Synergistic use of NMR and MD simulations to study the structural heterogeneity of proteins

Wiley Interdisciplinary Reviews: Computational Molecular Science

Volumn 2, Issue 3, 2012, Pages 466-478

  Esteban Martín, Santiago ^a   Bryn Fenwick, Robert ^a   Salvatella, Xavier ^a,b  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84859909909     PISSN: 17590876     EISSN: 17590884     Source Type: Journal    
DOI: 10.1002/wcms.1093     Document Type: Article

References (67)

1. Boehr DD, Dyson HJ, Wright PE. An NMR perspective on enzyme dynamics. Chem Rev 2006, 106:3055-3079.
2. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, Skalicky JJ, Kay LE, Kern D. Intrinsic dynamics of an enzyme underlies catalysis. Nature 2005, 438:117-121.
3. Wolf-Watz M, Thai V, Henzler-Wildman KA, Hadjipavlou G, Eisenmesser EZ, Kern D. Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat Struct Mol Biol 2004, 11:945-949.
4. Mittermaier A, Kay LE. New tools provide new insights in NMR studies of protein dynamics. Science 2006, 312:224-228.
5. Karplus M, McCammon JA. Molecular dynamics simulations of biomolecules. Nat Struct Biol 2002, 9:646-652.
6. van Gunsteren WF, Bakowies D, Baron R, Chandrasekhar I, Christen M, Daura X, Gee P, Geerke DP, Glättli A, Hünenberger PH, et al. Biomolecular modeling: goals, problems, perspectives. Angew Chem Int Ed Engl 2006, 45:4064-4092.
7. Scheraga HA, Khalili M, Liwo A. Protein-folding dynamics: overview of molecular simulation techniques. Annu Rev Phys Chem 2007, 58:57-83.
8. Klepeis JL, Lindorff-Larsen K, Dror RO, Shaw DE. Long-timescale molecular dynamics simulations of protein structure and function. Curr Opin Struct Biol 2009, 19:120-127.
9. Shaw DE, Maragakis P, Lindorff-Larsen K, Piana S, Dror RO, Eastwood MP, Bank JA, Jumper JM, Salmon JK, Shan Y, et al. Atomic-level characterization of the structural dynamics of proteins. Science 2010, 330:341-346.
10. Palmer AG 3rd, Kroenke CD, Loria JP. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 2001, 339:204-238.
11. Mulder FA, Mittermaier A, Hon B, Dahlquist FW, Kay LE. Studying excited states of proteins by NMR spectroscopy. Nat Struct Biol 2001, 8:932-935.
12. Kruschel D, Zagrovic B. Conformational averaging in structural biology: issues, challenges and computational solutions. Mol Biosyst 2009, 5:1606-1616.
13. Clore GM, Schwieters CD. How much backbone motion in ubiquitin is required to account for dipolar coupling data measured in multiple alignment media as assessed by independent cross-validation? J Am Chem Soc 2004, 126:2923-2938.
14. Lange OF, Lakomek NA, Farès C, Schröder GF, Walter KFA, Becker S, Meiler J, Grubmüller H, Griesinger C, de Groot BL. Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 2008, 320:1471-1475.
15. Fenwick RB, Esteban-Martín S, Richter B, Lee D, Walter KFA, Milovanovic D, Becker S, Lakomek NA, Griesinger C, Salvatella X. Weak long-range correlated motions in a surface patch of ubiquitin involved in molecular recognition. J Am Chem Soc 2011, 133:10336-10339.
16. Kohlhoff KJ, Robustelli P, Cavalli A, Salvatella X, Vendruscolo M. Fast and accurate predictions of protein NMR chemical shifts from interatomic distances. J Am Chem Soc 2009, 131:13894-1395.
17. Robustelli P, Kohlhoff K, Cavalli A, Vendruscolo M. Using NMR chemical shifts as structural restraints in molecular dynamics simulations of proteins. Structure 2010, 18:923-933.
18. Showalter SA, Brüschweiler R. Quantitative molecular ensemble interpretation of NMR dipolar couplings without restraints. J Am Chem Soc 2007, 129:4158-4159.
19. Lipari G, Szabo A. Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 1982, 104:4546-4559.
20. Lipari G, Szabo A. Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 2. Analysis of experimental results. J Am Chem Soc 1982, 104:4559-4570.
21. Lipari L, Szabo A, Levy RM. Protein dynamics and NMR relaxation: comparison of simulations with experiment. Nature 300, 197-198.
22. Markwick PR, Cervantes CF, Abel BL, Komives EA, Blackledge M, McCammon JA. Enhanced conformational space sampling improves the prediction of chemical shifts in proteins. J Am Chem Soc 2010, 132:1220-1221.
23. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dror RO, Shaw DE. Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 2010, 78:1950-1958.
24. Wickstrom L, Okur A, Simmerling C. Evaluating the performance of the ff99SB force field based on NMR scalar coupling data. Biophys J 2009, 97:853-856.
25. Showalter SA, Johnson E, Rance M, Brüschweiler R. Toward quantitative interpretation of methyl side-chain dynamics from NMR by molecular dynamics simulations. J Am Chem Soc 2007, 129:14146-1417.
26. Allison JR, van Gunsteren WF. A method to explore protein side chain conformational variability using experimental data. Chemphyschem 2009, 10:3213-3228.
27. Markwick PR, Bouvignies G, Blackledge M. Exploring multiple timescale motions in protein GB3 using accelerated molecular dynamics and NMR spectroscopy. J Am Chem Soc 2007, 129:4724-4730.
28. Salvatella X, Richter B, Vendruscolo M. Influence of the fluctuations of the alignment tensor on the analysis of the structure and dynamics of proteins using residual dipolar couplings. J Biomol NMR 2008, 40:71-81.
29. Louhivuori M, Otten R, Salminen T, Annila A. Evidence of molecular alignment fluctuations in aqueous dilute liquid crystalline media. J Biomol NMR 2007, 39:141-152.
30. Louhivuori M, Otten R, Lindorff-Larsen K, Annila A. Conformational fluctuations affect protein alignment in dilute liquid crystal media. J Am Chem Soc 2006, 128:4371-4376.
31. Brooks BR, Brooks CL, Mackerell AD, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, et al. CHARMM: the biomolecular simulation program. J Comput Chem 2009, 30:1545-1614.
32. Chang SL, Tjandra N. Temperature dependence of protein backbone motion from carbonyl 13C and amide 15N NMR relaxation. J Magn Reson 2005, 174:43-53.
33. Maragakis P, Lindorff-Larsen K, Eastwood MP, Dror RO, Klepeis J, Arkin I, Jensen M, Xu H, Trbovic N, Friesner RA, et al. Microsecond molecular dynamics simulation shows effect of slow loop dynamics on backbone amide order parameters of proteins. J Phys Chem B 2008, 112:6155-6158.
34. Li T, Jing Q, Yao L. Dynamics of the GB3 loop regions from MD simulation: how much of it is real? J Phys Chem B 2011, 115:3488-3495.
35. Best RB, Buchete NV, Hummer G. Are current molecular dynamics force fields too helical? Biophys J. 2008, 95:L07-9.
36. Lange OF, van der Spoel D, de Groot BL. Scrutinizing molecular mechanics force fields on the submicrosecond timescale with NMR data. Biophys J. 2010, 99:647-55.
37. Kent A, Jha AK, Fitzgerald JE, Freed KF. Benchmarking implicit solvent folding simulations of the amyloid beta(10-35) fragment. J Phys Chem B 2008, 112:6175-6186.
38. Sgourakis NG, Merced-Serrano M, Boutsidis C, Drineas P, Du Z, Wang C, Garcia AE. Atomic-level characterization of the ensemble of the Aβ(1-42) monomer in water using unbiased molecular dynamics simulations and spectral algorithms. J Mol Biol 2011, 405:570-583.
39. Case DA, Cheatham TE 3rd, Darden T, Gohlke H, Luo R, et al. The Amber biomolecular simulation programs. J Comput Chem 2005, 26:1668-1688.
40. MacKerell AD Jr, Banavali N, Foloppe N. Development and current status of the CHARMM force field for nucleic acids. Biopolymers 2000-2001, 56:257-265.
41. Jorgensen WL, Maxwell DS, Tirado-Rives J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 1996, 118:11225-11236.
42. Oostenbrink C, Villa A, Mark AE, van Gunsteren WF. A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J Comput Chem 2004, 25:1656-1676.
43. Best RB, Hummer G. Optimized molecular dynamics force fields applied to the helix-coil transition of polypeptides. J Phys Chem B 2009, 113:9004-9015.
44. Li DW, Brüschweiler R. NMR-based protein potentials. Angew Chem Int Ed Engl 2010, 49:6778-6780.
45. Norgaard AB, Ferkinghoff-Borg J, Lindorff-Larsen K. Experimental parameterization of an energy function for the simulation of unfolded proteins. Biophys J 2008, 94:182-192.
46. Bremi T, Bruschweiler R. Locally anisotropic internal polypeptide backbone dynamics by NMR relaxation. J Am Chem Soc 1997, 119:6672-6673.
