Exploring the helix-coil transition via all-atom equilibrium ensemble simulations

Biophysical Journal

Volumn 88, Issue 4, 2005, Pages 2472-2493

  Sorin, Eric J ^a   Pande, Vijay S ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE;

ALPHA HELIX; ARTICLE; ATOM; DIFFUSION; ENTROPY; KINETICS; MOLECULAR SIZE; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; SIMULATION; THERMODYNAMICS;

EID: 20544435097     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.051938     Document Type: Article

References (76)

1. 10-, and π-helix in helix-coil transitions. Protein Sci. 12:1145-1157.
2. Banavar, J. R., A. Maritan, C. Micheletti, and A. Trovato. 2002. Geometry and physics of proteins. Proteins. 47:315-322.
3. Berendsen, H., J. Postma, W. Vangunsteren, A. Dinola, and J. Haak. 1984. Molecular-dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
4. Bolhuis, P. G., C. Dellago, and D. Chandler. 2000. Reaction coordinates of biomolecular isomerization. Proc. Natl. Acad. Sci. USA. 97:5877-5882.
5. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy, minimisation, and dynamics calculations. J. Comput. Chem. 4:187-217.
6. Chowdhury, S., W. Zhang, C. Wu, G. Xiong, and Y. Duan. 2003. Breaking non-native hydrophobic clusters is the rate-limiting step in the folding of an alanine-based peptide. Biopolymers. 68:63-75.
7. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117:5179-5197.
8. Daggett, V., and A. Fersht. 2003. The present view of the mechanism of protein folding. Nat. Rev. Mol. Cell Biol. 4:497-502.
9. Drozdov, A. N., A. Grossfield, and R. V. Pappu. 2003. Role of solvent in determining conformational preferences of alanine dipeptide in water. J. Am. Chem. Soc. 126:2574-2581.
10. Du, R., V. S. Pande, A. Y. Grosberg, T. Tanaka, and E. S. Shakhnovich. 1998. On the transition coordinate for protein folding. J. Chem. Phys. 108:334-350.
11. Duan, Y., C. Wu, S. Chowdhury, M. C. Lee, G. Xiong, W. Zhang, R. Yang, P. Cieplak, R. Luo, T. Lee, J. Caldwell, J. Wang, and P. Kollman. 2003. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24:1999-2012.
12. Elmer, S. P., and V. S. Pande. 2004. Simulations of self-assembling nanopolymers: novel computational methods and applications to polyphenylacetylene oligomers. J. Chem. Phys. 121:12760-12771.
13. Feig, M., A. D. MacKerell, Jr., and C. L. Brooks. 2003. Force field influence on the observation of pi-helical protein structures in molecular dynamics simulations. J. Phys. Chem. B. 107:2831-2836.
14. Ferrara, P., J. Apostolakis, and A. Caflisch. 2000. Thermodynamics and kinetics of folding of two model peptides investigated by molecular dynamics simulations. J. Phys. Chem. B. 104:5000-5010.
15. Garcia, A. E. 2004. Characterization of non-alpha helical conformations in Ala peptides. Polym. 45:669-676.
16. Garcia, A. E., and K. Y. Sanbonmatsu. 2001. α-Helical stabilization by side chain shielding of backbone hydrogen bonds. Proc. Natl. Acad. Sci. USA. 99:2782-2787.
17. Geissler, P. L., C. Dellago, and D. Chandler. 1999. Kinetic pathways of ion pair dissociation in water. J. Phys. Chem. B. 103:3706-3710.
18. Hastie, T., R. Tibshirani, and J. H. Friedman. 2001. The Elements of Statistical Learning: Data Mining, Inference, and Prediction, with 200 Full-Color Illustrations. Springer, New York.
19. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
20. 6. J. Phys. Chem. B. 104:10080-10086.
