Interactions between the Fyn SH3-domain and adaptor protein Cbp/PAG derived ligands, effects on kinase activity and affinity

FEBS Journal

Volumn 275, Issue 19, 2008, Pages 4863-4874

  Solheim, Silje A ^a,b   Petsalaki, Evangelia ^c   Stokka, Anne J ^a,b   Russell, Robert B ^c   Taskén, Kjetil ^a,b   Berge, Torunn ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Kinase activity; Proline rich motifs; Protein protein interactions; SH3 domain; Tyrosine phosphorylation

Indexed keywords

ADAPTOR PROTEIN; GLYCOSPHINGOLIPID; MEMBRANE PROTEIN; PROTEIN CSK; PROTEIN KINASE FYN; PROTEIN PAG; PROTEIN SH3; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL ANALYSIS; DISSOCIATION CONSTANT; ENZYME ACTIVITY; ENZYME ASSAY; LIGAND BINDING; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CIRCULAR DICHROISM; COMPUTER SIMULATION; HUMANS; KINETICS; LIGANDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; PEPTIDES; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTO-ONCOGENE PROTEINS C-FYN; SRC HOMOLOGY DOMAINS; SURFACE PLASMON RESONANCE; T-LYMPHOCYTES;

EID: 51749107470     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06626.x     Document Type: Article

References (52)

