Direct Observation of Microscopic Reversibility in Single-molecule Protein Folding

Journal of Molecular Biology

Volumn 366, Issue 2, 2007, Pages 677-686

  Day, Ryan ^a   Daggett, Valerie ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

microscopic reversibility; nonnative interactions; protein dynamics; protein folding unfolding; protein refolding

Indexed keywords

HYDROGEN;

ALPHA HELIX; ARTICLE; BETA SHEET; CRYSTAL STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; SIMULATION; TEMPERATURE;

EID: 33846381622     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.11.043     Document Type: Article

References (47)

1. Li A., and Daggett V. Characterization of the transition state of protein unfolding using molecular dynamics: chymotrypsin inhibitor 2. Proc. Natl Acad. Sci. USA 91 (1994) 10430-10434
2. Li A., and Daggett V. Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations. J. Mol. Biol. 257 (1996) 412-429
3. Daggett V., Li A., Itzhaki L.S., Otzen D.E., and Fersht A.R. Structure of the transition state for folding of a protein derived from experiment and simulation. J. Mol. Biol. 257 (1996) 430-440
4. Ladurner A.G., Itzhaki L.S., Daggett V., and Fersht A.R. Synergy between simulation and experiment in describing the energy landscape of protein folding. Proc. Natl Acad. Sci. USA 95 (1998) 8473-8478
5. Kazmirski S.L., Wong K.-B., Freund S.M.V., Tan Y.-J., Fersht A.R., and Daggett V. Protein folding from a highly disordered denatured state: the folding pathway of chymotrypsin inhibitor 2 at atomic resolution. Proc. Natl Acad. Sci. USA 98 (2001) 4349-4354
6. Pan Y.P., and Daggett V. Direct comparison of experimental and calculated folding free energies for hydrophobic deletion mutants of chymotrypsin inhibitor 2: free energy perturbation calculations using transition and denatured states from molecular dynamics simulations of unfolding. Biochemistry 40 (2001) 2723-2731
7. Day R., Bennion B.J., Ham S., and Daggett V. Increasing temperature accelerates protein unfolding without changing the pathway of unfolding. J. Mol. Biol. 322 (2002) 189-203
8. Day R., and Daggett V. Sensitivity of the folding/unfolding transition state ensemble of chymotrypsin inhibitor 2 to changes in temperature and solvent. Protein Sci. 14 (2005) 1242-1252
9. Mayor U., Johnson C.M., Daggett V., and Fersht A.R. Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation. Proc. Natl Acad. Sci. USA 97 (2000) 13518-13522
10. Mayor U., Johnson C.M., Grossmann J.G., Sato S., Jas G.S., Freund S.M.V., et al. The complete folding pathway of a protein from nanoseconds to microseconds. Nature 421 (2003) 863-867
11. Gianni S., Guydosh N.R., Khan F., Caldas T.D., Mayor U., White G.W.N., et al. Unifying features in protein-folding mechanisms. Proc. Natl Acad. Sci. USA 100 (2003) 13286-13291
12. White, G. W. N., Gianni, S., Grossman, J. G., Jemth, P., Fersht, A. R., & Daggett, V. (2005). Simulation and experiment conspire to reveal cryptic intermediates and the slide from the nucleation-condensation to framework mechanism of folding. J. Mol. Biol., 350, 757-775.
13. Ferguson N., Day R., Johnson C.M., Allen M.D., Daggett V., and Fersht A.R. Simulation and experiment at high temperatures: ultrafast folding of a thermophilic protein by nucleation-condensation. J. Mol. Biol. 347 (2005) 855-870
14. Ferguson N., Pires J.R., Toepert F., Johnson C.J., Pan Y.P., Volkmer-Engert R., et al. Using flexible loop mimetics to extend Φ-value analysis to secondary structure interactions. Proc. Natl Acad. Sci. USA 98 (2001) 13008-13013
15. 3D, a de novo designed three-helix bundle protein. Proc. Natl Acad. Sci. USA 100 (2003) 15486-15491
16. Day R., and Daggett V. Ensemble versus single-molecule protein unfolding. Proc. Natl Acad. Sci. USA 102 (2005) 13445-13450
17. Beck, D. A. C., White, G. W. N., & Daggett, V. (2006). Exploring the energy landscape of protein folding using replica-exchange and conventional molecular dynamics simulations. J. Struct. Biol. In press and available on-line. doi:10.1016/j.jsb.2006.10.002
18. Garcia A.E., and Onuchic J.N. Folding a protein in a computer: an atomic description of the folding/unfolding of protein A. Proc. Natl Acad. Sci. USA 100 (2003) 13898-13903
19. Pitera J.W., and Swope W. Understanding folding and design: Replica-exchange simulations of "Trp-cage" fly miniproteins. Proc. Natl Acad. Sci. USA 100 (2003) 7587-7592
20. Zhou R.H. Trp-cage: folding free energy landscape in explicit water. Proc. Natl Acad. Sci. USA 100 (2003) 13280-13285
