Force field bias in protein folding simulations

Biophysical Journal

Volumn 96, Issue 9, 2009, Pages 3772-3780

  Freddolino, Peter L ^a   Park, Sanghyun ^b   Roux, Benoît ^c   Schulten, Klaus ^a  

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

^b ARGONNE NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONFORMATIONAL TRANSITION; ENERGY; FORCE; HUMAN; MOLECULAR DYNAMICS; PROTEIN FOLDING; SIMULATION; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; COMPUTER SIMULATION; PROTEIN SECONDARY STRUCTURE; TIME;

NIMA INTERACTING PEPTIDYLPROLYL ISOMERASE; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; PEPTIDYLPROLYL ISOMERASE;

COMPUTER SIMULATION; HUMANS; MODELS, MOLECULAR; PEPTIDYLPROLYL ISOMERASE; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SOFTWARE; TIME FACTORS;

EID: 67650359927     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.02.033     Document Type: Article

References (59)

1. Onuchic, J. N., and P. G. Wolynes. 2004. Theory of protein folding. Curr. Opin. Struct. Biol. 14:70-75.
2. Lei, H., and Y. Duan. 2007. Ab initio folding of albumin binding domain from all-atom molecular dynamics simulation. J. Phys. Chem. B. 111:5458-5463.
3. Duan, Y., and P. Kollman. 1998. Pathways to a protein folding intermediate observed in a 1 microsecond simulation in aqueous solution. Science. 282:740-744.
4. Simmerling, C., B. Strockbine, and A. E. Roitberg. 2002. All-atom structure prediction and folding simulations of a stable protein. J. Am. Chem. Soc. 124:11258-11259.
5. Chowdhury, S., M. C. Lee, G. Xiong, and Y. Duan. 2003. Ab initio folding simulation of the Trp-cage mini-protein approaches NMR resolution. J. Mol. Biol. 327:711-717.
6. Sanbonmatsu, K. Y., and A. E. Garca. 2002. Structure of Met-encephalin in explicit aqueous solution using replica exchange molecular dynamics. Proteins. 46:225-234.
7. Yang, W. Y., and M. Gruebele. 2004. Folding λ-repressor at its speed limit. Biophys. J. 87:596-608.
8. Kubelka, J., T. K. Chiu, D. R. Davies, W. A. Eaton, and J. Hofrichter. 2006. Sub-microsecond protein folding. J. Mol. Biol. 359:546-553.
9. Kubelka, J., J. Hofrichter, and W. A. Eaton. 2004. The protein folding "speed limit". Curr. Opin. Struct. Biol. 14:76-88.
10. Maragakis, P., K. Lindorff-Larsen, M. P. Eastwood, R. O. Dror, J. L. Klepeis, et al. 2008. Microsecond molecular dynamics simulation shows effect of slow loop dynamics on backbone amide order parameters of proteins. J. Phys. Chem. B. 112:6155-6158.
11. Ensign, D. L., P. M. Kasson, and V. S. Pande. 2007. 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. 374: 806-816.
12. Freddolino, P. L., F. Liu, M. Gruebele, and K. Schulten. 2008. Tenmicrosecond MD simulation of a fast-folding WW domain. Biophys. J. 94:L75-L77.
13. MacKerell, A. D. 2004. Empirical force fields for biological macromolecules: overview and issues. J. Comput. Chem. 25:1584-1604.
14. Wang, T., and R. Wade. 2006. Force field effects on a β-sheet protein domain structure in thermal unfolding simulations. J. Chem. Theory Comput. 2:140-148.
15. Best, R. B., N.-V. Buchete, and G. Hummer. 2008. Are current molecular dynamics force fields too helical? Biophys. J. 95:L07-L09.
16. Yoda, T., Y. Sugita, and Y. Okamoto. 2004. Secondary-structure preferences of force fields for proteins evaluated by generalized-ensemble simulations. Chem. Phys. 307:269-283.
17. Wroblewska, L., and J. Skolnick. 2007. Can a physics-based, all-atom potential find a protein's native structure among misfolded structures? I. Large scale AMBER benchmarking. J. Comput. Chem. 28:2059-2066.
