Calculations on folding of segment B1 of streptococcal protein G

Journal of Molecular Biology

Volumn 278, Issue 2, 1998, Pages 439-456

  Sheinerman, Felix B ^a   Brooks III, Charles L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Folding mechanism; Molecular dynamics; Potential of mean force; Protein folding; Protein G

Indexed keywords

BACTERIAL PROTEIN; PROTEIN G;

AMINO TERMINAL SEQUENCE; ARTICLE; DATA BASE; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; STREPTOCOCCUS; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOCOCCUS;

EID: 0032080053     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1688     Document Type: Article

References (73)

1. Acjari, A., Hale, S. P., Howard, A. J., Clore, G. M., Gronenborn, A. M., Hardman, K. D. & Whitlow, M. (1992). 1.67-Å X-ray structure of the B2 immunoglobulin-binding domain of streptococcal protein G and comparison to the NMR structure of the B1 domain. Biochemistry, 31, 10449-10457.
2. Alexander, P., Fahnestock, S., Lee, T., Orman, J. & Bryan, P. (1992a). Thermodynamic analysis of the folding of the streptococcal protein G IgG-binding domains B1 and B2: why small proteins tend to have high denaturation temperatures. Biochemistry, 31, 3597-3603.
3. Alexander, P., Orban, J. & Bryan, P. (1992b). Kinetic analysis of folding and unfolding the 56 amino acid IgG-binding domain of streptococcal protein G. Biochemistry, 31, 7243-7248.
4. Alonso, D. O. V. & Daggett, V. (1995). Molecular dynamics simulations of protein unfolding and limited refolding: characterization of partially unfolded states of ubiquitin in 60% methanol and in water. J. Mol. Biol. 247, 501-520.
5. Anfinsen, C. B. (1973). Principles that govern the folding of protein chains. Science, 181, 223-230.
6. Bai, Y. & Englander, S. W. (1996). Future directions in folding: the multi-state nature of protein structure. Proteins: Struct. Funct. Geomet. 24, 145-151.
7. Bai, Y., Sosnick, T. R., Mayne, L. & Englander, S. W. (1995). Protein folding intermediates: native-state hydrogen exchange. Science, 269, 192-197.
8. Balbach, J., Forge, V., van Nuland, N. A. J., Winder, S. L., Höre, P. J. & Dobson, C. M. (1995). Following protein folding in real time using NMR spectroscopy. Nature Struct. Biol. 2, 865-870.
9. Baldwin, R. L. (1995). The nature of protein folding pathways: the classical versus the new view. J. Biomol. NMR, 5, 103-109.
10. Blanco, F. J. & Serrano, L. (1995). Folding of protein G B1 domain studied by the conformational characterization of fragments comprising its secondary structure elements. Eur. J. Biochem. 230, 634-649.
11. Blanco, F. J., Jimenez, M. A., Pineda, A., Rico, M., Santoro, J. & Nieto, J. L. (1994a). NMR solution structure of the isolated N-terminal fragment of protein-G B1 domain. Evidence of trifluoroethanol induced native-like β-hairpin formation. Biochemistry, 33, 6004-6014.
12. Blanco, F. J., Rivas, G. & Serrano, L. (1994b). A short linear peptide that folds into a native stable β-hairpin in aqueous solution. Nature Struct. Biol. 1, 584-590.
13. Blanco, F. J., Ortiz, A. R. & Serrano, L. (1997). Role of a non-native interaction in the folding of the protein G B1 domain as inferred from the conformational analysis of the α-helix fragment. Folding Design, 2, 123-133.
14. Boczko, E. M. & Brooks, C. L., III (1993). Constant-temperature free energy surfaces for physical and chemical processes. J. Phys. Chem. 97, 4509-4513.
15. Boczko, E. M. & Brooks, C. L., III (1995). First-principles calculation of the folding free energy of a three-helix bundle protein. Science, 269, 393-396.
16. Brooks, C. L., III (1992). Characterization of "native" apolyoglobin by molecular dynamics simulation. J. Mol. Biol. 227, 375-380.
17. Brooks, C. L., III & Case, D. (1993). Simulations of peptide conformational dynamics and thermodynamics. Chem. Rev. 93, 2487-2502.
18. Bryngelson, J. D. & Wolynes, P. G. (1987). Spin glasses and the statistical mechanics of protein folding. Proc. Natl Acad. Sci. USA, 84, 7524-7528.
19. Bryngelson, J. D., Onuchic, J. N., Socci, N. D. & Wolynes, P. G. (1995). Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins: Struct. Funct. Genet. 21, 167-195.
