Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations

Journal of Molecular Biology

Volumn 257, Issue 2, 1996, Pages 412-429

  Li, Aijun ^a   Daggett, Valerie ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Chymotrypsin inhibitor 2; Conformational states; Protein unfolding; Solution simulations; Transition state

Indexed keywords

CHYMOTRYPSIN INHIBITOR;

ARTICLE; ENERGY; GENETIC ENGINEERING; MOLECULAR DYNAMICS; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SIMULATION; TEMPERATURE;

EID: 0029963345     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0172     Document Type: Article

References (41)

1. Chan, H. S. & Dill, K. A. (1990). Origins of structure in globular proteins. Proc. Natl Acad. Sci. USA, 87, 6388-6392.
2. Clore, G. M., Gronenborn, A. M., Kjaer, M. & Poulsen, F. M. (1987a). The determination of the three dimensional structure of barley serine proteinase inhibitor 2 by nuclear magnetic resonance, distance geometry and restrained molecular dynamics. Protein Eng. 1, 305-311.
3. Clore, G. M., Gronenborn, A. M., James, M. N. G., Kjaer, M., McPhalen C. A & Poulsen F M. (1987b). Comparison of the solution and X-ray structures of barley serine proteinase inhibitor 2. Protein Eng. 1, 313-318.
4. Creighton, T. E. (1993). Proteins: Structure and Molecular Properties, p. 142, W. H. Freeman and Company, New York.
5. Daggett, V. & Levitt, M. (1991). A molecular dynamics simulation of the C-terminal fragment of the L7/L12 ribosomal protein in solution. Chem. Phys. 158, 501-512.
6. Daggett, V. & Levitt, M. (1992). Molecular dynamics simulations of helix denaturation. J. Mol. Biol. 223, 1121-1138.
7. Daggett, V., Kollman, P. A. & Kuntz, I. D. (1991). A molecular dynamics simulation of polyalanine: An analysis of equilibrium motions and helix-coil transitions. Biopolymers, 31, 1115-1134.
8. Daggett, V., Li, A., Itzhaki, L. S., Otzen, D. E. & Fersht, A. R. (1996). Structure of the transition state for folding of a protein derived from experiment and simulations. J. Mol. Biol. 257, 430-440.
9. Evans, P. A. & Radford, S. E. (1994). Probing the structure of folding intermediates. Curr. Opin. Struct. Biol. 4, 100-106.
10. Ferrin, T. E., Huang, C. C., Jarvis, L. E. & Langridge, R. (1988). The MIDAS display system, J. Mol. Graphics, 6, 13-27.
11. Fersht, A. R. (1995). Characterizing transition states in protein folding: an essential step in the puzzle. Curr. Opin. Struct. Biol. 5, 79-84.
12. Fersht, A. R., Matouschek, A. & Serrano, L. (1992). The folding of an enzyme I. theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224, 771-782.
13. Goldenberg, D. P. & Creighton, T. E. (1985). Energetics of protein structure and folding. Biopolymers, 24, 167-182.
14. Haar, L., Gallagher, J. S. & Kell, G. S. (1984). NBS/NRC Steam Tables: Thermodynamic and Transport Properties and Computer Programs for Vapor and Liquid States of Water in SI Units. Hemisphere Publication Corporation, Washington, D.C.
15. Harpaz, Y, Elmasry N., Fersht, A. R. & Henrick, K. (1994). 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, 3-15.
16. Harrison, S. C. & Durbin, R. (1985). Is there a single pathway for the folding of a polypeptide chain? Proc. Natl Acad. Sci. USA, 87, 4028-4030.
17. Hubbard, S. J. & Thornton, J. M. (1993). NACCESS, Computer Program, Department of Biochemistry and Molecular Biology University College, London.
18. Hubbard, S. J., Campbell, S. F. & Thornton, J. M. (1991). Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors. J. Mol. Biol. 220, 507-530.
19. Itzhaki, L. S., Otzen, D. E. & Fersht, A. R. (1995). The structure of the transition state for folding of chymotrypsin inhibitor 2 analyzed by protein engineering methods: Evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254, 260-288.
20. Jackson, S. E. & Fersht, A. R. (1991a). Folding of chymotrypsin inhibitor 2: 1. Evidence for a two-state transition. Biochemistry, 30, 10428-10435.