18. Zhou, R. 2003. Free energy landscape of protein folding in water: explicit vs. implicit solvent. Proteins. 53:148-161.
19. Zhou, R., and B. J. Berne. 2002. Can a continuum solvent model reproduce the free energy landscape of a β-hairpin folding in water? Proc. Natl. Acad. Sci. USA. 99:12777-12782.
20. Liu, F., and M. Gruebele. 2007. Tuning λ6-85 towards downhill folding at its melting temperature. J. Mol. Biol. 370:574-584.
21. Nguyen, H., M. Jäger, J. W. Kelly, and M. Gruebele. 2005. Engineering a β-sheet protein toward the folding speed limit. J. Phys. Chem. B. 109:15182-15186.
22. Jäger, M., H. Nguyen, J. C. Crane, J. W. Kelly, and M. Gruebele. 2001. The folding mechanism of a β-sheet: the WW domain. J. Mol. Biol. 311:373-393.
23. Liu, F., D. Du, A. A. Fuller, J. E. Davoren, P. Wipf, et al. 2008. An experimental survey of the transition between two-state and downhill protein folding scenarios. Proc. Natl. Acad. Sci. USA. 105:2369-2374.
24. Cecconi, F., C. Guardiani, and R. Livi. 2006. Testing simplified proteins models of the hPin1 WW domain. Biophys. J. 91:694-704.
25. Karanicolas, J., and C. L. Brooks. 2003. Improved Gō-like models demonstrate the robustness of protein folding mechanisms to non-native interactions. J. Mol. Biol. 334:309-325.
26. Luo, Z., J. Ding, and Y. Zhou. 2007. Temperature-dependent folding pathways of Pin1 WW domain: an all-atom molecular dynamics simulation of a Gō model. Biophys. J. 93:2152-2161.
27. Park, S., A. Y. Lau, and B. Roux. 2008. Computing conformational free energy by deactivated morphing. J. Chem. Phys. 129:134102.
28. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, et al. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
29. Jäger, M., Y. Zhang, J. Bieschke, H. Nguyen, M. Dendle, et al. 2006. Structure-function-folding relationship in a WW domain. Proc. Natl. Acad. Sci. USA. 103:10648-10653.
30. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD - visual molecular dynamics. J. Mol. Graph. 14:33-38.
31. Frishman, D., and P. Argos. 1995. Knowledge-based secondary structure assignment. Proteins. 23:566-579.
32. Roberts, E., J. Eargle, D. Wright, and Z. Luthey-Schulten. 2006. Multi-Seq: unifying sequence and structure data for evolutionary analysis. BMC Bioinformatics. 7:382.
33. MacKerell, Jr., A. D., M. Feig, and C. L. Brooks, III. 2004. 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. 25:1400-1415.
34. Andersen, H. C. 1983. RATTLE: a "velocity" version of the SHAKE algorithm for molecular dynamics calculations. J. Chem. Phys. 52: 24-34.
35. Miyamoto, S., and P. A. Kollman. 1993. Absolute and relative binding free energy calculations of the interaction of biotin and its analogs with streptavidin using molecular dynamics/free energy perturbation approaches. Proteins Struct. Funct. Gen. 16:226-245.
36. van der Spoel, D., E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, et al. 2005. GROMACS: fast, flexible, and free. J. Comput. Chem. 26:1701-1718.
37. Daura, X., K. Gademann, B. Jaun, D. Seebach, W. F. van Gunsteren, et al. 1999. Peptide folding: when simulation meets experiment. Angew. Chem. Int. Ed. 38:236-240.
38. Anitescu, M., and S. Park. 2009. A linear programming approach for the least-squares protein morphing problem. Math. Program. In press.
39. Singhal, N., C. D. Snow, and V. S. Pande. 2004. Using path sampling to build better Markovian state models: predicting the folding rate and mechanism of a tryptophan zipper β-hairpin. J. Chem. Phys. 121:415-425.
40. Jayachandran, G., V. Vishal, and V. S. Pande. 2006. Using massively parallel simulation and Markovian models to study protein folding: examining the dynamics of the villin headpiece. J. Chem. Phys. 124:164902.
