Towards the complete structural characterization of a protein folding pathway: The structures of the denatured, transition and native states for the association/folding of two complementary fragments of cleaved chymotrypsin inhibitor 2. Direct evidence for a nucleation-condensation mechanism

Folding and Design

Volumn 1, Issue 3, 1996, Pages 189-208

  Neira, José L ^a   Davis, Ben ^a,b   Ladurner, Andreas G ^a   Buckle, Ashley M ^a   De Prat Gay, Gonzalo ^a,c   Fersht, Alan R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

NMR; Nucleus; Phi value; X ray crystallography

Indexed keywords

CHYMOTRYPSIN; CHYMOTRYPSIN INHIBITOR 2; PEPTIDE; PEPTIDE FRAGMENT; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLIZATION; DRUG ANTAGONISM; GENETICS; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; SOLUTION AND SOLUBILITY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CHYMOTRYPSIN; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PEPTIDE FRAGMENTS; PEPTIDES; PLANT PROTEINS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SOLUTIONS;

EID: 0030334851     PISSN: 13590278     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1359-0278(96)00031-4     Document Type: Article

References (73)

1. Tanford, C. (1968). Protein denaturation. Adv. Protein Chem. 23, 121-282.
2. Dyson, H.J. & Wright, P.E. (1993). Peptide conformation and protein folding. Curr. Opin. Struct. Biol. 3, 60-65.
3. Ludvigsen, S., Shen, H., Kjaer, M., Madsen, J.C. & Poulsen, P.M. (1991). Refinement of the three-dimensional solution structure of barley serine proteinase inhibitor 2 and comparison with the structures in crystals. J. Mol. Biol. 222, 621-635.
4. Clore, G.M., Gronenborn, A.M., James, M.N.G., Kjær, M., McPhalen, C.A. & Poulsen, P.M. (1987). Comparison of the solution structure and X-ray structure of barley serine proteinase inhibitor 2. Protein Eng. 1, 313-318.
5. McPhalen, C.A. & James, M.N.G. (1987). Crystal and molecular structure of the serine protease inhibitor (Cl-2) from barley seeds, Biochemistry 26, 261-259.
6. Harpaz, Y., elMasry, N.F., Fersht, A.R. & Henrick, K. (1994). Direct observation of 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, 311-315.
7. Jackson, S.E. & Fersht, A.R. (1991). Folding of chymotrypsin inhibitor-2. 1. Evidence for a two-state transition. Biochemistry 30, 10428-10435.
8. Jackson, S.E. & Fersht, A.R. (1991). Folding of chymotrypsin inhibitor-2. 2. Influence of proline isomerization on the folding kinetics and thermodynamic characterisation of the transition state of folding. Biochemistry 30, 10436-10443.
9. Jackson, S.E., elMasry, N.F. & Fersht, A.R. (1993). Structure of the hydrophobic core in the transition state for folding chymotrypsin inhibitor-2: a critical test of the protein engineering method of analysis. Biochemistry 32, 11270-11278.
10. 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 chymotrypsin inhibitor-2 and its implications for mechanisms of protein folding. Proc. Natl. Acad. Sci. USA 91, 10422-10425.
11. Itzhaki, L.S., Otzen, D.E. & Fersht, A.R. (1995). The structure of the transition state for folding of chymotrypsin inhibitor-2 analysed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254, 260-288.
12. Fersht, A.R. (1995). Optimization of rates of protein folding: the nucleation-condensation mechanism and its implications. Proc. Natl. Acad. Sci. USA 92, 10869-10873.
13. De Prat Gay, G. & Fersht, A.R. (1994). Generation of a family of protein fragments for structure-folding studies. 1. Folding complementation of two fragments of chymotrypsin inhibitor-2 formed by cleavage at its unique methionine residue. Biochemistry 33, 7957-7963.
14. De Prat Gay, G., Ruiz-Sanz, J. & Fersht, A.R. (1994). Generation of a family of protein fragments for structure-folding studies. 2. Kinetics of association of the two chymotrypsin inhibitor-2 fragments. Biochemistry 33, 7964-7970.
15. Fersht, A.R. (1995). Characterizing transition-states in protein folding-an essential step in the puzzle. Curr. Opin. Struct. Biol. 5, 79-84.
16. Ruiz-Sanz, J., De Prat Gay, G., Otzen, D.E. & Fersht, A.R. (1995). Protein-fragments as models for events in protein folding pathways. Protein engineering analysis of the association of two complementary fragments of the barley chymotrypsin inhibitor-2 (Cl-2) Biochemistry 34, 1695-1701.
