Extensive conformational heterogeneity within protein cores

Journal of Physical Chemistry B

Volumn 118, Issue 24, 2014, Pages 6417-6423

  Bowman, Gregory R ^a   Geissler, Phillip L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR DYNAMICS; STATISTICAL MECHANICS;

CONFORMATIONAL HETEROGENEITY; CRYSTALLOGRAPHIC DATA; CRYSTALLOGRAPHIC STRUCTURE; HIGH PACKING FRACTION; MOLECULAR DYNAMICS SIMULATIONS; STRUCTURAL CHARACTERIZATION; STRUCTURAL FLUCTUATIONS; THERMODYNAMICS AND KINETICS;

PROTEINS;

BETA LACTAMASE; PROTEIN; RIBONUCLEASE H; UBIQUITIN;

CHEMISTRY; KINETICS; METABOLISM; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROBABILITY; THERMODYNAMICS;

BETA-LACTAMASES; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MARKOV CHAINS; MOLECULAR DYNAMICS SIMULATION; PROTEINS; RIBONUCLEASE H; THERMODYNAMICS; UBIQUITIN;

EID: 84900528411     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp4105823     Document Type: Article

References (42)

1. Zhou, Y.; Vitkup, D.; Karplus, M. Native Proteins Are Surface-Molten Solids: Application of the Lindemann Criterion for the Solid Versus Liquid State J. Mol. Biol. 1999, 285, 1371-1375
2. Karplus, M.; McCammon, J. A. Dynamics of Proteins: Elements and Function Annu. Rev. Biochem. 1983, 53, 263-300
3. Brooks, C. L.; Karplus, M.; Pettitt, B. M. Proteins: a Theoretical Perspective of Dynamics, Structure, and Thermodynamics; Advances in Chemical Physics; Wiley: New York, 1988; Vol. 71.
4. DePristo, M. A.; de Bakker, P. I. W.; Blundell, T. L. Heterogeneity and Inaccuracy in Protein Structures Solved by X-Ray Crystallography Structure 2004, 12, 831-838
5. Wand, A. J.; Urbauer, J. L.; McEvoy, R. P.; Bieber, R. J. Internal Dynamics of Human Ubiquitin Revealed by 13C-Relaxation Studies of Randomly Fractionally Labeled Protein Biochemistry 1996, 35, 6116-6125
6. 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
7. Igumenova, T. I.; Frederick, K. K.; Wand, A. J. Characterization of the Fast Dynamics of Protein Amino Acid Side Chains Using NMR Relaxation in Solution Chem. Rev. 2006, 106, 1672-1699
8. DuBay, K. H.; Geissler, P. L. Calculation of Proteins' Total Side-Chain Torsional Entropy and Its Influence on Protein-Ligand Interactions J. Mol. Biol. 2009, 391, 484-497
9. Fraser, J.; van den Bedem, H.; Samelson, A. J.; Lang, P. T.; Holton, J. M.; Echols, N.; Alber, T. Accessing Protein Conformational Ensembles Using Room-Temperature X-Ray Crystallography Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16247-16252
10. Frauenfelder, H.; McMahon, B. H.; Austin, R. H.; Chu, K.; Groves, J. T. The Role of Structure, Energy Landscape, Dynamics, and Allostery in the Enzymatic Function of Myoglobin Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 2370-2374
11. Boehr, D.; McElheny, D.; Dyson, H. The Dynamic Energy Landscape of Dihydrofolate Reductase Catalysis Science 2006, 313, 1638-1642
12. Henzler-Wildman, K.; Kern, D. Dynamic Personalities of Proteins Nature 2007, 450, 964-972
13. Bowman, G. R.; Geissler, P. L. Equilibrium Fluctuations of a Single Folded Protein Reveal a Multitude of Potential Cryptic Allosteric Sites Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 11681-11686
14. Raschke, T. M.; Marqusee, S. Hydrogen Exchange Studies of Protein Structure Curr. Opin. Biotechnol. 1998, 9, 80-86
15. Bernstein, R.; Schmidt, K.; Harbury, P.; Marqusee, S. Structural and Kinetic Mapping of Side-Chain Exposure Onto the Protein Energy Landscape Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 10532-10537
16. Wrabl, J.; Gu, J.; Liu, T.; Schrank, T.; Whitten, S.; Hilser, V. The Role of Protein Conformational Fluctuations in Allostery, Function, and Evolution Biophys. Chem. 2011, 159, 129-141
17. Bowman, G. R.; Huang, X.; Pande, V. S. Network Models for Molecular Kinetics and Their Initial Applications to Human Health Cell Res. 2010, 20, 622-630
18. Prinz, J.-H.; Wu, H.; Sarich, M.; Keller, B.; Senne, M.; Held, M.; Chodera, J. D.; Schütte, C.; Noé, F. Markov Models of Molecular Kinetics: Generation and Validation J. Chem. Phys. 2011, 134, 174105
