Ligand-induced changes in dynamics in the RT loop of the C-terminal SH3 domain of Sem-5 indicate cooperative conformational coupling

Protein Science

Volumn 12, Issue 5, 2003, Pages 982-996

  Ferreon, Josephine C ^a   Hilser, Vincent J ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

15N relaxation; Backbone dynamics; Ligand binding; NMR; Order parameter; Polyproline peptide; Sem 5; SH3

Indexed keywords

PROLINE DERIVATIVE;

ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; ENERGY TRANSFER; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL;

BINDING SITES; CAENORHABDITIS ELEGANS PROTEINS; LIGANDS; MODELS, MOLECULAR; MOTION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; SRC HOMOLOGY DOMAINS;

EID: 0037407208     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0238003     Document Type: Article

References (58)

1. Abragam, A. 1961. Principles of nuclear magnetism. Clarendon Press, Oxford, UK.
2. 2+ binding by calbindin-d(9k). J. Am. Chem. Soc. 115: 9832-9833.
3. 15N backbone dynamics of the S-peptide from ribonuclease A in its free and S-protein bound forms: Toward a site-specific analysis of entropy changes upon folding. Protein Sci. 7: 389-402.
4. Booker, G.W., Gout, I., Downing, A.K., Driscoll, P.C., Boyd, J., Waterfield, M.D., and Campbell, I.D. 1993. Solution structure and ligand-binding site of the SH3 domain of the p85α subunit of phosphatidylinositol 3-kinase. Cell 73: 813-822.
5. Buday, L. 1999. Membrane-targeting of signalling molecules by SH2/SH3 domain-containing adaptor proteins. Biochim. Biophys. Acta 1422: 187-204.
6. Clark, S.G., Stern, M.J., and Horvitz, H.R. 1992. C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature 356: 340-344.
7. 1H NMR spectroscopy. Biochemistry 29: 7387-7401.
8. Collins, J.R., Burt, S.K., and Erickson, J.W. 1995. Flap opening in HIV-1 protease simulated by 'activated' molecular dynamics. Nat. Struct. Biol. 2: 334-338.
9. Cross, T.A. and Opella, S.J. 1983. Protein-structure by solid-state NMR. J. Am. Chem. Soc. 105: 306-308.
10. Dalgarno, D.C., Botfield, M.C., and Rickles, R.J. 1997. SH3 domains and drug design: Ligands, structure, and biological function. Biopolymers 43: 383-400.
11. Eftink, M.R., Anusiem, A.C., and Biltonen, R.L. 1983. Enthalpy-entropy compensation and heat capacity changes for protein-ligand interactions: General thermodynamic models and data for the binding of nucleotides to ribonuclease A. Biochemistry 22: 3884-3896.
12. Egan, S.E., Giddings, B.W., Brooks, M.W., Buday, L., Sizeland, A.M., and Weinberg, R.A. 1993. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature 363: 45-51.
13. 15N NMR relaxation. Biochemistry 33: 5984-6003.
14. Feher, V.A. and Cavanagh, J. 1999. Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F. Nature 400: 289-293.
15. Ferreon, J.C., Volk, D.E., Luxon, B.A., Gorrenstein, D.G., and Hilser, V.J. 2003. Solution structure, dynamics and thermodynamics of the native state ensemble of the Sem-5 C-terminal SH3 domain. Biochemistry (in press).
16. Gagné, S.M., Tsuda, S., Spyracopoulos, L., Kay, L.E., and 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.
17. Gómez, J. and Freire, E. 1995. Thermodynamic mapping of the inhibitor site of the aspartic protease endothiapepsin. J. Mol. Biol. 252: 337-350.
18. Hansson, H., Mattsson, P.T., Allard, P., Haapaniemi, P., Vihinen, M., Smith, C.I.E., and Härd, T. 1998. Solution structure of the SH3 domain from Bruton's tyrosine kinase. Biochemistry 37: 2912-2924.
19. Hiyama, Y., Niu, C.-H., Silverton, J.V., Bavoso, A., and Torchia, D.A. 1988. Determination of N-15 chemical-shift tensor via N-15-H-2 dipolar coupling in BOC-glycylglycyl[N-15]glycine benzyl ester. J. Am. Chem. Soc. 110: 2378-2383.
20. 1H exchange. Biochemistry 36: 2278-2290.
21. Horita, D.A., Baldisseri, D.M., Zhang, W., Altieri, A.S., Smithgall, T.E., Gmeimer, W.H., and Byrd, R.A. 1998. Solution structure of the human Hck SH3 domain and identification of its ligand binding site. J. Mol. Biol. 278: 253-265.
22. Horita, D.A., Zhang, W., Smithgall, T.E., Gmeiner, W.H., and Byrd, R.A. 2000. Dynamics of the Hck-SH3 domain: Comparison of experiment with multiple molecular dynamics simulations. Protein Sci. 9: 95-103.
23. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28: 8972-8979.
24. Kay, L.E., Muhandiram, D.R., Farrow, N.A., Aubin, Y., and Forman-Kay, J.D. 1996. Correlation between dynamics and high affinity binding in an SH2 domain interaction. Biochemistry 35: 361-368.
25. Kay, L.E., Muhandiram, D.R., Wolf, G., Shoelson, S.E., and Forman-Kay, J.D. 1998. Correlation between binding and dynamics at SH2 domain interfaces. Nat. Struct. Biol. 5: 156-163.
26. Koradi, R., Billeter, M., and Wüthrich, K. 1996. MOLMOL: A program for display and analysis of molecular structures. J. Mol. Graph. 14: 51-55.
