Crystallographic structure of the SH3 domain of the human c-Yes tyrosine kinase: Loop flexibility and amyloid aggregation

FEBS Letters

Volumn 581, Issue 9, 2007, Pages 1701-1706

  Martín García, José M ^a   Luque, Irene ^a   Mateo, Pedro L ^a   Ruiz Sanz, Javier ^a   Cámara Artigas, Ana ^b  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF ALMERÍA   (Spain)

Author keywords

Amyloid fibrils; Crystallization; Loop flexibility; SH3 domains; X ray structure

Indexed keywords

AMYLOID; PROTEIN KINASE YES; PROTEIN TYROSINE KINASE;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; AMYLOID; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-YES; SEQUENCE HOMOLOGY, AMINO ACID; SRC HOMOLOGY DOMAINS;

EID: 34247144140     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2007.03.059     Document Type: Article

References (37)

1. Summy J.M., Sudol M., Eck M.J., Monteiro A.N., Gatesman A., and Flynn D.C. Specificity in signaling by c-Yes. Front. Biosci. 8 (2003) s185-s205
2. Summy J.M., Guappone A.C., Sudol M., and Flynn D.C. The SH3 and SH2 domains are capable of directing specificity in protein interactions between the non-receptor tyrosine kinases cSrc and cYes. Oncogene 19 (2000) 155-160
3. Weng Z., Thomas S.M., Rickles R.J., Taylor J.A., Brauer A.W., Seidel-Dugan C., Michael W.M., Dreyfuss G., and Brugge J.S. Identification of Src, Fyn, and Lyn SH3-binding proteins: implications for a function of SH3 domains. Mol. Cell Biol. 14 (1994) 4509-4521
4. Feng S., Kapoor T.M., Shirai F., Combs A.P., and Schreiber S.L. Molecular basis for the binding of SH3 ligands with non-peptide elements identified by combinatorial synthesis. Chem. Biol. 3 (1996) 661-670
5. Borchert T.V., Mathieu M., Zeelen J.P., Courtneidge S.A., and Wierenga R.K. The crystal structure of human CskSH3: structural diversity near the RT-Src and n-Src loop. FEBS Lett. 341 (1994) 79-85
6. Bauer F., Schweimer K., Meiselbach H., Hoffmann S., Rosch P., and Sticht H. Structural characterization of Lyn-SH3 domain in complex with a herpesviral protein reveals an extended recognition motif that enhances binding affinity. Protein Sci. 14 (2005) 2487-2498
7. Noble M.E., Musacchio A., Saraste M., Courtneidge S.A., and Wierenga R.K. Crystal structure of the SH3 domain in human Fyn; comparison of the three-dimensional structures of SH3 domains in tyrosine kinases and spectrin. EMBO J. 12 (1993) 2617-2624
8. Musacchio A., Saraste M., and Wilmanns M. High-resolution crystal-structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nat. Struct. Biol. 1 (1994) 546-551
9. Musacchio A., Noble M., Pauptit R., Wierenga R., and Saraste M. Crystal structure of a Src-homology 3 (SH3) domain. Nature 359 (1992) 851-855
10. Morton C.J., Pugh D.J.R., Brown E.L.J., Kahmann J.D., Renzoni D.A.C., and Campbell I.D. Solution structure and peptide binding of the SH3 domain from human Fyn. Structure 4 (1996) 705-714
11. Schweimer K., Hoffmann S., Bauer F., Friedrich U., Kardinal C., Feller S.M., Biesinger B., and Sticht H. Structural investigation of the binding of a herpesviral protein to the SH3 domain of tyrosine kinase Lck. Biochemistry 41 (2002) 5120-5130
12. Kunkel T. Rapid and efficient site-directed mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82 (1985) 449-488
13. Peranen J., Rikkonen M., Hyvonen M., and Kaariainen L. T7 vectors with modified T7lac promoter for expression of proteins in Escherichia coli. Anal. Biochem. 236 (1996) 371-373
14. Musacchio A., Saraste M., and Wilmanns M. High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nat. Struct. Biol. 1 (1994) 546-551
15. Viguera A.R., Arrondo J.L., Musacchio A., Saraste M., and Serrano L. Characterization of the interaction of natural proline-rich peptides with five different SH3 domains. Biochemistry 33 (1994) 10925-10933
