Equilibrium kinetic network of the villin headpiece in implicit solvent

Biophysical Journal

Volumn 108, Issue 2, 2015, Pages 368-378

  Du, Weina ^a   Bolhuis, Peter G ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; SOLVENT; VILLIN; WATER;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHICKEN; KINETICS; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; CHICKENS; KINETICS; MICROFILAMENT PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SOLVENTS; WATER;

EID: 84921508588     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.11.3476     Document Type: Article

References (57)

1. C.J. McKnight, and D.S. Doering P.S. Kim A thermostable 35-residue subdomain within villin headpiece J. Mol. Biol. 260 1996 126 134
2. B.S. Frank, and D. Vardar C.J. McKnight The role of aromatic residues in the hydrophobic core of the villin headpiece subdomain Protein Sci. 11 2002 680 687
3. C.J. McKnight, P.T. Matsudaira, and P.S. Kim NMR structure of the 35-residue villin headpiece subdomain Nat. Struct. Biol. 4 1997 180 184
4. T.K. Chiu, and J. Kubelka D.R. Davies High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein Proc. Natl. Acad. Sci. USA 102 2005 7517 7522
5. J. Kubelka, W.A. Eaton, and J. Hofrichter Experimental tests of villin subdomain folding simulations J. Mol. Biol. 329 2003 625 630
6. M. Wang, and Y. Tang D.P. Raleigh Dynamic NMR line-shape analysis demonstrates that the villin headpiece subdomain folds on the microsecond time scale J. Am. Chem. Soc. 125 2003 6032 6033
7. S.H. Brewer, and D.M. Vu R.B. Dyer Effect of modulating unfolded state structure on the folding kinetics of the villin headpiece subdomain Proc. Natl. Acad. Sci. USA 102 2005 16662 16667
8. S.H. Brewer, and B. Song R.B. Dyer Residue specific resolution of protein folding dynamics using isotope-edited infrared temperature jump spectroscopy Biochemistry 46 2007 3279 3285
9. M.R. Bunagan, and J. Gao F. Gai Probing the folding transition state structure of the villin headpiece subdomain via side chain and backbone mutagenesis J. Am. Chem. Soc. 131 2009 7470 7476
10. R. Godoy-Ruiz, and E.R. Henry W.A. Eaton Estimating free-energy barrier heights for an ultrafast folding protein from calorimetric and kinetic data J. Phys. Chem. B 112 2008 5938 5949
11. A. Reiner, P. Henklein, and T. Kiefhaber An unlocking/relocking barrier in conformational fluctuations of villin headpiece subdomain Proc. Natl. Acad. Sci. USA 107 2010 4955 4960
12. B. Zagrovic, and C.D. Snow V.S. Pande Simulation of folding of a small α-helical protein in atomistic detail using worldwide-distributed computing J. Mol. Biol. 323 2002 927 937
13. P.L. Freddolino, and K. Schulten Common structural transitions in explicit-solvent simulations of villin headpiece folding Biophys. J. 97 2009 2338 2347
14. J.S. Yang, S. Wallin, and E.I. Shakhnovich Universality and diversity of folding mechanics for three-helix bundle proteins Proc. Natl. Acad. Sci. USA 105 2008 895 900
15. A. Fernández, and M.Y. Shen K.F. Freed Large-scale context in protein folding: villin headpiece Biochemistry 42 2003 664 671
16. S. Jang, and E. Kim Y. Pak Ab initio folding of helix bundle proteins using molecular dynamics simulations J. Am. Chem. Soc. 125 2003 14841 14846
17. H. Lei, and Y. Duan Two-stage folding of HP-35 from ab initio simulations J. Mol. Biol. 370 2007 196 206
18. H. Lei, and C. Wu Y. Duan Folding free-energy landscape of villin headpiece subdomain from molecular dynamics simulations Proc. Natl. Acad. Sci. USA 104 2007 4925 4930
19. H. Lei, and X. Deng Y. Duan The fast-folding HP35 double mutant has a substantially reduced primary folding free energy barrier J. Chem. Phys. 129 2008 155104 155107
20. Y. Duan, and P.A. Kollman Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution Science 282 1998 740 744
21. G.M. De Mori, G. Colombo, and C. Micheletti Study of the villin headpiece folding dynamics by combining coarse-grained Monte Carlo evolution and all-atom molecular dynamics Proteins 58 2005 459 471
22. J.R. Tusell, and P.R. Callis Simulations of tryptophan fluorescence dynamics during folding of the villin headpiece J. Phys. Chem. B 116 2012 2586 2594
23. K. Lindorff-Larsen, and S. Piana D.E. Shaw How fast-folding proteins fold Science 334 2011 517 520
24. J.D. Chodera, and N. Singhal W.C. Swope Automatic discovery of metastable states for the construction of Markov models of macromolecular conformational dynamics J. Chem. Phys. 126 2007 155101
