The role of protein conformational fluctuations in allostery, function, and evolution

Biophysical Chemistry

Volumn 159, Issue 1, 2011, Pages 129-141

  Wrabl, James O ^a,b   Gu, Jenny ^a,c   Liu, Tong ^a,d   Schrank, Travis P ^a   Whitten, Steven T ^a,e   Hilser, Vincent J ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

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

^c UNIVERSITY OF MÜNSTER   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Texas State University   (United States)

Author keywords

Allostery; COREX BEST algorithm; Protein energetics; Protein ensemble; Protein evolution; Protein functional adaptation; Spontaneous fluctuations

Indexed keywords

ARTICLE; MOLECULAR EVOLUTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

ALLOSTERIC REGULATION; ANIMALS; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEINS;

EID: 80052340812     PISSN: 03014622     EISSN: 18734200     Source Type: Journal    
DOI: 10.1016/j.bpc.2011.05.020     Document Type: Article

References (92)

1. A.L. Lehninger Biochemistry 2nd ed. 1975 Worth New York
2. A.R. Fersht Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding 1999 W.H. Freeman and Company New York
3. T.L. Creighton Proteins: Structures and Molecular Properties 2 ed. 1993 W.H. Freeman and Company New York
4. K. Henzler-Wildman, and D. Kern Dynamic personalities of proteins Nature 450 2007 964 972 (Pubitemid 350273626)
5. N. Tokuriki, and D.S. Tawfik Protein dynamism and evolvability Science (New York, N.Y) 324 2009 203 207
6. P.N. Bryan, and J. Orban Proteins that switch folds Current Opinion in Structural Biology 2010
7. S.J. Benkovic, and S. Hammes-Schiffer A perspective on enzyme catalysis Science (New York, N.Y) 301 2003 1196 1202 (Pubitemid 37052200)
8. Y. Bai, T.R. Sosnick, L. Mayne, and S.W. Englander Protein folding intermediates: native-state hydrogen exchange Science (New York, N.Y) 269 1995 192 197
9. A. Mittermaier, and L.E. Kay Observing biological dynamics at atomic resolution using NMR Trends in Biochemical Sciences 34 2009 601 611
10. D. Kern, and E.R. Zuiderweg The role of dynamics in allosteric regulation Current Opinion in Structural Biology 13 2003 748 757 (Pubitemid 37522151)
11. K.A. Henzler-Wildman, M. Lei, V. Thai, S.J. Kerns, M. Karplus, and D. Kern A hierarchy of timescales in protein dynamics is linked to enzyme catalysis Nature 450 2007 913 916 (Pubitemid 350231333)
12. F. Stengel, A.J. Baldwin, A.J. Painter, N. Jaya, E. Basha, L.E. Kay, E. Vierling, C.V. Robinson, and J.L. Benesch Quaternary dynamics and plasticity underlie small heat shock protein chaperone function Proceedings of the National Academy of Sciences of the United States of America 107 2010 2007 2012
13. V.A. Feher, and J. Cavanagh Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F Nature 400 1999 289 293 (Pubitemid 29334147)
14. K.K. Frederick, M.S. Marlow, K.G. Valentine, and A.J. Wand Conformational entropy in molecular recognition by proteins Nature 448 2007 325 328
15. P.J. Sapienza, and A.L. Lee Using NMR to study fast dynamics in proteins: methods and applications Current Opinion in Pharmacology 10 2010 723 730
16. C.M. Petit, J. Zhang, P.J. Sapienza, E.J. Fuentes, and A.L. Lee Hidden dynamic allostery in a PDZ domain Proceedings of the National Academy of Sciences of the United States of America 106 2009 18249 18254
17. J. Monod, J. Wyman, and J.P. Changeaux On the nature of allosteric transitions: a plausible model Journal of Molecular Biology 12 1965 88 118
18. D.E. Koshland, G. Nemethy, and D. Filmer Comparison of experimental binding data and theoretical models in proteins containing subunits Biochemistry 5 1966 365 385
19. J.A. Boyer, C.J. Clay, K.S. Luce, M.H. Edgell, and A.L. Lee Detection of native state nonadditivity in double mutant cycles via hydrogen exchange Journal of the American Chemical Society 132 2010 8010 8019
20. J.C. Lee, M. Natarajan, V. Nashine, M. Socolich, T. Vu, W.P. Russ, S.J. Benkovic, and R. Ranganathan Surface sites for engineering allosteric control in proteins Science (New York, N.Y) 322 2008 438 442
21. C.J. Tsai, A. del Sol, and R. Nussinov Protein allostery, signal transmission and dynamics: a classification scheme of allosteric mechanisms Molecular BioSystems 5 2009 207 216
