A survey of flexible protein binding mechanisms and their transition states using native topology based energy landscapes

Journal of Molecular Biology

Volumn 346, Issue 4, 2005, Pages 1121-1145

  Levy, Yaakov ^a   Cho, Samuel S ^a   Onuchic, José N ^a   Wolynes, Peter G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Fly casting mechanism; Funnel energy landscape; Induced fit mechanism; Protein binding; Protein folding

Indexed keywords

DIMER; MONOMER; PROTEIN;

CORRELATION ANALYSIS; ENERGY; MATHEMATICAL MODEL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS;

EID: 13444301037     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.12.021     Document Type: Article

References (117)

1. A.-C. Gavin, M. Bosche, R. Krause, P. Grandi, and M. Marzioch Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 415 2002 141 147
2. Y. Ho, A. Gruhler, A. Heilut, G.D. Bader, L. Moore, and S.-L. Adams Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry Nature 415 2002 180 183
3. L. Salwinski, and D. Eisenberg Computational methods of analyses of protein-protein interactions Curr. Opin. Struct. Biol. 13 2003 377 382
4. J. Janin, and B. Seraphin Genome-wide studies of protein-protein interaction Curr. Opin. Struct. Biol. 13 2003 383 388
5. E. Fischer Einfluss der configuration auf die Wirkung der Enzyme Ber. Dtsch. Chem. Ges. 27 1894 2985 2991
6. D.E.J. Koshland Application of a theory of enzyme specificity to protein synthesis Proc. Natl Acad. Sci. USA 44 1958 98 123
7. H. Frauenfelder, S.G. Sliger, and P.G. Wolynes The energy landscapes and motions of proteins Science 254 1991 1598 1603
8. Y. Levy, P.G. Wolynes, and J.N. Onuchic Protein topology determines binding mechanisms Proc. Natl Acad. Sci. USA 101 2004 511 516
9. G.M. Verkhivker, D. Bouzida, D.K. Gehlhaar, P.A. Rejto, S.T. Freer, and P.W. Rose Simulating disorder-order transitions in molecular recognition of unstructured proteins: where folding meets binding Proc. Natl Acad. Sci. USA 100 2003 5148 5153
10. N. Gupta, and A. Irback Coupled folding-binding versus docking: a lattice model study J. Chem. Phys. 120 2004 3983 3989
11. B. Ma, S. Kumar, C.-J. Tsai, and R. Nussinov Folding funnels and binding mechanisms Protein Eng. 12 1999 713 720
12. H.R. Bosshard Molecular recognition by induced fit: how fit is the concept? News Physiol. Sci. 16 2001 171 173
13. B.Y. Ma, M. Shatsky, H. Wolfson, and R. Nussinov Multiple diverse ligands binding at a single protein site: a matter of pre-existing populations Protein Sci. 11 2002 184 197
14. C.-S. Goh, D. Milburn, and M. Gerstein Conformational changes associated with protein-protein interactions Curr. Opin. Struct. Biol. 14 2004 1 6
15. J. Foote, and C. Milstein Conformational isomerism and the diversity of antibodies Proc. Natl Acad. Sci. USA 91 1994 10370 10374
16. C. Berger, S. Weber-Bornhauser, J. Eggenberger, J. Hanes, A. Plucjthun, and H.R. Bosshard Antigen recognition by conformational selection FEBS Letters 450 1999 149 153
17. B.F. Volkman, D. Lifson, D.E. Wemmer, and D. Kern Two-state allosteric behavior in a single-domain signaling protein Science 291 2001 2429 2433
18. C.J. Jeffery Moonlighting proteins Trends Biochem. Sci. 24 1999 8 11
19. S.D. Copley Enzymes with extra talents: moonlighting functions and catalytic promiscuity Curr. Opin. Chem. Biol. 7 2003 265 272
20. L.C. James, and S.S. Tawfik Conformational diversity and protein evolution - a 60-year-old hypothesis revisited Trends Biochem. Sci. 28 2003 361 368
21. M.J. Bennett, M.P. Schlunegger, and D. Eisenberg 3D domain swapping: a mechanism for oligomer assembly Protein Sci. 4 1995 2455 2468
22. Y. Liu, and D. Eisenberg 3D domain swapping: as domains continue to swap Protein Sci. 11 2002 1285 1299
23. J.D. Bryngelson, and P.G. Wolynes Spin glasses and the statistical mechanics of protein folding Proc. Natl Acad. Sci. USA 84 1987 7524 7528
