Pre-existing soft modes of motion uniquely defined by native contact topology facilitate ligand binding to proteins

Protein Science

Volumn 20, Issue 10, 2011, Pages 1645-1658

  Meireles, Lidio ^a   Gur, Mert ^a   Bakan, Ahmet ^a   Bahar, Ivet ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Coarse grained normal mode analysis; Collective motions; Elastic network models; Flexible docking; Intrinsic dynamics; Mechanism of ligand binding

Indexed keywords

COARSE GRAINED NORMAL MODE ANALYSIS; CONFORMATION; ELASTICITY; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; REVIEW; SIMULATION; THREE DIMENSIONAL IMAGING;

ANIMALS; HUMANS; LIGANDS; MODELS, BIOLOGICAL; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEINS;

EID: 80053142382     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.711     Document Type: Review

References (68)

1. Erickson JA, Jalaie M, Robertson DH, Lewis RA, Vieth M (2004) Lessons in molecular recognition: the effects of ligand and protein flexibility on molecular docking accuracy. J Med Chem 47:45-55. (Pubitemid 38040489)
2. Fischer E (1894) Einfluss der configuration auf die wirkung der enzyme. Ber Dtsch Chem Ges 27:2985-2993.
3. Koshland DE (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 44:98-104.
4. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12:88-118.
5. Boehr DD, Nussinov R, Wright PE (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5:789-796.
6. Bakan A, Bahar I (2009) The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding. Proc Natl Acad Sci USA 106:14349-14354.
7. Bahar I, Lezon TR, Yang LW, Eyal E (2010) Global dynamics of proteins: bridging between structure and function. Annu Rev Biophys 39:23-42.
8. Bahar I, Atilgan AR, Erman B (1997) Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Fold Des 2:173-181. (Pubitemid 127740467)
9. Haliloglu T, Bahar I, Erman B (1997) Gaussian dynamics of folded proteins. Phys Rev Lett 79:3090-3093. (Pubitemid 127645089)
10. Doruker P, Atilgan AR, Bahar I (2000) Dynamics of proteins predicted by molecular dynamics simulations and analytical approaches: application to alpha-amylase inhibitor. Proteins 40:512-524. (Pubitemid 30624460)
11. Atilgan AR, Durell SR, Jernigan RL, Demirel MC, Keskin O, Bahar I (2001) Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys J 80:505-515.
12. Tama F, Sanejouand YH (2001) Conformational change of proteins arising from normal mode calculations. Protein Eng 14:1-6. (Pubitemid 32318932)
13. Flory PJ (1976) Statistical thermodynamics of random networks. Proc R Soc London A 351:351-380.
14. Hinsen K (1998) Analysis of domain motions by approximate normal mode calculations. Proteins 33:417-429.
15. Hinsen K, Normal mode theory and harmonic potential approximations. In: Cui Q, Bahar I, Eds. (2006) Normal mode analysis: theory and applications to biological and chemical systems. Boca Raton, FL: Chapman & Hall/CRC, pp 1-16.
16. Yang L, Song G, Jernigan RL (2009) Protein elastic network models and the ranges of cooperativity. Proc Natl Acad Sci USA 106:12347-12352.
17. Riccardi D, Cui Q, Phillips GN (2009) Application of elastic network models to proteins in the crystalline state. Biophys J 96:464-475.
18. Hinsen K, Petrescu AJ, Dellerue S, Bellissent-Funel MC, Kneller GR (2000) Harmonicity in slow protein dynamics. Chem Phys 261:25-37.
19. Kovacs JA, Chacon P, Abagyan R (2004) Predictions of protein flexibility: first-order measures. Proteins 56:661-668. (Pubitemid 39063309)
20. Lezon TR, Bahar I (2010) Using entropy maximization to understand the determinants of structural dynamics beyond native contact topology. PLoS Comput Biol 6:e1000816.
21. Tirion MM (1996) Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 77:1905-1908.
22. Ma JP (2005) Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. Structure 13:373-380.
23. Bahar I, Chennubhotla C, Tobi D (2007) Intrinsic dynamics of enzymes in the unbound state and, relation to allosteric regulation. Curr Opin Struct Biol 17:633-640. (Pubitemid 350180409)
