Motif decomposition of the phosphotyrosine proteome reveals a new N-terminal binding motif for SHIP2

Molecular and Cellular Proteomics

Volumn 7, Issue 1, 2008, Pages 181-192

  Miller, Martin Lee ^a   Hanke, Stefan ^b   Hinsby, Anders Mørkeberg ^a   Friis, Carsten ^a   Brunak, Søren ^a   Mann, Matthias ^b   Blom, Nikolaj ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEIC ACID; PHOSPHATASE; PHOSPHOPROTEIN; PHOSPHOTYROSINE; PROTEIN SH2; PROTEOME; SH2 DOMAIN CONTAINING INOSITOL PHOSPHATASE 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HYDROPHOBICITY; IN VIVO STUDY; MASS SPECTROMETRY; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CLUSTER ANALYSIS; HUMANS; HYDROPHOBICITY; MOLECULAR SEQUENCE DATA; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHOTYROSINE; PHYLOGENY; PROTEIN BINDING; PROTEOME; REPRODUCIBILITY OF RESULTS;

EUKARYOTA;

EID: 39049154319     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700241-MCP200     Document Type: Article

References (56)

1. Yaffe, M. B. (2002) Phosphotyrosine-binding domains in signal transduction. Nat. Rev. Mol. Cell Biol. 3, 177-186
2. Pawson, T. (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116, 191-203
3. Bork, P., and Koonin, E. V. (1996) Protein sequence motifs. Curr. Opin. Struct. Biol. 6, 366-376
4. Songyang, Z., Shoelson, S. E., McGlade, J., Olivier, P., Pawson, T., Bustelo, X. R., Barbacid, M., Sabe, H., Hanafusa, H., and Yi, T. (1994) Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14, 2777-2785
5. Songyang, Z., Margolis, B., Chaudhuri, M., Shoelson, S. E., and Cantley, L. C. (1995) The phosphotyrosine interaction domain of SHC recognizes tyrosine-phosphorylated NPXY motif. J. Biol. Chem. 270, 14863-14866
6. Ballif, B. A., Villen, J., Beausoleil, S. A., Schwartz, D., and Gygi, S. P. (2004) Phosphoproteomic analysis of the developing mouse brain. Mol. Cell. Proteomics 3, 1093-1101
7. Beausoleil, S. A., Jedrychowski, M., Schwartz, D., Elias, J. E., Villen, J., Li, J., Cohn, M. A., Cantley, L. C., and Gygi, S. P. (2004) Large-scale characterization of HeLa call nuclear phosphoproteins. Proc. Natl. Acad. Sci. U. S. A. 101, 12130-12135
8. Brill, L. M., Salomon, A. R., Ficarro, S. B., Mukherji, M., Stettler-Gill, M., and Peters, E. C. (2004) Robust phosphoproteomic profiling of tyrosine phosphorylation sites from human T cells using immobilized metal affinity chromatography and tandem mass spectrometry. Anal. Chem. 76, 2763-2772
9. Ficarro, S., Chertihin, O., Westbrook, V. A., White, F., Jayes, F., Kalab, P., Marto, J. A., Shabanowitz, J., Herr, J. C., Hunt, D. F., and Visconti, P. E. (2003) Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J. Biol. Chem. 278, 11579-11589
10. Ficarro, S. B., Salomon, A. R., Brill, L. M., Mason, D. E., Stettler-Gill, M., Brock, A., and Peters, E. C. (2005) Automated immobilized metal affinity chromatography/nano-liquid chromatography/ electrospray ionization mass spectrometry platform for profiling protein phosphorylation sites. Rapid Commun. Mass Spectrom. 19, 57-71
11. 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
12. Rush, J., Moritz, A., Lee, K. A., Guo, A., Goss, V. L., Spek, E. J., Zhang, H., Zha, X. M., Polakiewicz, R. D., and Comb, M. J. (2005) Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 23, 94-101
13. Salomon, A. R., Ficarro, S. B., Brill, L. M., Brinker, A., Phung, Q. T., Ericson, C., Sauer, K, Brock, A., Hom, D. M., Schultz, P. G., and Peters, E. C. (2003) Profiling of tyrosine phosphorylation pathways in human cells using mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 100, 443-448
14. Zheng, H., Hu, P., Quinn, D. F., and Wang, Y. K. (2005) Phosphotyrosine proteomic study of interferon a signaling pathway using a combination of immunoprecipitation and immobilized metal affinity chromatography. Mol. Cell. Proteomics 4, 721-730
15. Jonassen, I., Collins, J. F., and Higgins, D. G. (1995) Finding flexible patterns in unaligned protein sequences. Protein Sci. 4, 1587-1595
16. Nevill-Manning, C. G., Wu, T. D., and Brutlag, D. L. (1998) Highly specific protein sequence motifs for genome analysis. Proc. Natl. Acad. Sci. U. S. A. 95, 5865-5871