21. Horn, H. W., W. C. Swope, J. W. Pilera, J. D. Madura, T. J. Dick, G. L. Hura, and T. Head-Gordon. 2004. Development of an improved four-site water model for biomolecular simulations: TIP4P-Ew. J. Chem. Phys. 120:9665-9678.
22. Hummer, G., A. E. Garcia, and S. Garde. 2000. Conformational diffusion and helix formation kinetics. Phys. Rev. Lett. 85:2637-2640.
23. Hummer, G., A. E. Garcia, and S. Garde. 2001. Helix nucleation kinetics from molecular simulations in explicit solvent. Proteins. 42:77-84.
24. Huang, C.-Y., Z. Getahun, Y. Zhu, J. W. Klemke, W. F. DeGrado, and F. Gai. 2002. Helix formation via conformation diffusion search. Proc. Natl. Acad. Sci. USA. 99:2788-2793.
25. Huang, C.-Y., J. W. Klemke, Z. Getahun, W. F. DeGrado, and F. Gai. 2001. Temperature-dependent helix-coil transition of an alanine based peptide. J. Am. Chem. Soc. 123:9235-9238.
26. Ianoul, A., A. Mikhonin, I. K. Lednev, and S. A. Asher. 2002. UV resonance Raman study of the spatial dependence of α-helix unfolding. J. Phys. Chem. A. 106:3621-3624.
27. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
28. Jorgensen, W. L., and J. Tirado-Rives. 1988. The OPLS potential functions for proteins, energy minimization for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1657-1666.
29. Kabsch, W., and C. Sander. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:2577-2637.
30. Kentsis, A., M. Mezei, T. Gindin, and R. Osman. 2004. Unfolded state of polyalanine is a segmented polyproline II helix. Proteins. 55:493-501.
31. Kimura, T., S. Takahashi, S. Akiyama, T. Uzawa, K. Ishimori, and I. Morishima. 2002. Direct observation of the multistep helix formation of poly-L-glutamic acids. J. Am. Chem. Soc. 124:11596-11597.
32. Kollman, P., R. Dixon, W. Cornell, T. Fox, C. Chipot, and A. Pohorille. 1997. The development/application of a "minimalist" organic/biochemical molecular mechanic force field using a combination of ab initio calculations and experimental data. In Computer Simulations of Biomolecular Systems: Theoretical and Experimental Applications. W. F. van Gunsteren and P. K. Wiener, editors. Escom, Dordrecht, The Netherlands. 83-96.
33. Lednev, I. K., A. S. Karnoup, M. C. Sparrow, and S. A. Asher. 1999a. α-Helix peptide folding and unfolding activation barriers: a nanosecond UV resonance Raman study. J. Am. Chem. Soc. 121:8074-8086.
34. Lednev, I. K., A. S. Karnoup, M. C. Sparrow, and S. A. Asher. 1999b. Nanosecond UV resonance Raman examination of initial steps in α-helix secondary structure evolution. J. Am. Chem. Soc. 121:4076-4077.
35. Lednev, I. K., A. S. Karnoup, M. C. Sparrow, and S. A. Asher. 2001. Transient UV Raman spectroscopy finds no crossing barrier between the peptide α-helix and fully random coil conformation. J. Am. Chem. Soc. 123:2388-2392.
36. Lifson, S., and A. Roig. 1961. Theory of helix-coil transition in polypeptides. J. Chem. Phys. 34:1963-1974.
37. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
38. Lockhart, D., and P. Kim. 1992. Internal stark effect measurement of the electric field at the amino terminus of an α-helix. Science. 257:947-951.
39. Lockhart, D., and P. Kim. 1993. Electrostatic screening of charge and dipole interactions with the helix backbone. Science. 260:198-202.
40. MacKerell, A. D., Jr., M. Feig, and C. L. Brooks, III. 2004a. 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.
