Achieving rigorous accelerated conformational sampling in explicit solvent

Journal of Physical Chemistry Letters

Volumn 5, Issue 7, 2014, Pages 1217-1224

  Doshi, Urmi ^a   Hamelberg, Donald ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

accelerated molecular dynamics; aMD; Chignolin; enhanced conformational sampling method; protein folding; RaMD; Trp cage

Indexed keywords

ACCELERATED MOLECULAR DYNAMICS; AMD; CHIGNOLIN; CONFORMATIONAL SAMPLINGS; RAMD; TRP-CAGE;

BIOMOLECULES; PROTEIN FOLDING; SOLVENTS;

MOLECULAR DYNAMICS;

EID: 84898076453     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/jz500179a     Document Type: Article

References (72)

1. Elber, R. Long-Timescale Simulation Methods Curr. Opin. Struct. Biol. 2005, 15, 151
2. Lei, H.; Duan, Y. Improved Sampling Methods for Molecular Simulation Curr. Opin. Struct. Biol. 2007, 17, 187
3. Stone, J. E.; Hardy, D. J.; Ufimtsev, I. S.; Schulten, K. GPU-Accelerated Molecular Modeling Coming of Age J. Mol. Graphics Modell. 2010, 29, 116
4. Shaw, D. E.; Dror, R. O.; Salmon, J. K.; Grossman, J. P.; Mackenzie, K. M.; Bank, J. A.; Young, C.; Deneroff, M. M.; Batson, B.; Bowers, K. J.; Chow, E.; Eastwood, M. P.; Ierardi, D. J.; Klepeis, J. L.; Kuskin, J. S.; Larson, R. H.; Lindorff-Larsen, K.; Maragakis, P.; Moraes, M. A.; Piana, S.; Shan, Y.; Towles, B. In Proceedings of the Conference on High Performance Computing Networking, Storage and Analysis; ACM: Portland, OR, 2009; p 1.
5. Friedrichs, M. S.; Eastman, P.; Vaidyanathan, V.; Houston, M.; Legrand, S.; Beberg, A. L.; Ensign, D. L.; Bruns, C. M.; Pande, V. S. Accelerating Molecular Dynamic Simulation on Graphics Processing Units J. Comput. Chem. 2009, 30, 864
6. Shirts, M.; Pande, V. S. COMPUTING: Screen Savers of the World Unite! Science 2000, 290, 1903
7. 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
8. Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T. E.; Laughton, C. A.; Orozco, M. Refinement of the Amber Force Field for Nucleic Acids: Improving the Description of Alpha/Gamma Conformers Biophys. J. 2007, 92, 3817
9. Zhu, X.; Lopes, P. E. M.; MacKerell, A. D. Recent Developments and Applications of the CHARMM Force Fields Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2012, 2, 167
10. Best, R. B.; Hummer, G. Optimized Molecular Dynamics Force Fields Applied to the Helix-Coil Transition of Polypeptides J. Phys. Chem. B 2009, 113, 9004
11. Doshi, U.; Hamelberg, D. Re-Optimization of the AMBER Force Field Parameters for Peptide Bond (Omega) Torsions Using Accelerated Molecular Dynamics J. Phys. Chem. B 2009, 113, 16590
12. MacKerell, A. D., Jr.; Feig, M.; Brooks, C. L., 3rd. Improved Treatment of the Protein Backbone in Empirical Force Fields J. Am. Chem. Soc. 2004, 126, 698
13. 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 2010, 78, 1950
14. Freddolino, P. L.; Harrison, C. B.; Liu, Y.; Schulten, K. Challenges in Protein-Folding Simulations Nat. Phys. 2010, 6, 751
15. Prigozhin, M. B.; Gruebele, M. Microsecond Folding Experiments and Simulations: A Match Is Made Phys. Chem. Chem. Phys. 2013, 15, 3372
16. Lane, T. J.; Shukla, D.; Beauchamp, K. A.; Pande, V. S. To Milliseconds and beyond: Challenges in the Simulation of Protein Folding Curr. Opin. Struct. Biol. 2013, 23, 58
