Multi-Timescale Dynamics in Intrinsically Disordered Proteins from NMR Relaxation and Molecular Simulation

Journal of Physical Chemistry Letters

Volumn 7, Issue 13, 2016, Pages 2483-2489

  Salvi, Nicola ^a   Abyzov, Anton ^a   Blackledge, Martin ^a  

^a UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR DYNAMICS; PROTEINS; TIME MEASUREMENT;

CONFORMATIONAL PLASTICITY; CONFORMATIONAL SAMPLINGS; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR SIMULATIONS; NUCLEAR MAGNETIC RESONANCE(NMR); RELAXATION MEASUREMENTS; WEALTH OF INFORMATION;

NUCLEAR MAGNETIC RESONANCE;

EID: 84978123695     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/acs.jpclett.6b00885     Document Type: Article

References (52)

1. Uversky, V. N. Natively Unfolded Proteins: A Point Where Biology Waits for Physics Protein Sci. 2002, 11 (4) 739-756 10.1110/ps.4210102
2. Dunker, A. K.; Brown, C. J.; Lawson, J. D.; Iakoucheva, L. M.; Obradović, Z. Intrinsic Disorder and Protein Function Biochemistry 2002, 41 (21) 6573-6582 10.1021/bi012159+
3. Dyson, H. J.; Wright, P. E. Coupling of Folding and Binding for Unstructured Proteins Curr. Opin. Struct. Biol. 2002, 12 (1) 54-60 10.1016/S0959-440X(02)00289-0
4. Dyson, H. J.; Wright, P. E. Intrinsically Unstructured Proteins and Their Functions Nat. Rev. Mol. Cell Biol. 2005, 6 (3) 197-208 10.1038/nrm1589
5. Tompa, P.; Fuxreiter, M. Fuzzy Complexes: Polymorphism and Structural Disorder in Protein-Protein Interactions Trends Biochem. Sci. 2008, 33 (1) 2-8 10.1016/j.tibs.2007.10.003
6. Dyson, H. J.; Wright, P. E. Unfolded Proteins and Protein Folding Studied by NMR Chem. Rev. 2004, 104 (8) 3607-3622 10.1021/cr030403s
7. Jensen, M. R.; Zweckstetter, M.; Huang, J.; Blackledge, M. Exploring Free-Energy Landscapes of Intrinsically Disordered Proteins at Atomic Resolution Using NMR Spectroscopy Chem. Rev. 2014, 114 (13) 6632-6660 10.1021/cr400688u
8. Mittag, T.; Forman-Kay, J. D. Atomic-Level Characterization of Disordered Protein Ensembles Curr. Opin. Struct. Biol. 2007, 17 (1) 3-14 10.1016/j.sbi.2007.01.009
9. 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 (49) 17908-17918 10.1021/ja9069024
10. Allison, J. R.; Varnai, P.; Dobson, C. M.; Vendruscolo, M. Determination of the Free Energy Landscape of Alpha-Synuclein Using Spin Label Nuclear Magnetic Resonance Measurements J. Am. Chem. Soc. 2009, 131 (51) 18314-18326 10.1021/ja904716h
11. 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 (24) 8407-8418 10.1021/ja101645g
12. Schwalbe, M.; Ozenne, V.; Bibow, S.; Jaremko, M.; Jaremko, L.; Gajda, M.; Jensen, M. R.; Biernat, J.; Becker, S.; Mandelkow, E. et al. Predictive Atomic Resolution Descriptions of Intrinsically Disordered hTau40 and α-Synuclein in Solution from NMR and Small Angle Scattering Structure 2014, 22 (2) 238-249 10.1016/j.str.2013.10.020
13. Mantsyzov, A. B.; Maltsev, A. S.; Ying, J.; Shen, Y.; Hummer, G.; Bax, A. A Maximum Entropy Approach to the Study of Residue-Specific Backbone Angle Distributions in α-Synuclein, an Intrinsically Disordered Protein Protein Sci. 2014, 23 (9) 1275-1290 10.1002/pro.2511