22. R. Elber Simulations of allosteric transitions Current Opinion in Structural Biology 21 2011 167 172
23. S.R. Tzeng, and C.G. Kalodimos Protein dynamics and allostery: an NMR view Current Opinion in Structural Biology 21 2011 62 67
24. P. Csermely, R. Palotai, and R. Nussinov Induced fit, conformational selection and independent dynamic segments: an extended view of binding events Trends in Biochemical Sciences 35 2010 539 546
25. K. Gunasekaran, B. Ma, and R. Nussinov Is allostery an intrinsic property of all dynamic proteins? Proteins: Struct Funct Bioinf 57 2004 433 443 (Pubitemid 39390799)
26. V.J. Hilser, and E. Freire Structure-based calculation of the equilibrium folding pathway of proteins. Correlation with hydrogen exchange protection factors Journal of Molecular Biology 262 1996 756 772 (Pubitemid 26343520)
27. V.J. Hilser, J. Gomez, and E. Freire The enthalpy change in protein folding and binding: refinement of parameters for structure-based calculations Proteins 26 1996 123 133 (Pubitemid 26365306)
28. J. Gomez, V.J. Hilser, D. Xie, and E. Freire The heat capacity of proteins Proteins 22 1995 404 412
29. V.J. Hilser Modeling the native state ensemble Methods in Molecular Biology (Clifton, N.J) 168 2001 93 116
30. T.P. Schrank, D.W. Bolen, and V.J. Hilser Rational modulation of conformational fluctuations in adenylate kinase reveals a local unfolding mechanism for allostery and functional adaptation in proteins Proceedings of the National Academy of Sciences of the United States of America 106 2009 16984 16989
31. S.T. Whitten, B.E. Garcia-Moreno, and V.J. Hilser Ligand effects on the protein ensemble: unifying the descriptions of ligand binding, local conformational fluctuations, and protein stability Methods in Cell Biology 84 2008 871 891
32. K. Sayar, O. Ugur, T. Liu, V.J. Hilser, and O. Onaran Exploring allosteric coupling in the alpha-subunit of heterotrimeric G proteins using evolutionary and ensemble-based approaches BMC Structural Biology 8 2008 23
33. V.J. Hilser, and E.B. Thompson Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins Proceedings of the National Academy of Sciences of the United States of America 104 2007 8311 8315 (Pubitemid 47175484)
34. S.T. Whitten, A.J. Kurtz, M.S. Pometun, A.J. Wand, and V.J. Hilser Revealing the nature of the native state ensemble through cold denaturation Biochemistry 45 2006 10163 10174 (Pubitemid 44384791)
35. T. Liu, S.T. Whitten, and V.J. Hilser Ensemble-based signatures of energy propagation in proteins: a new view of an old phenomenon Proteins 62 2006 728 738 (Pubitemid 43191259)
36. V.J. Hilser, E.B. Garcia-Moreno, T.G. Oas, G. Kapp, and S.T. Whitten A statistical thermodynamic model of the protein ensemble Chemical Reviews 106 2006 1545 1558 (Pubitemid 43792771)
37. H. Pan, J.C. Lee, and V.J. Hilser Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble Proceedings of the National Academy of Sciences of the United States of America 97 2000 12020 12025
38. V.J. Hilser, D. Dowdy, T.G. Oas, and E. Freire The structural distribution of cooperative interactions in proteins: analysis of the native state ensemble Proceedings of the National Academy of Sciences of the United States of America 95 1998 9903 9908 (Pubitemid 28415267)
39. J.O. Wrabl, and V.J. Hilser Investigating homology between proteins using energetic profiles PLoS Computational Biology 6 2010 e1000722
40. J. Vertrees, J.O. Wrabl, and V.J. Hilser Energetic profiling of protein folds Methods in Enzymology 455 2009 299 327
41. J. Gu, and V.J. Hilser Predicting the energetics of conformational fluctuations in proteins from sequence: a strategy for profiling the proteome Structure 16 2008 1627 1637
42. J. Gu, and V.J. Hilser Sequence-based analysis of protein energy landscapes reveals nonuniform thermal adaptation within the proteome Molecular Biology and Evolution 26 2009 2217 2227
43. J. Vertrees, P. Barritt, S. Whitten, and V.J. Hilser COREX/BEST server: a web browser-based program that calculates regional stability variations within protein structures Bioinformatics (Oxford, England) 21 2005 3318 3319 (Pubitemid 41418450)
44. A.J. Doig Recent advances in helix-coil theory Biophysical Chemistry 101-102 2002 281 293 (Pubitemid 35462053)
