Two-stage Folding of HP-35 from Ab Initio Simulations

Journal of Molecular Biology

Volumn 370, Issue 1, 2007, Pages 196-206

  Lei, Hongxing ^a   Duan, Yong ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AMBER FF03; generalized Born; molecular dynamics; protein folding; villin headpiece

Indexed keywords

PROTEIN; PROTEIN HP 35; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; ARTICLE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN FOLDING; SIMULATION; SOLVATION;

EID: 34249298006     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.04.040     Document Type: Article

References (73)

1. Onuchic J.N., Luthey-Schulten Z., and Wolynes P.G. Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem. 48 (1997) 545-600
2. Onuchic J.N., and Wolynes P.G. Theory of protein folding. Curr. Opin. Struct. Biol. 14 (2004) 70-75
3. Dill K.A., and Chan H.S. From Levinthal to pathways to funnels. Nature Struct. Biol. 4 (1997) 10-19
4. Skolnick J. Putting the pathway back into protein folding. Proc. Natl Acad. Sci. USA 102 (2005) 2265-2266
5. Liwo A., Khalili M., and Scheraga H.A. Ab initio simulations of protein-folding pathways by molecular dynamics with the united-residue model of polypeptide chains. Proc. Natl Acad. Sci. USA 102 (2005) 2362-2367
6. Simmerling C., Strockbine B., and Roitberg A.E. All-atom structure prediction and folding simulations of a stable protein. J. Am. Chem. Soc. 124 (2002) 11258-11259
7. Chowdhury S., Lee M.C., Xiong G., and Duan Y. Ab initio folding simulation of the Trp-cage mini-protein approaches NMR resolution. J. Mol. Biol. 327 (2003) 711-717
8. Pitera J.W., and Swope W. Understanding folding and design: replica-exchange simulations of "Trp-cage" miniproteins. Proc. Natl Acad. Sci. USA 100 (2003) 7587-7592
9. Zhou R. Trp-cage: folding free energy landscape in explicit water. Proc. Natl Acad. Sci. USA 100 (2003) 13280-13285
10. Snow C.D., Zagrovic B., and Pande V.S. The Trp cage: folding kinetics and unfolded state topology via molecular dynamics simulations. J. Am. Chem. Soc. 124 (2002) 14548-14549
11. Schug A., Herges T., and Wenzel W. Reproducible protein folding with the stochastic tunneling method. Phys. Rev. Letters 91 (2003) 158102
12. Carnevali P., Toth G., Toubassi G., and Meshkat S.N. Fast protein structure prediction using Monte Carlo simulations with modal moves. J. Am. Chem. Soc. 125 (2003) 14244-14245
13. Vila J.A., Ripoll D.R., and Scheraga H.A. Atomically detailed folding simulation of the B domain of staphylococcal protein A from random structures. Proc. Natl Acad. Sci. USA 100 (2003) 14812-14816
14. Khalili M., Liwo A., and Scheraga H.A. Kinetic studies of folding of the B-domain of staphylococcal protein A with molecular dynamics and a united-residue (UNRES) model of polypeptide chains. J. Mol. Biol. 355 (2006) 536-547
15. Snow C.D., Nguyen H., Pande V.S., and Gruebele M. Absolute comparison of simulated and experimental protein-folding dynamics. Nature 420 (2002) 102-106
16. Jang S., Kim E., and Pak Y. Free energy surfaces of miniproteins with a bba motif: replica exchange molecular dynamics simulation with an implicit solvation model. Proteins: Struct. Funct. Genet. 62 (2006) 663-671
17. Jang S., Kim E., Shin S., and Pak Y. Ab initio folding of helix bundle proteins using molecular dynamics simulations. J. Am. Chem. Soc. 125 (2003) 14841-14846
18. Berendsen H.J. A glimpse of the Holy Grail?. Science 282 (1998) 642-643
19. McKnight C.J., Doering D.S., Matsudaira P.T., and Kim P.S. A thermostable 35-residue subdomain within villin headpiece. J. Mol. Biol. 260 (1996) 126-134
20. McKnight C.J., Matsudaira P.T., and Kim P.S. NMR structure of the 35-residue villin headpiece subdomain. Nature Struct. Biol. 4 (1997) 180-184
21. Meng J., Vardar D., Wang Y., Guo H.C., Head J.F., and McKnight C.J. High-resolution crystal structures of villin headpiece and mutants with reduced F-actin binding activity. Biochemistry 44 (2005) 11963-11973
22. 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