14. Eliezer, D. Biophysical Characterization of Intrinsically Disordered Proteins Curr. Opin. Struct. Biol. 2009, 19 (1) 23-30 10.1016/j.sbi.2008.12.004
15. Fisher, C. K.; Stultz, C. M. Constructing Ensembles for Intrinsically Disordered Proteins Curr. Opin. Struct. Biol. 2011, 21 (3) 426-431 10.1016/j.sbi.2011.04.001
16. Jensen, M. R.; Ruigrok, R. W. H.; Blackledge, M. Describing Intrinsically Disordered Proteins at Atomic Resolution by NMR Curr. Opin. Struct. Biol. 2013, 23 (3) 426-435 10.1016/j.sbi.2013.02.007
17. Palmer, A. NMR Characterization of the Dynamics of Biomacromolecules Chem. Rev. 2004, 104 (8) 3623-3640 10.1021/cr030413t
18. Alexandrescu, A.; Shortlet, D. Backbone Dynamics of a Highly Disordered 131-Residue Fragment of Staphylococcal Nuclease J. Mol. Biol. 1994, 242 (4) 527-546 10.1006/jmbi.1994.1598
19. Yang, D. W.; Mok, Y. K.; FormanKay, J. D.; Farrow, N. A.; Kay, L. E. Contributions to Protein Entropy and Heat Capacity from Bond Vector Motions Measured by NMR Spin Relaxation J. Mol. Biol. 1997, 272 (5) 790-804 10.1006/jmbi.1997.1285
20. Buevich, A. V.; Baum, J. Dynamics of Unfolded Proteins: Incorporation of Distributions of Correlation Times in the Model Free Analysis of NMR Relaxation Data J. Am. Chem. Soc. 1999, 121 (37) 8671-8672 10.1021/ja9910412
21. Yao, J.; Chung, J.; Eliezer, D.; Wright, P. E.; Dyson, H. J. NMR Structural and Dynamic Characterization of the Acid-Unfolded State of Apomyoglobin Provides Insights into the Early Events in Protein Folding Biochemistry 2001, 40 (12) 3561-3571 10.1021/bi002776i
22. Ochsenbein, F.; Neumann, J. M.; Guittet, E.; Van Heijenoort, C. Dynamical Characterization of Residual and Non-Native Structures in a Partially Folded Protein by N-15 NMR Relaxation Using a Model Based on a Distribution of Correlation Times Protein Sci. 2002, 11 (4) 957-964 10.1110/ps.4000102
23. Klein-Seetharaman, J.; Oikawa, M.; Grimshaw, S. B.; Wirmer, J.; Duchardt, E.; Ueda, T.; Imoto, T.; Smith, L. J.; Dobson, C. M.; Schwalbe, H. Long-Range Interactions within a Nonnative Protein Science 2002, 295 (5560) 1719-1722 10.1126/science.1067680
24. Choy, W.-Y.; Kay, L. E. Probing Residual Interactions in Unfolded Protein States Using NMR Spin Relaxation Techniques: An Application to 131 J. Am. Chem. Soc. 2003, 125 (39) 11988-11992 10.1021/ja035705q
25. Modig, K.; Poulsen, F. M. Model-Independent Interpretation of NMR Relaxation Data for Unfolded Proteins: The Acid-Denatured State of ACBP J. Biomol. NMR 2008, 42 (3) 163-177 10.1007/s10858-008-9280-0
26. Gill, M. L.; Byrd, R. A.; Arthur, G.; Palmer, I. I. I. Dynamics of GCN4 Facilitate DNA Interaction: A Model-Free Analysis of an Intrinsically Disordered Region Phys. Chem. Chem. Phys. 2016, 18, 5839-5849 10.1039/C5CP06197K
27. Khan, S. N.; Charlier, C.; Augustyniak, R.; Salvi, N.; Dejean, V.; Bodenhausen, G.; Lequin, O.; Pelupessy, P.; Ferrage, F. Distribution of Pico- and Nanosecond Motions in Disordered Proteins from Nuclear Spin Relaxation Biophys. J. 2015, 109 (5) 988-999 10.1016/j.bpj.2015.06.069
