Structural basis for the requirement of two phosphotyrosine residues in signaling mediated by Syk tyrosine kinase

Journal of Molecular Biology

Volumn 356, Issue 5, 2006, Pages 1222-1236

  Groesch, Teresa D ^a   Zhou, Fei ^a   Mattila, Sampo ^a   Geahlen, Robert L ^a   Post, Carol Beth ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Immune signaling; Induced fit binding; Isotope filter NOESY; Phosphotyrosine recognition; Protein NMR

Indexed keywords

LYMPHOCYTE ANTIGEN RECEPTOR; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; PHOSPHOTYROSINE; PROTEIN KINASE SYK; PROTEIN KINASE SYK Y342; PROTEIN KINASE SYK Y346; PROTEIN SH2; TRANSCRIPTION FACTOR NFAT; TYROSINE; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; ARTICLE; B LYMPHOCYTE; CALCIUM MOBILIZATION; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; ELECTRICITY; NUCLEAR MAGNETIC RESONANCE; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

EID: 32044450797     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.11.095     Document Type: Article

References (43)

1. J.E. Hutchcroft, M.L. Harrison, and R.L. Geahlen Association of the 72-kDa protein-tyrosine kinase Ptk72 with the B-cell antigen receptor J. Biol. Chem. 267 1992 8613 8619
2. T. Yamada, T. Taniguchi, C. Yang, S. Yasue, H. Saito, and H. Yamamura Association with B-cell-antigen receptor with protein-tyrosine kinase-P72(Syk) and activation by engagement of membrane Igm Eur. J. Biochem. 213 1993 455 459
3. L.M. Keshvara, C.C. Isaacson, T.M. Yankee, R. Sarac, M.L. Harrison, and R.L. Geahlen Syk- and Lyn-dependent phosphorylation of Syk on multiple tyrosines following B cell activation includes a site that negatively regulates signaling J. Immunol. 161 1998 5276 5283
4. T.C.K. Chan, C.J. Chang, N.M. Koonchanok, and R.L. Geahlen Selective-inhibition of the growth of Ras-transformed human bronchial epithelial-cells by emodin, a protein-tyrosine kinase inhibitor Biochem. Biophy. Res. Commun. 193 1993 1152 1158
5. E.N. Neumeister, Y.X. Zhu, S. Richard, C. Terhorst, A.C. Chan, and A.S. Shaw Binding of Zap-70 to phosphorylated T-cell receptor-Zeta and receptor-Eta enhances its autophosphorylation and generates specific binding-sites for Sh2 domain-containing proteins Mol. Cell. Biol. 15 1995 3171 3178
6. M.L. Lupher, N. Rao, N.L. Lill, C.E. Andoniou, S. Miyake, and E.A. Clark Cbl-mediated negative regulation of the Syk tyrosine kinase - a critical role for Cbl phosphotyrosine-binding domain binding to Syk phosphotyrosine 323 J. Biol. Chem. 273 1998 35273 35281
7. N. Rao, M.L. Lupher, S. Ota, K.A. Reedquist, B.J. Druker, and H. Band The linker phosphorylation site Tyr(292) mediates the negative regulatory effect of Cbl on ZAP-70 in T cells J. Immunol. 164 2000 4616 4626
8. H.W. Sohn, H. Gu, and S.K. Pierce Cbl-b negatively regulates B cell antigen receptor signaling in mature B cells through ubiquitination of the tyrosine kinase Syk J. Expt. Med. 197 2003 1511 1524
9. A. Magnan, V. Di Bartolo, A.M. Mura, C. Boyer, M. Richelme, and Y.L. Lin T cell development and T cell responses in mice with mutations affecting tyrosines 292 or 315 of the ZAP-70 protein tyrosine kinase J. Expt. Med. 194 2001 491 505
10. Q. Gong, X.H. Jin, A.M. Akk, N. Foger, M. White, and Q.Q. Gong Requirement for tyrosine residues 315 and 319 within zeta chain-associated protein 70 for T cell development J. Expt. Med. 194 2001 507 518