20. Caflisch, A. & Karplus, M. (1994). Molecular dynamics simulation of protein denaturation: solvation of the hydrophobic cores and secondary structure of barnase. Proc. Natl Acad. Sci. USA, 91, 1746-1750.
21. Caflisch, A. & Karplus, M. (1995). Acid and thermal denaturation of barnase investigated by molecular dynamics simulations. J. Mol. Biol. 252, 672-708.
22. Daggett, V. & Levitt, M. (1992). A model of the molten globule state from molecular dynamics simulations. Proc. Natl Acad. Sci. USA, 89, 5142-5146.
23. 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 simulation. J. Mol. Biol. 257, 430-440.
24. Dill, K. A. & Chan, H. S. (1997). From Levinthal to pathways to funnels. Nature Struct. Biol. 4, 10-19.
25. Dill, K. A., Bromberg, S., Yue, K., Fiebig, K. M., Yee, D. P., Thomas, P. D. & Chan, H. S. (1995). Principles of protein folding a perspective from simple exact models. Protein Sci. 4, 561-602.
26. Eaton, W. A., Munoz, V., Thompson, P. A., Chan, C.-K. & Hofrichter, J. (1997). Submillisecond kinetics of protein folding. Curr. Opin. Struct. Biol. 7, 10-14.
27. Fan, P., Kominos, D., Kitchen, D. B., Levy, R. M. & Baum, J. (1991). Stabilization of α-helical secondary structure during high-temperature molecular-dynamics simulations of α-lactalbumin. Chem. Phys. 158, 295-301.
28. Ferrenberg, A. M. & Swendsen, R. H. (1989). Optimized Monte Carlo data analysis. Phys. Rev. Letters, 63, 1195-1198.
29. Frank, M. K., Clore, G. M. & Gronenborn, A. M. (1995). Structural and dynamic characterization of the urea denatured state of the immunoglobulin binding domain of streptococcal protein G by multidimensional heteronuclear NMR spectroscopy. Protein Sci. 4, 2605-2615.
30. Gallagher, T., Alexander, P., Bryan, P. & Gilliland, G. L. (1994). Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR. Biochemistry, 33, 4721-4729.
31. Gronenborn, A. M., Filpula, D. R., Essig, N. Z., Achari, A., Whitlow, M., Wingfield, P. T. & Clore, G. M. (1991). A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science, 253, 657-661.
32. Guo, Z. & Brooks, C. L., III (1997). Thermodynamics of protein folding: a statistical mechanical study of a small all β protein. Biopolymers, 42, 745-757.
33. Guo, Z. & Thirumalai, D. (1995). Kinetics of protein folding: nucleation mechanism, time scales, and pathways. Biopolymers, 36, 83-102.
34. Guo, Z., Brooks, C. L., III & Boczko, E. M. (1997). Exploring the folding free energy surface of a three-helix bundle protein. Proc. Natl Acad. Sci. USA, 94, 10161-10166.
35. Hagen, S. J., Hofrichter, J., Szabo, A. & Eaton, W. A. (1996). Diffusion-limited contact formation in unfolded cytochrom c: estimating the maximum rate of protein folding. Proc. Natl Acad. Sci. USA, 93, 11615-11617.
36. Hunenberger, P. H., Mark, A. E. & van Gunsteren, W. F. (1995). Computational approaches to study protein unfolding: henn egg white lysozyme as a case study. Proteins: Struct. Funct. Genet. 21, 196-213.
37. 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.
38. Jain, A. K. & Dubes, R. C. (1988). Algorithms for Clustering Data, Prentice Hall, Englewood Cliffs, NJ.
39. Jennings, P. A. & Wright, P. E. (1993). Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science, 262, 892-896.
40. Kiefhaber, T., Labhardt, A. M. & Baldwin, R. L. (1995). Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding of ribonuclease A. Nature, 375, 513-515.
41. Klimov, D. K. & Thirumalai, D. (1996). Factors governing the foldability of proteins. Proteins: Struct. Funct. Genet. 26, 411-441.
42. Kraulis, P. J. (1991). MOLSCRIPT: a programme to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
43. Kumar, S., Bouzida, D., Swendsen, R. H., Kollman, P. A. & Rosenberg, J. M. (1992). The weighted histogram analysis method for free-energy on biomolecules. I. The method. J. Comput. Chem. 13, 1011-1021.
44. Kuszewski, J., Clore, G. M. & Gronenborn, A. M. (1994). Fast folding of a prototypic polypeptide: the immunoglobulin binding domain of streptococcal protein G. Protein Sci. 3, 1945-1952.
45. Leopold, P. E., Montal, M. & Onuchic, J. N. (1992). Protein folding funnels: a kinetic approach to the sequence-structure relationship. Proc. Natl Acad. Sci. USA, 89, 8721-8725.
46. 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.