28. Abyzov, A.; Salvi, N.; Schneider, R.; Maurin, D.; Ruigrok, R. W. H.; Jensen, M. R.; Blackledge, M. Identification of Dynamic Modes in an Intrinsically Disordered Protein Using Temperature-Dependent NMR Relaxation J. Am. Chem. Soc. 2016, 138 (19) 6240-6251 10.1021/jacs.6b02424
29. Prompers, J. J.; Bruschweiler, R. General Framework for Studying the Dynamics of Folded and Nonfolded Proteins by NMR Relaxation Spectroscopy and MD Simulation J. Am. Chem. Soc. 2002, 124 (16) 4522-4534 10.1021/ja012750u
30. Xue, Y.; Skrynnikov, N. R. Motion of a Disordered Polypeptide Chain as Studied by Paramagnetic Relaxation Enhancements, 15N Relaxation, and Molecular Dynamics Simulations: How Fast Is Segmental Diffusion in Denatured Ubiquitin? J. Am. Chem. Soc. 2011, 133 (37) 14614-14628 10.1021/ja201605c
31. Lindorff-Larsen, K.; Trbovic, N.; Maragakis, P.; Piana, S.; Shaw, D. E. Structure and Dynamics of an Unfolded Protein Examined by Molecular Dynamics Simulation J. Am. Chem. Soc. 2012, 134 (8) 3787-3791 10.1021/ja209931w
32. Robustelli, P.; Trbovic, N.; Friesner, R. A.; Palmer, A. G. Conformational Dynamics of the Partially Disordered Yeast Transcription Factor GCN4 J. Chem. Theory Comput. 2013, 9 (11) 5190-5200 10.1021/ct400654r
33. Markwick, P. R. L.; 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 (46) 16968-16975 10.1021/ja907476w
34. Guerry, P.; Salmon, L.; Mollica, L.; Ortega Roldan, J.-L.; Markwick, P.; van Nuland, N. A. J.; McCammon, J. A.; Blackledge, M. Mapping the Population of Protein Conformational Energy Sub-States from NMR Dipolar Couplings Angew. Chem., Int. Ed. 2013, 52 (11) 3181-3185 10.1002/anie.201209669
35. Rauscher, S.; Gapsys, V.; Gajda, M. J.; Zweckstetter, M.; de Groot, B. L.; Grubmüller, H. Structural Ensembles of Intrinsically Disordered Proteins Depend Strongly on Force Field: A Comparison to Experiment J. Chem. Theory Comput. 2015, 11 (11) 5513-5524 10.1021/acs.jctc.5b00736
36. Best, R. B.; Zheng, W.; Mittal, J. Balanced Protein-Water Interactions Improve Properties of Disordered Proteins and Non-Specific Protein Association J. Chem. Theory Comput. 2014, 10 (11) 5113-5124 10.1021/ct500569b
37. Piana, S.; Donchev, A. G.; Robustelli, P.; Shaw, D. E. Water Dispersion Interactions Strongly Influence Simulated Structural Properties of Disordered Protein States J. Phys. Chem. B 2015, 119 (16) 5113-5123 10.1021/jp508971m
38. Communie, G.; Ruigrok, R. W.; Jensen, M. R.; Blackledge, M. Intrinsically Disordered Proteins Implicated in Paramyxoviral Replication Machinery Curr. Opin. Virol. 2014, 5, 72-81 10.1016/j.coviro.2014.02.001
39. Jensen, M. R.; Blackledge, M. On the Origin of NMR Dipolar Waves in Transient Helical Elements of Partially Folded Proteins J. Am. Chem. Soc. 2008, 130 (34) 11266-11267 10.1021/ja8039184