16. Gill S.C., and von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182 (1989) 319-326
17. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 33 (1968) 491-497
18. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
19. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D-Biol. Crystallogr. 60 (2004) 2126-2132
20. Winn M.D., Murshudov G.N., and Papiz M.Z. Macromolecular TLS refinement in REFMAC at moderate resolutions. Macromol. Crystal., Pt D 374 (2003) 300-321
21. Bailey S. The CCP4 suite - programs for protein crystallography. Acta Crystallogr. Sect. D-Biol. Crystallogr. 50 (1994) 760-763
22. Morel B., Casares S., and Conejero-Lara F. A single mutation induces amyloid aggregation in the alpha-spectrin SH3 domain: analysis of the early stages of fibril formation. J. Mol. Biol. 356 (2006) 453-468
23. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
24. Krissinel E., and Henrick K. Detection of protein assemblies in crystals. Comput. Life Sci. Proc. 3695 (2005) 163-174
25. Ball L.J., Kuhne R., Schneider-Mergener J., and Oschkinat H. Recognition of proline-rich motifs by protein-protein-interaction domains. Angew. Chem. Int. Ed. Engl. 44 (2005) 2852-2869
26. Kay B.K., Williamson M.P., and Sudol M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 232 (2000) 231-241
27. Wittekind M., Mapelli C., Lee V., Goldfarb V., Friedrichs M.S., Meyers C.A., and Mueller L. Solution structure of the Grb2 N-terminal SH3 domain complexed with a ten-residue peptide derived from SOS: direct refinement against NOEs, J-couplings and 1H and 13C chemical shifts. J. Mol. Biol. 267 (1997) 933-952
28. Wang W., Lim W.A., Jakalian A., Wang J., Luo R., Bayly C.I., and Kollman P.A. An analysis of the interactions between the Sem-5 SH3 domain and its ligands using molecular dynamics, free energy calculations, and sequence analysis. J. Am. Chem. Soc. 123 (2001) 3986-3994
29. Arold S., O'Brien R., Franken P., Strub M.-P., Hoh F., Dumas C., and Ladbury J.E. RT loop flexibility enhances the specificity of Src family SH3 domains for HIV-1 Nef. Biochemistry 37 (1998) 14683-14691
30. Dutta K., Shi H., Cruz-Chu E.R., Kami K., and Ghose R. Dynamic influences on a high-affinity, high-specificity interaction involving the C-terminal SH3 domain of p67phox. Biochemistry 43 (2004) 8094-8106
31. Feng S., Kasahara C., Rickles R.J., and Schreiber S.L. Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc. Natl. Acad. Sci. USA 92 (1995) 12408-12415
32. Bader R., Bamford R., Zurdo J., Luisi B.F., and Dobson C.M. Probing the mechanism of amyloidogenesis through a tandem repeat of the PI3-SH3 domain suggests a generic model for protein aggregation and fibril formation. J. Mol. Biol. 356 (2006) 189-208
33. Zurdo J., Guijarro J.I., Jimenez J.L., Saibil H.R., and Dobson C.M. Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain. J. Mol. Biol. 311 (2001) 325-340
34. Ventura S., Lacroix E., and Serrano L. Insights into the origin of the tendency of the PI3-SH3 domain to form amyloid fibrils. J. Mol. Biol. 322 (2002) 1147-1158
35. Ventura S., Zurdo J., Narayanan S., Parreno M., Mangues R., Reif B., Chiti F., Giannoni E., Dobson C.M., Aviles F.X., and Serrano L. Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case. Proc. Natl. Acad. Sci. USA 101 (2004) 7258-7263
36. Ding F., Dokholyan N.V., Buldyrev S.V., Stanley H.E., and Shakhnovich E.I. Molecular dynamics simulation of the SH3 domain aggregation suggests a generic amyloidogenesis mechanism. J. Mol. Biol. 324 (2002) 851-857
37. Romir J., Lilie H., Egerer-Sieber C., Bauer F., Sticht H., and Muller Y.A. Crystal structure analysis and solution studies of human Lck-SH3: Zinc-induced homodimerization competes with the binding of proline-rich motifs. J. Mol. Biol. 365 (2007) 1417-1428