On the Dynamic Nature of the Transition State for Protein-Protein Association as Determined by Double-mutant Cycle Analysis and Simulation

Journal of Molecular Biology

Volumn 371, Issue 1, 2007, Pages 180-196

  Harel, Michal ^a   Cohen, Mati ^a   Schreiber, Gideon ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

double mutant cycle; protein protein association; transition state

Indexed keywords

ALPHA2 INTERFERON; BARNASE; BARSTAR; BETA LACTAMASE INHIBITOR; BETA LACTAMASE TEM 1; INTERFERON REGULATORY FACTOR 2; MUTANT PROTEIN;

ARTICLE; DYNAMICS; ELECTRICITY; PERIODICITY; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIMULATION; STEREOSPECIFICITY; WILD TYPE;

EID: 34447101383     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.05.032     Document Type: Article

References (62)

1. Schreiber G. Kinetic studies of protein-protein interactions. Curr. Opin. Struct. Biol. 12 (2002) 41-47
2. Kuttner Y.Y., Kozer N., Segal E., Schreiber G., and Haran G. Separating the contribution of translational and rotational diffusion to protein association. J. Am. Chem. Soc. 127 (2005) 15138-15144
3. Kozer N., Kuttner Y.Y., Haran G., and Schreiber G. Protein-protein association in polymer solutions: from dilute to semidilute to concentrated. Biophys. J. 92 (2007) 2139-2149
4. Fersht A.R. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (1999), W.H. Freeman and Company, New York
5. Gabdoulline R.R., and Wade R.C. Brownian dynamics simulation of protein-protein diffusional encounter. Methods 14 (1998) 329-341
6. Elcock A.H., Sept D., and McCammon J.A. Computer simulation of protein-protein interactions. J. Phys. Chem. 105 (2002) 1504-1518
7. Gabdoulline R.R., and Wade R.C. Simulation of the diffusional association of barnase and barstar. Biophys. J. 72 (1997) 1917-1929
8. Spaar A., Dammer C., Gabdoulline R.R., Wade R.C., and Helms V. Diffusional encounter of barnase and barstar. Biophys. J. 90 (2006) 1913-1924
9. Camacho C.J., Weng Z., Vajda S., and DeLisi C. Free energy landscapes of encounter complexes in protein-protein association. Biophys. J. 76 (1999) 1166-1178
10. Spaar A., and Helms V. Free energy landscape of protein-protein encounter resulting from brownian dynamics simulations of Barnase:Barstar. J. Chem. Theory Comput. 1 (2005) 723-736
11. Spaar A., and Volkhard H. Ionic strength effects on the association funnel of barnase and barstar investigated by Brownian dynamics simulations. J. Non-cryst. Solids 352 (2006) 4437-4444
12. Alsallaq R., and Zhou H.X. Energy landscape and transition state of protein-protein association. Biophys. J. 92 (2007) 1486-1502
13. Alsallaq R., and Zhou H.X. Prediction of protein-protein association rates from a transition-state theory. Structure 15 (2007) 215-224
14. Tang C., Iwahara J., and Clore G.M. Visualization of transient encounter complexes in protein-protein association. Nature 444 (2006) 383-386
15. Schreiber G., and Fersht A.R. Rapid, electrostatically assisted association of proteins. Nature Struct. Biol. 3 (1996) 427-431
16. Fersht A.R., and Daggett V. Protein folding and unfolding at atomic resolution. Cell 108 (2002) 573-582
17. Wu L.C., Tuot D.S., Lyons D.S., Garcia K.C., and Davis M.M. Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature 418 (2002) 552-556
18. Mateu M.G., Sanchez Del Pino M.M., and Fersht A.R. Mechanism of folding and assembly of a small tetrameric protein domain from tumor suppressor p53. Nature Struct. Biol. 6 (1999) 191-198
19. Levy Y., Cho S.S., Onuchic J.N., and Wolynes P.G. A survey of flexible protein binding mechanisms and their transition states using native topology based energy landscapes. J. Mol. Biol. 346 (2005) 1121-1145
20. Taylor M.G., Rajpal A., and Kirsch J.F. Kinetic epitope mapping of the chicken lysozyme.HyHEL-10 Fab complex: delineation of docking trajectories. Protein Sci. 7 (1998) 1857-1867
21. Kiel C., Selzer T., Shaul Y., Schreiber G., and Herrmann C. Electrostatically optimized Ras-binding Ral guanine dissociation stimulator mutants increase the rate of association by stabilizing the encounter complex. Proc. Natl Acad. Sci. USA 101 (2004) 9223-9228