45. K.P. Murphy, and E. Freire Thermodynamics of structural stability and cooperative folding behavior in proteins Advances in Protein Chemistry 43 1992 313 361
46. K.P. Murphy, and S.J. Gill Solid model compounds and the thermodynamics of protein unfolding Journal of Molecular Biology 222 1991 699 709
47. K.P. Murphy, P.L. Privalov, and S.J. Gill Common features of protein unfolding and dissolution of hydrophobic compounds Science (New York, N.Y) 247 1990 559 561
48. J.A. D'Aquino, J. Gomez, V.J. Hilser, K.H. Lee, L.M. Amzel, and E. Freire The magnitude of the backbone conformational entropy change in protein folding Proteins 25 1996 143 156 (Pubitemid 26231105)
49. D.A. McQuarrie, and J.D. Simon Molecular Thermodynamics 1999 University Science Books Sausalito, CA
50. J.O. Wrabl, S.A. Larson, and V.J. Hilser Thermodynamic environments in proteins: fundamental determinants of fold specificity Protein Science 11 2002 1945 1957 (Pubitemid 34791414)
51. J.O. Wrabl, S.A. Larson, and V.J. Hilser Thermodynamic propensities of amino acids in the native state ensemble: implications for fold recognition Protein Science 10 2001 1032 1045 (Pubitemid 32367495)
52. J.O. Wooll, J.O. Wrabl, and V.J. Hilser Ensemble modulation as an origin of denaturant-independent hydrogen exchange in proteins Journal of Molecular Biology 301 2000 247 256
53. C.R. Babu, V.J. Hilser, and A.J. Wand Direct access to the cooperative substructure of proteins and the protein ensemble via cold denaturation Nature Structural & Molecular Biology 11 2004 352 357 (Pubitemid 38436800)
54. S.T. Whitten, E.B. Garcia-Moreno, and V.J. Hilser Local conformational fluctuations can modulate the coupling between proton binding and global structural transitions in proteins Proceedings of the National Academy of Sciences of the United States of America 102 2005 4282 4287 (Pubitemid 40397103)
55. A. Manson, S.T. Whitten, J.C. Ferreon, R.O. Fox, and V.J. Hilser Characterizing the role of ensemble modulation in mutation-induced changes in binding affinity Journal of the American Chemical Society 131 2009 6785 6793
56. S.A. Larson, and V.J. Hilser Analysis of the "thermodynamic information content" of a Homo sapiens structural database reveals hierarchical thermodynamic organization Protein Science 13 2004 1787 1801 (Pubitemid 38822118)
57. A. Cooper, and D.T.F. Dryden Allostery without conformational change European Biophysics Journal 11 1984 105 109
58. Q. Cui, and M. Karplus Allostery and cooperativity revisited Protein Science 17 2008 1295 1307
59. T. Liu, S.T. Whitten, and V.J. Hilser Functional residues serve a dominant role in mediating the cooperativity of the protein ensemble Proceedings of the National Academy of Sciences of the United States of America 104 2007 4347 4352 (Pubitemid 47186229)
60. M.J. Osborne, J. Schnell, S.J. Benkovic, H.J. Dyson, and P.E. Wright Backbone dynamics in dihydrofolate reductase complexes: role of loop flexibility in the catalytic mechanism Biochemistry 40 2001 9846 9859 (Pubitemid 32769533)
61. C.A. Fierke, K.A. Johnson, and S.J. Benkovic Construction and evaluation of the kinetic scheme associated with dihydrofolate reductase from Escherichia coli Biochemistry 26 1987 4085 4092
62. J.M. Berg, J.L. Tymoczko, and L. Stryer Biochemistry 6th ed. 2007 W.H. Freeman and Company New York
63. J. Liu, N.B. Perumal, C.J. Oldfield, E.W. Su, V.N. Uversky, and A.K. Dunker Intrinsic disorder in transcription factors Biochemistry 45 2006 6873 6888 (Pubitemid 43856673)
64. Y. Minezaki, K. Homma, A.R. Kinjo, and K. Nishikawa Human transcription factors contain a high fraction of intrinsically disordered regions essential for transcriptional regulation Journal of Molecular Biology 359 2006 1137 1149 (Pubitemid 43831930)
65. A.S. Garza, N. Ahmad, and R. Kumar Role of intrinsically disordered protein regions/domains in transcriptional regulation Life Sciences 84 2009 189 193
66. I. Luque, S.A. Leavitt, and E. Freire The linkage between protein folding and functional cooperativity: two sides of the same coin? Annual Review of Biophysics and Biomolecular Structure 31 2002 235 256 (Pubitemid 34666832)
67. P.A. Fields, and G.N. Somero Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenoid fishes Proceedings of the National Academy of Sciences of the United States of America 95 1998 11476 11481 (Pubitemid 28450154)
