Ensemble-based interpretations of NMR structural data to describe protein internal dynamics

Molecules

Volumn 18, Issue 9, 2013, Pages 10548-10567

  Ángyán, Annamária F ^a   Gáspári, Zoltán ^a  

^a PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

Author keywords

Dynamic structural ensembles; Ensemble generation; Molecular dynamics simulation; Protein mobility; Protein NMR spectroscopy

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; INTRINSICALLY DISORDERED PROTEIN; NCOA3 PROTEIN, HUMAN; PEPTIDE HYDROLASE; STEROID RECEPTOR COACTIVATOR 3; VIRUS PROTEIN; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN BINDING;

ALGORITHM; CHEMISTRY; HUMAN; MOLECULAR DYNAMICS; MONTE CARLO METHOD; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW;

ALGORITHMS; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR DYNAMICS SIMULATION; MONTE CARLO METHOD; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEAR RECEPTOR COACTIVATOR 3; PEPTIDE HYDROLASES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84885162175     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules180910548     Document Type: Review

References (78)

1. Markwick, P.R.; Malliavin, T.; Nilges, M. Structural biology by NMR: structure, dynamics, and interactions. PLoS Comp. Biol. 2008, 4, e1000168.
2. Boehr, D.D.; Nussinov, R.; Wright, P.E. The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 2009, 5, 789-796.
3. Fenwick, R.B.; Esteban-Martín, S.; Salvatella, X. Understanding biomolecular motion, recognition, and allostery by use of conformational ensembles. Eur. Biophys. J. 2011, 40, 1339-1355.
4. Gáspári, Z.; Perczel, A. Protein dynamics as reported by NMR. Annu. Rep. NMR Spect. 2010, 71,35-75.
5. Gáspári, Z.; Várnai, P.; Szappanos, B.; Perczel, A. Reconciling the lock-and-key and dynamic views of canonical serine protease inhibitor action. FEBS Lett. 2010, 584, 203-206.
6. Dyson, J.H; Wright, P.E. [12] Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states. Meth. Enzymol. 2001, 339, 258-270. (Pubitemid 32666564)
7. Ferreon, A.C.M.; Ferreon, J.C.; Wright, P.E.; Deniz, A.A. Modulation of allostery by protein intrinsic disorder. Nature 2013, 498, 390-394.
8. Laskowski, R.A. Structural Quality Assurance. In Structural Bioinformatics, 2nd Ed.; Wiley: Hoboken, NJ, USA, 2009.
9. Wütrich, K. NMR of Proteins and Nucleic Acids; Wiley: Hoboken, NJ, USA, 1986.
10. Bürgi, R.; Pitera, J.; van Gunsteren, W.F. Assessing the effect of conformational averaging on the measured values of observables. J. Biomol. NMR 2001, 19, 305-320. (Pubitemid 32401470)
11. Allison, J.R. Assessing and refining molecular dynamics simulations of proteins with nuclear magnetic resonance data. Biophys. Rev. 2012, 4, 189-203.
12. Best, R.B.; Vendruscolo, M. Structural interpretation of hydrogen exchange protection factors in proteins: Characterization of the native state fluctuations of CI2. Structure 2006, 14, 97-106. (Pubitemid 43350077)
13. Paci, E.; Karplus, M. Forced unfolding of fibronectin type 3 modules: an analysis by biased molecular dynamics simulations. J. Mol. Biol. 1999, 288, 441-459. (Pubitemid 29221813)
14. Jarymowycz, V.A.; Stone, M.J. Fast time scale dynamics of protein backbones: NMR relaxation methods, applications, and functional consequences. Chem. Rev. 2006, 106, 1624-1671. (Pubitemid 43792775)
15. Schwieters, C.D.; Kuszewski, J.J.; Clore, M.G. Using Xplor-NIH for NMR molecular structure determination. Prog. Nucl. Magn. Reson. Spectrosc. 2006, 48, 47-62.
16. Best, R.B.; Vendruscolo, M. Determination of protein structures consistent with NMR order parameters. J. Am. Chem. Soc. 2004, 126, 8090-8091. (Pubitemid 38878936)
