The 2.35 Å crystal structure of the inactivated form of chicken Src: A dynamic molecule with multiple regulatory interactions

Journal of Molecular Biology

Volumn 274, Issue 5, 1997, Pages 757-775

  Williams, John C ^a   Weijland, Albert ^a   Gonfloni, Stefania ^a   Thompson, Andy ^b   Courtneidge, Sara A ^a,c   Superti Furga, Giulio ^a   Wierenga, Rik K ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^c SUGEN INC   (United States)

Author keywords

Conformational dynamics; Crystal structure; Signal transduction; Src; Tyrosine kinase

Indexed keywords

PHOSPHOPROTEIN; PROTEIN TYROSINE KINASE; HCK PROTEIN, HUMAN; HEMATOPOIETIC CELL KINASE; ONCOPROTEIN; PROTEIN KINASE P60;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME INACTIVATION; ENZYME REGULATION; ENZYME STRUCTURE; HUMAN; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; METHODOLOGY; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SRC HOMOLOGY DOMAIN; X RAY CRYSTALLOGRAPHY;

GALLUS GALLUS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHICKENS; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-HCK; PROTO-ONCOGENE PROTEINS PP60(C-SRC); SEQUENCE ALIGNMENT; SRC HOMOLOGY DOMAINS;

EID: 0031578579     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1426     Document Type: Article

References (62)