21. Jackson, S. E. & Fersht, A. R. (1991b). Folding of chymotrypsin inhibitor 2: 2. Influence of proline isomerization on the folding kinetics and thermodynamic characterization of the transition state of folding. Biochemistry, 30, 10436-10443.
22. Jackson, S. E., Moracci, M., elMasry N., Johnson, C. M. & Fersht, A. R. (1993a). Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor 2. Biochemistry, 32, 11259-11269.
23. Jackson, S. E., elMasry N. & Fersht, A. R. (1993b). Structure of the hydrophobic core in the transition state for folding of chymotrypsin inhibitor 2: a critical test of the protein engineering method of analysis. Biochemistry, 32, 11270-11278.
24. Karplus, M. & Weaver, D. L. (1994). Protein folding dynamics: the diffusion-collision model and experimental data. Protein Sci. 3, 650-668.
25. Kell, G. S. (1967). Precise representation of volume properties of water at one atmosphere. J. Chem. Eng. Data, 12, 66-68.
26. Kim, P. & Baldwin, R. (1990). Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 59, 631-660.
27. Levitt, M. (1983). Molecular dynamics of native protein II. Analysis and nature of motion. J. Mol. Biol. 168, 621-657.
28. Levitt, M. (1989). Molecular dynamics of macromolecules in water. Chemica Scripta, 29A, 197-203.
29. Levitt, M. (1990). ENCAD - Energy Calculation and Dynamics, Molecular Applications Group, Stanford, CA and Yeda, Rehovot, Israel.
30. Levitt, M., Hirshberg, M., Sharon, R. & Daggett, V. (1995). Potential energy function and parameters for simulations of the molecular dynamics of proteins and nucleic acids in solution. Comp. Phys. Commun., 91, 215-231.
31. Li, A. & Daggett, V. (1994). Characterization of the transition state of protein unfolding by use of molecular dynamics: chymotrypsin inhibitor 2. Proc. Natl Acad. Sci. USA, 91, 10430-10434.
32. Li, A. & Daggett, V. (1995). Investigation of the solution structure of chymotrypsin inhibitor 2 using molecular dynamics: comparison to X-ray crystallographic and NMR data. Protein Eng. 8, 1117-1128.
33. Ludvigsen, S., Shen, H., Kjaer, M., Madsen, J. C. & Poulsen, F. M. (1991). Refinement of the three-dimensional solution structure of barley serine proteinase inhibitor 2 and comparison with the structures in crystal. J. Mol. Biol. 222, 621-635.
34. Matouschek, A., Kellis, J. T., Jr, Serrano, L. & Fersht, A. L. (1989). Mapping the transition state and pathway of protein folding by protein engineering. Nature, 340, 122-126.
35. Matouschek, A., Serrano, L. & Fersht, A. R. (1992). The folding of an enzyme IV. Structure of an intermediate in the refolding of barnase analyzed by a protein engineering procedure. J. Mol. Biol. 224, 819-835.
36. McPhalen, C. A. & James, M. N. G. (1987). Crystal and molecular structure of the serine proteinase inhibitor CI2 from barley seeds. Biochemistry, 26, 261-269.
37. Otzen, D. E., Itzhaki, L. S., ElMasry N. F., Jackson, S. E. & Fersht, A. R. (1994). Structure of the transition state for the folding/unfolding of the barley chymotrypsin inhibitor 2 and its implications for mechanisms of protein folding. Proc. Natl Acad. Sci. USA, 91, 10422-10425.
38. Prat Gay, G. D., Ruiz-Sanz, J., Neira, J. L., Itzhaki, L. S. & Fersht, A. R. (1995). Folding of a nascent polypeptide chain in vitro: cooperative formation of structure in a protein module. Proc. Natl Acad. Sci. USA, 92, 3683-3686.
39. Ptitsyn, O. B. (1994). Kinetic and equilibrium intermediates in protein folding. Protein Eng. 7, 593-596.
40. Sancho, J., Meiering, E. M. & Fersht, A. L. (1991). Mapping transition states of protein unfolding by protein engineering of ligand-binding sites. J. Mol. Biol. 221, 1007-1014.
41. Serrano, L, Matouschek, A. & Fersht, A. R. (1992). The folding of an enzyme III. Structure of the transition state for unfolding of barnase analyzed by a protein engineering procedure. J. Mol. Biol. 224, 805-818.