Folding λ-repressor at its speed limit

Biophysical Journal

Volumn 87, Issue 1, 2004, Pages 596-608

  Yang, Wei Yuan ^a   Gruebele, Martin ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; GLUCOSE; LAMBDA REPRESSOR PROTEIN; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONCENTRATION (PARAMETERS); CORRELATION ANALYSIS; DYNAMICS; ENERGY; KINETICS; PHASE TRANSITION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE; SIMULATION; STRUCTURE ANALYSIS;

MUS;

EID: 3042814557     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.103.039040     Document Type: Article

References (70)

1. Baker, D. 2000. A surprising simplicity to protein folding. Nature. 405:39-42.
2. Ballew, R. M., J. Sabelko, and M. Gruebele. 1996a. Direct observation of fast protein folding: the initial collapse of apomyoglobin. Proc. Natl. Acad. Sci. USA. 93:5759-5764.
3. Ballew, R. M., J. Sabelko, C. Reiner, and M. Gruebele. 1996b. A single-sweep, nanosecond time resolution laser temperature-jump apparatus. Rev. Sci. Instrum. 67:3694-3699.
4. Becker, O. M., and M. Karplus. 1997. The topology of multidimensional potential energy surfaces: theory and application to peptide structure and kinetics. J. Chem. Phys. 22:1495-1517.
5. Berne, B. J. 1993. Theoretical and numerical methods in rate theory. In Activated Barrier Crossing: Applications in Physics, Chemistry and Biology. P. Hänggi and G. R. Fleming, editors. World Scientific, Singapore. 82-119.
6. Bieri, O., J. Wirz, B. Hellrung, M. Schutkowski, M. Drewello, and T. Kiefhaber. 1999. The speed limit for protein folding measured by triplet-triplet energy transfer. Proc. Natl. Acad. Sci. USA. 96:9597-601.
7. Bryngelson, J. D., J. N. Onuchic, N. D. Socci, and P. G. Wolynes. 1995. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins. 21:167-195.
8. 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.
9. Burton, R. E., G. S. Huang, M. A. Daugherty, T. L. Calderone, and T. G. Oas. 1997. The energy landscape of a fast-folding protein mapped by Ala→Gly substitutions. Nat. Struct. Biol. 4:305-10.
10. Burton, R. E., J. K. Myers, and T. G. Oas. 1998. Protein folding dynamics: quantitative comparison between theory and experiment. Biochemistry. 37:5337-43.
11. Camacho, C. J., and D. Thirumalai. 1993. Kinetics and thermodynamics of folding in model proteins. Proc. Nat. Acad. Sci. USA. 90:6369-6372.
12. Camacho, C. J., and D. Thirumalai. 1995. From minimal models to real proteins: timescales for folding kinetics. J. de Physique I. 5:1457-1467.
13. Chandler, D. 1989. Modern Statistical Mechanics. Oxford University Press, Oxford, UK.
14. Chang, I. J., J. C. Lee, J. R. Winkler, and H. B. Gray. 2003. The protein-folding speed limit: intrachain diffusion times set by electron-transfer rates in denatured Ru(NH3)(5)(His-33)-Zn-cytochrome c. Proc. Nat. Acad. Sci. USA. 100:3838-3840.
15. 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.
16. Creighton, G. E. 1993. Proteins, 2nd ed. W. H. Freeman and Company, New York.
17. Feng, H. Q., J. Takei, R. Lipsitz, N. Tjandra, and Y. W. Bai. 2003. Specific non-native hydrophobic interactions in a hidden folding intermediate: Implications for protein folding. Biochemistry. 42:12461-12465.
18. Garcia, C., C. Nishimura, S. Cavagnero, H. J. Dyson, and P. E. Wright. 2000. Changes in the apomyoglobin folding pathway caused by mutation of the distal histidine residue. Biochemistry. 39:11227-11237.
19. Ghaemmaghami, S., J. M. Word, R. E. Burton, J. S. Richardson, and T. G. Oas. 1998. Folding kinetics of a fluorescent variant of monomeric lambda repressor. Biochemistry. 37:9179-85.
20. Gruebele, M. 2002. Protein folding: the free energy surface. Curr. Opinion. Struct. Biol. 12:161-168.