1. Abagyan R., Totrov M., Kuznetsov D. ICM-A new method for protein modelling and design: applications to docking and structure prediction from the distorted native conformation. J. Comput. Chem. 15:1994;488-506.
2. Cas. Genes Dev. 10:1996;1341-1355.
3. Bellus G. A., McIntosh I., Smith E. A., Aylsworth A. S., Kaitila I., Horton W. A., Greenhaw G. A., Hecht J. T., Francomano C. A. A recurrent mutation in the tyrosine kinase domain of fibroblast growth factor receptor 3 causes hypochondroplasia. Nature Genet. 10:1995;357-359.
4. Bernstein B. E., Michels P. A. M., Hol W. G. J. Synergistic effects of substrate-induced conformational changes in phosphoglycerate kinase activation. Nature. 385:1997;275.
5. Borchert T., Mathieu M., Zeelen J., Courtneidge S., Wierenga R. K. The crystal structure of human CskSH3: structural diversity near the RT-Src and n-Src loop. FEBS Letters, 341:1994;79-85.
6. Brown M. T., Cooper J. A. Regulation, substrates and functions of Src. Biochim. Biophys. Acta. 1287:1996;121-149.
7. Brünger, A. T. 1992a, X-PLOR, Version 3.1: A System for X-ray Crystallography and NMR, Yale University Press, New Haven, CT.
8. Brünger A. T. The free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992b;472-477.
9. Brünger A. T., Krukowski A. Slow-cooling protocols for crystallographic refinement by simulated annealing. Acta Crystallog. sect. A, 46:1990;585-593.
10. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D, 50:1994;760-763.
11. Connolly M. L. The molecular surface package. J. Mol. Graphics. 11:1993;139-141.
12. Cooper J. A., Howell B. The when and how of Src regulation. Cell. 73:1993;1051-1054.
13. c-src. EMBO J. 4:1985;1471-1477.
14. De Bondt H. L., Rosenblatt J., Jancarik J., Jones H. D., Morgan D. O., Kim S.-H. Crystal structure of cyclin-dependent kinase 2. Nature. 363:1993;595-602.
15. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucl. Acids Res. 12:1984;387-395.
16. Erpel T., Superti-Furga G., Courtneidge S. A. Mutational analysis of the Src SH3 domain: the same residues of the ligand binding surface are important for intra- and inter-molecular interactions. EMBO J. 14:1995;963-975.
17. Felder S., Zhou M., Hu P., Urena J., Ullrich A., Chaudhurl M., White M., Shoelson S. E., Schlessinger J. SH2 domains exhibit high-affinity binding to tyrosine-phosphorylated peptides yet also exhibit rapid dissociation and exchange. Mol. Cell. Biol. 13:1993;1449-1455.
18. Gerstein M., Lesk A. M., Chothia C. Structural mechanisms for domain movements in proteins. Biochemistry. 33:1994;6739-6749.
19. Gonfloni S., Williams J. C., Hattula K., Weijland A., Wierenga R. K., Superti-Furga G. The role of the linker between SH2 domain and catalytic domain in the regulation and function of Src. EMBO J. ? 1997;In the press-?
20. Hanks S. K., Quinn A. M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 241:1988;42-52.
21. Hubbard S. R., Wei L., Ellis L., Hendrickson W. A. Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature. 372:1994;746-754.
22. Hunter T. Protein tyrosine kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell. 80:1995;225-236.
23. Janin J., Chothia C. The structure of protein-protein recognition sites. J. Biol. Chem. 265:1990;16027-16030.
24. Jeffrey P. D., Russo A. A., Polyak K., Gibbs E., Hurwitz J., Massague J., Pavletich N. P. Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature. 376:1995;313-320.
25. Jones T. A., Zou J. Y., Cowan S. W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47:1991;110-119.
26. Karlsson R., Zheng J., Xuong N. H., Taylor S. S., Sowadski J. M. Structure of the mammalian catalytic subunit of cAMP-dependent protein kinase and an inhibitor peptide displays an open conformation. Acta Crystallog. sect. D, 49:1993;381-388.
27. Kato J., Takeya T., Grandori C., Iba H., Levy J. B., Hanafusa H. Amino acid substitutions sufficient to convert the nontransforming p60c-Src to a transforming protein. Mol. Cell. Biol. 6:1986;4155-4160.
28. Koegl M., Courtneidge S. A., Superti-Furga G. Structural requirements for the efficient regulation of the Src protein tyrosine kinase by Csk. Oncogene. 11:1995;2317-2329.
29. Laskowski R. A., MacArthur M. W., Moss D., Thornton J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
30. Lee C. H., Kominos D. S. J., Margolis B., Schlessinger J., Shoelson S. E., Kuriyan J. Crystal structures of peptide complexes of the amino-terminal SH2 domain of the Syp tyrosine phosphatase. Structure. 2:1994;423-438.
31. Lee C. H., Saksela K., Mirza U. A., Chait B. T., Kuriyan J. Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain. Cell. 85:1996;931-942.
32. Lim W. A., Richards F. M., Fox R. O. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature. 372:1994;375-379.
33. Liu X., Brodeur S. R., Gish G., Song-Yang Z., Cantley L. C., Laudano A. P., Pawson T. Regulation of c-Src tyrosine kinase activity by the Src SH2 domain. Oncogene, 8:1993;1119-1126.