41. Thompson, J. B., H. G. Hansma, P. K. Hansma, and K. W. Plaxco. 2002. The backbone conformational entropy of protein folding: experimental measures from atomic force microscopy. J. Mol. Biol. 322: 645-652.
42. Lii, J.-H., and N. L. Allinger. 1998. Directional hydrogen bonding in the MM3 force field: II. J. Comput. Chem. 19:1001-1016.
43. Fabiola, F., R. Bertram, A. Korostelev, and M. S. Chapman. 2002. An improved hydrogen bond potential: impact on medium resolution protein structures. Protein Sci. 11:1415-1423.
44. Morozov, A. V., T. Kortemme, K. Tsemekhman, and D. Baker. 2004. Close agreement between the orientation dependence of hydrogen bonds observed in protein structures and quantum mechanical calculations. Proc. Natl. Acad. Sci. USA. 101:6946-6951.
45. Kortemme, T., A. V. Morozov, and D. Baker. 2003. An orientation-dependent hydrogen bonding potential improves prediction of specificity and structure for proteins and protein-protein complexes. J. Mol. Biol. 326:1239-1259.
46. Cramer, C., and D. Truhlar. 1999. Implicit solvation models: equilibria, structure, spectra, and dynamics. Chem. Rev. 99:2161-2200.
47. Lum, K., D. Chandler, and J. Weeks. 1999. Hydrophobicity at small and large length scales. J. Phys. Chem. B. 103:4570-4577.
48. Huang, D. M., and D. Chandler. 2000. Temperature and length scale dependence of hydrophobic effects and their possible implications for protein folding. Proc. Natl. Acad. Sci. USA. 97:8324-8327.
49. Wagoner, J. A., and N. A. Baker. 2006. Assessing implicit models for nonpolar mean solvation forces: the importance of dispersion and volume terms. Proc. Natl. Acad. Sci. USA. 103:8331-8336.
50. Chen, J., and C. L. Brooks. 2008. Implicit modeling of nonpolar solvation for simulating protein folding and conformational transitions. Phys. Chem. Chem. Phys. 10:471-481.
51. Tanizaki, S., J. Clifford, B. D. Connelly, and M. Feig. 2008. Conformational sampling of peptides in cellular environments. Biophys. J. 94:747-759.
52. Feig, M. 2008. Is alanine dipeptide a good model for representing the torsional preferences of protein backbones? J. Chem. Theory Comput. 4:1555-1564.
53. Harder, E., V. Anisimov, I. Vorobyov, P. Lopes, S. Noskov, et al. 2006. Atomic level anisotropy in the electrostatic modeling of lone pairs for a polarizable force field based on the classical Drude oscillator. J. Chem. Theory Comput. 2:1587-1597.
54. Weber, W., P. Hünenberger, and J. McCammon. 2000. Molecular dynamics simulations of a polyalanine octapeptide under Ewald boundary conditions: influence of artificial periodicity on peptide conformation. J. Phys. Chem. B. 104:3668-3675.
55. Hünenberger, P. H., and J. A. McCammon. 1999. Effect of artificial periodicity in simulations of biomolecules under Ewald boundary conditions: a continuum electrostatics study. Biophys. Chem. 78:69-88.
56. Kastenholz, M., and P. Hünenberger. 2004. Influence of artificial periodicity and ionic strength in molecular dynamics simulations of charged biomolecules employing lattice-sum methods. J. Phys. Chem. B. 108:774-788.
57. Shirts, M. R., and V. S. Pande. 2005. Solvation free energies of amino acid side chain analogs for common molecular mechanics water models. J. Chem. Phys. 122:134508.
58. Deng, Y., and B. Roux. 2009. Computations of standard binding free energies with molecular dynamics simulations. J. Phys. Chem. B. In press.
59. Jagielska, A., L. Wroblewska, and J. Skolnick. 2008. Protein model refinement using an optimized physics-based all-atom force field. Proc. Natl. Acad. Sci. USA. 105:8268-8273