47. Li, A. & Daggett, V. (1996). Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations. J. Mol. Biol. 257, 412-429.
48. Luthey-Schulten, Z., Ramirez, B. E. & Wolynes, P. G. (1995). Helix-coil, liquid crystal and spin glass transitions of a collapsed heteropolymer. J. Phys. Chem. 99, 2177-2185.
49. Mark, A. E. & van Gunsteren, W. F. (1992). Simulation of the thermal denaturation of hen egg white lysozyme: trapping the molten globule state. Biochemistry, 31, 7745-7748.
50. Monor, D. L., Jr & Kim, P. S. (1994). Context is a major determinant of β-sheet propensity. Nature, 371, 264-267.
51. Miranker, A. D. & Dobson, C. M. (1996). Collapse and cooperativity in protein folding. Curr. Opin. Struct. Biol. 6, 31-42.
52. Miranker, A. D., Robinson, C. V., Radford, S. E. & Dobson, C. M. (1996). Investigation of protein folding by mass spectrometry. FASEB J. 10, 93-101.
53. Neira, J. L., Davis, B., Ladurner, A. G., Buckle, A. M., de Prat, Gay G. & Gersht, A. R. (1996). 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 Design, 1, 189-208.
54. Onuchic, J. N., Luthey-Schulten, Z. & Wolynes, P. G. (1997). Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem. 48, 545-600.
55. Rahman, A. & Stillinger, F. H. (1971). Molecular dynamics study of liquid water. J. Phys. Chem. 55, 3336-3359.
56. Sali, A., Shakhnovich, E. & Karplus, M. (1994). Kinetics of protein folding. A lattice model study of the requirements for folding to the native state. J. Mol. Biol. 235, 1614-1636.
57. Saven, J. & Wolynes, P. G. (1996). Local conformational signals and the statistical thermodynamics of collapsed helical proteins. J. Mol. Biol. 257, 199-216.
58. Shakhnovich, E. I. (1997). Theoretical studies of protein-folding thermodynamics and kinetics. Curr. Opin. Struct. Biol. 7, 29-40.
59. Shakhnovich, E. I. & Finkelstein, A. V. (1989). Theory of cooperative transition in protein molecules. I. Why denaturation of globular protein is a first-order phase transition. Biopolymers, 28, 1667-1680.
60. Shakhnovich, E. I. & Gutin, A. M. (1989). Formation of unique structure in polypeptide chains. Theoretical investigation with the aid of a replica approach. Biophys. Chem. 34, 187-199.
61. Sheinerman, F. B. & Brooks, C. L., III (1997). A molecular dynamics simulation study of segment B1 of protein G. Proteins: Struct. Funct. Genet. 29, 193-202.
62. Shoemaker, B. A., Wang, J. & Wlynes, P. G. (1997). Structural correlations in protein folding funnels. Proc. Natl Acad. Sci. USA, 94, 777-782.
63. Skolnick, J., Kolinski, A. & Ortiz, A. R. (1997). MONSSTER: a method for folding proteins with a small number of distance restraints. J. Mol. Biol. 265, 217-241.
64. Smith, C. K. & Regan, L. (1995). Guidelines for protein design: the energetics of β-sheet side chain interactions. Science, 270, 980-982.
65. Smith, C. K., Withka, J. M. & Regan, L. (1994). A thermodynamic scale for the β-sheet forming tendencies of the amino acids. Biochemistry, 33, 5510-5517.
66. Socci, N. D., Onuchic, J. N. & Wolynes, P. G. (1996). Diffusive dynamics of the reaction coordinate for protein folding funnels. J. Chem. Phys. 104, 5860-5868.
67. Tirado-Rives, J. & Jorgensen, W. L. (1993). Molecular dynamics simulations of the unfolding of apolyoglobin in water. Biochemistry, 32, 4175-4184.
68. Valleau, J. P. & Torrie, G. M. (1977). Byways in statistical mechanics. In A Guide to Monte Carlo for Statistical Mechanics (Berne, B. J., ed.), Part A, pp. 169-194, Plenum, New York.
69. Vijayakumar, S., Vishveshwara, S., Ravishanker, G. & Beveridge, D. L. (1993). Differential stability of β-sheets and α-helices in β-lactamase: a high temperature molecular dynamics study of unfolding intermediates. Biophys. J. 65, 2304-2312.
70. Ward, J. H., Jr (1963). Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236-244.
71. Wesson, L. & Eisenberg, D. (1992). Atomic solvation parameters applied to molecular dynamics of proteins in solution. Protein Sci. 1, 227-235.
72. Xu, S., Kamath, M. V. & Capson, D. W. (1993). Selection of partitions from hierarchy. Patt. Recog. Letters, 14, 7-15.
73. Young, W. S. & Brooks, C. L., III (1996). A microscopic view of helix propagation: N and C-terminal helix growth in alanine helices. J. Mol. Biol. 259, 560-572.