17. Batta, G.; Barna, T.; Gáspári, Z.; Sándor, S.; Kövér, K.E.; Binder, U., Sarg, B.; Kaiserer, L.; Chhillar, A.K.; Eigentler, A.; et al. Functional aspects of the solution structure and dynamics of PAF-A highly-stable antifungal protein from Penicillium chrysogenum. FEBS J. 2009, 276, 2875-2890.
18. Bonvin, A.M.; Brünger, A.T. Conformational variability of solution nucelar magnetic resonance structures. J. Mol. Biol. 1995, 250, 80-93.
19. 1H-nuclear magnetic resonance spectroscopy in peptides related to the N terminus of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 1993, 230, 312-322. (Pubitemid 23093565)
20. Bonvin, A.M.; Boelens, R.; Kaptein, R. Time-and ensemble-averaged direct NOE restraints. J. Biomol. NMR 1994, 4, 143-149.
21. Richter, B.; Gsponer, J.; Várnai, P.; Salvatella, X.; Vendruscolo, M. The MUMO (minimal under-restraining minimal over-restraining) method for the determination of native state ensembles of proteins. J. Biomol. NMR 2007, 37, 117-135. (Pubitemid 46157977)
22. Lakomek, N.A.; Lange, O.; Walter, K.F.; Fares, C.; Egger, D.; Lunkenheimer, P.; Meiler, J.; Grubmüller, H.; Becker, S.; de Groot, B.L.; et al. Residual dipolar couplings as a tool to study molecular recognition of ubiquitin. Biochem. Soc. Trans. 2008, 36, 1433-1437.
23. Higman, V.A.; Boyd, J.; Smith, L.J.; Redfield, C. Residual dipolar couplings: are multiple independent alignments always possible. J. Biomol. NMR 2011, 49, 53-60.
24. Hess, B.; Scheek, R.M. Orientation restraints in molecular dynamics simulations using time and ensemble averaging. J. Magn. Reson. 2003, 164, 19-27.
25. 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.
26. Montalvao, R.W.; de Simone, A.; Vendruscolo, M. Determination of structural fluctuations of proteins from structure-based calculations of residual dipolar couplings. J. Biomol. NMR 2012, 53, 281-292.
27. De Simone, A.R.W.; Montalvao, R.W; Vendruscolo, M. Determination of conformational equilibria in proteins using residual dipolar couplings. J. Chem. Theory Comput. 2011, 7, 4189-4195.
28. Shen, Y.; Lange, O.; Delaglio, F.; Rossi, P.; Aramini, J.M.; Liu, G.; Eletsky, A.; Wu, Y.; Singarapu, K.K.; Lemak, A.; et al. Consistent blind protein structure generation from NMR chemical shift data. Proc. Natl. Acad. Sci. USA 2008, 105, 4685-4690. (Pubitemid 351753807)
29. 15N chemical shifts. J. Biomol. NMR 2003, 26, 215-240. (Pubitemid 36758442)
30. 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.
31. Camilloni, C.; Cavalli, A.; Vendruscolo, M. Assessment of the use of NMR chemical shifts as replica-averaged structural restraints in molecular dynamics simulations to characterise the dynamics of proteins. J. Phys. Chem. B 2013, 117, 1838-1843.
32. Camilloni, C., Robustelli, P., Simone, A.D., Cavalli, A., Vendruscolo, M. Characterization of the conformational equilibrium between the two major substates of RNase a using NMR chemical shifts. J. Am. Chem. Soc. 2012, 134, 3968-3971.
33. Dedmon, M.M.; Lindorff-Larsen, K.; Christodoulou, J.; Vendruscolo, M.; Dobson, C.M. Mapping long-range interactions in α-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J. Am. Chem. Soc. 2005, 127, 476-477. (Pubitemid 40174345)
34. Lindorff-Larsen, K.; Best, R.B.; DePristo, M.A.; Dobson, C.M.; Vendruscolo, M. Simultaneous determination of protein structure and dynamics. Nature 2005, 433, 128-132.
35. Lindorff-Larsen, K.; Best, R.B.; Vendruscolo, M. Interpreting dynamically-averaged scalar couplings in proteins. J. Biomol. NMR 2005, 32, 273-280. (Pubitemid 41511509)
36. Allison, J.R.; Várnai, P.; Dobson, C.M.; Vendruscolo, M. Determination of the free energy landscape of α-synuclein using spin label nuclear magnetic resonance measurements. J. Am. Chem. Soc. 2009, 131, 18314-18326.
37. Im, W.; Jo, S.; Kim, T. An ensemble dynamics approach to decipher solid-state NMR observables of membrane proteins. Biochim. Biophys. Acta 2012, 1818, 252-262.