11. M. Simon, L. Vanes, R.L. Geahlen, and V.L.J. Tybulewicz Distinct roles for the linker region tyrosines of Syk in Fc epsilon RI signaling in primary mast cells J. Biol. Chem. 280 2005 4510 4517
12. J.J. Hong, T.M. Yankee, M.L. Harrison, and R.L. Geahlen Regulation of signaling in B cells through the phosphorylation of Syk on linker region tyrosines - a mechanism for negative signaling by the Lyn tyrosine kinase J. Biol. Chem. 277 2002 31703 31714
13. C.L. Law, K.A. Chandran, S.P. Sidorenko, and E.A. Clark Phospholipase C-gamma 1 interacts with conserved phosphotyrosyl residues in the linker region of Syk and is a substrate for Syk Mol. Cell. Biol. 16 1996 1305 1315
14. M. Deckert, S. Tartare-Deckert, C. Couture, T. Mustelin, and A. Altman Functional and physical interactions of Syk family kinases with the Vav proto-oncogene product Immunity 5 1996 591 604
15. J. Zhang, E. Berenstein, and R.P. Siraganian Phosphorylation of Tyr342 in the linker region of Syk is critical for Fc epsilon RI signaling in mast cells Mol. Cell. Biol. 22 2002 8144 8154
16. J. Wu, Q.H. Zhao, T. Kurosaki, and A. Weiss The Vav binding site (Y315) in ZAP-70 is critical for antigen receptor-mediated signal transduction J. Expt. Med. 185 1997 1877 1882
17. B.L. Williams, B.J. Irvin, S.L. Sutor, C.C.S. Chini, E. Yacyshyn, and J.B. Wardenburg Phosphorylation of Tyr319 in ZAP-70 is required for T-cell antigen receptor-dependent phospholipase C-gamma 1 and Ras activation EMBO J. 18 1999 1832 1844
18. M. Pelosi, V. Di Bartolo, V. Mounier, D. Mege, J.M. Pascussi, and E. Dufour Tyrosine 319 in the interdomain B of ZAP-70 is a binding site for the Src homology 2 domain of Lck J. Biol. Chem. 274 1999 14229 14237
19. T. Brdicka, T.A. Kadlecek, J.P. Roose, A.W. Pastuszak, and A. Weiss Intramolecular regulatory switch in ZAP-70: analogy with receptor tyrosine kinases Mol. Cell. Biol. 25 2005 4924 4933
20. L.E. Wybenga-Groot, B. Baskin, S.H. Ong, J. Tong, T. Pawson, and F. Sicheri Structural basis for autoinhibition of the EphB2 receptor tyrosine kinase by the unphosphorylated juxtamembrane region Cell (Cambridge, MA) 106 2001 745 757
21. J.M. Bradshaw, V. Mitaxov, and G. Waksman Investigation of phosphotyrosine recognition by the SH2 domain of the Src kinase J. Mol. Biol. 293 1999 971 985
22. Z. Songyang, S.E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, and W.G. Haser Sh2 domains recognize specific phosphopeptide sequences Cell 72 1993 767 778
23. F.B. Sheinerman, B. Al-Lazikani, and B. Honig Sequence, structure and energetic determinants of phosphopeptide selectivity of SH2 domains J. Mol. Biol. 334 2003 823 841
24. S.M. Pascal, A.U. Singer, G. Gish, T. Yamazaki, S.E. Shoelson, and T. Pawson Nuclear-magnetic-resonance structure of an Sh2 domain of phospholipase C-gamma-1 complexed with a high-affinity binding peptide Cell 77 1994 461 472
25. G. Carpenter, and Q.S. Ji Phospholipase C-gamma as a signal-transducing element Expt. Cell Res. 253 1999 15 24
26. C.M. Vines, J.W. Potter, Y. Xu, R.L. Geahlen, P.S. Costello, and V.L. Tybulewicz Inhibition of beta 2 integrin receptor and Syk kinase signaling in monocytes by the Src family kinase Fgr Immunity 15 2001 507 519