17. Kubelka, J.; Hofrichter, J.; Eaton, W. A. The Protein Folding Speed Limit Curr. Opin. Struct. Biol. 2004, 14, 76
18. Shaw, D. E.; Maragakis, P.; Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Eastwood, M. P.; Bank, J. A.; Jumper, J. M.; Salmon, J. K.; Shan, Y.; Wriggers, W. Atomic-Level Characterization of the Structural Dynamics of Proteins Science 2010, 330, 341
19. Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Shaw, D. E. How Fast-Folding Proteins Fold Science 2011, 334, 517
20. Best, R. B.; Mittal, J. Microscopic Events in ?-Hairpin Folding from Alternative Unfolded Ensembles Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 11087
21. Best, R. B.; Mittal, J. Balance between α and β Structures in Ab Initio Protein Folding J. Phys. Chem. B 2010, 114, 8790
22. Best, R. B.; Mittal, J. Protein Simulations with an Optimized Water Model: Cooperative Helix Formation and Temperature-Induced Unfolded State Collapse J. Phys. Chem. B 2010, 114, 14916
23. Mittal, J.; Best, R. B. Tackling Force-Field Bias in Protein Folding Simulations: Folding of Villin HP35 and Pin WW Domains in Explicit Water Biophys. J. 2010, 99, L26
24. Juraszek, J.; Bolhuis, P. G. Sampling the Multiple Folding Mechanisms of Trp-cage in Explicit solvent Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 15859
25. Marinelli, F.; Pietrucci, F.; Laio, A.; Piana, S. a Kinetic Model of trp-cage Folding from Multiple Biased Molecular Dynamics Simulations PLoS Comput. Biol. 2009, 5, e1000452
26. Piana, S.; Laio, A. a Bias-Exchange Approach to Protein Folding J. Phys. Chem. B 2007, 111, 4553
27. Wang, L.; Friesner, R. A.; Berne, B. J. Replica Exchange with Solute Scaling: A More Efficient Version of Replica Exchange with Solute Tempering (REST2) J. Phys. Chem. B 2011, 115, 9431
28. Shao, Q.; Shi, J.; Zhu, W. Enhanced Sampling Molecular Dynamics Simulation Captures Experimentally Suggested Intermediate and Unfolded States in the Folding Pathway of Trp-cage Miniprotein J. Chem. Phys. 2012, 137
29. Han, W.; Schulten, K. Characterization of Folding Mechanisms of Trp-cage and WW-domain by Network Analysis of Simulations with a Hybrid-Resolution Model J. Phys. Chem. B 2013, 117, 13367
30. Ding, F.; Buldyrev, S. V.; Dokholyan, N. V. Folding Trp-Cage to NMR Resolution Native Structure Using a Coarse-Grained Protein Model Biophys. J. 2005, 88, 147
31. Duan, L.; Mei, Y.; Li, Y.; Zhang, Q.; Zhang, D.; Zhang, J. Simulation of the Thermodynamics of Folding and Unfolding of the Trp-cage Mini-Protein TC5b Using Different Combinations of Force Fields and Solvation Models Sci. China Chem. 2010, 53, 196
32. Chowdhury, S.; Lee, M. C.; Duan, Y. Characterizing the Rate-Limiting Step of Trp-cage Folding by All-Atom Molecular Dynamics Simulations J. Phys. Chem. B 2004, 108, 13855
33. Pitera, J. W.; Swope, W. Understanding Folding and Design: Replica-Exchange Simulations of "Trp-cage" Miniproteins Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 7587
34. Snow, C. D.; Zagrovic, B.; Pande, V. S. The Trp Cage: Folding Kinetics and Unfolded State Topology via Molecular Dynamics Simulations J. Am. Chem. Soc. 2002, 124, 14548
35. Zhou, R. Trp-cage: folding Free Energy Landscape in Explicit Water Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 13280