17. Rigoutsos, I., and Floratos, A. (1998) Combinatorial pattern discovery in biological sequences: the TEIRESIAS algorithm. Bioinformatics 14, 55-67
18. Schwartz, D., and Gygi, S. P. (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 23, 1391-1398
19. Forman-Kay, J. D., and Pawson, T. (1999) Diversity in protein recognition by PTB domains. Curr. Opin. Struct Biol. 9, 690-695
20. Schulze, W. X., and Mann, M. (2004) A novel proteomic screen for peptide-protein interactions. J. Biol. Chem. 279, 10756-10764
21. Songyang, Z., and Cantley, L. C. (1995) Recognition and specificity in protein tyrosine kinase-mediated signalling. Trends Biochem. Sci. 20, 470-475
22. Vely, F., and Vivier, E. (1997) Conservation of structural features reveals the existence of a large family of inhibitory cell surface receptors and non-inhibitory/activatory counterparts. J. Immunol. 159, 2075-2077
23. Burshtyn, D. N., Yang, W., Yi, T., and Long, E. O. (1997) A novel phospho-tyrosine motif with a critical amino acid at position -2 for the SH2 domain-mediated activation of the tyrosine phosphatase SHP-1. J. Biol. Chem. 272, 13066-13072
24. Hinsby, A. M., Olsen, J. V., Bennett, K. L., and Mann, M. (2003) Signaling initiated by overexpression of the fibroblast growth factor receptor-1 investigated by mass spectrometry. Mol. Cell. Proteomics 2, 29-36
25. Hinsby, A. M., Olsen, J. V., and Mann, M. (2004) Tyrosine phosphoproteomics of fibroblast growth factor signaling: a role for insulin receptor substrate-4. J. Biol. Chem. 279, 46438-46447
26. Diella, F., Cameron, S., Gemund, C., Linding, R., Via, A., Kuster, B., Sicheritz-Ponten, T., Blom, N., and Gibson, T. J. (2004) Phospho.ELM: a database of experimentally verified phosphorylation sites in eukaryotic proteins. BMC Bioinformatics 5, 79
27. Nielsen, M., Lundegaard, C., Woming, P., Hvid, C. S., Lamberth, K., Buus, S., Brunak, S., and Lund, O. (2004) Improved prediction of MHC class I and class II epitopes using a novel Gibbs sampling approach. Bioinformatics 20, 1388-1397
28. Kaufman, L., and Rousseeuw, P. J. (1990) Finding Groups in Data: an Introduction to Cluster Analysis, John Wiley, New York
29. Fraley, C., and Raftery, A. E. (1998) How many clusters? Which clustering method? Answers via model-based cluster analysis. Comput. J. 41, 578-588
30. Jain, A. K., Murth, M. N., and Flynn, P. J. (1999) Data clustering: a review. ACM Comput. Surv. 31, 264-323
31. Ester, M., Kriegel, H. P., Sander, S., and Xu, X. (1996) A density-based algorithm for discovering clusters in large spatial databases with noise, in Proceedings of 2nd International Conference on Knowledge Discovery and Data Mining, Portland, August 2-4, 1996 (Simoudis, E., Han, J., and Fayyad, U., eds) Vol. 1, pp. 226-231, Association for the Advancement of Artificial Intelligence (AAAI) Press, Menlo Park, CA
32. Lund, O., Nielsen, M., Kesmir, C., Petersen, A. G., Lundegaard, C., Woming, P., Sylvester-Hvid, C., Lamberth, K, Roder, G., Justesen, S., and Buus, S., and Brunak, S. (2004) Definition of supertypes for HLA molecules using clustering of specificity matrices. Immunogenetics 55, 797-810
33. Schneider, T. D., and Stephens, R. M. (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 18, 6097-6100
34. Johnson, L. N., Kotz, S., and Kemp, A. W. (1992) Univariate Discrete Distributions, 2nd Ed., Wiley-Interscience, New York
35. 13C-substituted arginine in stable isotope labeling by amino acids in cell culture (SILAC). J. Proteome Res. 2, 173-181
36. Schulze, W. X, Deng, L., and Mann, M. (2005) Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol. Syst Biol. 1, 2005 0008
37. 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
38. Ishihama, Y., Rappsilber, J., Andersen, J. S., and Mann, M. (2002) Micro-columns with self-assembled particle frits for proteomics. J. Chromatogr. A 979, 233-239
39. 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
40. Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S. R., Griffiths-Jones, S., Howe, K. L., Marshall, M., and Sonnhammer, E. L. (2002) The Pfam protein families database. Nucleic Acids Res. 30, 276-280