47. Meiler J, Prompers JJ, Peti W, Griesinger C, Brüschweiler R. Model-free approach to the dynamic interpretation of residual dipolar couplings in globular proteins. J Am Chem Soc 2001, 123:6098-6107.
48. Bouvignies G, Markwick PR, Blackledge M. Characterization of protein dynamics from residual dipolar couplings using the three-dimensional Gaussian axial fluctuation model. Proteins 2008, 71:353-363.
49. Almond A, Axelsen JB. Physical interpretation of residual dipolar couplings in neutral aligned media. J Am Chem Soc 2002, 124:9986-9987.
50. Esteban-Martín S, Salgado J. The dynamic orientation of membrane-bound peptides: bridging simulations and experiments. Biophys J 2007, 93:4278-42788.
51. Ozdirekcan S, Etchebest C, Killian JA, Fuchs PF. On the orientation of a designed transmembrane peptide: toward the right tilt angle? J Am Chem Soc 2007, 129:15174-15181.
52. Esteban-Martín S, Strandberg E, Fuertes G, Ulrich AS, Salgado J. Influence of whole-body dynamics on 15N PISEMA NMR spectra of membrane proteins: a theoretical analysis. Biophys J 2009, 96:3233-3241.
53. Strandberg E, Esteban-Martín S, Salgado J, Ulrich AS. Orientation and dynamics of peptides in membranes calculated from 2H-NMR data. Biophys J 2009, 96:3223-3232.
54. Mukrasch MD, Markwick PRL, Biernat J, Bergen Mv, Bernadó P, Griesinger C, Mandelkow E, Zweckstetter M, Blackledge M. Highly populated turn conformations in natively unfolded tau protein identified from residual dipolar couplings and molecular simulation. J Am Chem Soc 2007, 129:5235-5243.
55. Muñoz V, Serrano L. Intrinsic secondary structure propensities of the amino acids, using statistical Phi-Psi matrices: comparison with experimental scales. Proteins 1994, 20:301-311.
56. Smith LJ, Bolin KA, Schwalbe H, MacArthur MW, Thornton JM, Dobson CM. Analysis of main chain torsion angles in proteins: prediction of NMR coupling constants for native and random coil conformations. J Mol Biol 1996, 255:494-506.
57. Zagrovic B, van Gunsteren WF. Comparing atomistic simulation data with the NMR experiment: how much can NOEs actually tell us? Proteins 2006, 63:210-218.
58. Markwick PR, Showalter SA, Bouvignies G, Brüschweiler R, Blackledge M. Structural dynamics of protein backbone phi angles: extended molecular dynamics simulations versus experimental (3) J scalar couplings. J Biomol NMR 2009, 45:17-21.
59. Bonvin AM, Brünger AT. Do NOE distances contain enough information to assess the relative populations of multi-conformer structures? J Biomol NMR 1996, 7:72-76.
60. Lindorff-Larsen K, Best RB, Depristo MA, Dobson CM, Vendruscolo M. Simultaneous determination of protein structure and dynamics. Nature 2005, 433:128-132.
61. Esteban-Martín S, Fenwick RB, Salvatella X. Refinement of ensembles describing unstructured proteins using NMR residual dipolar couplings. J Am Chem Soc 2010, 132:4626-4632.
62. Huang JR, Grzesiek S. Ensemble calculations of unstructured proteins constrained by RDC and PRE data: a case study of urea-denatured ubiquitin. J Am Chem Soc 2010, 132:694-705.
63. Allison JR, Varnai P, Dobson CM, Vendruscolo M. Determination of the free energy landscape of alpha-synuclein using spin label nuclear magnetic resonance measurements. J Am Chem Soc 2009, 131:18314-18326.
64. Jha AK, Colubri A, Freed KF, Sosnick TR. Statistical coil model of the unfolded state: resolving the reconciliation problem. Proc Natl Acad Sci USA 2005, 102:13099-13104.
65. Bernadó P, Blanchard L, Timmins P, Marion D, Ruigrok RWH, Blackledge M. A structural model for unfolded proteins from residual dipolar couplings and small-angle X-ray scattering. Proc Natl Acad Sci USA 2005, 102:17002-17007.
66. Clore GM, Tang C, Iwahara J. Elucidating transient macromolecular interactions using paramagnetic relaxation enhancement. Curr Opin Struct Biol 2007, 17:603-616.
67. Meier S, Strohmeier M, Blackledge M, Grzesiek S. Direct observation of dipolar couplings and hydrogen bonds across a beta-hairpin in 8 M urea. J Am Chem Soc 2007, 129:754-755.