24. P.E. Leopold, M. Montal, and J.N. Onuchic Protein folding funnels: a kinetic approach to the sequence-structure relationship Proc. Natl Acad. Sci. USA 89 1992 8721 8725
25. J.N. Onuchic, P.G. Wolynes, Z. Luthey-Schulten, and N.D. Socci Toward an outline of the topography of a realistic protein-folding funnel Proc. Natl Acad. Sci. USA 92 1995 3626 3630
26. D.M. Taverna, and R.A. Goldstein Why are proteins so robust to site mutations? J. Mol. Biol. 315 2002 479 484
27. Yang, S., Cho, S., Levy, Y., Cheung, M.S., Levine, H., Wolynes, P. G. & Onuchic, J. N. (2004). Domain Swapping is a consequence of the principle of minimal frustration. Proc. Natl Acad. Sci. USA, 101, 12786-12791.
28. F. Rousseau, J.W.H. Schymkowitz, and L.S. Itzhaki The unfolding story of three-dimensional domain swapping Structure 11 2003 243 251
29. K.E. Neet, and D.E. Timm Conformational stability of dimeric proteins: quantitative studies by equilibrium denaturation Protein Sci. 3 1994 2167 2174
30. D. Xu, C.-J. Tsai, and R. Nussinov Mechanism and evolution of protein dimerization Protein Sci. 7 1998 533 544
31. H.J. Dyson, and P.E. Wright Coupling of folding and binding for unstructured proteins Curr. Opin. Struct. Biol. 12 2002 54 60
32. P. Tompa Intrinsically unstructured proteins Trends Biochem. Sci. 27 2002 527 533
33. V.N. Uversky Natively unfolded proteins: a point where biology waits for physics Protein Sci. 11 2002 739 756
34. A.K. Dunker, J.D. Lawson, C.J. Brown, R.M. Williams, P. Romero, and J.S. Oh Intrinsically disordered protein J. Mol. Graph. Model. 19 2001 26 59
35. G.A. Papoian, and P.G. Wolynes The physics and bioinformatics of binding and folding - an energy landscape perspective Biopolymers 68 2003 333 349
36. R. Kirwacki, L. Hengst, L. Tennant, S. Reed, and P. Wright Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity Proc. Natl Acad. Sci. USA 93 1996 11504 11509
37. R. Spolar, and M. Record Coupling of local folding to site-specific binding of protein to DNA Science 263 1994 777 784
38. K. Gunasekaran, C.-J. Tsai, S. Kumar, D. Zanuy, and R. Nussinov Extended disordered proteins: targeting function with less scaffold Trends Biochem. Sci. 28 2003 81 85
39. B.A. Shoemaker, J.J. Portman, and P.G. Wolynes Speeding molecular recognition by using the folding funnel: the fly-casting mechanism Proc. Natl Acad. Sci. USA 97 2000 8868 8873
40. J. Janin, K. Henrick, J. Moult, L.T. Eyck, M.J.E. Sternberg, and S. Vajda CAPRI: a critical assessment of predicted interactions Proteins: Struct. Funct. Genet. 52 2003 2 9
41. E. Ben-Zeev, A. Berchanski, A. Heifetz, B. Shapira, and M. Eisenstein Prediction of the unknown: inspiring experience with the CAPRI experiments Proteins: Struct. Funct. Genet. 52 2003 41 46
42. R. Mendez, R. Laplae, L.D. Maria, and S.J. Wodak Assessment of blind predictions of protein-protein interactions: current status of docking methods Proteins: Struct. Funct. Genet. 52 2003 51 67
43. A.R. Fersht Characterizing transition states in protein folding: an essential step in the puzzle Curr. Opin. Struct. Biol. 5 1994 79 84
44. V. Daggett, and A.R. Fersht The present view of the mechanism of protein folding Nature Rev. Mol. Cell Biol. 4 2003 497 502
45. A.R. Fersht, and S. Sato F-values analysis and the nature of protein-folding transition states Proc. Natl Acad. Sci. USA 101 2004 7976 7981
46. M.E. Milla, B.M. Brown, C.D. Waldburger, and R.T. Sauer P22 Arc repressor: transition state properties inferred from mutational effects on the rates of protein unfolding and refolding Biochemistry 34 1995 13914 13919
47. M.G. Taylor, A. Rajpal, and J.F. Kirsch Kinetic epitope mapping of the chicken lysozyme HyHEL-10 Fab complex: delineation of docking trajectories Protein Sci. 7 1998 1857 1867
48. M.G. Mateu, M.M.S.D. Pino, and A.R. Fersht Mechanism of folding and assembly of a small tetrameric protein domain from tumor suppressor p53 Nature Struct. Biol. 6 1999 191 198
