Heterogeneity Even at the Speed Limit of Folding: Large-scale Molecular Dynamics Study of a Fast-folding Variant of the Villin Headpiece

Journal of Molecular Biology

Volumn 374, Issue 3, 2007, Pages 806-816

  Ensign, Daniel L ^a   Kasson, Peter M ^a   Pande, Vijay S ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

distributed computing; laser temperature jump; molecular dynamics; protein folding; villin headpiece

Indexed keywords

HISTIDINE; PHENYLALANINE; TRYPTOPHAN; VILLIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CHEMICAL REACTION KINETICS; HYDROPHOBICITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROBABILITY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE;

EID: 35648943228     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.09.069     Document Type: Article

References (53)

1. Arora P., Oas T.G., and Myers J.K. Fast and faster: a designed variant of the B-domain of protein A folds in 3 μs. Protein Sci. 13 (2004) 847-853
2. Chiu T.K., Kubelka J., Herbst-Irmer R., Eaton W.A., Hofrichter J., and Davies D.R. High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein. Proc. Natl Acad. Sci. USA 102 (2005) 7517-7522
3. Nguyen H., Jäger M., Kelly J.W., and Gruebele M. Engineering a β-sheet protein toward the folding speed limit. J. Phys. Chem. ser. B 109 (2005) 15182-15186
4. Snow C.D., Nguyen N., Pande V.S., and Gruebele M. Absolute comparison of simulated and experimental protein-folding dynamics. Nature 420 (2002) 102-106
5. Xu Y., Purkayastha P., and Gai F. Nanosecond folding dynamics of a three-stranded β-sheet. J. Amer. Chem. l Soc. 128 (2006) 15836-15842
6. Yang W.Y., and Gruebele M. Folding at the speed limit. Nature 423 (2003) 193-197
7. 6-85 folding. Biochemistry 43 (2004) 13018-13025
8. Yang W.Y., and Gruebele M. Folding λ-repressor at its speed limit. Biophys. J. 87 (2004) 596-608
9. Zhu Y.J., Fu X.R., Wang T., Tamura A., Takada S., Savan J.G., and Gai F. Guiding the search for a protein's maximum rate of folding. Chem. Phys. 307 (2004) 99-109
10. Faccioli P., Sega M., Pederiva F., and Orland H. Dominant pathways in protein folding. Physical Rev. Letters 97 (2006) Art. No. 108101
11. Jayachandran G., Vishal V., and Pande V.S. Using massively parallel simulation and Markovian models to study protein folding: examining the dynamics of the villin headpiece. J. Chem. Phys. 124 (2006) Art. No. 164902
12. Shen M.Y., and Freed K.F. All-atom fast protein folding simulations: the villin headpiece. Proteins:Struct. Funct. Genet. 49 (2002) 439-445
13. Zagrovic B., and Pande V. Solvent viscosity dependence of the folding rate of a small protein: distributed computing study. J. Computat. Chem. 24 (2003) 1432-1436
14. Zagrovic B., Snow C.D., Khaliq S., Shirts M.R., and Pande V.S. Native-like mean structure in the unfolded ensemble of small proteins. J. Mol. Biol. 323 (2002) 153-164
15. Zagrovic B., Snow C.D., Shirts M.R., and Pande V.S. Simulation of folding of a small alpha-helical protein in atomistic detail using worldwide-distributed computing. J. Mol. Biol. 323 (2002) 927-937
16. Lei H.X., and Duan Y. Two-stage folding of HP-35 from ab initio simulations. J. Mol. Biol. 370 (2007) 196-206
17. Lei H.X., Wu C., Liu H.G., and Duan Y. Folding free-energy landscape of villin headpiece subdomain from molecular dynamics simulations. Proc. Natl Acad. Sci. USA 104 (2007) 4925-4930
18. Eaton W.A. Searching for "downhill scenarios" in protein folding. Proc. Natl Acad. Sci. USA 96 (1999) 5897-5899
19. Garcia-Mira M.M., Sadqi M., Fischer N., Sanchez-Ruiz J.M., and Munoz V. Experimental identification of downhill protein folding. Science 298 (2002) 2191-2195
20. Duan Y., and Kollman P.A. Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution. Science 282 (1998) 740-744
21. Rhee Y.M., Sorin E.J., Jayachandran G., Lindahl E., and Pande V.S. Simulations of the role of water in the protein-folding mechanism. Proc. Natl Acad. Sci. USA 101 (2004) 6456-6461
22. Snow C.D., Sorin E.J., Rhee Y.M., and Pande V.S. How well can simulation predict protein folding kinetics and thermodynamics? Annu. Rev. Biophys. Biomol. Struct. 34 (2005) 43-69
23. Kubelka J., Chiu T.K., Davies D.R., Eaton W.A., and Hofrichter J. Sub-microsecond protein folding. J. Mol. Biol. 359 (2006) 546-553
24. Shirts M., and Pande V.S. Computing - Screen savers of the world unite!. Science 290 (2000) 1903-1904
25. Berendsen H.J.C., Vanderspoel D., and Vandrunen R. Gromacs - a message-passing parallel molecular-dynamics implementation. Comput. Phys. Commun. 91 (1995) 43-56