41. MacKerell, A. D., Jr., M. Feig, and C. L. Brooks, III. 2004b. Improved treatment of the protein backbone in empirical force fields. J. Am. Chem. Soc. 126:698-699.
42. Mezei, M., P. J. Fleming, R. Srinivasan, and G. D. Rose. 2004. Polyproline II helix is the preferred conformation for unfolded polyalanine in water. Proteins. 55:502-507.
43. 10-helix and α-helix in Ala-rich peptides: a hydrogen exchange and high field NMR study. J. Mol. Biol. 267:963-974.
44. Nymeyer, H., and A. E. Garcia. 2003. Simulation of the folding equilibrium of α-helical peptides: a comparison of the generalized Born approximation with explicit solvent. Proc. Natl. Acad. Sci. USA. 100:13934-13939.
45. Okur, A., B. Strockbine, V. Hornak, and C. Simmerling. 2003. Using PC clusters to evaluate the transferability of molecular mechanics force fields for proteins. J. Comput. Chem. 24:21-31.
46. Ono, S., N. Nakajima, J. Higo, and H. Nakamura. 2000. Peptide free-energy profile is strongly dependent on the force field: comparison of C96 and AMBER95. J. Comput. Chem. 21:748-762.
47. Pande, V. S., I. Baker, J. Chapman, S. Elmer, S. Kaliq, S. Larson, Y. M. Rhee, M. R. Shirts, C. Snow, E. J. Sorin, and B. Zagrovic. 2003. Atomistic protein folding simulations on the submillisecond timescale using worldwide distributed computing. Biopolymers. 68:91-109.
48. Pande, V. S., and D. S. Rokhsar. 1999. Molecular dynamics simulations of unfolding and refolding of a beta-hairpin fragment of protein G. Proc. Natl. Acad. Sci. USA. 96:9062-9067.
49. Pappu, R. V., R. Srinivasan, and G. D. Rose. 2000. The Flory isolated-pair hypothesis is not valid for polypeptide chains: implications for protein folding. Proc. Natl. Acad. Sci. USA. 9:12565-12570.
50. Qian, H., and J. A. Schellman. 1992. Helix-coil theories: a comparative study for finite length polypeptides. J. Phys. Chem. 96:3987-3994.
51. Qiu, D., P. S. Shenkin, F. P. Hollinger, and W. C. Still. 1997. The GB/SA continuum model for solvation. A fast analytical method for the calculation of approximate Born radii. J. Phys. Chem. A. 101:3005-3014.
52. Radhakrishnan, R., and T. Schlick. 2004. Orchestration of cooperative events in DNA synthesis and repair mechanism unraveled by transition path sampling of DNA polymerase β's closing. Proc. Natl. Acad. Sci. USA. 101:5970-5975.
53. Rhee, Y. M., and V. S. Pande. 2003. Multiplexed replica exchange molecular dynamics method for protein folding simulation. Biophys. J. 84:775-786.
54. Rhee, Y. M., E. J. Sorin, G. Jayachandran, E. Lindahl, and V. S. Pande. 2004. Simulations of the role of water in the protein-folding mechanism. Proc. Natl. Acad. Sci. USA. 101:6456-6461.
55. Rohl, C. A., and R. L. Baldwin. 1997. Comparison of NH exchange and circular dichroism as techniques for measuring the parameters of the helix-coil transition in peptides. Biochemistry. 36:8435-8442.
56. Shi, Z., C. A. Olson, G. D. Rose, R. L. Baldwin, and N. R. Kallnbach. 2002. Polyproline II structure in a sequence of seven alanine residues. Proc. Natl. Acad. Sci. USA. 99:9190-9195.
57. Shimada, J., and E. I. Shakhnovich. 2002. The ensemble folding kinetics of protein G from an all-atom Monte Carlo simulation. Proc. Natl. Acad. Sci. USA. 99:11175-11180.
58. Shirts, M. R., J. W. Pitera, W. C. Swope, and V. S. Pande. 2003. Extremely precise free energy calculations of amino acid side chain analogs: comparison of common molecular mechanics force fields for proteins. J. Chem. Phys. 119:5740-5761.