49. B. Nolting, and K. Andert Mechanism of protein folding Proteins: Struct. Funct. Genet. 41 2000 288 298
50. L.C. Wu, D.S. Tuot, D.S. Lyons, K.C. Garcia, and M.M. Davis Two-step binding mechanism of T-cell receptor recognition of peptide-MHC Nature 418 2002 552 555
51. J.N. Onuchic, Z. Luthey-Schulten, and P.G. Wolynes Theory of protein folding: the energy landscape perspective Annu. Rev. Phys. Chem. 48 1997 539 594
52. J.N. Onuchic, N.D. Socci, Z. Luthey-Schulten, and P.G. Wolynes Protein folding funnels: the nature of the transition state ensemble Fold. Des. 1 1996 441 450
53. C.-J. Tsai, S. Kumar, B. Ma, and R. Nussinov Folding funnels, binding funnels, and protein function Protein Sci. 8 1999 1181 1190
54. C. Zhang, J. Chen, and C. DeLisi Protein-protein recognition: exploring the energy funnels near the binding sites Proteins: Struct. Funct. Genet. 34 1999 255 267
55. A. Tovchigrechko, and I.A. Vakser How common is the funnel-like energy landscape in protein-protein interactions? Protein Sci. 10 2001 1572 1583
56. S. Kumar, B. Ma, C.-J. Tsai, N. Sinha, and R. Nussinov Folding and binding cascades: dynamic landscapes and population shifts Protein Sci. 9 2000 10 19
57. G.M. Verkhivker, D. Bouzida, D.K. Gehlhaar, P.A. Rejto, S.T. Freer, and P.W. Rose Complexity and simplicity of ligand-macromolecule interactions: the energy landscape perspective Curr. Opin. Struct. Biol. 12 2002 197 203
58. J. Wang, and G.M. Verkhivker Energy landscape theory, funnels, specificity, and optimal criterion of biomolecular binding Phys. Rev. Letters 90 2003 188101
59. G.A. Papoian, J. Ulander, and P.G. Wolynes Role of water mediated interactions in protein-protein recognition landscapes J. Am. Chem. Soc. 125 2003 9170 9178
60. G.A. Papoian, J. Ulander, M.E. Eastwood, and P.G. Wolynes Water in protein structure prediction Proc. Natl Acad. Sci. USA 101 2004 3352 3357
61. S. Jones, and J.M. Thornton Principles of proetin-protein interactions Proc. Natl Acad. Sci. USA 93 1996 13 20
62. L.L. Conte, C. Chotia, and J. Janin The atomic structure of protein-protein recognition sites J. Mol. Biol. 285 1999 2177 2198
63. Y. Ofran, and B. Rost Analyzing six types of protein-protein interfaces J. Mol. Biol. 325 2003 377 387
64. R.P. Bahadur, P. Chakrabarti, F. Rodier, and J. Janin Dissecting subunit interfaces in homodimeric proteins Proteins: Struct. Funct. Genet. 53 2003 708 719
65. F.B. Sheinerman, R. Norel, and B. Honig Electrostatic aspects of protein-protein interactions Curr. Opin. Struct. Biol. 10 2000 153 159
66. G. Schreiber Kinetic studies of protein-protein interactions Curr. Opin. Struct. Biol. 12 2002 41 47
67. C.R. Robinson, and R.T. Sauer Equilibrium stability and sub-millisecond refolding of a designed single-chain Arc repressor Biochemistry 35 1996 13878 13884
68. J.U. Bowie, and R.T. Sauer Equilibrium dissociation of the Arc repressor dimer Biochemistry 28 1989 7139 7143
69. O.D. Monera, G.S. Shaw, B.-Y. Zho, B.D. Sykes, C.M. Kay, and R.S. Hodges Role of interchain a-helical hydrophobic interactions in Ca2+ affinity, formation, and stability of a two-site domain in troponin C Protein Sci. 1 1992 945 955
70. S.A. Hobart, S. Ilin, D.F. Moriarty, R. Osuna, and W. Colon Equilibrium denaturation studies of the Escherichia coli factor for inversion stimulation: implication for in vivo function Protein Sci. 11 2002 1671 1680
71. L.M. Gloss, and C.R. Matthews The barriers in the bimolacular and unimolecular folding reactions of the dimeric core domain of Escherichia coli Trp repressor are dominated by enthalpic contributions Biochemistry 37 1998 16000 16010
72. M. Huang, and T. Oas Submillisecond folding of monomeric l repressor Proc. Natl Acad. Sci. USA 92 1995 6878 6882
73. R. Jana, T.R. Hazbun, A.K.M.M. Mollah, and M.C. Mossing A folded monomeric intermediate in the formation of lambda Cro dimer-DNA complexes J. Mol. Biol. 273 1997 402 416