1. Pawson T (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116, 191 203.
2. Hubbard SR Till JH (2000) Protein tyrosine kinase structure and function. Annu Rev Biochem 69, 373 398.
3. Palacios EH Weiss A (2004) Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene 23, 7990 8000.
4. Gschwind A, Fischer OM Ullrich A (2004) The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat Rev Cancer 4, 361 370.
5. Hermiston ML, Xu Z Weiss A (2003) CD45: a critical regulator of signaling thresholds in immune cells. Annu Rev Immunol 21, 107 137.
6. Hunter T (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80, 225 236.
7. Pao LI, Badour K, Siminovitch KA Neel BG (2007) Nonreceptor protein-tyrosine phosphatases in immune cell signaling. Annu Rev Immunol 25, 473 523.
8. Boggon TJ Eck MJ (2004) Structure and regulation of Src family kinases. Oncogene 23, 7918 7927.
9. Xu W, Harrison SC Eck MJ (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595 602.
10. Guappone AC Flynn DC (1997) The integrity of the SH3 binding motif of AFAP-110 is required to facilitate tyrosine phosphorylation by, and stable complex formation with, Src. Mol Cell Biochem 175, 243 252.
11. Nakamoto T, Sakai R, Ozawa K, Yazaki Y Hirai H (1996) Direct binding of C-terminal region of p130Cas to SH2 and SH3 domains of Src kinase. J Biol Chem 271, 8959 8965.
12. Richard S, Yu D, Blumer KJ, Hausladen D, Olszowy MW, Connelly PA Shaw AS (1995) Association of p62, a multifunctional SH2- and SH3-domain-binding protein, with src family tyrosine kinases, Grb2, and phospholipase C gamma-1. Mol Cell Biol 15, 186 197.
13. Straus DB Weiss A (1992) Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70, 585 593.
14. Yasuda K, Nagafuku M, Shima T, Okada M, Yagi T, Yamada T, Minaki Y, Kato A, Tani-Ichi S, Hamaoka T et al. (2002) Cutting edge: Fyn is essential for tyrosine phosphorylation of Csk-binding protein/phosphoprotein associated with glycolipid-enriched microdomains in lipid rafts in resting T cells. J Immunol 169, 2813 2817.
15. Posevitz-Fejfar A, Smida M, Kliche S, Hartig R, Schraven B Lindquist JA (2008) A displaced PAG enhances proximal signaling and SDF-1-induced T cell migration. Eur J Immunol 38, 250 259.
16. Brdicka T, Pavlistova D, Leo A, Bruyns E, Korinek V, Angelisova P, Scherer J, Shevchenko A, Hilgert I, Cerny J et al. (2000) Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J Exp Med 191, 1591 1604.
17. Kawabuchi M, Satomi Y, Takao T, Shimonishi Y, Nada S, Nagai K, Tarakhovsky A Okada M (2000) Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 404, 999 1003.
18. Torgersen KM, Vang T, Abrahamsen H, Yaqub S, Horejsi V, Schraven B, Rolstad B, Mustelin T Tasken K (2001) Release from tonic inhibition of T cell activation through transient displacement of C-terminal Src kinase (Csk) from lipid rafts. J Biol Chem 276, 29313 29318.
19. Tauzin S, Ding H, Khatib K, Ahmad I, Burdevet D, van Echten-Deckert G, Lindquist JA, Schraven B, Din NU, Borisch B et al. (2008) Oncogenic association of the Cbp/PAG adaptor protein with the Lyn tyrosine kinase in human B-NHL rafts. Blood 111, 2310 2320.
20. Smida M, Posevitz-Fejfar A, Horejsi V, Schraven B Lindquist JA (2007) A novel negative regulatory function of PAG: blocking Ras activation. Blood 110, 596 615.
21. Davidson D, Schraven B Veillette A (2007) PAG-associated FynT regulates calcium signaling and promotes anergy in T lymphocytes. Mol Cell Biol 27, 1960 1973.
22. Solheim SA, Torgersen KM, Tasken K Berge T (2008) Regulation of FynT function by dual-domain docking on PAG/Cbp. J Biol Chem 283, 2773 2783.
23. Pellicena P Miller WT (2001) Processive phosphorylation of p130Cas by Src depends on SH3-polyproline interactions. J Biol Chem 276, 28190 28196.
24. Ingley E, Schneider JR, Payne CJ, McCarthy DJ, Harder KW, Hibbs ML Klinken SP (2006) Csk-binding protein mediates sequential enzymatic down-regulation and degradation of Lyn in erythropoietin-stimulated cells. J Biol Chem 281, 31920 31929.
25. Musacchio A, Saraste M Wilmanns M (1994) High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nat Struct Biol 1, 546 551.
26. Renzoni DA, Pugh DJ, Siligardi G, Das P, Morton CJ, Rossi C, Waterfield MD, Campbell ID Ladbury JE (1996) Structural and thermodynamic characterization of the interaction of the SH3 domain from Fyn with the proline-rich binding site on the p85 subunit of PI3-kinase. Biochemistry, 35, 15646 15653.
27. Rickles RJ, Botfield MC, Weng Z, Taylor JA, Green OM, Brugge JS Zoller MJ (1994) Identification of Src, Fyn, Lyn, PI3K and Abl SH3 domain ligands using phage display libraries. EMBO J, 13, 5598 5604.
28. Weng Z, Rickles RJ, Feng S, Richard S, Shaw AS, Schreiber SL Brugge JS (1995) Structure-function analysis of SH3 domains: SH3 binding specificity altered by single amino acid substitutions. Mol Cell Biol 15, 5627 5634.
29. Sparks AB, Quilliam LA, Thorn JM, Der CJ Kay BK (1994) Identification and characterization of Src SH3 ligands from phage-displayed random peptide libraries. J Biol Chem 269, 23853 23856.
30. Morton CJ, Pugh DJ, Brown EL, Kahmann JD, Renzoni DA Campbell ID (1996) Solution structure and peptide binding of the SH3 domain from human Fyn. Structure 4, 705 714.
31. Feng S, Kasahara C, Rickles RJ Schreiber SL (1995) Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc Natl Acad Sci USA 92, 12408 12415.
32. Kay BK, Williamson MP Sudol M (2000) The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14, 231 241.
33. Shelton H Harris M (2008) Hepatitis C virus NS5A protein binds the SH3 domain of the Fyn tyrosine kinase with high affinity: mutagenic analysis of residues within the SH3 domain that contribute to the interaction. Virol J 5, 24.
34. Rath A, Davidson AR Deber CM (2005) The structure of 'unstructured' regions in peptides and proteins: role of the polyproline II helix in protein folding and recognition. Biopolymers 80, 179 185.
35. Li SS (2005) Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem J 390, 641 653.
36. Drake AF, Siligardi G Gibbons WA (1988) Reassessment of the electronic circular dichroism criteria for random coil conformations of poly(l-lysine) and the implications for protein folding and denaturation studies. Biophys Chem 31, 143 146.
37. Scott MP Miller WT (2000) A peptide model system for processive phosphorylation by Src family kinases. Biochemistry 39, 14531 14537.
38. Viguera AR, Arrondo JL, Musacchio A, Saraste M Serrano L (1994) Characterization of the interaction of natural proline-rich peptides with five different SH3 domains. Biochemistry 33, 10925 10933.
39. Okishio N, Tanaka T, Fukuda R Nagai M (2003) Differential ligand recognition by the Src and phosphatidylinositol 3-kinase Src homology 3 domains: circular dichroism and ultraviolet resonance Raman studies. Biochemistry 42, 208 216.
40. Bousquet JA, Garbay C, Roques BP Mely Y (2000) Circular dichroic investigation of the native and non-native conformational states of the growth factor receptor-binding protein 2 N-terminal src homology domain 3: effect of binding to a proline-rich peptide from guanine nucleotide exchange factor. Biochemistry 39, 7722 7735.
41. Kang H, Freund C, Duke-Cohan JS, Musacchio A, Wagner G Rudd CE (2000) SH3 domain recognition of a proline-independent tyrosine-based RKxxYxxY motif in immune cell adaptor SKAP55. EMBO J 19, 2889 2899.
42. Bhaskar K, Yen SH Lee G (2005) Disease-related modifications in tau affect the interaction between Fyn and Tau. J Biol Chem 280, 35119 35125.
43. Lim CS, Seet BT, Ingham RJ, Gish G, Matskova L, Winberg G, Ernberg I Pawson T (2007) The K15 protein of Kaposi's sarcoma-associated herpesvirus recruits the endocytic regulator intersectin 2 through a selective SH3 domain interaction. Biochemistry 46, 9874 9885.
44. Feng S, Chen JK, Yu H, Simon JA Schreiber SL (1994) Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266, 1241 1247.
45. Alexandropoulos K, Cheng G Baltimore D (1995) Proline-rich sequences that bind to Src homology 3 domains with individual specificities. Proc Natl Acad Sci USA 92, 3110 3114.
46. Rickles RJ, Botfield MC, Zhou XM, Henry PA, Brugge JS Zoller MJ (1995) Phage display selection of ligand residues important for Src homology 3 domain binding specificity. Proc Natl Acad Sci USA 92, 10909 10913.
47. Saksela K, Cheng G Baltimore D (1995) Proline-rich (PxxP) motifs in HIV-1 Nef bind to SH3 domains of a subset of Src kinases and are required for the enhanced growth of Nef+ viruses but not for down-regulation of CD4. EMBO J 14, 484 491.
48. Briggs SD, Lerner EC Smithgall TE (2000) Affinity of Src family kinase SH3 domains for HIV Nef in vitro does not predict kinase activation by Nef in vivo. Biochemistry 39, 489 495.
49. Bauer F, Hofinger E, Hoffmann S, Rosch P, Schweimer K Sticht H (2004) Characterization of Lck-binding elements in the herpesviral regulatory Tip protein. Biochemistry 43, 14932 14939.
50. Greenfield NJ (2006) Using circular dichroism spectra to estimate protein secondary structure. Nat Protoc 1, 2876 2890.
51. Sali A Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234, 779 815.
52. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28, 235 242.