21. Gruebele, M., and A. H. Zewail. 1990. Ultrafast reaction dynamics. Phys. Today. 43:24-33.
22. Hagen, S. J., J. Hofrichter, A. Szabo, and W. A. Eaton. 1996. Diffusion-limited contact formation in unfolded cytochrome c: estimating the maximum rate of protein folding. Proc. Natl. Acad. Sci. USA. 93:11615-7.
23. Hecht, M. H., J. M. Sturtevant, and R. T. Sauer. 1984. Effect of single amino acid replacements on the thermal stability of the NH2 terminal domain of phage lambda repressor. Proc. Nat. Acad. Sci. USA. 81:5685-5689.
24. Huang, G. S., and T. G. Oas. 1995. Submillisecond folding of monomeric lambda repressor. Proc. Natl. Acad. Sci. USA. 92:6878-6882.
25. Ikura, T., T. Hayano, N. Takahashi, and K. Kuwajima. 2000. Fast folding of E. coli cyclophilin A: a hypothesis of a unique hydrophobic core with a phenylalanine cluster. J. Mol. Biol. 297:791-802.
26. Ivankov, D. N., S. O. Garbuzynskiy, E. Alm, K. W. Plaxco, D. Baker, and A. V. Finkelstein. 2003. Contact order revisited: influence of protein size on the folding rate. Protein Sci. 12:2057-2062.
27. Jackson, S. E. 1998. How do small single-domain proteins fold? Fold. Des. 3:R81-91.
28. Jackson, S. E., N. elMasry, and A. R. Fersht. 1993. 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.
29. Jacob, M., M. Geeves, G. Holtermann, and F. X. Schmid. 1999. Diffusional barrier crossing in a two-state protein folding reaction. Nat. Struct. Biol. 6:923-926.
30. Jacob, M., T. Schindler, J. Balbach, and F. X. Schmid. 1997. Diffusion control in an elementary protein folding reaction. Proc. Nat. Acad. Sci. USA. 94:5622-5627.
31. Jacob, M., and F. X. Schmid. 1999. Protein folding as a diffusional process. Biochemistry. 38:13773-13779.
32. Jas, G. S., W. A. Eaton, and J. Hofrichter. 2001. Effect of viscosity on the kinetics of alpha-helix and beta-hairpin formation. J. Phys. Chem. B. 105:261-272.
33. Jennings, P., and P. Wright. 1993. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science. 262:892-895.
34. Klimov, D. K., and D. Thirumalai. 1997. Viscosity dependence of the folding rates of proteins. Phys. Rev. Lett. 79:317-20.
35. Koga, N., and S. Takada. 2001. Roles of native topology and chain-length scaling in protein folding: a simulation study with a Go-like model. J. Mol. Biol. 313:171-180.
36. Kramers, H. A. 1940. Brownian motion in a field of force and the diffusion model of chemical reactions. Physica. 7:284-306.
37. Lacroix, E., A. R. Viguera, and L. Serrano. 1998. Elucidating the folding problem of alpha-helices: local motifs, long-range electrostatics, ionic-strength dependence and prediction of NMR parameters. J. Mol. Biol. 284:173-191.
38. Ladurner, A. G., and A. R. Fersht. 1999. Upper limit of the timescale for diffusion and chain collapse in chymotrypsin inhibitor 2. Nat. Struct. Biol. 6:28-31.
39. Lapidus, L. J., W. A. Eaton, and J. Hofrichter. 2000. Measuring the rate of intramolecular contact formation in polypeptides. Proc. Natl. Acad. Sci. USA. 97:7220-7225.
40. Levinthal, C. 1969. Mossbauer spectroscopy in biological systems. Proceedings of a meeting held at Allerton House, Monticello, IL. University of Illinois, Urbana-Champaign, IL. 22-24.
41. Mayor, U., N. R. Guydosh, C. M. Johnson, J. G. Grossmann, S. Sato, G. S. Jas, S. M. Freund, D. O. Alonso, V. Daggett, and A. R. Fersht. 2003. The complete folding pathway of a protein from nanoseconds to microseconds. Nature. 421:863-867.
42. Metzler, R., J. Klafter, and J. Jortner. 1999. Hierarchies and logarithmic oscillations in the temporal relaxation patterns of proteins and other complex systems. Proc. Natl. Acad. Sci. USA. 96:11085-11089.