25. G.R. Bowman, X. Huang, and V.S. Pande Using generalized ensemble simulations and Markov state models to identify conformational states Methods 49 2009 197 201
26. J.-H. Prinz, and H. Wu F. Noé Markov models of molecular kinetics: generation and validation J. Chem. Phys. 134 2011 174105
27. C. Dellago, and P.G. Bolhuis D. Chandler Transition path sampling and the calculation of rate constants J. Chem. Phys. 108 1998 1964 1977
28. C. Dellago, P.G. Bolhuis, and P.L. Geissler Transition path sampling Adv. Chem. Phys. 123 2002 1 84
29. W.N. Du, and P.G. Bolhuis Adaptive single replica multiple state transition interface sampling J. Chem. Phys. 139 2013 044105
30. W. Du, and P.G. Bolhuis Sampling the equilibrium kinetic network of Trp-cage in explicit solvent J. Chem. Phys. 140 2014 195102
31. E. Weinan, and E. Vanden-Eijnden Towards a theory of transition paths J. Stat. Phys. 123 2006 503 523
32. F. Noé, and C. Schütte T.R. Weikl Constructing the equilibrium ensemble of folding pathways from short off-equilibrium simulations Proc. Natl. Acad. Sci. USA 106 2009 19011 19016
33. B. Hess, and C. Kutzner E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
34. D. Van Der Spoel, and E. Lindahl H.J.C. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718
35. E. Lindahl, B. Hess, and D. van der Spoel GROMACS 3.0: A package for molecular simulation and trajectory analysis J. Mol. Model. 7 2001 306 317
36. H.J.C. Berendsen, D. van der Spoel, and R. van Drunen GROMACS: A message-passing parallel molecular dynamics implementation Comput. Phys. Commun. 91 1995 43 56
37. A.D. MacKerell, and D. Bashford M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
38. A.D. MacKerell Jr., M. Feig, and C.L. Brooks 3rd Improved treatment of the protein backbone in empirical force fields J. Am. Chem. Soc. 126 2004 698 699
39. A.D. Mackerell Jr., M. Feig, and C.L. Brooks 3rd Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415
40. R.B. Best, and J. Mittal A.D. MacKerell Jr. Inclusion of many-body effects in the additive CHARMM protein CMAP potential results in enhanced cooperativity of α-helix and β-hairpin formation Biophys. J. 103 2012 1045 1051
41. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28
42. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity rescaling J. Chem. Phys. 126 2007 014101
43. B. Hess, and H. Bekker J.G.E.M. Fraaije LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472
44. W.C. Still, and A. Tempczyk T. Hendrickson Semianalytical treatment of solvation for molecular mechanics and dynamics J. Am. Chem. Soc. 112 1990 6127 6129
45. M. Scarsi, J. Apostolakis, and A. Caflisch Continuum electrostatic energies of macromolecules in aqueous solutions J. Phys. Chem. A 101 1997 8098 8106
46. A. Ghosh, C.S. Rapp, and R.A. Friesner Generalized Born model based on a surface integral formulation J. Phys. Chem. B 102 1997 10983 10990
47. M.S. Lee, J.F.R. Salsbury, and I.C.L. Brooks Novel generalized Born methods J. Chem. Phys. 116 2002 10606 10614
48. M.S. Lee, and M. Feig C.L. Brooks 3rd New analytic approximation to the standard molecular volume definition and its application to generalized Born calculations J. Comput. Chem. 24 2003 1348 1356
49. W. Im, M.S. Lee, and C.L. Brooks 3rd Generalized Born model with a simple smoothing function J. Comput. Chem. 24 2003 1691 1702
50. B.K. Ho, and K.A. Dill Folding very short peptides using molecular dynamics PLOS Comput. Biol. 2 2006 e27
51. R. Zhou Free energy landscape of protein folding in water: explicit vs. implicit solvent Proteins 53 2003 148 161
52. T. Gonzalez Clustering to minimize the maximum intercluster distance Theor. Comput. Sci. 38 1985 293 306
53. S. Dasgupta, and P.M. Long Performance guarantees for hierarchical clustering J. Comput. Syst. Sci. 70 2005 555 569
54. P.G. Bolhuis Transtion path sampling on diffusive barriers J. Phys. Condens. Matter 15 2003 S113 S120
55. T.S. van Erp Reaction rate calculation by parallel path swapping Phys. Rev. Lett. 98 2007 268301
56. P.G. Bolhuis Rare events via multiple reaction channels sampled by path replica exchange J. Chem. Phys. 129 2008 114108
57. W.-N. Du, K.A. Marino, and P.G. Bolhuis Multiple state transition interface sampling of alanine dipeptide in explicit solvent J. Chem. Phys. 135 2011 145102