41. Peri, S., Navarro, J. D., Amanchy, R., Kristiansen, T. Z., Jonnalagadda, C. K., Surendranath, V., Niranjan, V., Muthusamy, B., Gandhi, T. K., Gronborg, M., Ibarrola, N., Deshpande, N., Shanker, K., Shivashankar, H. N., Rashmi, B. P., Ramya, M. A., Zhao, Z., Chandrika, K. N., Padma, N., Harsha, H. C., Yatish, A. J., Kavitha, M. P., Menezes, M., Choudhury, D. R., Suresh, S., Ghosh, N., Saravana, R., Chandran, S., Krishna, S., Joy, M., Anand, S. K., Madavan, V., Joseph, A., Wong, G. W., Schiemann, W. P., Constantinescu, S. N., Huang, L., Khosravi-Far, R., Steen, H., Tewari, M., Ghaffari, S., Blobe, G. C., Dang, C. V., Garcia, J. G., Pevsner, J., Jensen, O. N., Roepstorff, P., Deshpande, K. S., Chinnaiyan, A. M., Hamosh, A., Chakravarti, A., and Pandey, A. (2003) Development of human protein reference database as an initial platform for approaching systems biology in humans. Genome Res. 13, 2363-2371
42. 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
43. Dovat, S., Ronni, T., Russell, D., Ferrini, R., Cobb, B. S., and Smale, S. T. (2002) A common mechanism for mitotic inactivation of C2H2 zinc finger DNA-binding domains. Genes Dev. 16, 2985-2990
44. Saydam, N., Adams, T. K., Steiner, F., Schaffner, W., and Freedman, J. H. (2002) Regulation of metallothionein transcription by the metal-responsive transcription factor MTF-1: identification of signal transduction cascades that control metal-inducible transcription. J. Biol. Chem. 277, 20438-20445
45. Jantz, D., and Berg, J. M. (2004) Reduction in DNA-binding affinity of Cys2His2 zinc finger proteins by linker phosphorylation. Proc. Natl. Acad. Sci. U. S. A. 101, 7589-7593
46. Wu, X., Suetsugu, S., Cooper, L. A., Takenawa, T., and Guan, J. L. (2004) Focal adhesion kinase regulation of N-WASP subcellular localization and function. J. Biol. Chem. 279, 9565-9576
47. Eck, M. J., Pluskey, S., Trub, T., Harrison, S. C., and Shoelson, S. E. (1996) Spatial constraints on the recognition of phosphoproteins by the tandem SH2 domains of the phosphatase SH-PTP2. Nature 379, 277-280
48. Huyer, G., and Ramachandran, C. (1998) The specificity of the N-terminal SH2 domain of SHP-2 is modified by a single point mutation. Biochemistry 37, 2741-2747
49. Beebe, K. D., Wang, P., Arabaci, G., and Pei, D. (2000) Determination of the binding specificity of the SH2 domains of protein tyrosine phosphatase SHP-1 through the screening of a combinatorial phosphotyrosyl peptide library. Biochemistry 39, 13251-13260
50. Liu, B. A., Jablonowski, K., Raina, M., Arce, M., Pawson, T., and Nash, P. D. (2006) The human and mouse complement of SH2 domain proteins-establishing the boundaries of phosphotyrosine signaling. Mol. Cell 22, 851-868
51. Poy, F., Yaffe, M. B., Sayos, J., Saxena, K., Morra, M., Sumegi, J., Cantley, L. C., Terhorst, C., and Eck, M. J. (1999) Crystal structures of the XLP protein SAP reveal a class of SH2 domains with extended, phosphotyrosine-independent sequence recognition. Mol. Cell 4, 555-561
52. Muraille, E., Bruhns, P., Pesesse, X., Daeron, M., and Erneux, C. (2000) The SH2 domain containing inositol 5-phosphatase SHIP2 associates to the immunoreceptor tyrosine-based inhibition motif of Fc γRIIB in B cells under negative signaling. Immunol. Lett. 72, 7-15
53. Bruhns, P., Vely, F., Malbec, O., Fridman, W. H., Vivier, E., and Daeron, M. (2000) Molecular basis of the recruitment of the SH2 domain-containing inositol 5-phosphatases SHIP1 and SHIP2 by fcγ RIIB. J. Biol. Chem. 275, 37357-37364
54. Damen, J. E., Liu, L., Rosten, P., Humphries, R. K., Jefferson, A. B., Majerus, P. W., and Krystal, G. (1996) The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc. Natl. Acad. Sci. U. S. A. 93, 1689-1693
55. Marion, E., Kaisaki, P. J., Pouillon, V., Gueydan, C., Levy, J. C., Bodson, A., Krzentowski, G., Daubresse, J. C., Mockel, J., Behrends, J., Servais, G., Szpirer, C., Kruys, V., Gauguier, D., and Schurmans, S. (2002) The gene INPPL1, encoding the lipid phosphatase SHIP2, is a candidate for type 2 diabetes in rat and man. Diabetes 51, 2012-2017
56. Sleeman, M. W., Wortley, K. E., Lai, K. M., Gowen, L. C., Kintner, J., Kline, W. O., Garcia, K., Stitt, T. N., Yancopoulos, G. D., Wiegand, S. J., and Glass, D. J. (2005) Absence of the lipid phosphatase SHIP2 confers resistance to dietary obesity. Nat. Med. 11, 199-205