Structural characterization of γ-repressor folding from all-atom molecular dynamics simulations

Journal of Physical Chemistry Letters

Volumn 3, Issue 9, 2012, Pages 1117-1123

  Liu, Yanxin ^a,b   Strümpfer, Johan ^a,c   Freddolino, Peter L ^a,c,d   Gruebele, Martin ^a,b,c   Schulten, Klaus ^a,b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; COMPUTATIONAL CHALLENGES; EXPLICIT SOLVENTS; FAST-FOLDING PROTEINS; FOLDING KINETICS; FOLDING PROCESS; INTERMEDIATE TEMPERATURES; MD SIMULATION; MOLECULAR DYNAMICS SIMULATIONS; REVERSIBLE FOLDING; STRUCTURAL CHARACTERIZATION;

AMINO ACIDS; COMPUTATIONAL CHEMISTRY;

MOLECULAR DYNAMICS;

EID: 84860521165     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/jz300017c     Document Type: Article

References (46)

1. Onuchic, J. N.; Luthey-Schulten, Z.; Wolynes, P. G. Theory of Protein Folding: The Energy Landscape Perspective Annu. Rev. Phys. Chem. 1997, 48, 545-600
2. Thirumalai, D.; OBrien, E. P.; Morrison, G.; Hyeon, C. Theoretical Perspectives on Protein Folding Annu. Rev. Biochem. 2010, 39, 159-183
3. Kubelka, J.; Hofrichter, J.; Eaton, W. A. The Protein Folding Speed Limit Curr. Opin. Struct. Biol. 2004, 14, 76-88
4. Clementi, C. Coarse-Grained Models of Protein Folding: Toy Models or Predictive Tools? Curr. Opin. Struct. Biol. 2007, 18, 10-15
5. Freddolino, P. L.; Liu, F.; Gruebele, M.; Schulten, K. Ten-Microsecond Molecular Dynamics Simulation of a Fast-Folding WW Domain Biophys. J. 2008, 94, L75-L77
6. Freddolino, P. L.; Schulten, K. Common Structural Transitions in Explicit-Solvent Simulations of Villin Headpiece Folding Biophys. J. 2009, 97, 2338-2347
7. Freddolino, P. L.; Harrison, C. B.; Liu, Y.; Schulten, K. Challenges in Protein Folding Simulations Nature Phys. 2010, 6, 751-758
8. Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Shaw, D. E. How Fast-Folding Proteins Fold Science 2011, 334, 517-520
9. Duan, Y.; Kollman, P. Pathways to a Protein Folding Intermediate Observed in a 1 Microsecond Simulation in Aqueous Solution Science 1998, 282, 740-744
10. 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. Atomic-Level Characterization of the Structural Dynamics of Proteins Science 2010, 330, 341-346
11. Sugita, Y.; Okamoto, Y. Replica-Exchange Molecular Dynamics Method for Protein Folding Chem. Phys. Lett. 1999, 314, 141-151
12. Onuchic, J. N.; García, A. E. Folding a Protein in a Computer: An Atomic Description of the Folding/Unfolding of Protein A Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 13898-13903
13. Rosta, E.; Hummer, G. Error and Efficiency of Replica Exchange Molecular Dynamics Simulations J. Chem. Phys. 2009, 131, 165102
14. Day, R.; Paschek, D.; García, A. E. Microsecond Simulations of the Folding/Unfolding Thermodynamics of the Trp-Cage Miniprotein Proteins: Struct., Funct., Genet. 2010, 78, 1889-1899
15. Fukunishi, H.; Watanabe, O.; Takada, S. On the Hamiltonian Replica Exchange Method for Efficient Sampling of Biomolecular Systems: Application to Protein Structure Prediction J. Chem. Phys. 2002, 116, 9058-9067
16. Zhang, C.; Ma, J. Enhanced Sampling in Generalized Ensemble with Large Gap of Sampling Parameter: Case Study in Temperature Space Random Walk J. Chem. Phys. 2009, 130, 194112
17. Zhang, C.; Ma, J. Enhanced Sampling and Applications in Protein Folding in Explicit Solvent J. Chem. Phys. 2010, 132, 244101
18. Freddolino, P. L.; Park, S.; Roux, B.; Schulten, K. Force Field Bias in Protein Folding Simulations Biophys. J. 2009, 96, 3772-3780
19. Rajan, A.; Freddolino, P. L.; Schulten, K. Going Beyond Clustering in MD Trajectory Analysis: an Application to Villin Headpiece Folding PLoS One 2010, 5:e9890, 12