23. Lee M.R., Duan Y., and Kollman P.A. Use of MM-PB/SA in estimating the free energies of proteins: application to native, intermediates, and unfolded villin headpiece. Proteins: Struct. Funct. Genet. 39 (2000) 309-316
24. Kubelka J., Eaton W.A., and Hofrichter J. Experimental tests of villin subdomain folding simulations. J. Mol. Biol. 329 (2003) 625-630
25. Tang Y., 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
26. Wang M., Tang Y., Sato S., Vugmeyster L., McKnight C.J., and Raleigh D.P. 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
27. Brewer S.H., Vu D.M., Tang Y., Li Y., Franzen S., Raleigh D.P., and Dyer R.B. Effect of modulating unfolded state structure on the folding kinetics of the villin headpiece subdomain. Proc. Natl Acad. Sci. USA 102 (2005) 16662-16667
28. Havlin R.H., and Tycko R. Probing site-specific conformational distributions in protein folding with solid-state NMR. Proc. Natl Acad. Sci. USA 102 (2005) 3284-3289
29. Herges T., and Wenzel W. Free-energy landscape of the villin headpiece in an all-atom force field. Structure 13 (2005) 661-668
30. Srinivasan R., Fleming P.J., and Rose G.D. Ab initio protein folding using LINUS. Methods Enzymol. 383 (2004) 48-66
31. Ripoll D.R., Vila J.A., and Scheraga H.A. Folding of the villin headpiece subdomain from random structures. Analysis of the charge distribution as a function of pH. J. Mol. Biol. 339 (2004) 915-925
32. Lin C.Y., Hu C.K., and Hansmann U.H. Parallel tempering simulations of HP-36. Proteins: Struct. Funct. Genet. 52 (2003) 436-445
33. 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
34. Duan Y., Wang L., and Kollman P.A. The early stage of folding of villin headpiece subdomain observed in a 200-nanosecond fully solvated molecular dynamics simulation. Proc. Natl Acad. Sci. USA 95 (1998) 9897-9902
35. 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
36. Shen M.Y., and Freed K.F. All-atom fast protein folding simulations: the villin headpiece. Proteins: Struct. Funct. Genet. 49 (2002) 439-445
37. Zagrovic B., and Pande V.S. Simulated unfolded-state ensemble and the experimental NMR structures of villin headpiece yield similar wide-angle solution X-ray scattering profiles. J. Am. Chem. Soc. 128 (2006) 11742-11743
38. Jayachandran G., Vishal V., Garcia A.E., and Pande V.S. Local structure formation in simulations of two small proteins. J. Struct. Biol. 157 (2007) 491-499
39. Colubri A., Jha A.K., Shen M.Y., Sali A., Berry R.S., Sosnick T.R., and Freed K.F. Minimalist representations nearest neighbor effects in and the importance of protein folding simulations. J. Mol. Biol. 363 (2006) 535-557
40. Bandyopadhyay S., Chakraborty S., and Bagchi B. Coupling between hydration layer dynamics and unfolding kinetics of HP-36. J. Chem. Phys. 125 (2006) 084912
41. 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) 164902
42. Lei H., Wu C., Liu H., and Duan Y. Folding free-energy landscape of villin headpiece subdomain from molecular dynamics simulations. Proc. Natl Acad. Sci. USA 104 (2007) 4925-4930
43. Karplus M., and Weaver D.L. Protein-folding dynamics- the diffusion-collision model and experimental-data. Protein Sci. 3 (1994) 650-668
44. Baldwin R.L. Intermediates in protein folding reactions and mechanism of protein folding. Annu. Rev. Biochem. 44 (1975) 453-475
45. Fersht A.R. Optimization of rates of protein folding: the nucleation-condensation mechanism and its implications. Proc. Natl Acad. Sci. USA 92 (1995) 10869-10873
46. 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
47. Vermeulen W., Troys M.V., Bourry D., Dewitte D., Rossenu S., Goethals M., et al. Identification of the PXW Sequence as a Structural Gatekeeper of the Headpiece C-terminal Subdomain Fold. J. Mol. Biol. 359 (2006) 1277-1292
48. Plaxco K.W., Simons K.T., and Baker D. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277 (1998) 985-994
49. Weikl T.R., and Dill K.A. Folding rates and low-entropy-loss routes of two-state proteins. J. Mol. Biol. 329 (2003) 585-598
50. Jewett A.I., Pande V.S., and Plaxco K.W. Cooperativity, smooth energy landscapes and the origins of topology-dependent protein folding rates. J. Mol. Biol. 326 (2003) 247-253