59. Snow, C. D., H. Nguyen, V. S. Pande, and M. Gruebele. 2002. Absolute comparison of simulated and experimental protein-folding dynamics. Nature. 420:102-106.
60. Sorin, E. J., B. J. Nakatani, Y. M. Rhee, G. Jayachandran, V. Vishal, and V. S. Pande. 2004. Does native state topology determine the RNA folding mechanism? J. Mol. Biol. 337:789-797.
61. Sorin, E. J., and V. S. Pande. 2005. Empirical force field assessment: the interplay between backbone torsions and non-covalent term scaling. J. Comput. Chem. In press.
62. Sorin, E. J., Y. M. Rhee, B. J. Nakatani, and V. S. Pande. 2003. Insights into nucleic acid conformational dynamics from massively parallel stochastic simulations. Biophys. J. 85:790-803.
63. Thompson, P. A., W. A. Eaton, and J. Hofrichter. 1997. Laser temperature jump study of the helix-coil kinetics of an alanine peptide interpreted with a 'kinetic zipper' model. Biochemistry. 36:9200-9210.
64. Thompson, P. A., V. Munoz, G. S. Jas, E. R. Henry, W. A. Eaton, and J. Hofrichter. 2000. The Helix-coil kinetics of a heteropeptide. J. Phys. Chem. B. 104:378-389.
65. Vila, J. A., D. R. Ripoll, and H. A. Scheraga. 2000. Physical reasons for the unusual α-helix stabilization afforded by charged or neutral polar residues in alanine-rich peptides. Proc. Natl. Acad. Sci. USA. 97:13075-13079.
66. Wang, J., P. Cieplak, and P. A. Kollman. 2000. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21:1049-1074.
67. Weise, C. F., and J. C. Weisshaar. 2003. Conformational analysis of alanine dipeptide from dipolar couplings in a water-based liquid crystal. J. Phys. Chem. B. 107:3265-3277.
68. Williams, S., T. P. Causgrove, R. Gilmanshin, K. S. Fang, R. H. Callender, W. H. Woodruff, and R. B. Dyer. 1996. Fast events in protein folding: helix melting and formation in a small peptide. Biochemistry. 35:691-697.
69. Wu, X., and S. Wang. 2001. Helix folding of an alanine-based peptide in explicit water. J. Phys. Chem. B. 105:2227-2235.
70. 2 (n=1-4), using vibrational circular dichroism and Fourier transform infrared. Conformational determination and thermal unfolding. Biochemistry. 36:15123-15133.
71. Zagrovic, B., and V. Pande. 2003a. Solvent viscosity dependence of the folding rate of a small protein. Distributed computing study. J. Comput. Chem. 24:1432-1436.
72. Zagrovic, B., and V. S. Pande. 2003b. Structural correspondence between the α-helix and the random-flight chain resolves how unfolded proteins can have native-like properties. Nat. Struct. Biol. 10:955-961.
73. Zagrovic, B., E. J. Sorin, I. S. Milieu, W. F. van Gunsteren, S. Doniach, and V. S. Pande. 2005. Local versus global structural information in a flexible peptide: a case study. Proc. Natl. Acad. Sci. USA. In press.
74. Zagrovic, B., E. J. Sorin, and V. Pande. 2001. β-Hairpin folding simulations in atomistic detail using an implicit solvent model. J. Mol. Biol. 313:151-169.
75. Zaman, M. H., M.-Y. Shen, R. S. Berry, K. F. Freed, and T. R. Sosnick. 2003. Investigations into sequence and conformational dependence of backbone entropy, inter-basin dynamics and the Flory isolated-pair hypothesis for peptides. J. Mol. Biol. 331:693-711.
76. Zhang, W., H. Lei, S. Chowdhury, and Y. Duan. 2004. Fs-21 peptides can form both single helix and helix-turn-helix. J. Phys. Chem. B. 108:7479-7489.