Equilibrium and kinetic folding pathways of a TIM barrel with a funneled energy landscape

Biophysical Journal

Volumn 89, Issue 1, 2005, Pages 488-505

  Finke, John M ^a   Onuchic, José N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN; PROTEIN SUBUNIT; TIM BARREL PROTEIN; TRYPTOPHAN SYNTHASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CHIRALITY; ENERGY; ESCHERICHIA COLI; HOMEOSTASIS; KINETICS; MODEL; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN FOLDING; PROTEIN STRUCTURE; SALMONELLA TYPHIMURIUM; SIMULATION; THERMODYNAMICS;

ESCHERICHIA COLI; SALMONELLA TYPHIMURIUM;

EID: 23244433815     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.059147     Document Type: Article

References (59)

1. Bryngelson, J. D., and P. G. Wolynes. 1987. Spin glasses and the statistical mechanics of protein folding. Proc. Natl. Acad. Sci. USA. 84:7524-7528.
2. Onuchic, J. N., Z. Luthey-Schulten, and P. G. Wolynes. 1997. Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem. 48:545-600.
3. Leopold, P. E., M. Montal, and J. N. Onuchic. 1992. Protein folding funnels: a kinetic approach to the sequence-structure relationship. Proc. Natl. Acad. Sci. USA. 89:8721-8725.
4. Garel, T., and H. Orland. 1988. Mean-field model for protein folding. Europhys. Lett. 6:307-310.
5. Shakhnovich, E. I., and A. M. Gutin. 1989. The nonergodic (spin-glass-like) phase of heteropolymer with quenched disordered sequence of links. Europhys. Lett. 8:327-332.
6. Dill, K. A., S. Bromberg, K. Yue, K. M. Fiebig, D. P. Yee, P. D. Thomas, and H. S. Chan. 1995. Principles of protein folding-a perspective from simple exact models. Protein Sci. 4:561-602.
7. Karplus, M., and A. Sali. 1995. Theoretical studies of protein folding and unfolding. Curr. Opin. Struct. Biol. 5:58-73.
8. Camacho, C. J., and D. Thirumalai. 1996. Denaturants can accelerate folding rates in a class of globular proteins. Protein Sci. 5:1826-1832.
9. Marqusee, S., V. H. Robbins, and R. L. Baldwin. 1989. Unusually stable helix formation in short alanine-based peptides. Proc. Natl. Acad. Sci. USA. 86:5286-5290.
10. Munoz, V., P. A. Thompson, J. Hofrichter, and W. A. Eaton. 1997. Folding dynamics and mechanism of beta-hairpin formation. Nature. 390:196-199.
11. Yang, W. Y., J. W. Pitera, W. C. Swope, and M. Gruebele. 2004. Heterogeneous folding of the trpzip hairpin: full atom simulation and experiment. J. Mol. Biol. 336:241-251.
12. Zagrovic, B., and V. S. Pande. 2003. Solvent viscosity dependence of the folding rate of a small protein: distributed computing study. J. Comput. Chem. 24:1432-1436.
13. Bursulaya, B. D., and C. L. Brooks. 1999. The folding free energy surface of a three-stranded beta-sheet protein. J. Am. Chem. Soc. 121:9947-9951.
14. Garcia, A. E., and K. Y. Sanbonmatsu. 2002. Alpha-helical stabilization by side chain shielding of backbone hydrogen bonds. Proc. Natl. Acad. Sci. USA. 99:2782-2787.
15. Daggett, V., and M. Levitt. 1992. Molecular dynamics simulations of helix denaturation. J. Mol. Biol. 223:1121-1138.
16. Garcia, A. E., and J. N. Onuchic. 2003. Folding a protein in a computer: an atomic description of the folding/unfolding of protein A. Proc. Natl. Acad. Sci. USA. 100:13898-13903.
17. Cheung, M. S., J. M. Finke, B. Callahan, and J. N. Onuchic. 2003. Exploring the interplay between topology and secondary structural formation in the protein folding problem. J. Phys. Chem. B. 107:11193-11200.
18. Chan, H. S., and K. A. Dill. 1993. The protein folding problem. Phys. Today. 46:24-32.
19. Clementi, C., P. A. Jennings, and J. N. Onuchic. 2000. How native-state topology affects the folding of dihydrofolate reductase and interleukin-1beta. Proc. Natl. Acad. Sci. USA. 97:5871-5876.
20. Ding, F., N. V. Dokholyan, S. V. Buldyrev, H. E. Stanley, and E. I. Shakhnovich. 2002. Direct molecular dynamics observation of protein folding transition state ensemble. Biophys. J. 83:3525-3532.
