Rapid determination of multiple linear kinase substrate motifs by mass spectrometry

Chemistry and Biology

Volumn 19, Issue 5, 2012, Pages 608-618

  Kettenbach, Arminja N ^a   Wang, Tuobin ^c   Faherty, Brendan K ^b   Madden, Dean R ^b   Knapp, Stefan ^d   Bailey Kellogg, Chris ^c   Gerber, Scott A ^a,b  

^a NORRIS COTTON CANCER CENTER   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c Dartmouth Department of Computer Science_Dartmouth College   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NOCODAZOLE; PACLITAXEL; PHOSPHOTRANSFERASE; POLO LIKE KINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ASSAY; ENZYME ISOLATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; HELA CELL; HIGH THROUGHPUT SEQUENCING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; ION EXCHANGE CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PURIFICATION; TANDEM MASS SPECTROMETRY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; HELA CELLS; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; PEPTIDES; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; SUBSTRATE SPECIFICITY; TIME FACTORS;

EID: 84861592048     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2012.04.011     Document Type: Article

References (48)

1. J. Alexander, D. Lim, B.A. Joughin, B. Hegemann, J.R. Hutchins, T. Ehrenberger, F. Ivins, F. Sessa, O. Hudecz, and E.A. Nigg Spatial exclusivity combined with positive and negative selection of phosphorylation motifs is the basis for context-dependent mitotic signaling Sci. Signal. 4 2011 ra42
2. F.A. Barr, H.H. Silljé, and E.A. Nigg Polo-like kinases and the orchestration of cell division Nat. Rev. Mol. Cell Biol. 5 2004 429 440
3. A.N. Bullock, J. Debreczeni, A.L. Amos, S. Knapp, and B.E. Turk Structure and substrate specificity of the Pim-1 kinase J. Biol. Chem. 280 2005 41675 41682
4. A.N. Bullock, S. Das, J.E. Debreczeni, P. Rellos, O. Fedorov, F.H. Niesen, K. Guo, E. Papagrigoriou, A.L. Amos, and S. Cho Kinase domain insertions define distinct roles of CLK kinases in SR protein phosphorylation Structure 17 2009 352 362
5. L.E. Campbell, and C.G. Proud Differing substrate specificities of members of the DYRK family of arginine-directed protein kinases FEBS Lett. 510 2002 31 36
6. P. Cohen The regulation of protein function by multisite phosphorylation - a 25 year update Trends Biochem. Sci. 25 2000 596 601
7. G.E. Crooks, G. Hon, J.M. Chandonia, and S.E. Brenner WebLogo: a sequence logo generator Genome Res. 14 2004 1188 1190
8. J. Dai, S. Sultan, S.S. Taylor, and J.M. Higgins The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment Genes Dev. 19 2005 472 488
9. N. Echols, P. Harrison, S. Balasubramanian, N.M. Luscombe, P. Bertone, Z. Zhang, and M. Gerstein Comprehensive analysis of amino acid and nucleotide composition in eukaryotic genomes, comparing genes and pseudogenes Nucleic Acids Res. 30 2002 2515 2523
10. J.E. Elias, and S.P. Gygi Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 4 2007 207 214
11. S. Elowe, S. Hümmer, A. Uldschmid, X. Li, and E.A. Nigg Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions Genes Dev. 21 2007 2205 2219
12. J.K. Eng, A.L. McCormack, and J.R. Yates Iii An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database J. Am. Soc. Mass Spectrom. 5 1994 976 989
13. J. Eswaran, D. Patnaik, P. Filippakopoulos, F. Wang, R.L. Stein, J.W. Murray, J.M. Higgins, and S. Knapp Structure and functional characterization of the atypical human kinase haspin Proc. Natl. Acad. Sci. USA 106 2009 20198 20203
14. B.K. Faherty, and S.A. Gerber MacroSEQUEST: efficient candidate-centric searching and high-resolution correlation analysis for large-scale proteomics data sets Anal. Chem. 82 2010 6821 6829
15. J.M. Gilmore, A.N. Kettenbach, and S.A. Gerber Increasing phosphoproteomic coverage through sequential digestion by complementary proteases Anal. Bioanal. Chem. 402 2012 711 720
16. W. Haas, B.K. Faherty, S.A. Gerber, J.E. Elias, S.A. Beausoleil, C.E. Bakalarski, X. Li, J. Villén, and S.P. Gygi Optimization and use of peptide mass measurement accuracy in shotgun proteomics Mol. Cell. Proteomics 5 2006 1326 1337
17. D.K. Han, J. Eng, H. Zhou, and R. Aebersold Quantitative profiling of differentiation-induced microsomal proteins using isotope-coded affinity tags and mass spectrometry Nat. Biotechnol. 19 2001 946 951
18. S. Himpel, W. Tegge, R. Frank, S. Leder, H.G. Joost, and W. Becker Specificity determinants of substrate recognition by the protein kinase DYRK1A J. Biol. Chem. 275 2000 2431 2438
19. E.J. Hsieh, M.R. Hoopmann, B. MacLean, and M.J. MacCoss Comparison of database search strategies for high precursor mass accuracy MS/MS data J. Proteome Res. 9 2010 1138 1143
20. T. Hunter, and B.M. Sefton Transforming gene product of Rous sarcoma virus phosphorylates tyrosine Proc. Natl. Acad. Sci. USA 77 1980 1311 1315