22. Carter P.J., Winter G., Wilkinson A.J., and Fersht A.R. The use of double mutants to detect structural changes in the active site of the tyrosyl-tRNA synthetase (Bacillus stearothermophilus). Cell 38 (1984) 835-840
23. Horovitz A. Double-mutant cycles: a powerful tool for analyzing protein structure and function. Fold. Des. 1 (1996) R121-R126
24. Serrano L., Horovitz A., Avron B., Bycroft M., and Fersht A.R. Estimating the contribution of engineered surface electrostatic interactions to protein stability by using double-mutant cycles. Biochemistry 29 (1990) 9343-9352
25. Horovitz A. Non-additivity in protein-protein interactions. J. Mol. Biol. 196 (1987) 733-735
26. Horovitz A., and Fersht A.R. Strategy for analysing the co-operativity of intramolecular interactions in peptides and proteins. J. Mol. Biol. 214 (1990) 613-617
27. Schreiber G., and Fersht A.R. Energetics of protein-protein interactions: analysis of the barnase-barstar interface by single mutations and double mutant cycles. J. Mol. Biol. 248 (1995) 478-486
28. Vijayakumar M., Wong K.Y., Schreiber G., Fersht A. R., Szabo A., and Zhou H.X. Electrostatic enhancement of diffusion-controlled protein-protein association: comparison of theory and experiment on barnase and barstar. J. Mol. Biol. 278 (1998) 1015-1024
29. Schreiber G., and Fersht A.R. Interaction of barnase with its polypeptide inhibitor barstar studied by protein engineering. Biochemistry 32 (1993) 5145-5150
30. Frisch C., Fersht A.R., and Schreiber G. Experimental assignment of the structure of the transition state for the association of barnase and barstar. J. Mol. Biol. 308 (2001) 69-77
31. Frisch C., Schreiber G., Johnson C.M., and Fersht A.R. Thermodynamics of the interaction of barnase and barstar: changes in free energy versus changes in enthalpy on mutation. J. Mol. Biol. 267 (1997) 696-706
32. Miyashita O., Onuchic J.N., and Okamura M.Y. Transition state and encounter complex for fast association of cytochrome c2 with bacterial reaction center. Proc. Natl Acad. Sci. USA 101 (2004) 16174-16179
33. Tetreault M., Cusanovich M., Meyer T., Axelrod H., and Okamura M.Y. Double mutant studies identify electrostatic interactions that are important for docking cytochrome c2 onto the bacterial reaction center. Biochemistry 41 (2002) 5807-5815
34. Tetreault M., Rongey S.H., Feher G., and Okamura M. Y. Interaction between cytochrome c2 and the photosynthetic reaction center from Rhodobacter sphaeroides: effects of charge-modifying mutations on binding and electron transfer. Biochemistry 40 (2001) 8452-8462
35. Miyashita O., Onuchic J.N., and Okamura M.Y. Continuum electrostatic model for the binding of cytochrome c2 to the photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry 42 (2003) 11651-11660
36. Albeck S., and Schreiber G. Biophysical characterization of the interaction of the beta-lactamase TEM-1 with its protein inhibitor BLIP. Biochemistry 38 (1999) 11-21
37. Lim D., Park H.U., De Castro L., Kang S.G., Lee H. S., Jensen S., et al. Crystal structure and kinetic analysis of beta-lactamase inhibitor protein-II in complex with TEM-1 beta-lactamase. Nature Struct. Biol. 8 (2001) 848-852
38. Strynadka N.C., Adachi H., Jensen S.E., Johns K., Sielecki A., Betzel C., et al. Molecular structure of the acyl-enzyme intermediate in beta-lactam hydrolysis at 1.7 Å resolution. Nature 359 (1992) 700-705
39. Strynadka N.C., Jensen S.E., Alzari P.M., and James M.N. A potent new mode of beta-lactamase inhibition revealed by the 1.7 Å X-ray crystallographic structure of the TEM-1-BLIP complex. Nature Struct. Biol. 3 (1996) 290-297
40. Strynadka N.C., Jensen S.E., Johns K., Blanchard H., Page M., Matagne A., et al. Structural and kinetic characterization of a beta-lactamase-inhibitor protein. Nature 368 (1994) 657-660
