Side-chain dynamics of the SAP SH2 domain correlate with a binding hot spot and a region with conformational plasticity

Journal of Molecular Biology

Volumn 322, Issue 3, 2002, Pages 605-620

  Finerty Jr, Patrick J ^a,b   Muhandiram, Ranjith ^b   Forman Kay, Julie D ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Dynamics; NMR; Plasticity; Relaxation; SH2

Indexed keywords

METHYL GROUP; PROTEIN; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DEUTERON NUCLEAR MAGNETIC RESONANCE; DYNAMICS; LIGAND BINDING; PLASTICITY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

EID: 0036385729     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00803-3     Document Type: Article

References (48)

1. Sullivan, J. L. (1999). The abnormal gene in X-linked lymphoproliferative syndrome. Curr. Opin. Immunol. 11, 431-434.
2. Sayos, J., Wu, C., Morra, M., Wang, N., Zhang, X., Allen, D. et al. (1998). The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature, 395, 462-469.
3. Pawson, T. & Schlessinger, J. (1993). SH2 and SH3 domains. Curr. Biol. 3, 434-442.
4. Cohen, G. B., Ren, R. & Baltimore, D. (1995). Modular binding domains in signal transduction proteins. Cell, 80, 237-248.
5. Poy, F., Yaffe, M. B., Sayos, J., Saxena, K., Morra, M., Sumegi, J. et al. (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.
6. Li, S. C., Gish, G., Yang, D., Coffey, A. J., Forman-Kay, J. D., Ernberg, I. et al. (1999). Novel mode of ligand binding by the SH2 domain of the human XLP disease gene product SAP/SH2D1A. Curr. Biol. 9, 1355-1362.
7. Moran, M. F., Koch, C. A., Anderson, D., Ellis, C., England, L., Martin, G. S. & Pawson, T. (1990). Src homology region 2 domains direct protein-protein interactions in signal transduction. Proc. Natl Acad. Sci. USA, 87, 8622-8626.
8. Hwang, P. M., Li, C., Morra, M., Lillywhite, J., Gertler, F., Terhorst, A., et al. (2002). A three-pronged binding mechanism for the SAP/SH2D1A SH2 domain - structural basis and relevance to the XLP syndrome. EMBO J. 21, 314-323.
9. Kay, L. E., Muhandiram, D. R., Farrow, N. A., Aubin, Y. & Forman-Kay, J. D. (1996). Correlation between dynamics and high affinity binding in an SH2 domain interaction. Biochemistry, 35, 361-368.
10. Kay, L. E., Muhandiram, D. R., Wolf, G., Shoelson, S. E. & Forman-Kay, J. D. (1998). Correlation between binding and dynamics at SH2 domain interfaces. Nature Struct. Biol. 5, 156-163.
11. Gagne, S. M., Tsuda, S., Spyracopoulos, L., Kay, L. E. & Sykes, B. D. (1998). Backbone and methyl dynamics of the regulatory domain of troponin C: anisotropic rotational diffusion and contribution of conformational entropy to calcium affinity. J. Mol. Biol. 278, 667-686.
12. Lee, A. L., Kinnear, S. A. & Wand, A. J. (2000). Redistribution and loss of side-chain entropy upon formation of a calmodulin-peptide complex. Nature Struct. Biol. 7, 72-77.
13. Loh, A. P., Pawley, N., Nicholson, L. K. & Oswald, R. E. (2001). An increase in side-chain entropy facilitates effector binding: NMR characterization of the side-chain methyl group dynamics in Cdc42Hs. Biochemistry, 40, 4590-4600.
14. 15N NMR relaxation studies of free and inhibitor-bound 4-oxalocrotonate tautomerase: backbone dynamics and entropy changes of an enzyme upon inhibitor binding. Biochemistry, 35, 16036-16047.
15. Yu, L., Zhu, C. X., Tse-Dinh, Y. C. & Fesik, S. W. (1996). Backbone dynamics of the C-terminal domain of Escherichia coli topoisomerase I in the absence and presence of single-stranded DNA. Biochemistry, 35, 9661-9666.
16. 15N NMR relaxation. Biochemistry, 33, 5984-6003.
17. Kay, L. E. (1995). Pulsed field gradient multi-dimensional NMR methods for the study of protein structure and dynamics in solution. Prog. Biophys. Mol. Biol. 63, 277-299.
18. Sattler, M., Schleucher, J. & Griesinger, C. (1999). Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Magn. Reson. Spectr. 34, 93-158.
19. Zhang, W., Smithgall, T. E. & Gmeiner, W. H. (1998). Self-association and backbone dynamics of the hck SH2 domain in the free and phosphopeptide-complexed forms. Biochemistry, 37, 7119-7126.
20. Pintar, A., Hensmann, M., Jumel, K., Pitkeathly, M., Harding, S. E. & Campbell, I. D. (1996). Solution studies of the SH2 domain from the fyn tyrosine kinase: secondary structure, backbone dynamics and protein association. Eur. Biophys. J. 24, 371-380.
21. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry, 28, 8972-8979.
22. 13C labeled proteins in solution. J. Am. Chem. Soc. 117, 11536-11544.
23. Lipari, G. & Szabo, A. (1982). Model-free approach to the interpretation of nuclear magnetic resonance relaxation of macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104, 4546-4559.
24. Lipari, G. & Szabo, A. (1982). Model-free approach to the interpretation of nuclear magnetic resonance relaxation of macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104, 4559-4570.
25. Clore, G. M., Szabo, A., Bax, A., Kay, L. E., Driscoll, P. C. & Gronenborn, A. M. (1990). Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 112, 4989-4991.
26. Mittermaier, A., Kay, L. E. & Forman-Kay, J. D. (1999). Analysis of deuterium relaxation-derived methyl axis order parameters and correlation with local structure. J. Biomol. NMR, 13, 181-185.
27. Conte, L. L., Chothia, C. & Janin, J. (1999). The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285, 2177-2198.
28. 13C NMR spectroscopy. Application to the leucine residues of staphylococcal nuclease. Biochemistry, 31, 5253-5263.
29. Engen, J. R., Gmeiner, W. H., Smithgall, T. E. & Smith, D. L. (1999). Hydrogen exchange shows peptide binding stabilizes motions in Hck SH2. Biochemistry, 38, 8926-8935.
30. Zidek, L., Novotny, M. V. & Stone, M. J. (1999). Increased protein backbone conformational entropy upon hydrophobic ligand binding. Nature Struct. Biol. 6, 1118-1121.
31. 15N NMR relaxation in Abl SH(32). Biochemistry, 38, 10225-10230.
32. Kristensen, S. M., Siegal, G., Sankar, A. & Driscoll, P. C. (2000). Backbone dynamics of the C-terminal SH2 domain of the p85alpha subunit of phosphoinositide 3-kinase: effect of phosphotyrosine-peptide binding and characterization of slow conformational exchange processes. J. Mol. Biol. 299, 771-788.
33. Engen, J. R., Smithgall, T. E., Gmeiner, W. H. & Smith, D. L. (1999). Comparison of SH3 and SH2 domain dynamics when expressed alone or in an SH(3 + 2) construct: the role of protein dynamics in functional regulation. J. Mol. Biol. 287, 645-656.
34. Pascal, S. M., Yamazaki, T., Singer, A. U., Kay, L. E. & Forman-Kay, J. D. (1995). Structural and dynamic characterization of the phosphotyrosine binding region of a Src homology 2 domain-phosphopeptide complex by NMR relaxation, proton exchange, and chemical shift approaches. Biochemistry, 34, 11353-11362.
35. DeLano, W. L. (2002). Unraveling hot spots in binding interfaces: progress and challenges. Curr. Opin. Struct. Biol. 12, 14-20.
36. Morra, M., Lu, J., Poy, F., Martin, M., Sayos, J., Calpe, S. et al. (2001). Structural basis for the interaction of the free SH2 domain EAT-2 with SLAM receptors in hematopoietic cells. EMBO J. 20, 5840-5852.
37. Gill, S. C. & von-Hippel, P. H. (1989). Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
38. Johnson, P. E., Joshi, M. D., Tomme, P., Kilburn, D. G. & McIntosh, L. P. (1996). Structure of the N-terminal cellulose-binding domain of Cellulomonas fimi CenC determined by nuclear magnetic resonance spectroscopy. Biochemistry, 35, 14381-14394.
39. 13C labeling. Biochemistry, 28, 7510-7516.
40. Johnson, B. A. & Blevins, R. A. (1994). NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR, 4, 603-614.
41. 1 constant-relaxation-time NMR spectroscopy. J. Am. Chem. Soc. 118, 911-912.
42. Delaglio, F., Grzesiek, S., Vuister, G., Zhu, G., Pfeifer, J. & Bax, A. (1995). NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6, 277-293.
43. Vetterling, W. T., Press, W. H., Teukolsky, S. A. & Flannery, B. R. (1988). Numerical Recipes in C, Cambridge University Press, Cambridge, UK.
44. Kamath, U. & Shriver, J. W. (1989). Characterization of the thermotropic state changes in myosin sub-fragment-1 and heavy meromyosin by UV difference spectroscopy. J. Biol. Chem. 264, 5586-5592.
45. 13C heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113, 4371-4380.
46. Mandel, A. M., Akke, M. & Palmer, A. G. (1995). Backbone dynamics of Escherichia coli ribonuclease H1: correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163.
47. Krishnan, V. V. & Cosman, M. (1998). An empirical relationship between rotational correlation time and solvent accessible surface area. J. Biomol. NMR, 12, 177-182.
48. Koradi, R., Billeter, M. & Wüthrich, K. (1996). MOL-MOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55.