17. De Prat Gay, G., Ruiz-Sanz, J., Davis, B. & Fersht, A.R. (1994). The structure of the transition state for the association of two fragments of the barley chymotrypsin inhibitor-2 to generate native-like protein and implications for mechanism of protein folding. Proc. Natl. Acad. Sci. USA 91, 10943-10946.
18. Itzhaki, L.S., Neira, J.L., Ruiz-Sanz, J., De Prat Gay, G. & Fersht, A.R. (1995). Search for nucleation sites in smaller fragments of chymotrypsin inhibitor-2. J. Mol. Biol. 254, 289-304.
19. Shakhnovich, E.U., Abkevich, V. & Ptitsyn, O. (1996). Conserved residues and the mechanism of protein folding. Nature 379, 96-98.
20. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids. John Wiley & Sons, Inc., New York.
21. Kjær, M., Ludvingsen, S., Sorensen, O.W., Denys, L.A., Kindler, J. & Poulsen, F.M. (1987). Sequence specific assignment of the proton nuclear magnetic resonance spectrum of barley serine proteinase inhibitor 2. Carlsberg Res. Commun. 52, 353-362.
22. 1H NMR assignments of its pH-denatured state. Proc. Natl. Acad Sci. USA 91, 9412-9416.
23. Wishart, D.S., Sykes, B.D. & Richards, F.M. (1992). The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31, 1647-1651.
24. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of the nearest-neighbour effects. J. Biomol. NMR 5, 67-81.
25. Simmerling, C.L. & Elber, R. (1995). Computer determination of peptide conformations in water: different roads to structure. Proc. Natl. Acad. Sci USA 92, 3190-3193.
26. 1H nuclear magnetic resonance techniques. Eur. J. Biochem. 91, 201-203.
27. 1H nuclear magnetic resonance (COSY). J. Mol. Biol. 179, 283-288.
28. 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series. J. Biomol. NMR 5, 14-24.
29. Johnson, C. & Fersht, A.R. (1995). Protein stability as a function of denaturant concentration: the thermal stability of barnase in the presence of urea. Biochemistry 34, 6795-6804.
30. Makhatadze, G.I. & Privalov, P.L. (1992). Protein interactions with urea and guanidinum chloride. A calorimetric study. J. Mol. Biol. 226, 491-505.
31. Pike, A.C.W. & Acharya, K.R. (1994). A structural basis for the interaction of urea with lysozyme. Protein Sci. 3, 706-710.
32. Evans, P.A., Topping, K.D., Woolfson, D.N. & Dobson, C.M. (1991). Hydrophobic clustering in nonnative states of a protein. Interpretation of chemical shifts in NMR spectra of denatured states of lysozyme. Proteins 9, 248-266.
33. Rooman, M.J., Kocher, J.-P.A. & Wodak, S.J. (1991). Prediction of protein backbone conformation based on seven structure assignments. Influence of local interactions. J. Mol. Biol. 221, 961-979.
34. Rooman, M.J., Kocher, J.-P.A. & Wodak, S.J. (1992). Extracting information from the amino-acid-sequence. Accurate predictions for protein regions with preferred conformation in the absence of tertiary interactions. Biochemistry 31, 10226-10238.
35. Shaw, G.L., Davis, B., Keeler, J. & Fersht, A.R. (1995). 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, 2225-2233.
36. Laskowski, R.A., MacArthur, M.W., Moss, D. & Thornton, J.M. (1993). PROCHECK, a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
37. Wyckoff, H.W., Tsernoglou, D., Hanson, A.W., Knox, J.R., Lee, B. & Richards, F.M. (1970). The three-dimensional structure of ribonuclease S. J. Biol. Chem. 245, 305-328.
38. Walkenhorst, W.F., Krezel, A.M., Rhyu, G.I. & Markley, J.L. (1994). Solution structure of the active site hydrolysed turkey ovomucoid third domain by nuclear magnetic resonance and distance geometry methods. J. Mol. Biol. 242, 215-230.
39. Tasayco, M.L. & Chao, K. (1995). NMR study of the reconstitution of the β-sheet of thioredoxin by fragment complementation. Proteins 22, 41-44.
40. Fersht, A.R., Itzhaki, L.S., Mathews, J.M. & Otzen, D.E. (1994). Single versus parallel pathways of protein folding and fractional formation of structure in the transition state. Proc. Natl. Acad. Sci. USA 91, 10426-10429.
41. De Prat Gay, G., et al., & Fersht, A.R. (1995). Conformational pathway of the polypeptide chain of chymotrypsin inhibitor-2 growing from its N terminus in vitro. Parallels with the protein folding pathway. J. Mol. Biol. 254, 968-979.
42. Wetlaufer, D.B. (1973). Nucleation, rapid folding, and globular intrachain regions in proteins. Proc. Natl. Acad. Sci. USA 70, 697-701.
43. Matthews, J.M. & Fersht, A.R. (1995). Exploring the energy surface of protein folding by structure-reactivity relationships and engineered proteins: observation of Hammond behaviour for the gross structure of the transition state and anti-Hammond behaviour for structural elements for unfolding/folding of barnase. Biochemistry 34, 6805-6814.