74. B. Leiting, R.D. Francesco, L. Tomei, R. Cortese, G. Otting, and K. Wuthrich The three-dimensional NMR-solution structure of the polypeptide fragment 195-286 of the LFB1/HNF1 transcription factor from rat liver comprises a non-classical homeodomain EMBO J. 12 1993 1797 1803
75. Y. Levy, G.A. Papoian, J. Onuchic, and P.G. Wolynes The energy landscape of protein dimers Isr. J. Chem. 2004 in the press
76. Y. Levy, A. Caflisch, J.N. Onuchic, and P.G. Wolynes The folding and dimerization of HIV-1 protease: evidence for a stable monomer from simulations J. Mol. Biol. 340 2004 67 79
77. P.N. Bryan Prodomain and protein folding catalysis Chem. Rev. 102 2002 4805 4816
78. K.R. LeFevre, and M.H.J. Cordes Retroevolution of lambda Cro toward a stable monomer Proc. Natl Acad. Sci. USA 100 2003 2345 2350
79. T. Newlove, J.H. Koniezka, and M.H. Cordes Secondary structure switching in Cro protein evolution Structure 12 2004 569 581
80. E.I. Shakhnovich Folding by association Nature Struct. Biol. 6 1999 99 102
81. L.T. Chong, C.D. Snow, Y.M. Rhee, and V.S. Pande Dimerization of the p53 oligomerization domain: identification of a folding nucleus by molecular dynamics simulations J. Mol. Biol. 2005 in the press
82. M. McCoy, E.S. Stavridi, J.L.F. Waterman, A.M. Wieczorek, S.J. Opella, and T.D. Halazonetis Hydrophobic side-chain size is a determinant of the three-dimensional structure of the p53 oligomerization domain EMBO J. 16 1997 6230 6236
83. M.G. Mateu, and A.R. Fersht Nine hydrophobic side chains are key determinants of the thermodynamic stability and oligomerization status of tumor EMBO J. 17 1998 2748 2758
84. I. Jelesarov, and M. Lu Thermodynamics of trimer-of-hairpins formation by the SIV gp41 envelope protein J. Mol. Biol. 307 2001 637 656
85. D.N. Marti, S. Bjelic, M. Lu, H.R. Bosshard, and I. Jelesarov Fast folding of the HIV-1 and SIV gp41 six-helix bundles J. Mol. Biol. 336 2004 1 8
86. B.C. Braden, and R.J. Poljak Structure and energetics of anti-lysozyme antibodies C. Leanthous Protein-protein Recognition 1st edit. 2000 Oxford University Press Oxford
87. A. Rajpal, M.G. Taylor, and J.F. Kirsch Quantitative evaluation of the chicken lysozyme epitope in the HyHEL-10 Fab complex: free energies and kinetics Protein Sci. 7 1998 1868 1874
88. Y. Li, M. Urrutia, S.J. Smith-Gill, and R.A. Mariuzza Dissection of binding interactions in the complex between the anti-lysozyme antibody HyHEL-63 and its antigen Biochemistry 42 2003 11 22
89. J. Pons, A. Rajpal, and J.F. Kirsch Energetic analysis of an antigen/antibody interface: alanine scanning mutagenesis and double mutant cycles on the HyHEL-10/lysozyme interaction Protein Sci. 8 1999 958 968
90. T.N. Bhat, G.A. Bentley, G. Boulot, M.I. Greene, D. Tello, and W. Dall'Acqua Bound water molecules and conformational stabilization help mediate an antigen-antibody association Proc. Natl Acad. Sci. USA 91 1994 1089 1093
91. F.A. Goldbaum, F.P. Schwarz, E. Eisenstein, A. Cauerhff, R.A. Mariuzza, and R.J. Pojak The effect of water activity on the association constant and the enthalpy of reaction between lysozyme and the specific antibodies D1.3 and D44.1 J. Mol. Recogn. 9 1996 6 12
92. H. Kondo, M. Shiroishi, M. Matsushima, K. Tsumoto, and I. Kumagai Crystal structure of anti-hen egg white lysozyme antibody (HyHEL-10) Fv-antigen complex J. Biol. Chem. 274 1999 27623 27631
93. A. Yokota, K. Tsumoto, M. Shiroishi, H. Kondo, and I. Kumagai The role of hydrogen bonding via interfacial water molecules in antigen-antibody complexation J. Biol. Chem. 278 2003 5410 5418
94. M. Adachi, Y. Kurihara, H. Nojima, M. Takeda-Shitaka, K. Kamiya, and H. Umeyama Interaction between the antigen and antibody is controlled by the constant domains: normal mode dynamics of the HEL-HyHEL-10 complex Protein Sci. 12 2003 2125 2131