41. Jelsch C., Mourey L., Masson J.M., and Samama J.P. Crystal structure of Escherichia coli TEM1 beta-lactamase at 1.8 Å resolution. Proteins: Struct. Funct. Genet. 16 (1993) 364-383
42. Piehler J., and Schreiber G. Biophysical analysis of the interaction of human ifnar2 expressed in E. coli with IFNalpha2. J. Mol. Biol. 289 (1999) 57-67
43. Roisman L.C., Piehler J., Trosset J.Y., Scheraga H. A., and Schreiber G. Structure of the interferon-receptor complex determined by distance constraints from double-mutant cycles and flexible docking. Proc. Natl Acad. Sci. USA 98 (2001) 13231-13236
44. Klaus W., Gsell B., Labhardt A.M., Wipf B., and Senn H. The three-dimensional high resolution structure of human interferon alpha-2a determined by heteronuclear NMR spectroscopy in solution. J. Mol. Biol. 274 (1997) 661-675
45. Piehler J., Roisman L.C., and Schreiber G. New structural and functional aspects of the type I interferon-receptor interaction revealed by comprehensive mutational analysis of the binding interface. J. Biol. Chem. 275 (2000) 40425-40433
46. Chill J.H., Nivasch R., Levy R., Albeck S., Schreiber G., and Anglister J. The human interferon receptor: NMR-based modeling, mapping of the IFN-alpha 2 binding site, and observed ligand-induced tightening. Biochemistry 41 (2002) 3575-3585
47. Bycroft M., Ludvigsen S., Fersht A.R., and Poulsen F. M. Determination of the three-dimensional solution structure of barnase using nuclear magnetic resonance spectroscopy. Biochemistry 30 (1991) 8697-8701
48. Guillet V., Lapthorn A., Hartley R.W., and Mauguen Y. Recognition between a bacterial ribonuclease, barnase, and its natural inhibitor, barstar. Structure 1 (1993) 165-176
49. 13C assignments of barstar using nuclear magnetic resonance spectroscopy. Biochemistry 33 (1994) 8866-8877
50. Mauguen Y., Hartley R.W., Dodson E.J., Dodson G. G., Bricogne G., Chothia C., and Jack A. Molecular structure of a new family of ribonucleases. Nature 297 (1982) 162-164
51. Selzer T., Albeck S., and Schreiber G. Rational design of faster associating and tighter binding protein complexes. Nature Struct. Biol. 7 (2000) 537-541
52. Selzer T., and Schreiber G. New insights into the mechanism of protein-protein association. Proteins: Struct. Funct. Genet. 45 (2001) 190-198
53. Reichmann D., Rahat O., Albeck S., Meged R., Dym O., and Schreiber G. The modular architecture of protein-protein binding interfaces. Proc. Natl Acad. Sci. USA 102 (2005) 57-62
54. Albeck S., Unger R., and Schreiber G. Evaluation of direct and cooperative contributions towards the strength of buried hydrogen bonds and salt bridges. J. Mol. Biol. 298 (2000) 503-520
55. Slutzki M., Jaitin D.A., Yehezkel T.B., and Schreiber G. Variations in the unstructured C-terminal tail of interferons contribute to differential receptor binding and biological activity. J. Mol. Biol. 360 (2006) 1019-1030
56. Dominguez C., Boelens R., and Bonvin A.M. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125 (2003) 1731-1737
57. Katchalski-Katzir E., Shariv I., Eisenstein M., Friesem A.A., Aflalo C., and Vakser I.A. Molecular surface recognition: determination of geometric fit between proteins and their ligands by correlation techniques. Proc. Natl Acad. Sci. USA 89 (1992) 2195-2199
58. Shaul Y., and Schreiber G. Exploring the charge space of protein-protein association: a proteomic study. Proteins: Struct. Funct. Genet. 60 (2005) 341-352
59. Rajamani D., Thiel S., Vajda S., and Camacho C.J. Anchor residues in protein-protein interactions. Proc. Natl Acad. Sci. USA 101 (2004) 11287-11292
60. Volkov A.N., Worrall J.A., Holtzmann E., and Ubbink M. Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proc. Natl. Acad. Sci. USA 103 (2006) 18945-18950
61. Selzer T., and Schreiber G. Predicting the rate enhancement of protein complex formation from the electrostatic energy of interaction. J. Mol. Biol. 287 (1999) 409-419
62. Chill J.H., Quadt S.R., Levy R., Schreiber G., and Anglister J. The human type I interferon receptor: NMR structure reveals the molecular basis of ligand binding. Structure 11 (2003) 791-802