26. Lindahl E., Hess B., and van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7 (2001) 306-317
27. Chodera J.D., Singhal N., Pande V.S., Dill K.A., and Swope W.C. Automatic discovery of metastable states for the construction of Markov moldes of macromolecular conformational dynamics. J. Chem. Phys. 126 (2007) 155101-155117
28. Chodera J.D., Swope W.C., Pitera J.W., and Dill K.A. Long-time protein folding dynamics from short-time molecular dynamics simulations. Multiscale Model. Simulat. 5 (2006) 1214-1226
29. Park S., and Pande V.S. Validation of Markov state models using Shannon's entropy. J. Chem. Phys. 124 (2006) Art. No. 054118
30. Singhal N., and Pande V.S. Error analysis and efficient sampling in Markovian state models for molecular dynamics. J. Chem. Phys. 123 (2005) Art. No. 204909
31. Swope W.C., Pitera J.W., and Suits F. Describing protein folding kinetics by molecular dynamics simulations. 1. Theory. J. Phys. Chem. ser. B 108 (2004) 6571-6581
32. Swope W.C., Pitera J.W., Suits F., Pitman M., Eleftheriou M., Fitch B.G., et al. Describing protein folding kinetics by molecular dynamics simulations. 2. Example applications to alanine dipeptide and beta-hairpin peptide. J. Phys. Chem. ser. B 108 (2004) 6582-6594
33. Mahoney M.W., and Jorgensen W.L. Diffusion constant of the TIP5P model of liquid water. J. Chem. Phys. 114 (2001) 363-366
34. Shen M.Y., and Freed K.F. Long time dynamics of met-enkephalin: comparison of explicit and implicit solvent models. Biophys. J. 82 (2002) 1791-1808
35. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., and Klein M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79 (1983) 926-935
36. Cover T.M., and Thomas J.A. Elements of Information Theory (1991), John Wiley & Sons, New York
37. Schenker N., and Gentleman J.F. On judging the significance of differences by examining the overlap between confidence intervals. Amer. Statist. 55 (2001) 182-186
38. Kubelka J., Eaton W.A., and Hofrichter J. Experimental tests of villin subdomain folding simulations. J. Mol. Biol. 329 (2003) 625-630
39. Wickstrom L., Okur A., Song K., Hornak V., Raleigh D.P., and Simmerling C.L. The unfolded state of the villin headpiece helical subdomain: computational studies of the role of locally stabilized structure. J. Mol. Biol. 360 (2006) 1094-1107
40. Tang Y.F., Rigotti D.J., Fairman R., and Raleigh D.P. Peptide models provide evidence for significant structure in the denatured state of a rapidly folding protein: the villin headpiece subdomain. Biochemistry 43 (2004) 3264-3272
41. Mayor U., Grossmann J.G., Foster N.W., Freund S. M.V., and Fersht A.R. The denatured state of engrailed homeodomain under denaturing and native conditions. J. Mol. Biol. 333 (2003) 977-991
42. Religa T.L., Markson J.S., Mayor U., Freund S.M.V., and Fersht A.R. Solution structure of a protein denatured state and folding intermediate. Nature 437 (2005) 1053-1056
43. Frank B.S., Vardar D., Buckley D.A., and McKnight C. J. The role of aromatic residues in the hydrophobic core of the villin headpiece subdomain. Protein Sci. 11 (2002) 680-687
44. Wang J.M., Cieplak P., and Kollman P.A. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules?. J. Comput. Chem. 21 (2000) 1049-1074
45. Tatsumi R., Fukunishi Y., and Nakamura H. A hybrid method of molecular dynamics and harmonic dynamics for docking of flexible ligand to flexible receptor. J. Computat. Chem. 25 (2004) 1995-2005
46. Ryckaert J.P., Ciccotti G., and Berendsen H.J.C. Numerical-integration of Cartesian equations of motion of a system with constraints - molecular-dynamics of N-alkanes. J. Computat. Phys. 23 (1977) 327-341
47. Miyamoto S., and Kollman P.A. Settle - an analytical version of the shake and rattle algorithm for rigid water models. J. Computat. Chem. 13 (1992) 952-962
48. Hoover W.G. Canonical dynamics - equilibrium phase-space distributions. Phys. Rev. A 31 (1985) 1695-1697
49. Nose S., and Klein M.L. Constant pressure molecular-dynamics for molecular-systems. Mol. Phys. 50 (1983) 1055-1076
50. Nose S. A molecular-dynamics method for simulations in the canonical ensemble. Mol. Phys. 52 (1984) 255-268
51. Parrinello M., and Rahman A. Polymorphic transitions in single-crystals - a new molecular-dynamics method. J. Appl. Phys. 52 (1981) 7182-7190
52. Pande V.S., Baker I., Chapman J., Elmer S.P., Khaliq S., Larson S.M., et al. Atomistic protein simulations on the submillisecond time scale using worldwide distributed computing. Biopolymers 68 (2002) 91-109
53. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 14 (1996) 33-38