44. Abkevich, V.I., Gutin, A.M. & Shakhnovich, E.I. (1994). Specific nucleus as the transition state for protein folding. Evidence from the lattice model. Biochemistry 33, 10026-10036.
45. Guo, Z.Y. & Thirumalai, D. (1995). Kinetics of protein folding. Nucleation mechanism, time scales and folding. Biopolymers 36, 83-102.
46. Jackson, S.E., Moracci, M., elMasry, N.F., Johnson, C. & Fersht, A.R. (1993). The effect of cavity creating mutations in the hydrophobic core of chymotrypsin inhibitor-2. Biochemistry 32, 11262-11269.
47. Gill, S.C. & Von Hippel, P.H. (1989). Extinction coefficients from amino acid sequence data. Analyt. Biochem. 182, 319-326.
48. Bax, A. & Davis, D.G. (1985). MLEV-17 based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360.
49. Braunschweiler, L. & Ernst, R.R. (1983). Coherence transfer by isotropic mixing-application to proton correlation spectroscopy. J. Magn. Reson. 53, 521-528.
50. Bax, A., Ikura, M., Kay, LE., Torchia, DA & Tschudin, R. (1990). Comparison of different modes of two-dimensional reverse-correlation NMR for the study of proteins. J. Magn. Reson. 86, 304-318.
51. Jeener, J., Meier, B., Backman, P. & Ernst, R.R. (1979). Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4550.
52. Bothner-By, AA, Stephens, R.L., Lee, J.M., Warren, C.D. &. Jeanloz, R.W. (1984). Structure determination of a tetrasaccharide: transient nuclear Overhauser effects in the rotating frame. J. Am. Chem. Soc. 106, 811-813.
53. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 11, 967-975.
54. 2O solutions. J. Magn. Reson. 85, 608-613.
55. Shaka, A.J., Barker, P.B. & Freeman, R. (1985). Computer optimized decoupling scheme for wide band applications and low-level operation. J. Magn. Reson. 64, 547-552.
56. 13C levels. J. Magn. Reson. 71, 379-383.
57. 1H multiple quantum coherence spectroscopy. FEBS Lett. 243, 93-98.
58. 15N Hartmann-Hahn multiple quantum coherence and nuclear Overhauser multiple quantum coherence spectroscopy. Application to interleukin-1β. Biochemistry 28, 6150-6156.
59. Piantini, U., Sorensen, D.W. & Ernst, R.R. (1982). Multiple quantum filter for elucidating NMR coupling networks. J. Am. Chem. Soc. 104, 6800-6801.
60. Kadkhodaie, M., Rivas, O., Tan, M., Mohebbi, A. & Shaka, A.J. (1991). Broad-band homonuclear cross polarization using flip-flop spectroscopy. J. Magn. Reson. 91, 437-443.
61. Marion, D., Ikura, M. & Bax, A. (1989). Practical aspects of 3D heteronuclear NMR of proteins. J. Magn. Reson. 84, 425-430.
62. Kim, P.S., Bierzynski, A. & Baldwin, R.L. (1982). A competing saltbridge suppresses helix formation by the isolated C-peptide carboxylate of ribonuclease A. J. Mol. Biol. 162, 187-199.
63. Wagner, G., Braun, W., Havel, T.F. & Wüthrich, K. (1987). Protein structures in solution by nuclear magnetic resonance and distance geometry. The polypeptide fold of the basic pancreatic trypsin inhibitor determined using two different algorithms: DISGEO and DISMAN. J. Mol. Biol. 196, 611-639.
64. Stonehouse, J. & Keeler, J. (1995). A convenient and accurate method for the measurement of the values of spin-spin coupling constants. J. Magn. Reson. A series 112, 43-57.
65. Barsukov, I.L. & Lian, L.-Y. (1993). NMR of Macromolecules. A Practical Approach, pp. 315-357. IRL Press, Oxford.
66. Brunger, A.T. (1992). X-PLOR, Version 3.1: A System for X-ray Crystallography and NMR. Yale University Press, New Haven, CT.
67. Nilges, M., Gronenborn, A.M. & Clore, G.M. (1988). Determination of three-dimensional structure of proteins from interproton distance data by dynamical simulated annealing from a random array of atoms. Circumventing problems associated with folding. FEBS Lett. 229, 317-324.
68. Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, DJ., Swaminthan, S. & Karplus, M. (1983). CHARMM: a program for macromolecular energy, minimization and dynamics calculations. J. Comput. Chem. 4, 187-217.
69. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure. Pattern recognition of hydrogen-bond and geometrical features. Biopolymers 22, 2577-2637.
70. McPherson, A. (1982). The Preparation and Analysis of Protein Crystals. New York, John Wiley & Sons.
71. CCP4 (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50, 760-763
72. Leslie, A.G.W. (1990). Crystallographic Computing. Oxford University Press.
73. Kraulis, P.J. (1991). MOLSCRIPT, a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.