40. Jensen, M. R.; Houben, K.; Lescop, E.; Blanchard, L.; Ruigrok, R. W. H.; Blackledge, M. Quantitative Conformational Analysis of Partially Folded Proteins from Residual Dipolar Couplings: Application to the Molecular Recognition Element of Sendai Virus Nucleoprotein J. Am. Chem. Soc. 2008, 130 (25) 8055-8061 10.1021/ja801332d
41. Houben, K.; Marion, D.; Tarbouriech, N.; Ruigrok, R. W. H.; Blanchard, L. Interaction of the C-Terminal Domains of Sendai Virus N and P Proteins: Comparison of Polymerase-Nucleocapsid Interactions within the Paramyxovirus Family J. Virol. 2007, 81 (13) 6807-6816 10.1128/JVI.00338-07
42. Schneider, R.; Maurin, D.; Communie, G.; Kragelj, J.; Hansen, D. F.; Ruigrok, R. W. H.; Jensen, M. R.; Blackledge, M. Visualizing the Molecular Recognition Trajectory of an Intrinsically Disordered Protein Using Multinuclear Relaxation Dispersion NMR J. Am. Chem. Soc. 2015, 137 (3) 1220-1229 10.1021/ja511066q
43. Abascal, J. L. F.; Vega, C. A General Purpose Model for the Condensed Phases of Water: TIP4P/2005 J. Chem. Phys. 2005, 123 (23) 234505 10.1063/1.2121687
44. Henriques, J.; Cragnell, C.; Skepö, M. Molecular Dynamics Simulations of Intrinsically Disordered Proteins: Force Field Evaluation and Comparison with Experiment J. Chem. Theory Comput. 2015, 11 (7) 3420-3431 10.1021/ct501178z
45. Lindorff-Larsen, K.; Piana, S.; Palmo, K.; Maragakis, P.; Klepeis, J. L.; Dror, R. O.; Shaw, D. E. Improved Side-Chain Torsion Potentials for the Amber ff99SB Protein Force Field Proteins: Struct., Funct., Genet. 2010, 78 (8) 1950-1958 10.1002/prot.22711
46. Hess, B. Convergence of Sampling in Protein Simulations Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip. Top. 2002, 65 (3) 31910 10.1103/PhysRevE.65.031910
47. Urbańczyk, M.; Bernin, D.; Koźmiński, W.; Kazimierczuk, K. Iterative Thresholding Algorithm for Multiexponential Decay Applied to PGSE NMR Data Anal. Chem. 2013, 85 (3) 1828-1833 10.1021/ac3032004
48. Fisher, C. K.; Stultz, C. M. Constructing Ensembles for Intrinsically Disordered Proteins Curr. Opin. Struct. Biol. 2011, 21 (3) 426-431 10.1016/j.sbi.2011.04.001
49. Affentranger, R.; Tavernelli, I.; Di Iorio, E. E. A Novel Hamiltonian Replica Exchange MD Protocol to Enhance Protein Conformational Space Sampling J. Chem. Theory Comput. 2006, 2 (2) 217-228 10.1021/ct050250b
50. Sugita, Y.; Okamoto, Y. Replica-Exchange Molecular Dynamics Method for Protein Folding Chem. Phys. Lett. 1999, 314 (1-2) 141-151 10.1016/S0009-2614(99)01123-9
51. Soranno, A.; Buchli, B.; Nettels, D.; Cheng, R. R.; Müller-Späth, S.; Pfeil, S. H.; Hoffmann, A.; Lipman, E. A.; Makarov, D. E.; Schuler, B. Quantifying Internal Friction in Unfolded and Intrinsically Disordered Proteins with Single-Molecule Spectroscopy Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (44) 17800-17806 10.1073/pnas.1117368109
52. Milles, S.; Lemke, E. A. Mapping Multivalency and Differential Affinities within Large Intrinsically Disordered Protein Complexes with Segmental Motion Analysis Angew. Chem., Int. Ed. 2014, 53 (28) 7364-7367 10.1002/anie.201403694