19. McClendon, C.; Friedland, G.; Mobley, D.; Amirkhani, H.; Jacobson, M. P. Quantifying Correlations Between Allosteric Sites in Thermodynamic Ensembles J. Chem. Theory Comput. 2009, 5, 2486-2502
20. Chatfield, D. C.; Szabo, A.; Brooks, B. R. Molecular Dynamics of Staphylococcal Nuclease: Comparison of Simulation with 15N and 13C NMR Relaxation Data J. Am. Chem. Soc. 1998, 120, 5301-5311
21. 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
22. Tjandra, N.; Feller, S. E.; Pastor, R. W.; Bax, A. Rotational Diffusion Anisotropy of Human Ubiquitin From 15N NMR Relaxation J. Am. Chem. Soc. 1995, 117, 12562-12566
23. Mandel, A. M.; Akke, M.; Palmer, A. G., III. Backbone Dynamics of Escherichia Coli Ribonuclease HI: Correlations with Structure and Function in an Active Enzyme J. Mol. Biol. 1995, 246, 144-163
24. Savard, P.-Y.; Gagné, S. M. Backbone Dynamics of TEM-1 Determined by NMR: Evidence for a Highly Ordered Protein Biochemistry 2006, 45, 11414-11424
25. Kroenke, C. D.; Rance, M.; Palmer, A. G. Variability of the 15N Chemical Shift Anisotropy in Escherichia Coli Ribonuclease H in Solution J. Am. Chem. Soc. 1999, 121, 10119-10125
26. Pronk, S.; Páll, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M. R.; Smith, J. C.; Kasson, P. M.; van der Spoel, D. GROMACS 4.5: a High-Throughput and Highly Parallel Open Source Molecular Simulation Toolkit Bioinformatics 2013, 29, 845-854
27. van der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. C. GROMACS: Fast, Flexible, and Free J. Comput. Chem. 2005, 26, 1701-1718
28. Shirts, M.; Pande, V. S. COMPUTING: Screen Savers of the World Unite! Science 2000, 290, 1903-1904
29. Bowman, G. R.; Huang, X.; Pande, V. S. Using Generalized Ensemble Simulations and Markov State Models to Identify Conformational States Methods 2009, 49, 197-201
30. Beauchamp, K. A.; Bowman, G. R.; Lane, T. J.; Maibaum, L.; Haque, I. S.; Pande, V. S. MSMBuilder2: Modeling Conformational Dynamics at the Picosecond to Millisecond Scale J. Chem. Theory Comput. 2011, 7, 3412-3419
31. DeLano, W. L. The PyMOL Molecular Graphics System; Schrödinger, LLC: New York, 2002.
32. Voelz, V. A.; Bowman, G. R.; Beauchamp, K.; Pande, V. S. Molecular Simulation of Ab Initio Protein Folding for a Millisecond Folder NTL9 (1-39) J. Am. Chem. Soc. 2010, 132, 1526-1528
33. Vijay-kumar, S.; Bugg, C. E.; Cook, W. J. Structure of Ubiquitin Refined at 1.8 Å Resolution J. Mol. Biol. 1987, 194, 531-544
34. Kollman, P. A. Advances and Continuing Challenges in Achieving Realistic and Predictive Simulations of the Properties of Organic and Biological Molecules Acc. Chem. Res. 1996, 29, 461-469
35. Onufriev, A.; Bashford, D.; Case, D. A. Exploring Protein Native States and Large-Scale Conformational Changes with a Modified Generalized Born Model Proteins 2004, 55, 383-394
36. Goedken, E. R.; Keck, J. L.; Berger, J. M.; Marqusee, S. Divalent Metal Cofactor Binding in the Kinetic Folding Trajectory of Escherichia Coli Ribonuclease HI Protein Sci. 2000, 9, 1914-1921
37. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M. C. A Point-Charge Force Field for Molecular Mechanics Simulations of Proteins Based on Condensed-Phase Quantum Mechanical Calculations J. Comput. Chem. 2003, 24, 1999-2012
38. Wang, X.; Minasov, G.; Shoichet, B. K. Evolution of an Antibiotic Resistance Enzyme Constrained by Stability and Activity Trade-Offs J. Mol. Biol. 2002, 320, 85-95
39. Bowman, G. R.; Beauchamp, K. A.; Boxer, G.; Pande, V. S. Progress and Challenges in the Automated Construction of Markov State Models for Full Protein Systems J. Chem. Phys. 2009, 131, 124101
40. Cn Couplings J. Am. Chem. Soc. 2003, 125, 8959-8966
41. Farès, C.; Lakomek, N.-A.; Walter, K. F. A.; Frank, B. T. C.; Meiler, J.; Becker, S.; Griesinger, C. Accessing Ns-Ms Side Chain Dynamics in Ubiquitin with Methyl RDCs J. Biomol. NMR 2009, 45, 23-44
42. Lakomek, N.-A.; Walter, K. F. A.; Farès, C.; Lange, O. F.; de Groot, B. L.; Grubmüller, H.; Brüschweiler, R.; Munk, A.; Becker, S.; Meiler, J. Self-Consistent Residual Dipolar Coupling Based Model-Free Analysis for the Robust Determination of Nanosecond to Microsecond Protein Dynamics J. Biomol. NMR 2008, 41, 139-155