Alternate Binding Modes for a Ubiquitin-SH3 Domain Interaction Studied by NMR Spectroscopy

Journal of Molecular Biology

Volumn 386, Issue 2, 2009, Pages 391-405

  Korzhnev, Dmitry M ^a,b   Bezsonova, Irina ^b   Lee, Soyoung ^b   Chalikian, Tigran V ^b   Kay, Lewis E ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

binding modes; relaxation dispersion NMR; SH3 domain; ubiquitin

Indexed keywords

ADAPTOR PROTEIN; SH3 C PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONFORMATION; DISPERSION; ENTHALPY; ENTROPY; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; THERMODYNAMICS;

EID: 59149097809     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.11.055     Document Type: Article

References (40)

1. Fersht A. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (1999), W. H. Freeman, New York, NY
2. Schuck P.W. Protein Interactions: Biophysical Approaches for the Study of Complex Reversible Systems (2007), Springer, New York, NY
3. Lo Conte L., Chothia C., and Janin J. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285 (1999) 2177-2198
4. Jelesarov I., and Bosshard H.R. Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition. J. Mol. Recognit. 12 (1999) 3-18
5. Schreiber G. Kinetic studies of protein-protein interactions. Curr. Opin. Struct. Biol. 12 (2002) 41-47
6. Kay L.E. NMR studies of protein structure and dynamics. J. Magn. Reson. 173 (2005) 193-207
7. Palmer A.G., Kroenke C.D., and Loria J.P. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol. 339 (2001) 204-238
8. Kern D., Eisenmesser E.Z., and Wolf-Watz M. Enzyme dynamics during catalysis measured by NMR spectroscopy. Methods Enzymol. 394 (2005) 507-524
9. Ishima R., and Torchia D.A. Protein dynamics from NMR. Nat. Struct. Biol. 7 (2000) 740-743
10. Montelione G.T., and Wagner G. 2D chemical exchange NMR spectroscopy by proton-detected heteronuclear correlation. J. Am. Chem. Soc. 111 (1989) 3096-3098
11. Takeuchi K., and Wagner G. NMR studies of protein interactions. Curr. Opin. Struct. Biol. 16 (2006) 109-117
12. Zuiderweg E.R.P. Mapping protein-protein interactions in solution by NMR spectroscopy. Biochemistry 41 (2002) 1-7
13. Shuker S.B., Hajduk P.J., Meadows R.P., and Fesik S.W. Discovering high-affinity ligands for proteins: SAR by NMR. Science 274 (1996) 1531-1534
14. Kern D., and Zuiderweg E.R.P. The role of dynamics in allosteric regulation. Curr. Opin. Struct. Biol. 13 (2003) 748-757
15. Matsuo H., Walters K.J., Teruya K., Tanaka T., Gassner G.T., Lippard S.J., et al. Identification by NMR spectroscopy of residues at contact surfaces in large, slowly exchanging macromolecular complexes. J. Am. Chem. Soc. 121 (1999) 9903-9904
16. Korchuganov D.S., Nolde S.B., Reibarkh M.Y., Orekhov V.Y., Schulga A.A., Ermolyuk Y.S., et al. NMR study of monomer-dimer equilibrium of barstar in solution. J. Am. Chem. Soc. 123 (2001) 2068-2069
17. Mittag T., Schaffhausen B., and Gunther U.L. Tracing kinetic intermediates during ligand binding. J. Am. Chem. Soc. 126 (2004) 9017-9023
18. Haglund K., Shimokawa N., Szymkiewicz I., and Dikic I. Cbl-directed monoubiquitination of CIN85 is involved in regulation of ligand-induced degradation of EGF receptors. Proc. Natl Acad. Sci. USA 99 (2002) 12191-12196
19. Soubeyran P., Kowanetz K., Szymkiewicz I., Langdon W.Y., and Dikic I. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416 (2002) 183-187
20. Bezsonova I., Bruce M.C., Wiesner S., Lin H., Rotin D., and Forman-Kay J.D. Interactions between the three CIN85 SH3 domains and ubiquitin: implications for CIN85 ubiquitination. Biochemistry 47 (2008) 8937-8949
21. Hicke L., Schubert H.L., and Hill C.P. Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6 (2005) 610-621
22. Korzhnev D.M., Salvatella X., Vendruscolo M., Di Nardo A.A., Davidson A.R., Dobson C.M., and Kay L.E. Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 430 (2004) 586-590
23. Grey M.J., Tang Y.F., Alexov E., McKnight C.J., Raleigh D.P., and Palmer A.G. Characterizing a partially folded intermediate of the villin headpiece domain under non-denaturing conditions: contribution of His41 to the pH-dependent stability of the N-terminal subdomain. J. Mol. Biol. 355 (2006) 1078-1094
24. Sugase K., Dyson H.J., and Wright P.E. Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447 (2007) 1021-1025
25. Sugase K., Lansing J.C., Dyson H.J., and Wright P.E. Tailoring relaxation dispersion experiments for fast-associating protein complexes. J. Am. Chem. Soc. 129 (2007) 13406-13407
26. 15N NMR relaxation dispersion spectroscopy: binding of an antithrombin peptide to human prothrombin. J. Am. Chem. Soc. 125 (2003) 12432-12442
27. Carr H.Y., and Purcell E.M. Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys. Rev. 94 (1954) 630-638
28. Meiboom S., and Gill D. Modified spin-echo method for measuring nuclear relaxation times. Rev. Sci. Instrum. 29 (1958) 688-691
29. 2 upon the Carr-Purcell pulse separation. J. Magn. Reson. 6 (1972) 89-105
30. Eyring H. The activated complex in chemical reactions. J. Chem. Phys. 3 (1935) 107-115
31. 2 CPMG methods. J. Magn. Reson., Ser. B 104 (1994) 266-275
32. Ross P.D., and Subramanian S. Thermodynamics of protein association reactions-forces contributing to stability. Biochemistry 20 (1981) 3096-3102
33. Alsallaq R., and Zhou H.X. Electrostatic rate enhancement and transient complex of protein-protein association. Proteins 71 (2008) 320-335
34. Press W.H., Teukolsky S.A., Vetterling W.T., and Flannery B.P. Numerical Recipes in C: The Art of Scientific Computing. 2nd edit. (1997), Cambridge University Press, Cambridge, UK
35. Wishart D.S., and Case D.A. Use of chemical shifts in macromolecular structure determination. Methods Enzymol. 338 (2001) 3-34
36. Pawson T., and Nash P. Assembly of cell regulatory systems through protein interaction domains. Science 300 (2003) 445-452
37. Pawson T. Protein modules and signaling networks. Nature 373 (1995) 573-580
38. Tollinger M., Skrynnikov N.R., Mulder F.A.A., Forman-Kay J.D., and Kay L.E. Slow dynamics in folded and unfolded states of an SH3 domain. J. Am. Chem. Soc. 123 (2001) 11341-11352
39. Millet O., Loria J.P., Kroenke C.D., Pons M., and Palmer A.G. The static magnetic field dependence of chemical exchange line-broadening defines the NMR chemical shift time scale. J. Am. Chem. Soc. 122 (2000) 2867-2877
40. McConnell H.M. Reaction rates by nuclear magnetic resonance. J. Chem. Phys. 28 (1958) 430-431