38. Lange, O.F.; Lakomek, N.A.; Farès, C.; Schröder, G.F.; Walter, K.F.; Becker, S.; de Groot, B.L. Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 2008, 320, 1471-1475. (Pubitemid 351929422)
39. Fenwick, R.B.; Esteban-Martín, S.; Richter, B.; Lee, D.; Walter, K.F.; Milovanovic, D.; Becker, S.; Lakomek, N.A.; 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.
40. Hamelberg, D.; Mongan, J.; McCammon, J.A. Accelerated molecular dynamics: A promising and efficient simulation method for biomolecules. J. Chem. Phys. 2004, 120, 11919-11929.
41. Fisher, C.K.; Stultz, C.M. Constructing ensembles for intrinsically disordered proteins. Curr. Opin. Struct. Biol. 2011, 21, 426-431.
42. Ozenne, V.; Bauer, F.; Salmon, L.; Huang, J.R.; Jensen, M.R.; Segard, S.; Bernadó, P.; Charavay, C.; Blackledge, M. Flexible-meccano: A tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics 2012, 28, 1463-1470.
43. Feldman, H.J.; Hogue, C.W. Probabilistic sampling of protein conformations: New hope for brute force? Proteins 2002, 46, 8-23. (Pubitemid 34033572)
44. Petoukhov, M.V.; Svergun, D.I. Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys J. 2005, 89, 1237-1250. (Pubitemid 41099005)
45. Bernadó, P.; Mylonas, E.; Petoukhov, M.V.; Blackledge, M.; Svergun, D.I. Structural characterization of flexible proteins using small-angle X-ray scattering. J. Am. Chem. Soc. 2007, 129, 5656-5664. (Pubitemid 46697655)
46. Bertini, I.; Ferella, L.; Luchinat, C.; Parigi, G.; Petoukhov, M.V.; Ravera, E.; Rosato, A.; Svergun, D.I. MaxOcc: A web portal for maximum occurrence analysis. J. Biomol. NMR 2012, 53, 271-280.
47. Louhivuori, M.; Pääkkönen, K.; Fredriksson, K.; Permi, P.; Lounila, J.; Annila, A. On the origin of residual dipolar couplings from denatured proteins. J. Am. Chem. Soc. 2003, 125, 15647-15650. (Pubitemid 37532209)
48. Louhivuori, M.; Fredriksson, K.; Pääkkönen, K.; Permi, P.; Annila, A. Alignment of chain-like molecules. J. Biomol. NMR 2004, 29, 517-524. (Pubitemid 38967362)
49. Jha, A.K.; Colubri, A.; Freed, K.F.; Sosnick, T.R. Statistical coil model of the unfolded state: Resolving the reconciliation problem. Proc. Natl. Acad. Sci. USA 2005, 102, 13099-13104. (Pubitemid 41324985)
50. Bernadó, P.; Blanchard, L.; Timmins, P.; Marion, D.; Ruigrok, R.W.; 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. (Pubitemid 41692673)
51. Meier, S.; Grzesiek, S.; Blackledge, M. Mapping the conformational landscape of urea-denatured ubiquitin using residual dipolar couplings. J. Am. Chem. Soc. 2007, 129, 9799-9807. (Pubitemid 47237494)
52. Mukrasch, M.D.; Markwick, P.; Biernat, J.; von Bergen, M.; 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. (Pubitemid 46651401)
53. Choy, W.Y.; Forman-Kay, J.D. Calculation of ensembles of structures representing the unfolded state of an SH3 domain. J. Mol. Biol. 2001, 308, 1011-1032. (Pubitemid 32577079)
54. Krzeminski, M., Marsh, J.A., Neale, C., Choy, W.Y., Forman-Kay, J.D. Characterization of disordered proteins with ENSEMBLE. Bioinformatics 2013, 29, 398-399.
55. Nodet, G.; Salmon, L.; Ozenne, V.; Meier, S.; Jensen, M.R.; Blackledge, M. Quantitative description of backbone conformational sampling of unfolded proteins at amino acid resolution from NMR residual dipolar couplings. J. Am. Chem. Soc. 2009, 131, 17908-17918.
56. Salmon, L.; Nodet, G.; Ozenne, V.; Yin, G.; Jensen, M.R.; Zweckstetter, M.; Blackledge, M. NMR characterization of long-range order in intrinsically disordered proteins. J. Am. Chem. Soc. 2010, 132, 8407-8418.
57. Jensen, M.R.; Communie, G.; Ribeiro, E.A.; Martinez, N.; Desfosses, A.; Salmon, L.; Mollica, L.; Gabel, F.; Jamin, M.; Longhi, S.; et al. Intrinsic disorder in measles virus nucleocapsids. Proc. Natl. Acad. Sci. USA 2011, 108, 9839-9844.