24. Tama F, Brooks CL (2006) Symmetry, form, and shape: guiding principles for robustness in macromolecular machines. Annu Rev Biophys Biomol Struct 35:115-133. (Pubitemid 43877372)
25. Yang LW, Chng CP (2008) Coarse-grained models reveal functional dynamics. I. Elastic network models - theories, comparisons and perspectives. Bioinform Biol Insights 2:25-45.
26. Eyal E, Yang LW, Bahar I (2006) Anisotropic network model: systematic evaluation and a new web interface. Bioinformatics 22:2619-2627. (Pubitemid 44642600)
27. Xu CY, Tobi D, Bahar I (2003) Allosteric changes in protein structure computed by a simple mechanical model: hemoglobin T 〈-〉 R2 transition. J Mol Biol 333:153-168. (Pubitemid 37153272)
28. Brüschweiler R (1995) Collective protein dynamics and nuclear-spin relaxation. J Chem Phys 102:3396-3403.
29. Yang L, Song G, Carriquiry A, Jernigan RL (2008) Close correspondence between the motions from principal component analysis of multiple HIV-1 protease structures and elastic network modes. Structure 16:321-330. (Pubitemid 351215213)
30. Tobi D, Bahar I (2005) Structural changes involved in protein binding correlate with intrinsic motions of proteins in the unbound state. Proc Natl Acad Sci USA 102:18908-18913. (Pubitemid 43049540)
31. Keskin O (2007) Binding induced conformational changes of proteins correlate with their intrinsic fluctuations: a case study of antibodies. BMC Struct Biol 7:31.
32. Lange OF, Lakomek NA, Fares C, Schroder GF, Walter KFA, Becker S, Meiler J, Grubmuller H, Griesinger C, De Groot BL (2008) Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320:1471-1475. (Pubitemid 351929422)
33. Gsponer J, Christodoulou J, Cavalli A, Bui JM, Richter B, Dobson CM, Vendruscolo M (2008) A coupled equilibrium shift mechanism in calmodulin-mediated signal transduction. Structure 16:736-746. (Pubitemid 351615020)
34. Bakan A, Meireles LM, Bahar I (2011) ProDy: protein dynamics inferred from theory and experiments. Bioinformatics 27:1575-1577.
35. Bakan A, Bahar I (2011) Computational generation inhibitor-bound conformers of p38 map kinase and comparison with experiments. Pac Symp Biocomput 16:181-192.
36. Cavasotto CN, Kovacs JA, Abagyan RA (2005) Representing receptor flexibility in ligand docking through relevant normal modes. J Am Chem Soc 127:9632-9640. (Pubitemid 40934775)
37. Totrov M, Abagyan R (2008) Flexible ligand docking to multiple receptor conformations: a practical alternative. Curr Opin Struct Biol 18:178-184.
38. Suhre K, Sanejouand YH (2004) ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res 32:W610-W614. (Pubitemid 38997408)
39. Camps J, Carrillo O, Emperador A, Orellana L, Hospital A, Rueda M, Cicin-Sain D, D'Abramo M, Gelpi JL, Orozco M (2009) FlexServ: an integrated tool for the analysis of protein flexibility. Bioinformatics 25:1709-1710.
40. Mashiach E, Nussinov R, Wolfson HJ (2010) FiberDock: a web server for flexible induced-fit backbone refinement in molecular docking. Nucleic Acids Res 38:W457-W461.
41. Mashiach E, Nussinov R, Wolfson HJ (2010) FiberDock: flexible induced-fit backbone refinement in molecular docking. Proteins 78:1503-1519.
42. Rueda M, Bottegoni G, Abagyan R (2009) Consistent improvement of cross-docking results using binding site ensembles generated with elastic network normal modes. J Chem Inf Model 49:716-725.
43. Floquet N, Marechal JD, Badet-Denisot MA, Robert CH, Dauchez M, Perahia D (2006) Normal mode analysis as a prerequisite for drug design: application to matrix metalloproteinases inhibitors. FEBS Lett 580:5130-5136. (Pubitemid 44415782)
44. Sperandio O, Mouawad L, Pinto E, Villoutreix BO, Perahia D, Miteva MA (2010) How to choose relevant multiple receptor conformations for virtual screening: a test case of Cdk2 and normal mode analysis. Eur Biophys J 39:1365-1372.
45. Zacharias M, Sklenar H (1999) Harmonic modes as variables to approximately account for receptor flexibility in ligand-receptor docking simulations: application to DNA minor groove ligand complex. J Comput Chem 20:287-300. (Pubitemid 129652404)