21. Shea, J. E., J. N. Onuchic, and C. L. Brooks. 1999. Exploring the origins of topological frustration: design of a minimally frustrated model of fragment B of protein A. Proc. Natl. Acad. Sci. USA. 96:12512-12517.
22. Klimov, D. K., and D. Thirumalai. 2000. Mechanisms and kinetics of beta-hairpin formation. Proc. Natl. Acad. Sci. USA. 97:2544-2549.
23. Godzik, A., J. Skolnick, and A. Kolinski. 1992. Simulations of the folding pathway of triose phosphate isomerase-type alpha/beta barrel proteins. Proc. Natl. Acad. Sci. USA. 89:2629-2633.
24. Finke, J. M., M. S. Cheung, and J. N. Onuchic. 2004. A structural model of polyglutamine determined from a host-guest method combining experiments and landscape theory. Biophys. J. 87:1900-1918.
25. Benitez-Cardoza, C. G., A. Rojo-Dominguez, and A. Hernandez-Arana. 2001. Temperature-induced denaturation and renaturation of triosephosphate isomerase from Saccharomyces cerevisiae: evidence of dimerization coupled to refolding of the thermally unfolded protein. Biochemistry. 40:9049-9058.
26. Najera, H., M. Costas, and D. A. Fernandez-Velasco. 2003. Thermodynamic characterization of yeast triosephosphate isomerase refolding: insights into the interplay between function and stability as reasons for the oligomeric nature of the enzyme. Biochem. J. 370:785-792.
27. Silverman, J. A., and P. B. Harbury. 2002. The equilibrium unfolding pathway of a (beta/alpha)8 barrel. J. Mol. Biol. 324:1031-1040.
28. Chanez-Cardenas, M. E., D. A. Fernandez-Velasco, E. Vazquez-Contreras, R. Coria, G. Saab-Rincon, and R. Perez-Montfort. 2002. Unfolding of triosephosphate isomerase from Trypanosoma brucei: identification of intermediates and insight into the denaturation pathway using tryptophan mutants. Arch. Biochem. Biophys. 399:117-129.
29. Vadrevu, R., C. J. Falzone, and C. R. Matthews. 2003. Partial NMR assignments and secondary structure mapping of the isolated alpha subunit of Escherichia coli tryptophan synthase, a 29-kD TIM barrel protein. Protein Sci. 12:185-191.
30. Beasty, A. M., and C. R. Matthews. 1985. Characterization of an early intermediate in the folding of the alpha subunit of tryptophan synthase by hydrogen exchange measurement. Biochemistry. 24:3547-3553.
31. Forsyth, W. R., and C. R. Matthews. 2002. Folding mechanism of indole-3-glycerol phosphate synthase from Sulfolobus solfataricus: a test of the conservation of folding mechanisms hypothesis in (beta(alpha))(8) barrels. J. Mol. Biol. 320:1119-1133.
32. Jasanoff, A., B. Davis, and A. R. Fersht. 1994. Detection of an intermediate in the folding of the (beta alpha)8-barrel N-(5′- phosphoribosyl) anthranilate isomerase from Escherichia coli. Biochemistry. 33:6350-6355.
33. Soberon, X., P. Fuentes-Gallego, and G. Saab-Rincon. 2004. In vivo fragment complementation of a (beta/alpha)(8) barrel protein: generation of variability by recombination. FEBS Lett. 560:167-172.
34. Pan, H., and D. L. Smith. 2003. Quaternary structure of aldolase leads to differences in its folding and unfolding intermediates. Biochemistry. 42:5713-5721.
35. Deng, Y., and D. L. Smith. 1999. Rate and equilibrium constants for protein unfolding and refolding determined by hydrogen exchange-mass spectrometry. Anal. Biochem. 276:150-160.
36. Pan, H., A. S. Raza, and D. L. Smith. 2004. Equilibrium and kinetic folding of rabbit muscle triosephosphate isomerase by hydrogen exchange mass spectrometry. J. Mol. Biol. 336:1251-1263.
37. Rojsajjakul, T., P. Wintrode, R. Vadrevu, C. Robert Matthews, and D. L. Smith. 2004. Multi-state unfolding of the alpha subunit of tryptophan synthase, a TIM barrel protein: insights into the secondary structure of the stable equilibrium intermediates by hydrogen exchange mass spectrometry. J. Mol. Biol. 341:241-253.
38. Saab-Rincon, G., P. J. Gualfetti, and C. R. Matthews. 1996. Mutagenic and thermodynamic analyses of residual structure in the alpha-subunit of tryptophan synthase. Biochemistry. 35:1988-1994.