36. Doshi, U.; Hamelberg, D. Improved Statistical Sampling and Accuracy with Accelerated Molecular Dynamics on Rotatable Torsions J. Chem. Theor. Comput. 2012, 8, 4004
37. Hamelberg, D.; Mongan, J.; McCammon, J. A. Accelerated Molecular Dynamics: A Promising and Efficient Simulation Method for Biomolecules J. Chem. Phys. 2004, 120, 11919
38. Xin, Y.; Doshi, U.; Hamelberg, D. Examining the Limits of Time Reweighting and Kramers Rate Theory to Obtain Correct Kinetics from Accelerated Molecular Dynamics J. Chem. Phys. 2010, 132, 224101
39. Doshi, U.; Hamelberg, D. Extracting Realistic Kinetics of Rare Activated Processes from Accelerated Molecular Dynamics Using Kramers Theory J. Chem. Theor. Comput. 2011, 7, 575
40. Markwick, P. R.; 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
41. Markwick, P. R.; McCammon, J. A. Studying Functional Dynamics in Bio-Molecules Using Accelerated Molecular Dynamics Phys. Chem. Chem. Phys. 2011, 13, 20053
42. McGowan, L. C.; Hamelberg, D. Conformational Plasticity of an Enzyme during Catalysis: Intricate Coupling between Cyclophilin A Dynamics and Substrate Turnover Biophys. J. 2013, 104, 216
43. Hamelberg, D.; McCammon, J. A. Fast Peptidyl Cis-Trans Isomerization within the Flexible Gly-Rich Flaps of HIV-1 Protease J. Am. Chem. Soc. 2005, 127, 13778
44. Hamelberg, D.; McCammon, J. A. Mechanistic Insight into the Role of Transition-State Stabilization in Cyclophilin A J. Am. Chem. Soc. 2009, 131, 147
45. Doshi, U.; McGowan, L. C.; Ladani, S. T.; Hamelberg, D. Resolving the Complex Role of Enzyme Conformational Dynamics in Catalytic Function Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 5699
46. 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
47. Hamelberg, D.; de Oliveira, C. A.; McCammon, J. A. Sampling of Slow Diffusive Conformational Transitions with Accelerated Molecular Dynamics J. Chem. Phys. 2007, 127, 155102
48. Lindorff-Larsen, K.; Maragakis, P.; Piana, S.; Eastwood, M. P.; Dror, R. O.; Shaw, D. E. Systematic Validation of Protein Force Fields against Experimental Data PLoS One 2012, 7, e32131
49. Neidigh, J. W.; Fesinmeyer, R. M.; Andersen, N. H. Designing a 20-Residue Protein Nat. Struct. Biol. 2002, 9, 425
50. Kubelka, J.; Chiu, T. K.; Davies, D. R.; Eaton, W. A.; Hofrichter, J. Sub-Microsecond Protein Folding J. Mol. Biol. 2006, 359, 546
51. Honda, S.; Akiba, T.; Kato, Y. S.; Sawada, Y.; Sekijima, M.; Ishimura, M.; Ooishi, A.; Watanabe, H.; Odahara, T.; Harata, K. Crystal Structure of a Ten-Amino Acid Protein J. Am. Chem. Soc. 2008, 130, 15327
52. Cino, E. A.; Choy, W. Y.; Karttunen, M. Comparison of Secondary Structure Formation Using 10 Different Force Fields in Microsecond Molecular Dynamics Simulations J. Chem. Theor. Comput. 2012, 8, 2725
53. Qiu, L.; Pabit, S. A.; Roitberg, A. E.; Hagen, S. J. Smaller and Faster: the 20-Residue Trp-cage Protein Folds in 4 Micros J. Am. Chem. Soc. 2002, 124, 12952
54. Simmerling, C.; Strockbine, B.; Roitberg, A. E. All-Atom Structure Prediction and Folding Simulations of a Stable Protein J. Am. Chem. Soc. 2002, 124, 11258
55. Son, W. J.; Jang, S.; Pak, Y.; Shin, S. Folding Simulations with Novel Conformational Search Method J. Chem. Phys. 2007, 126, 104906
56. Day, R.; Paschek, D.; Garcia, A. E. Microsecond Simulations of the Folding/Unfolding Thermodynamics of the Trp-Cage Miniprotein Proteins 2010, 78, 1889