95. N. Bascos, J. Guidry, and P. Wittung-Stafshede Monomer topology defines folding speed of heptamer Protein Sci. 13 2004 1317 1321
96. R. Piccoli, M. Tamburrini, G. Piccialli, A.D. Donato, A. Parente, and G. D'Alessio The dual-mode quaternary structure of seminal RNase Proc. Natl Acad. Sci. USA 89 1992 1870 1874
97. G. D'Alessio Evolution of oligomeric proteins. The unusual case of a dimeric ribonuclease Eur. J. Biochem. 266 1999 699 708
98. V. Sobolev, R.C. Wade, G. Vriend, and M. Edelman Molecular docking using surface complementarity Proteins: Struct. Funct. Genet. 25 1996 120 129
99. L. Pacios Distinct molecular surfaces and hydrophobicity of amino acid residues in proteins J. Chem. Inf. Comput. Sci. 41 2001 1427 1435
100. M. Vendruscolo, N.V. Dokholyan, E. Paci, and M. Karplus Small-world view of the amino acids that play a key role in protein folding Phys. Rev. E 65 2002 061910 061911
101. N.V. Dokholyan, L. Li, F. Ding, and E.I. Shakhnovich Topological determinants of protein folding Proc. Natl Acad. Sci. USA 99 2002 8637 8641
102. A.R. Atilgan, P. Akan, and C. Baysal Small-world communication of residues and significance for protein dynamics Biophys. J. 86 2004 85 91
103. L.H. Greene, and V.A. Higman Uncovering network systems within protein structures J. Mol. Biol. 334 2003 781 791
104. N. Koga, and S. Takada Roles of native topology and chain-length scaling in protein folding: a simulation study with a Go-like model J. Mol. Biol. 313 2001 171 180
105. L.L. Chavez, J.N. Onuchic, and C. Clementi Quantifying the roughness on the free energy landscape: entropic bottlenecks and protein folding rates J. Am. Chem. Soc. 126 2004 8426 8432
106. C. Clementi, H. Nymeyer, and J.N. Onuchic Topological and energetical factors: what determines the structural details of the transition state ensemble and "En-route" intermediate for protein folding? An investigation of small globular proteins J. Mol. Biol. 298 2000 937 953
107. C. Clementi, P.A. Jennings, and J.N. Onuchic How native-state topology affects the folding of dihydrofolate reductase and interleukin-1 β Proc. Natl Acad. Sci. USA 97 2000 5871 5876
108. A.D. Stoycheva, C.L. Brooks III, and J.N. Onuchic Gatekeepers in the ribosomal protein S6: thermodynamics, kinetics, and folding pathways revealed by a minimalist protein model J. Mol. Biol. 340 2004 571 585
109. M.P. Eastwood, and P.G. Wolynes Role of explicitly cooperative interactions in protein folding funnels: a simulation study J. Chem. Phys. 114 2001 4702 4716
110. H.S. Chan, S. Shimizu, and H. Kaya Cooperativity principles in protein folding Methods Enzymol. 380 2004 350 379
111. M.R. Ejtehadi, S.P. Avall, and S.S. Plotkin Three-body interactions improve the prediction of rate and mechanism in protein folding models Proc. Natl Acad. Sci. USA 101 2004 15088 15093
112. C. Clementi, and S. Plotkin The effects of nonnative interactions on protein folding rates: theory and simulation Protein Sci. 13 2004 1750 1766
113. M.S. Cheung, A.E. Garcia, and J.N. Onuchic Protein folding mediated by solvation: water expulsion and formation of the hydrophobic core occur after the structural collapse Proc. Natl Acad. Sci. USA 99 2002 685 690
114. Y. Levy, and J.N. Onuchic Water and proteins: a love-hate relationship Proc. Natl Acad. Sci. USA 101 2004 3325 3326
115. A.M. Ferrenberg, and R.H. Swendsen Optimized Monte Carlo data analysis Phys. Rev. Letters 63 1989 1195 1198
116. C. Clementi, A.E. Garcia, and J.N. Onuchic Interplay among tertiary contacts, secondary structure formation and side-chain packing in the protein folding mechanism all-atom representation study of protein L J. Mol. Biol. 326 2003 879 890
117. J.-E. Shea, J.N. Onuchic, and C.L. Brooks III Exploring the origins of topological frustration: design of a minimally frustrated model of fragment B of protein A Proc. Natl Acad. Sci. USA 96 1999 12512 12517