39. Gualfetti, P. J., O. Bilsel, and C. R. Matthews. 1999. The progressive development of structure and stability during the equilibrium folding of the alpha subunit of tryptophan synthase from Escherichia coli. Protein Sci. 8:1623-1635.
40. Zitzewitz, J. A., P. J. Gualfetti, I. A. Perkons, S. A. Wasta, and C. R. Matthews. 1999. Identifying the structural boundaries of independent folding domains in the alpha subunit of tryptophan synthase, a beta/alpha barrel protein. Protein Sci. 8:1200-1209.
41. Bilsel, O., J. A. Zitzewitz, K. E. Bowers, and C. R. Matthews. 1999. Folding mechanism of the alpha-subunit of tryptophan synthase, an alpha/beta barrel protein: global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels. Biochemistry. 38:1018-1029.
42. Wu, Y., and C. R. Matthews. 2003. Proline replacements and the simplification of the complex, parallel channel folding mechanism for the alpha subunit of Trp synthase, a TIM barrel protein. J. Mol. Biol. 330:1131-1144.
43. Sanchez del Pino, M. M., and A. R. Fersht. 1997. Nonsequential unfolding of the alpha/beta barrel protein indole-3-glycerol-phosphate synthase. Biochemistry. 36:5560-5565.
44. Andreotti, G., M. V. Cubellis, M. D. Palo, D. Fessas, G. Sannia, and G. Marino. 1997. Stability of a thermophilic TIM-barrel enzyme: indole-3-glycerol phosphate synthase from the thermophilic archaeon Sulfolobus solfataricus. Biochem. J. 323:259-264.
45. Tsuji, T., B. A. Chrunyk, X. Chen, and C. R. Matthews. 1993. Mutagenic analysis of the interior packing of an alpha/beta barrel protein. Effects on the stabilities and rates of interconversion of the native and partially folded forms of the alpha subunit of tryptophan synthase. Biochemistry. 32:5566-5575.
46. Anderson, W. L., and D. B. Wetlaufer. 1976. The folding pathway of reduced lysozyme. J. Biol. Chem. 251:3147-3153.
47. Finke, J. M., and P. A. Jennings. 2001. Early aggregated states in the folding of interleukin-Iβ. J. Biol. Phys. 27:119-131.
48. Clementi, C., H. Nymeyer, and J. N. Onuchic. 2000. Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol. 298:937-953.
49. Pearlman, D. A., D. A. Case, J. W. Caldwell, W. R. Ross, T. E. Cheatham III, S. DeBolt, D. Ferguson, G. Seibel, and P. A. Kollman. 1995. AMBER, a computer program for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to elucidate the structures and energies of molecules. Campus. Phys. Commun. 91:1-41.
50. Berendsen, H. J. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
51. Hurle, M. R., N. B. Tweedy, and C. R. Matthews. 1986. Synergism in folding of a double mutant of the alpha subunit of tryptophan synthase. Biochemistry. 25:6356-6360.
52. Go, N. 1983. Theoretical studies of protein folding. Annu. Rev. Biophys. Bioeng. 12:183-210.
53. Sobolev, V., A. Sorokine, J. Prilusky, E. E. Abola, and M. Edelman. 1999. Automated analysis of interatomic contacts in proteins. Bioinformatics. 15:327-332.
54. Kumar, S., D. Bouzida, R. H. Swendsen, P. A. Kollman, and J. M. Rosenberg. 1992. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem. 13:1011-1021.
55. Barshop, B. A., R. F. Wrenn, and C. Frieden. 1983. Analysis of numerical methods for computer simulation of kinetic processes: development of KINSIM-a flexible, portable system. Anal. Biochem. 130:134-145.
56. Socci, N. D., and J. N. Onuchic. 1994. Folding kinetics of protein like heteropolymers. J. Chem. Phys. 101:1519-1528.
57. Camacho, C. J., and D. Thirumalai. 1995. Theoretical predictions of folding pathways by using the proximity rule, with applications to bovine pancreatic trypsin inhibitor. Proc. Natl. Acad. Sci. USA. 92:1277-1281.
58. Kiefhaber, T. 1995. Kinetic traps in lysozyme folding. Proc. Natl. Acad. Sci. USA. 92:9029-9033.
59. Kuwata, K., R. Shastry, H. Cheng, M. Hoshino, C. A. Batt, Y. Goto, and H. Roder. 2001. Structural and kinetic characterization of early folding events in beta-lactoglobulin. Nat. Struct. Biol. 8:151-155.