27. K.D. Moon, C.B. Post, D.L. Dirdem, Q. Zhou, P. De, M.L. Harrison, and R.L. Geahlen Molecular basis for a direct interaction between the Syk protein-tyrosine kinase and phosphoinositide 3-kinase J. Biol. Chem. 280 2005 1543 1551
28. M.J. Eck, S.K. Atwell, S.E. Shoelson, and S.C. Harrison Structure of the regulatory domains of the Src-family tyrosine kinase Lck Nature 368 1994 764 769
29. M.J. Eck, S.E. Shoelson, and S.C. Harrison Recognition of a high-affinity phosphotyrosyl peptide by the Src homology-2 domain of P56(Lck) Nature 362 1993 87 91
30. J.J. Hu, J. Liu, R. Ghirlando, A.R. Saltiel, and S.R. Hubbard Structural basis for recruitment of the adaptor protein APS to the activated insulin receptor Mol. Cell. 12 2003 1379 1389
31. L.E. Kay, D.R. Muhandiram, G. Wolf, S.E. Shoelson, and J.D. Forman-Kay Correlation between binding and dynamics at SH2 domain interfaces Nature Struct. Biol. 5 1998 156 163
32. P. Nioche, W.Q. Liu, I. Broutin, F. Charbonnier, M.T. Latreille, and M. Vidal Crystal structures of the SH2 domain of Grb2: highlight on the binding of a new high-affinity inhibitor J. Mol. Biol. 315 2002 1167 1177
33. G. Waksman, D. Kominos, S.C. Robertson, N. Pant, D. Baltimore, and R.B. Birge Crystal structure of the phosphotyrosine recognition domain Sh2 of V-Src complexed with tyrosine phosphorylated peptides Nature 358 1993 646 653
34. P.M. Hwang, C.J. Li, M. Morra, J. Lillywhite, D.R. Muhandiram, and F. Gertler A 'three-pronged' binding mechanism for the SAP/SH2D1A SH2 domain: structural basis and relevance to the XLP syndrome EMBO J. 21 2002 314 323
35. A.L. Breeze, B.V. Kara, D.G. Barratt, M. Anderson, J.C. Smith, and R.W. Luke Structure of a specific peptide complex of the carboxy-terminal SH2 domain from the p85 alpha subunit of phosphatidylinositol 3-kinase EMBO J. 15 1996 3579 3589
36. G. Siegal, B. Davis, S.M. Kristensen, A. Sankar, J. Linacre, and R.C. Stein Solution structure of the C-terminal SH2 domain of the p85 alpha regulatory subunit of phosphoinositide 3-kinase J.M. Biol. 276 1998 461 478
37. T. Weber, B. Schaffhausen, Y.X. Liu, and U.L. Gunther NMR structure of the N-SH2 of the p85 subunit of phosphoinositide 3-kinase complexed to a doubly phosphorylated peptide reveals a second phosphotyrosine binding site Biochemistry 39 2000 15860 15869
38. R.J. Mallis, K.N. Brazin, D.B. Fulton, and A.H. Andreotti Structural characterization of a proline-driven conformational switch within the Itk SH2 domain Nature Struct. Biol. 9 2002 900 905
39. A.R. Salomon, S.B. Ficarro, L.M. Brill, A. Brinker, Q.T. Phung, and C. Ericson Profiling of tyrosine phosphorylation pathways in human cells using mass spectrometry Proc. Natl Acad. Sci. USA 100 2003 443 448
40. O.Y. Lubman, and G. Waksman Structural and thermodynamic basis for the interaction of the Src SH2 domain with the activated form of the PDGF beta-receptor J. Mol. Biol. 328 2003 655 668
41. M.H.P. West, R.S. Wu, and W.M. Bonner Polyacrylamide-gel electrophoresis of small peptides Electrophoresis 5 1984 133 138
42. G. Cornilescu, F. Delaglio, and A. Bax Protein backbone angle restraints from searching a database for chemical shift and sequence homology J. Biomol. NMR 13 1999 289 302
43. C.D. Schwieters, J.J. Kuszewski, N. Tjandra, and G.M. Clore The XPLOR-NIH NMR molecular structure determination package J. Magn. Reson. 160 2003 66 74