51. Fernandez A., Shen M.Y., Colubri A., Sosnick T.R., Berry R.S., and Freed K.F. Large-scale context in protein folding: villin headpiece. Biochemistry 42 (2003) 664-671
52. Nymeyer H., and Garcia A.E. Simulation of the folding equilibrium of alpha-helical peptides: a comparison of the generalized born approximation with explicit solvent. Proc. Natl Acad. Sci. USA 100 (2003) 13934-13939
53. Zhou R., and Berne B.J. Can a continuum solvent model reproduce the free energy landscape of a beta-hairpin folding in water?. Proc. Natl Acad. Sci. USA 99 (2002) 12777-12782
54. Chowdhury S., Lei H., and Duan Y. Denatured-state ensemble and the early-stage folding of the G29A mutant of the B-domain of protein A. J. Phys. Chem. B 109 (2005) 9073-9081
55. Lei H., Dastidar S.G., and Duan Y. Folding transition-state and denatured-state ensembles of FSD-1 from folding and unfolding simulations. J. Phys. Chem. 110 (2006) 22001-22008
56. Lei H., and Duan Y. The role of plastic beta-hairpin and weak hydrophobic core in the stability and unfolding of a full sequence design protein. J. Chem. Phys. 121 (2004) 12104-12111
57. Lei H., Wu C., Wang Z., and Duan Y. Molecular dynamics simulations and free energy analyses on the dimer formation of an amyloidogenic heptapeptide from human beta2-microglobulin: implication for the protofibril structure. J. Mol. Biol. 356 (2006) 1049-1063
58. Ponder J.W., and Case D.A. Force fields for protein simulations. Advan. Protein Chem: Protein Sim. 66 (2003) 27-85
59. Duan Y., Wu C., Chowdhury S., Lee M.C., Xiong G., Zhang W., et al. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24 (2003) 1999-2012
60. Roe D.R., Hornak V., and Simmerling C. Folding cooperativity in a three-stranded beta-sheet model. J. Mol. Biol. 352 (2005) 370-381
61. Maple J.R., Cao Y.X., Damm W.G., Halgren T.A., Kaminski G.A., Zhang L.Y., and Friesner R.A. A polarizable force field and continuum solvation methodology for modeling of protein-ligand interactions. J. Chem. Theory Comput. 1 (2005) 694-715
62. Kaminski G.A., Friesner R.A., Tirado-Rives J., and Jorgensen W.L. Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J. Phys. Chem. B 105 (2001) 6474-6487
63. Kaminski G.A., Stern H.A., Berne B.J., Friesner R.A., Cao Y.X.X., Murphy R.B., et al. Development of a polarizable force field for proteins via ab initio quantum chemistry: first generation model and gas phase tests. J. Comput. Chem. 23 (2002) 1515-1531
64. Anisimov V.M., Lamoureux G., Vorobyov I.V., Huang N., Roux B., and MacKerell A.D. Determination of electrostatic parameters for a polarizable force field based on the classical Drude oscillator. J. Chem. Theory Comput. 1 (2005) 153-168
65. MacKerell A.D., Feig M., and Brooks C.L. Improved treatment of the protein backbone in empirical force fields. J. Am. Chem. Soc. 126 (2004) 698-699
66. Grossfield A., Ren P.Y., and Ponder J.W. Ion solvation thermodynamics from simulation with a polarizable force field. J. Am. Chem. Soc. 125 (2003) 15671-15682
67. Ren P.Y., and Ponder J.W. Temperature and pressure dependence of the AMOEBA water model. J. Phys. Chem. B 108 (2004) 13427-13437
68. Oostenbrink C., Villa A., Mark A.E., and van Gunsteren W.F. A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J. Comput. Chem. 25 (2004) 1656-1676
69. Bashford D., and Case D.A. Generalized born models of macromolecular solvation effects. Annu. Rev. Phys. Chem. 51 (2000) 129-152
70. Rizzo R.C., Aynechi T., Case D.A., and Kuntz I.D. Estimation of absolute free energies of hydration using continuum methods: accuracy of partial, charge models and optimization of nonpolar contributions. J. Chem. Theory Comput. 2 (2006) 128-139
71. Case D.A., Cheatham T.E., Darden T., Gohlke H., Luo R., Merz K.M., et al. The Amber biomolecular simulation programs. J. Comput. Chem. 26 (2005) 1668-1688
72. Onufriev A., Case D.A., and Bashford D. Effective Born radii in the generalized Born approximation: the importance of being perfect. J. Comput. Chem. 23 (2002) 1297-1304
73. Onufriev A., Bashford D., and Case D.A. Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins: Struct. Funct. Genet. 55 (2004) 383-394