21. Minkin V.I. Commission on physical organic chemistry. Pure Appl. Chem. 71 (1999) 1919-1981
22. Westheimer F.H. Pseudo-rotation in the hydrolysis of phosphate esters. Accts. Chem. Res. 1 (1968) 70-78
23. Lahti D.W., and Espenson J.H. Issues of microscopic reversibility and an isomeric intermediate in ligand substitution reactions of five-coordinate oxorhenium(V) dithiolate complexes. J. Am. Chem. Soc. 123 (2001) 6014-6024
24. Fersht A.R. Structure and Mechanism in Protein Science (1999), W.H. Freeman and Company, New York
25. Fersht A.R., and Daggett V. Protein folding and unfolding at atomic resolution. Cell 108 (2002) 573-582
26. Daggett V., and Fersht A.R. Is there a unifying mechanism for protein folding?. Trends Biochem. Sci. 28 (2003) 18-25
27. Daggett V., and Fersht A.R. The present view of the mechanism of protein folding. Nature Rev. Mol. Cell. Biol. 4 (2003) 497-502
28. Alonso D.O.V., and Daggett V. Molecular dynamics simulations of protein unfolding and limited refolding: characterization of partially unfolded states of ubiquitin in methanol and in pure water. J. Mol. Biol. 247 (1995) 501-520
29. Alonso D.O.V., and Daggett V. Molecular dynamics simulations of hydrophobic collapse of ubiquitin. Protein Sci. 7 (1998) 860-874
30. De Jong D., Riley R., Alonso D.O.V., and Daggett V. Probing the energy landscape of protein folding/unfolding transition states. J. Mol. Biol. 319 (2002) 229-242
31. 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
32. Jackson S.E., and Fersht A.R. Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry 30 (1991) 10428-10435
33. Harpaz Y., elMasry N., Fersht A.R., and Henrick K. Direct observation of a better hydration at the N-terminus of an α-helix with glycine rather than alanine as the N-cap residue. Proc. Natl Acad. Sci. USA 91 (1994) 3-15
34. Ludvigsen S., Shen H., Kjaer M., Madsen J.C., and Poulsen F.M. Refinement of the three-dimensional solution structure of barley serine proteinase inhibitor 2 and comparison with the structures in crystals. J. Mol. Biol. 222 (1991) 621-635
35. Shaw G.L., Davis B., Keeler J., and Fersht A.R. Backbone dynamics of chymotrypsin inhibitor 2: effect of breaking the active site bond and its implications for the mechanism of inhibition of serine proteases. Biochemistry 34 (1995) 2225-2233
36. Li A., and Daggett V. Investigation of the solution structure of chymotrypsin inhibitor 2 using molecular dynamics: comparison to X-ray and NMR data. Protein Eng. 8 (1995) 1117-1128
37. de Prat Gay G., Ruiz-Sanz J., Davis B., and Fersht A.R. The structure of the transition state for the association of two fragments of the barley chymotrypsin inhibitor 2 to generate native-like protein: implications for mechanisms of protein folding. Proc. Natl Acad. Sci. USA 91 (1994) 10943-10946
38. Frauenfelder H., Hartmann H., Karplus M., Kuntz I.D., Kuriyan J., Parak F., et al. Thermal expansion of a protein. Biochemistry 26 (1987) 254-261
39. Tilton R.F., Dewan J.C., and Petsko G.A. Effects of temperature on protein structure and dynamics: X-ray crystallographic studies of the protein ribonuclease-A at nine different temperatures from 98 to 320 K. Biochemistry 31 (1992) 2469-2481
40. Leeson D.T., Gai F., Rodriguez H.M., Gregoret L.M., and Dyer R.B. Protein folding and unfolding on a complex energy landscape. Proc. Natl Acad. Sci. USA 97 (2000) 2527-2532
41. Rhoades E., Gussakovsky E., and Haran G. Watching proteins fold one molecule at a time. Proc. Natl Acad. Sci. USA 100 (2003) 3197-3202
42. Levitt, M. (1990). ENCAD-Energy Calculations and Dynamics, Yeda, Rehovat, Israel and Stanford University, Stanford, CA.
43. Levitt M., Hirshberg M., Sharon R., and Daggett V. Potential energy function and parameters for simulations of the molecular dynamics of proteins and nucleic acids in solution. Comput. Phys. Commun. 91 (1995) 215-231
44. Levitt M., Hirshberg M., Sharon R., Laidig K.E., and Daggett V. Calibration and testing of a water model for simulation of the molecular dynamics of proteins and nucleic acids in solution. J. Phys. Chem. B 101 (1997) 5051-5061
45. Beck, D. A. C., Armen, R. S., & Daggett, V. (2005). Cutoff size need not strongly influence molecular dynamics results on solvated polypeptides. Biochemistry, 44, 609-616.
46. Haar L., Gallagher J.S., and Kell G.S. NBS/NRC Steam Tables: Thermodynamic and Transport Properties and Computer Programs for Vapor and Liquid States Of Water in SI units (1984), Hemisphere Pub. Corp., Washington, DC
47. DeLano W.L. The PyMOL molecular graphics system (2002), DeLano Scientific, San Carlos, CA