58. Guerry, P.; Salmon, L.; Mollica, L.; Ortega Roldan, J.L.; Markwick, P.; van Nuland, N.A.; Blackledge, M. Mapping the population of protein conformational energy sub-states from NMR dipolar couplings. Angew. Chem. Int. Ed. 2013, 52, 3181-3185.
59. Ángyán, A.F.; Szappanos, B.; Perczel, A.; Gáspári, Z. CoNSEnsX: An ensemble view of protein structures and NMR-derived experimental data. BMC Struct. Biol. 2010, 10, 39.
60. Gáspári, Z.; Ángyán, A.F; Dhir, S.; Franklin, D.; Perczel, A.; Pintar, A.; Pongor, S. Probing dynamic protein ensembles with atomic proximity measures. Curr. Prot. Pept. Sci. 2010, 11, 515-522.
61. Dhulesia, A.; Gsponer, J.; Vendruscolo, M. Mapping of two networks of residues that exhibit structural and dynamical changes upon binding in a PDZ domain protein. J. Am. Chem. Soc. 2008, 130, 8931-8939. (Pubitemid 352000832)
62. Bakan, A.; Meireles, L.M.; Bahar, I. ProDy: Protein dynamics inferred from theory and experiments. Bioinformatics 2011, 27, 1575-1577.
63. Lindorff-Larsen, K.; Ferkinghoff-Borg, J. Similarity measures for protein ensembles. PLoS One 2009, 4, e4203.
64. Rieping, W.; Habeck, M.; Nilges, M. Inferential structure determination. Science 2005, 309, 303-306.
65. Fisher, C.K.; Huang, A.; Stultz, C.M. Modeling intrinsically disordered proteins with bayesian statistics. J. Am. Chem. Soc. 2010, 132, 14919-14927.
66. Pitera, J.W.; Chodera, J.D. On the use of experimental observations to bias simulated ensembles. J. Chem. Theory Comput. 2012, 8, 3445-3451.
67. Cavalli, A.; Camilloni, C.; Vendruscolo, M. Molecular dynamics simulations with replica-averaged structural restraints generate structural ensembles according to the maximum entropy principle. J. Chem. Phys. 2013, 138, 094112.
68. Roux, B.; Weare, J. On the statistical equivalence of restrained-ensemble simulations with the maximum entropy method. J. Chem. Phys. 2013, 138, 084107.
69. Torda, A.E.; Scheek, R. M.; van Gunsteren, W.F. Time-dependent distance restraints in molecular dynamics simulations. Chem. Phys. Lett. 1989, 157, 289-294.
70. Torda, A.E.; Brunne, R.M.; Huber, T.; Kessler, H.; van Gunsteren, W.F. Structure refinement using time-averaged J-coupling constant restraints. J. Biomol. NMR 1993, 3, 55-66.
71. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins 2006, 65, 712-725. (Pubitemid 44583220)
72. Li, D.W.; Brüschweiler, R. NMR-based protein potentials. Angew. Chem. Int. Ed. 2010, 49, 6778-6780.
73. Markwick, P.R., Bouvignies, G., Salmon, L., McCammon, J.A., Nilges, M., Blackledge, M. Toward a unified representation of protein structural dynamics in solution. J. Am. Chem. Soc. 2009, 131, 16968-16975.
74. Markwick, P.R.; Cervantes, C.F.; Abel, B.L.; Komives, E.A.; Blackledge, M.; McCammon, J.A. Enhanced conformational space sampling improves the prediction of chemical shifts in proteins. J. Am. Chem. Soc. 2010, 132, 1220-1221.
75. Salmon, L.; Bascom, G.; Andricioaei, I.; Al-Hashimi, H.M. A general method for constructing atomic-resolution RNA ensembles using NMR residual dipolar couplings: the basis for interhelical motions revealed. J. Am. Chem. Soc. 2013, 135, 5457-5466.
76. Li, D.W.; Brüschweiler, R. Iterative optimization of molecular mechanics force fields from NMR data of full-length proteins. J. Chem. Theory Comput. 2011, 7, 1773-1782.
77. Iesmantavicius, V.; Jensen, M.R.; Ozenne, V.; Blackledge, M.; Poulsen, F.M.; Kjaergaard, M. Modulation of the intrinsic helix propensity of an intrinsically disordered protein reveals long-range helix-helix interactions. J. Am. Chem. Soc. 2013, 135, 10155-10163.
78. Jo, S.; Im, W. Transmembrane helix orientation and dynamics: insights from ensemble dynamics with solid-state NMR observables. Biophys. J. 2011, 100, 2913-2921.