34. Mayer B. J. Signal transduction: clamping down on Src activity. Curr. Biol. 7:1997;R295-R298.
35. Moarefi I., LaFevre-Bernt M., Sicheri F., Huse M., Lee C. H., Kuriyan J., Miller W. T. Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature. 385:1997;650-653.
36. Mohammadi M., Schlessinger J., Hubbard S. R. Structure of the Fgf receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell. 86:1996;577-587.
37. Murshudov, G. Vagin, A. Dodson, E. 1996, Application of maximum likelihood methods for macromolecular refinement, Proceedings of the CCP4 Study Weekend: Macromolecular Refinement, CLRC, Daresbury.
38. Musacchio A., Saraste M., Wilmanns M. High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nature Struct. Biol. 1:1994;546-551.
39. Narayana N., Cox S., Xuong N. H., Ten Eyck L. F., Taylor S. S. A binary complex of the catalytic subunit of cAMP-dependent protein kinase and adenosine further defines conformational flexibility. Structure. 5:1997;921-935.
40. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A, 50:1994;157-163.
41. Noble M. E. M., Zeelen J. P., Wierenga R. K., Mainfroid V., Goraj K., Gohimont A. C., Martial J. A. Structure of triosephosphate isomerase fromEscherichia coli. Acta Crystallog. sect. D, 49:1993a;403-417.
42. Noble M. E. M., Musacchio A., Saraste M., Courtneidge S. A., 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. 12:1993b;2617-2624.
43. Otwinowski Z. Oscillation Data Reduction Program. Sawyer L., Isaacs N., Baily S. Proceedings of the CCP4 Study Weekend: Data Collection and Processing. 1993;SERC, Daresbury.
44. Owen D. J., Noble M. E. M., Garman E. F., Papageorgiou A. C., Johnson L. N. Two structures of the catalytic domain of phosphorylase kinase: an active protein kinase complexed with substrtae analogue and product. Structure. 3:1995;467-482.
45. Kip1. Nature. 382:1996;325-331.
46. Shalloway D., Coussens P. M., Yaciuk P. Overexpression of the c-Src protein does not induce transformation of NIH 3T3 cells. Proc. Natl Acad. Sci. USA. 81:1984;7071-7075.
47. Sicheri F., Moarefi I., Kuriyan J. Crystal structure of the Src family tyrosine kinase Hck. Nature. 385:1997;602-609.
48. Steitz T. A., Shoham M., Bennett W. S. Structural dynamics of yeast hexokinase during catalysis. Phil. Trans. Roy. Soc. ser. B, 293:1981;43-52.
49. Stover D. R., Furet P., Kydon N. B. Modulation of the SH2 binding specificity and kinase activity of Src by tyrosine phosphorylation within its SH2 domain. J. Biol. Chem. 271:1996;12481-12487.
50. Superti-Furga G., Courtneidge S. A. Structure-function relationships in Src family and related protein tyrosine kinases. Bioessays. 17:1995;321-330.
51. Taylor S. S., Radzio-Andzelm E. Three protein kinase structures define a common motif. Structure. 2:1994;345-355.
52. Tong L., Warren T. C., King J., Betageri R., Rose J., Jakes S. Crystal structures of the human p56lck SH2 domain in complex with two short phosphotyrosyl peptides at 1.0 Å and 1.8 Å resolution. J. Mol. Biol. 256:1996;601-610.
53. Veron M., Radzio-Andzelm E., Tsigelny I., Ten Eyck L. F., Taylor S. S. A conserved helix motif complements the protein kinase core. Proc. Natl Acad. Sci. USA. 90:1993;10618-10622.
54. Vonrhein C., Schlauderer G. J., Schulz G. E. Movie of the structural changes during a catalytic cycle of nucleoside monophosphae kinases. Structure. 3:1995;483-490.
55. Vriend G. WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8:1990;52-56.
56. Weijland A., Neubauer G., Courtneidge S. A., Mann M., Wierenga R. K., Superti-Furga G. The purification and characterisation of the catalytic domain of Src expressed inSchizosaccharomyces pombe. Eur. J. Biochem. 240:1996;756-764.
57. Weijland A., Williams J. C., Neubauer G., Courtneidge S. A., Wierenga R. K., Superti-Furga G. Src regulated by C-terminal phosphorylation is monomeric. Proc. Natl Acad. Sci. USA. 94:1997;3590-3595.
58. Wierenga R. K., Noble M. E. M., Davenport R. C. Comparison of the refined crystal structures of liganded and unliganded chicken, yeast and trypanosomal triosephosphate isomerase. J. Mol. Biol. 224:1992;1115-1126.
59. Xu W., Harrison S. C., Eck M. J. Three-dimensional structure of the tyrosine kinase c-Src. Nature. 385:1997;595-602.
60. Yamaguchi H., Hendrickson W. A. Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature. 384:1996;484-489.
61. Zheng J., Knighton D. R., Xuong N. H., Taylor S. S., Sowadski J. M., Ten Eyck L. Crystal structures of the myristylated catalytic subunit of cAMP-dependent protein kinase reveal open and closed conformations. Protein Sci. 2:1993a;1559-1573.
62. Zheng J., Trafny E. A., Knighton D. R., Xuong N. H., Taylor S. S., Ten Eyck L. F., Sowadski J. M. 2.2 Å Refined structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor. Acta Crystallog. sect. D, 49:1993b;362-365.