20. Piana, S.; Sarkar, K.; Lindorff-Larsen, K.; Guo, M.; Gruebele, M.; Shaw, D. E. Computational Design and Experimental Testing of the Fastest-Folding β-Sheet Protein J. Mol. Biol. 2011, 405, 43-48
21. Huang, G. S.; Oas, T. G. Submillisecond Folding of Monomeric γ Repressor Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 6878-6882
22. Yang, W. Y.; Gruebele, M. Folding at the Speed Limit Nature 2003, 423, 193-197
23. Liu, F.; Gao, Y. G.; Gruebele, M. A Survey of lambda Repressor Fragments from Two-State to Downhill Folding J. Mol. Biol. 2010, 397, 789-798
24. Portman, J. J.; Takada, S.; Wolynes, P. G. Microscopic Theory of Protein Folding Rates. II. Local Reaction Coordinates and Chain Dynamics J. Chem. Phys. 2001, 114, 5082-5096
25. Portman, J. J.; Takada, S.; Wolynes, P. G. Microscopic Theory of Protein Folding Rates. I. Fine Structure of the Free Energy Profile and Folding Routes from a Variational Approach J. Chem. Phys. 2001, 114, 5069-5081
26. Pogorelov, T. V.; Luthey-Schulten, Z. Variations in the Fast Folding Rates of the γ-Repressor: a Hybrid Molecular Dynamics Study Biophys. J. 2004, 87, 207-214
27. Allen, L. R.; Krivov, S. V.; Paci, E. Analysis of the Free-Energy Surface of Proteins from Reversible Folding Simulations PLoS Comput. Biol. 2009, 5, e1000428
28. 6-85 Structure with Kinetics and Thermodynamics Chem. Phys. 2006, 323, 45-53
29. 6-85 J. Am. Chem. Soc. 2011, 133, 664-667
30. 6-85 J. Am. Chem. Soc. 2011, 133, 19338-19341
31. 6-85 Towards Downhill Folding at its Melting Temperature J. Mol. Biol. 2007, 370, 574-584
32. Mackerell, A. D. Empirical Force Fields for Biological Macromolecules: Overview and Issues J. Comput. Chem. 2004, 25, 1584-1604
33. MacKerell, A. D., Jr.; Bashford, D.; Bellott, M.; Dunbrack, R. L., Jr.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
34. Buck, M.; Bouguet-Bonnet, S.; Pastor, R. W.; MacKerell, A. D. Importance of the CMAP Correction to the CHARMM22 Protein Force Field: Dynamics of Hen Lysozyme Biophys. J. 2006, 90, L36-38
35. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935
36. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
37. 6-85 Protein Proc. Natl. Acad. Sci. U.S.A. 2005, 71, 2283-2287
38. Vega, C.; Abascal, J. L. F.; Conde, M. M.; Aragones, J. L. What Ice Can Teach Us About Water Interactions: a Critical Comparison of the Performance of Different Water Models Faraday Discuss. 2009, 141, 251-276
39. Florová, P.; Sklenovský, P.; Banáš, P.; Otyepka, M. Explicit Water Models Affect the Specific Solvation and Dynamics of Unfolded Peptides While the Conformational Behavior and Flexibility of Folded Peptides Remain Intact J. Chem. Theor. Comput. 2010, 6, 3569-3579
40. 6-85 Protein Sci. 2006, 15, 2596-2604
41. Camacho, C. J.; Thirumalai, D. Minimum Energy Compact Structures of Random Sequences of Heteropolymers Phys. Rev. Lett. 1993, 71, 2505-2508
42. Garcia-Manyes, S.; Dougan, L.; Badilla, C. L.; Brujic, J.; Fernandez, J. Direct Observation of an Ensemble of Stable Collapsed States in the Mechanical Folding of Ubiquitin Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 10534-10539
43. Dougan, L.; Li, J.; Badilla, C. L.; Berne, B. J.; Fernandeza, J. M. Single Homopolypeptide Chains Collapse into Mechanically Rigid Conformations Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 12605-12610
44. Prigozhin, M. B.; Sarkar, K.; Law, D.; Swope, W. C.; Gruebele, M.; Pitera, J. Reducing γ Repressor to the Core J. Phys. Chem. B 2011, 115, 2090-2096
45. Shaw, D. E.; Deneroff, M. M.; Dror, R. O.; Kuskin, J. S.; Larson, R. H.; Salmon, J. K.; Young, C.; Batson, B.; Bowers, K. J.; Chao, J. C. Anton, a Special-Purpose Machine for Molecular Dynamics Simulation Commun. ACM 2008, 51, 91-97
46. Humphrey, W.; Dalke, A.; Schulten, K. VMD - Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38