46. Zacharias M (2004) Rapid protein-ligand docking using soft modes from molecular dynamics simulations to account for protein deformability: binding of FK506 to FKBP. Proteins 54:759-767.
47. May A, Zacharias M (2007) Protein-protein docking in CAPRI using ATTRACT to account for global and local flexibility. Proteins 69:774-780. (Pubitemid 350210137)
48. May A, Zacharias M (2008) Energy minimization in low-frequency normal modes to efficiently allow for global flexibility during systematic protein-protein docking. Proteins 70:794-809. (Pubitemid 351161939)
49. May A, Zacharias M (2008) Protein-ligand docking accounting for receptor side chain and global flexibility in normal modes: evaluation on kinase inhibitor cross docking. J Med Chem 51:3499-3506. (Pubitemid 351875006)
50. Lindahl E, Delarue M (2005) Refinement of docked protein-ligand and protein-DNA structures using low frequency normal mode amplitude optimization. Nucleic Acids Res 33:4496-4506. (Pubitemid 41222564)
51. Horiuchi T, Go N (1991) Projection of Monte-Carlo and molecular-dynamics trajectories onto the normal mode axes - human lysozyme. Proteins 10:106-116.
52. Elber R, Karplus M (1987) Multiple conformational states of proteins - a molecular dynamics analysis of myoglobin. Science 235:318-321. (Pubitemid 17232557)
53. Go N, Noguti T (1989) Structural basis of hierarchical multiple substates of a protein. Chem Scr A 29:151-164.
54. Noguti T, Go N (1989) Structural basis of hierarchical multiple substates of a protein. I. Introduction. Proteins 5:97-103.
55. Noguti T, Go N (1989) Structural basis of hierarchical multiple substates of a protein. II. Monte-Carlo simulation of native thermal fluctuations and energy minimization. Proteins 5:104-112.
56. Noguti T, Go N (1989) Structural basis of hierarchical multiple substates of a protein. IV. Rearrangements in atom packing and local deformations. Proteins 5:125-131.
57. Noguti T, Go N (1989) Structural basis of hierarchical multiple substates of a protein. V. Nonlocal deformations. Proteins 5:132-138.
58. Noguti T, Go N (1989) Structural basis of hierarchical multiple substates of a protein. III. Side-chain and main chain local conformations. Proteins 5:113-124.
59. Yang Z, Majek P, Bahar I (2009) Allosteric transitions of supramolecular systems explored by network models: application to chaperonin GroEL. PLoS Comput Biol 5: e1000360.
60. Isin B, Schulten K, Tajkhorshid E, Bahar I (2008) Mechanism of signal propagation upon retinal isomerization: insights from molecular dynamics simulations of rhodopsin restrained by normal modes. Biophys J 95:789-803.
61. Zhang ZY, Shi YY, Liu HY (2003) Molecular dynamics simulations of peptides and proteins with amplified collective motions. Biophys J 84:3583-3593.
62. Kantarci-Carsibasi N, Haliloglu T, Doruker P (2008) Conformational transition pathways explored by Monte Carlo simulation integrated with collective modes. Biophys J 95:5862-5873.
63. Isin B, Tirupula K, Oltvai ZN, Klein-Seetharaman J, Bahar I. 2011 Identification of motions in membrane proteins by elastic network models and their experimental validation.
64. Maragakis P, Karplus M (2005) Large amplitude conformational change in proteins explored with a plastic network model: adenylate kinase. J Mol Biol 352: 807-822. (Pubitemid 41267070)
65. Miyashita O, Onuchic JN, Wolynes PG (2003) Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proc Natl Acad Sci USA 100:12570-12575. (Pubitemid 37339939)
66. Okazaki K, Koga N, Takada S, Onuchic JN, Wolynes PG (2006) Multiple-basin energy landscapes for largeamplitude conformational motions of proteins: structure-based molecular dynamics simulations. Proc Natl Acad Sci USA 103:11844-11849. (Pubitemid 44215774)
67. Temiz NA, Meirovitch E, Bahar I (2004) Escherichia coli adenylate kinase dynamics: comparison of elastic network model modes with mode-coupling N-15-NMR relaxation data. Proteins 57:468-480. (Pubitemid 39390802)
68. Tokuriki N, Tawfik DS (2009) Protein dynamism and evolvability. Science 324:203-207.