57. Kannan, S.; Zacharias, M. Folding Simulations of Trp-Cage Mini Protein in Explicit Solvent Using Biasing Potential Replica-Exchange Molecular Dynamics Simulations Proteins: Struct., Funct., Bioinf. 2009, 76, 448
58. Freddolino, P. L.; Schulten, K. Common Structural Transitions in Explicit-Solvent Simulations of Villin Headpiece Folding Biophys. J. 2009, 97, 2338
59. Duan, Y.; Kollman, P. A. Pathways to a Protein Folding Intermediate Observed in a 1-Microsecond Simulation in Aqueous Solution Science 1998, 282, 740
60. Ensign, D. L.; Kasson, P. M.; Pande, V. S. Heterogeneity Even at the Speed Limit of Folding: Large-Scale Molecular Dynamics Study of a Fast-Folding Variant of the Villin Headpiece J. Mol. Biol. 2007, 374, 806
61. Kuhrova, P.; De Simone, A.; Otyepka, M.; Best, R. B. Force-Field Dependence of Chignolin Folding and Misfolding: Comparison with Experiment and Redesign Biophys. J. 2012, 102, 1897
62. Ahmed, Z.; Beta, I. A.; Mikhonin, A. V.; Asher, S. A. UV-Resonance Raman Thermal Unfolding Study of Trp-Cage Shows That It Is Not a Simple Two-State Miniprotein J. Am. Chem. Soc. 2005, 127, 10943
63. Neuweiler, H.; Doose, S.; Sauer, M. a Microscopic View of Miniprotein Folding: Enhanced Folding Efficiency through Formation of an Intermediate Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 16650
64. Streicher, W. W.; Makhatadze, G. I. Unfolding Thermodynamics of Trp-Cage, A 20 Residue Miniprotein, Studied by Differential Scanning Calorimetry and Circular Dichroism Spectroscopy Biochemistry 2007, 46, 2876
65. Mok, K. H.; Kuhn, L. T.; Goez, M.; Day, I. J.; Lin, J. C.; Andersen, N. H.; Hore, P. J. a Pre-Existing Hydrophobic Collapse in the Unfolded State of an Ultrafast Folding Protein Nature 2007, 447, 106
66. Culik, R. M.; Serrano, A. L.; Bunagan, M. R.; Gai, F. Achieving Secondary Structural Resolution in Kinetic Measurements of Protein Folding: A Case Study of the Folding Mechanism of Trp-Cage Angew. Chem. 2011, 50, 10884
67. Barua, B.; Lin, J. C.; Williams, V. D.; Kummler, P.; Neidigh, J. W.; Andersen, N. H. The Trp-Cage: Optimizing the Stability of a Globular Miniprotein Protein Eng., Des. Sel. 2008, 21, 171
68. Rovo, P.; Straner, P.; Lang, A.; Bartha, I.; Huszar, K.; Nyitray, L.; Perczel, A. Structural Insights into the Trp-Cage Folding Intermediate Formation Chemistry 2013, 19, 2628
69. Lai, Z.; Preketes, N. K.; Mukamel, S.; Wang, J. Monitoring the Folding of Trp-Cage Peptide by Two-Dimensional Infrared (2dir) Spectroscopy J. Phys. Chem. B 2013, 117, 4661
70. Heyda, J.; Kozisek, M.; Bednarova, L.; Thompson, G.; Konvalinka, J.; Vondrasek, J.; Jungwirth, P. Urea and Guanidinium Induced Denaturation of a Trp-Cage Miniprotein J. Phys. Chem. B 2011, 115, 8910
71. Meuzelaar, H.; Marino, K. A.; Huerta-Viga, A.; Panman, M. R.; Smeenk, L. E. J.; Kettelarij, A. J.; van Maarseveen, J. H.; Timmerman, P.; Bolhuis, P. G.; Woutersen, S. Folding Dynamics of the Trp-Cage Miniprotein: Evidence for a Native-Like Intermediate from Combined Time-Resolved Vibrational Spectroscopy and Molecular Dynamics Simulations J. Phys. Chem. B 2013, 117, 11490
72. Fajer, M.; Hamelberg, D.; McCammon, J. A. Replica-Exchange Accelerated Molecular Dynamics (REXAMD) Applied to Thermodynamic Integration J. Chem. Theor. Comput. 2008, 4, 1565