol. Cell. Proteomics 8, 1751-1764
65. Murata-Hori, M., Tatsuka, M., and Wang, Y. L. (2002) Probing the dynamics and functions of aurora B kinase in living cells during mitosis and cytokinesis. Mol. Biol. Cell 13, 1099-1108 (Pubitemid 34309608)
66. Gassmann, R., Carvalho, A., Henzing, A. J., Ruchaud, S., Hudson, D. F., Honda, R., Nigg, E. A., Gerloff, D. L., and Earnshaw, W. C. (2004) Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle. J. Cell Biol. 166, 179-191 (Pubitemid 38988771)
67. Neef, R., Gruneberg, U., Kopajtich, R., Li, X., Nigg, E. A., Sillje, H., and Barr, F. A. (2007) Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat. Cell Biol. 9, 436-444 (Pubitemid 46511077)
68. Wilker, E. W., van Vugt, M. A., Artim, S. A., Huang, P. H., Petersen, C. P., Reinhardt, H. C., Feng, Y., Sharp, P. A., Sonenberg, N., White, F. M., and Yaffe, M. B. (2007) 14-3-3sigma controls mitotic translation to facilitate cytokinesis. Nature 446, 329-332 (Pubitemid 46426148)
69. Villén, J., and Gygi, S. P. (2008) The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat. Protoc. 3, 1630-1638
70. McNulty, D. E., and Annan, R. S. (2008) Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol. Cell. Proteomics 7, 971-980