68. T.P. Schrank, W.A. Elam, J. Li, and V.J. Hilser Strategies for the thermodynamic characterization of linked binding/local folding reactions within the native state: application to the LID domain of adenylate kinase from Escherichia coli Methods in Enzymology 492 2011 253 282
69. B. Grainger, M.I. Sadowski, and W.R. Taylor Re-evaluating the "rules" of protein topology Journal of Computational Biology 17 2010 1371 1384
70. H. Li, C. Tang, and N.S. Wingreen Are protein folds atypical? Proceedings of the National Academy of Sciences of the United States of America 95 1998 4987 4990 (Pubitemid 28208537)
71. P. Cossio, A. Trovato, F. Pietrucci, F. Seno, A. Maritan, and A. Laio Exploring the universe of protein structures beyond the protein data bank PLoS Computational Biology 6 2010 e1000957
72. N. Nagano, C.A. Orengo, and J.M. Thornton One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions Journal of Molecular Biology 321 2002 741 765
73. A.N. Lupas, C.P. Ponting, and R.B. Russell On the evolution of protein folds: are similar motifs in different protein folds the result of convergence, insertion, or relics of an ancient peptide world? Journal of Structural Biology 134 2001 191 203
74. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures Journal of Molecular Biology 247 1995 536 540
75. Y. Qi, and N.V. Grishin Structural classification of thioredoxin-like fold proteins Proteins: Structure, Function, and Bioinformatics 58 2005 376 388 (Pubitemid 40076051)
76. R.B. Russell, P.D. Sasieni, and M.J.E. Sternberg Supersites within superfolds: binding site similarity in the absence of homology Journal of Molecular Biology 282 1998 903 918 (Pubitemid 28442355)
77. A.B. Law, E.J. Fuentes, and A.L. Lee Conservation of side-chain dynamics within a protein family Journal of the American Chemical Society 131 2009 6322 6333
78. S.M. Hollup, E. Fuglebakk, W.R. Taylor, and N. Reuter Exploring the factors determining the dynamics of different protein folds Protein Science 20 2011 197 209
79. J. Vertrees, J.O. Wrabl, and V.J. Hilser An energetic representation of protein architecture that is independent of primary and secondary structure Biophysical Journal 97 2009 1461 1470
80. J.A. Spudich, and S. Sivaramakrishnan Myosin VI: an innovative motor that challenged the swinging lever arm hypothesis Nature Reviews Molecular Cell Biology 11 2010 128 137
81. A.L. Horwich, G.W. Farr, and W.A. Fenton GroEL-GroES-mediated protein folding Chemical Reviews 106 2006 1917 1930 (Pubitemid 43792786)
82. T.A. Steitz The structural changes of T7 RNA polymerase from transcription initiation to elongation Current Opinion in Structural Biology 19 2009 683 690
83. M.J. Whitley, and A.L. Lee Frameworks for understanding long-range intra-protein communication Current Protein Peptide Science 10 2009 116 127
84. G.K. Ackers Deciphering the molecular code of hemoglobin allostery Advances in Protein Chemistry 51 1998 185 253 (Pubitemid 28252474)
85. E. DiCera Thrombin Molecular Aspects of Medicine 29 2008 203 254
86. J.A. Hardy, and J.A. Wells Searching for new allosteric sites in enzymes Current Opinion in Structural Biology 14 2004 706 715 (Pubitemid 39592582)
87. P. Hauske, C. Ottmann, M. Meltzer, M. Ehrmann, and M. Kaiser Allosteric regulation of proteases ChemBioChem 9 2008 2920 2928
88. U. Haupts, J. Tittor, and D. Oesterhelt Closing in on bacteriorhodopsin: progress in understanding the molecule Annual Review of Biophysics and Biomolecular Structure 28 1999 367 399 (Pubitemid 29319263)
89. F. Gai, K.C. Hasson, J.C. McDonald, and P.A. Anfinrud Chemical dynamics in proteins: the photoisomerization of retinal in bacteriorhodopsin Science (New York, NY) 279 1998 1886 1891 (Pubitemid 28168636)
90. M. Tyska, and D.M. Warshaw The myosin power stroke Cell Motility and the Cytoskeleton 51 2002 1 15 (Pubitemid 34101413)
91. L. Holm, and J. Park DaliLite workbench for protein structure comparison Bioinformatics (Oxford, England) 16 2000 566 567
92. A. Andreeva, D. Howorth, J.M. Chandonia, S.E. Brenner, T.J. Hubbard, C. Chothia, and A.G. Murzin Data growth and its impact on the SCOP database: new developments Nucleic Acids Research 36 2008 D419 D425