27. Kristensen, S.M., Siegal, G., Sankar, A., and Driscoll, P.C. 2000. Backbone dynamics of the C-terminal SH2 domain of the p85α subunit of phosphoinositide 3-kinase: Effect of phosphotyrosine-peptide binding and characterization of slow conformational exchange processes. J. Mol. Biol. 299: 771-788.
28. Lian, L. and Roberts, G.C.K. 1993. Effects of chemical exchange on NMR spectra. In NMR of macromolecules. A practical approach (ed. G.C.K. Roberts), pp. 153-182. Oxford University Press, Oxford, UK.
29. Lim, W.A., Fox, R.O., and Richards, F.M. 1994a. Stability and peptide binding affinity of an SH3 domain from the Caenorhabditis elegans signaling protein Sem-5. Protein Sci. 3: 1261-1266.
30. Lim, W.A., Richards, F.M., and Fox, R.O. 1994b. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature 372: 375-379.
31. Lipari, G. and Szabo, A. 1982a. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104: 4559-4570.
32. -. 1982b. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104: 4546-4559.
33. Lowenstein, E.J., Daly, R.J., Batzer, A.G., Li, W., Margolis, B., Lammers, R., Ullrich, A., Skolnik, E.Y., Bar-Sagi, D., and Schlessinger, J. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70: 431-442.
34. Mandel, A.M., Akke, M., and Palmer III, A.G. 1995. Backbone dynamics of Escherichia coli ribonuclease HI: Correlations with structure and function in an active enzyme. J. Mol. Biol. 246: 144-163.
35. -. 1996. Dynamics of ribonuclease H: Temperature dependence of motions on multiple time scales. Biochemistry 35: 16009-16023.
36. Nicholson, L.K., Yamazaki, T., Torchia, D.A., Grzesiek, S., Bax, A., Stahl, S.J., Kaufman, J.D., Wingfield, P.T., Lam, P.Y.S., Jadhav, P.K., et al. 1995. Flexibility and function in HIV-1 protease. Nat. Struct. Biol. 2: 274-279.
37. Olejniczak, E.T., Zhou, M.-M., and Fesik, S.W. 1997. Changes in the NMR-derived motional parameters of the insulin receptor substrate 1 phosphotyrosine binding domain upon binding to an interleukin 4 receptor phosphopeptide. Biochemistry 36: 4118-4124.
38. Olivier, J.P., Raabe, R., Henkemeyer, M., Dickson, B., Mbamalu, G., Margolis, B., Schlessinger, J., Hafen, E., and Pawson, T. 1993. A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73: 179-191.
39. 13C heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113: 4371-4380.
40. 15N relaxation parameters. J. Biomol. NMR 20: 149-165.
41. Pawson, T. 1995. Protein modules and signalling networks. Nature 373: 575-579.
42. Renzoni, D.A., Pugh, D.J.R., Siligardi, G., Das, P., Rossi, C., Waterfield, M.D., Campbell, I.D., and Ladbury, J.E. 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 P13-kinase. Biochemistry 35: 15646-15653.
43. Spyracopoulos, L., Gagné, S.M., Li, M.X., and Sykes, B.D. 1998. Dynamics and thermodynamics of the regulatory domain of human cardiac troponin C in the apo- and calcium-saturated states. Biochemistry 37: 18032-18044.
44. 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.
45. Stock, A. 1999. Relating dynamics and function. Nature 400: 221-222.
46. 15N NMR relaxation measurements. Biochemistry 32: 426-435.
47. 15N NMR relaxation. J. Am. Chem. Soc. 117: 12562-12566.
48. 15N chemical shift anisotropy from quantitative measurement of relaxation interference effects. J. Am. Chem Soc. 118: 6986-6991.
49. Wagner, G. 1995. The importance of being floppy. Nat. Struct. Biol. 2: 255-257.
50. Wang, C., Pawley, N.H., and Nicholson, L.K. 2001. The role of backbone motions in ligand binding to the c-Src SH3 domain. J. Mol. Biol. 313: 873-887.
51. Weber, G. 1992. Protein interactions. Chapman and Hall, London
52. Wiseman, T., Williston, S., Brandts, J.F., and Lin, L. 1989. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179: 131-137.
53. Wittekind, M., Mapelli, C., Farmer II, B.T., Suen, K., Goldfarb, V., Tsao, J., Lavoie, T., Barbacid, M., Meyers, C.A., and Mueller, L. 1994. Orientation of peptide fragments from Sos proteins bound to the N-terminal SH3 domain of Grb2 determined by NMR spectroscopy. Biochemistry 33: 13531-13539.
54. Wyman, J. 1964. Linked functions and reciprocal effects in hemoglobin: A second look. Adv. Protein Chem. 19: 223-286.
55. Yang, D.W. and Kay, L.E. 1996. Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: Application to protein folding. J. Mol. Biol. 263: 369-382.
56. Ye, J., Mayer, K.L., and Stone, M.J. 1999. Backbone dynamics of the human CC-chemokine eotaxin. J. Biomol. NMR 15: 115-124.
57. Yu, H., Rosen, M.K., Shin, T.B., Seidel-Dugan, C., Brugge, J.S., and Schreiber, S.L. 1992. Solution structure of the SH3 domain of Src and identification of its ligand-binding site. Science 258: 1665-1667.
58. Zidek, L., Novotny, M.V., and Stone, M.J. 1999. Increased protein backbone conformational entropy upon hydrophobic ligand binding. Nat. Struct. Biol. 6: 1118-1121.