21. R.L. Hurley, K.A. Anderson, J.M. Franzone, B.E. Kemp, A.R. Means, and L.A. Witters The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases J. Biol. Chem. 280 2005 29060 29066
22. J.E. Hutti, E.T. Jarrell, J.D. Chang, D.W. Abbott, P. Storz, A. Toker, L.C. Cantley, and B.E. Turk A rapid method for determining protein kinase phosphorylation specificity Nat. Methods 1 2004 27 29
23. A.N. Kettenbach, and S.A. Gerber Rapid and reproducible single-stage phosphopeptide enrichment of complex peptide mixtures: application to general and phosphotyrosine-specific phosphoproteomics experiments Anal. Chem. 83 2011 7635 7644
24. A.N. Kettenbach, J. Rush, and S.A. Gerber Absolute quantification of protein and post-translational modification abundance with stable isotope-labeled synthetic peptides Nat. Protoc. 6 2011 175 186
25. A.N. Kettenbach, D.K. Schweppe, B.K. Faherty, D. Pechenick, A.A. Pletnev, and S.A. Gerber Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells Sci. Signal. 4 2011 rs5
26. G.C. Leung, C.S. Ho, I.M. Blasutig, J.M. Murphy, and F. Sicheri Determination of the Plk4/Sak consensus phosphorylation motif using peptide spots arrays FEBS Lett. 581 2007 77 83
27. W. Li, and A. Godzik Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences Bioinformatics 22 2006 1658 1659
28. R. Linding, L.J. Jensen, A. Pasculescu, M. Olhovsky, K. Colwill, P. Bork, M.B. Yaffe, and T. Pawson NetworKIN: a resource for exploring cellular phosphorylation networks Nucleic Acids Res. 36 Database issue 2008 D695 D699
29. A.J. Link, J. Eng, D.M. Schieltz, E. Carmack, G.J. Mize, D.R. Morris, B.M. Garvik, and J.R. Yates 3rd Direct analysis of protein complexes using mass spectrometry Nat. Biotechnol. 17 1999 676 682
30. G. Manning, D.B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam The protein kinase complement of the human genome Science 298 2002 1912 1934
31. M.L. Miller, L.J. Jensen, F. Diella, C. Jorgensen, M. Tinti, L. Li, M. Hsiung, S.A. Parker, J. Bordeaux, and T. Sicheritz-Ponten Linear motif atlas for phosphorylation-dependent signaling Sci. Signal. 1 2008 ra2
32. J. Mok, P.M. Kim, H.Y. Lam, S. Piccirillo, X. Zhou, G.R. Jeschke, D.L. Sheridan, S.A. Parker, V. Desai, and M. Jwa Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs Sci. Signal. 3 2010 ra12
33. Y. Moshe, J. Boulaire, M. Pagano, and A. Hershko Role of Polo-like kinase in the degradation of early mitotic inhibitor 1, a regulator of the anaphase promoting complex/cyclosome Proc. Natl. Acad. Sci. USA 101 2004 7937 7942
34. H. Nakajima, F. Toyoshima-Morimoto, E. Taniguchi, and E. Nishida Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate J. Biol. Chem. 278 2003 25277 25280
35. S.B. Needleman, and C.D. Wunsch A general method applicable to the search for similarities in the amino acid sequence of two proteins J. Mol. Biol. 48 1970 443 453
36. S.E. Ong, B. Blagoev, I. Kratchmarova, D.B. Kristensen, H. Steen, A. Pandey, and M. Mann Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 1 2002 376 386
37. M.W.H. Pinkse, P.M. Uitto, M.J. Hilhorst, B. Ooms, and A.J.R. Heck Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns Anal. Chem. 76 2004 3935 3943
38. V. Pogacic, A.N. Bullock, O. Fedorov, P. Filippakopoulos, C. Gasser, A. Biondi, S. Meyer-Monard, S. Knapp, and J. Schwaller Structural analysis identifies imidazo[1,2-b]pyridazines as PIM kinase inhibitors with in vitro antileukemic activity Cancer Res. 67 2007 6916 6924
39. O. Schilling, and C.M. Overall Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites Nat. Biotechnol. 26 2008 685 694
40. D. Schwartz, and S.P. Gygi An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets Nat. Biotechnol. 23 2005 1391 1398
41. Z. Songyang, S. Blechner, N. Hoagland, M.F. Hoekstra, H. Piwnica-Worms, and L.C. Cantley Use of an oriented peptide library to determine the optimal substrates of protein kinases Curr. Biol. 4 1994 973 982
42. N. Sugiyama, T. Masuda, K. Shinoda, A. Nakamura, M. Tomita, and Y. Ishihama Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications Mol. Cell. Proteomics 6 2007 1103 1109
43. T. Taus, T. Köcher, P. Pichler, C. Paschke, A. Schmidt, C. Henrich, and K. Mechtler Universal and confident phosphorylation site localization using phosphoRS J. Proteome Res. 10 2011 5354 5362
44. J.A. Ubersax, and J.E. Ferrell Jr. Mechanisms of specificity in protein phosphorylation Nat. Rev. Mol. Cell Biol. 8 2007 530 541
45. J. Villén, and S.P. Gygi The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry Nat. Protoc. 3 2008 1630 1638
46. J. Villén, S.A. Beausoleil, S.A. Gerber, and S.P. Gygi Large-scale phosphorylation analysis of mouse liver Proc. Natl. Acad. Sci. USA 104 2007 1488 1493
47. M.B. Yaffe Novel at the library Nat. Methods 1 2004 13 14
48. M.B. Yaffe, G.G. Leparc, J. Lai, T. Obata, S. Volinia, and L.C. Cantley A motif-based profile scanning approach for genome-wide prediction of signaling pathways Nat. Biotechnol. 19 2001 348 353