43. Metzler, R., J. Klafter, J. Jortner, and M. Volk. 1998. Multiple timescales for dispersive kinetics in early events of peptide folding. Chem. Phys. Lett. 293:477-484.
44. Myers, J. K., and T. G. Oas. 1999. Contribution of a buried hydrogen bond to lambda repressor folding kinetics. Biochemistry. 38:6761-6768.
45. Osváth, S., J. Sabelko, and M. Gruebele. 2003. Tuning the heterogeneous early folding dynamics of phosphoglycerate kinase. J. Mol. Biol. 333:187-199.
46. Ozkan, S. B., K. A. Dill, and I. Bahar. 2002. Fast-folding protein kinetics, hidden intermediates, and the sequential stabilization model. Protein Sci. 11:1958-1970.
47. Pace, C. N. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131:266-280.
48. Pappenberger, G., C. Saudan, M. Becker, A. E. Merbach, and T. Kiefhaber. 2000. Denaturant-induced movement of the transition state of protein folding revealed by high-pressure stopped-flow measurements. Proc. Nat. Acad. Sci. USA. 97:17-22.
49. Plaxco, K. W., and D. Baker. 1998. Limited internal friction in the rate-limiting step of a two-state protein folding reaction. Proc. Natl. Acad. Sci. USA. 95:13591-13596.
50. Plaxco, K. W., K. T. Simons, and D. Baker. 1998. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277:985-994.
51. Pogorelov, T. V., and Z. Luthey-Schulten. Variations in the fast folding rates of the λ-repressor: a hybrid molecular dynamics study. Biophys. J. 87:207-214.
52. Portman, J. J., S. Takada, and P. G. Wolynes. 1998. Variational theory for site resolved protein folding free energy surfaces. Phys. Rev. Lett. 81:5237-5240.
53. Portman, J. J., S. Takada, and P. G. Wolynes. 2001a. Microscopic theory of protein folding rates. I. Fine structure of the free energy profile and folding routes from a variational approach. J. Chem. Phys. 114:5069-5081.
54. Portman, J. J., S. Takada, and P. G. Wolynes. 2001b. Microscopic theory of protein folding rates. II. Local reaction coordinates and chain dynamics. J. Chem. Phys. 114:5082-5096.
55. Qiu, L., C. Zachariah, and S. J. Hagen. 2003. Fast chain contraction during protein folding: "foldability" and collapse dynamics. Phys. Rev. Lett. 90:168103.
56. Qiu, L. L., S. A. Pabit, A. E. Roitberg, and S. J. Hagen. 2002. Smaller and faster: the 20-residue Trp-cage protein folds in 4 micros. J. Am. Chem. Soc. 124:12952-12953.
57. Sabelko, J., J. Ervin, and M. Gruebele. 1999. Observation of strange kinetics in protein folding. Proc. Nat. Acad. Sci. USA. 96:6031-6036.
58. Sadqi, M., L. J. Lapidus, and V. Muñoz. 2003. How fast is protein hydrophobic collapse. Proc. Nat. Acad. Sci. USA. 100:12117-12122.
59. Schuler, B., E. A. Lipman, and W. A. Eaton. 2002. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature. 419:743-747.
60. Shea, J., and C. L. Brooks. 2001. From folding theories to folding proteins: a review and assessment of simulation studies of protein folding and unfolding. Annu. Rev. Phys. Chem. 52:499-535.
61. Silow, M., Y. Tan, A. R. Fersht, and M. Oliveberg. 1999. Formation of short-lived protein aggregates directly from the coil in two-state folding. Biochemistry. 38:13006-13012.
62. Socci, N. D., J. N. Onuchic, and P. G. Wolynes. 1998. Protein folding mechanisms and the multidimensional folding funnel. Proteins. 32:136-158.
63. Tanford, C. 1968. Protein denaturation. Adv. Protein Chem. 23:121-282.
64. Thompson, P. A., W. A. Eaton, and J. Hofrichter. 1997. Laser temperature jump study of the helix ↔ coil kinetics of an alanine peptide interpreted with a 'kinetic zipper' model. Biochemistry. 36:9200-9210.
65. 562 folding triggered by electron transfer. J. Am. Chem. Soc. 119:9562-9563.
66. Yang, W., and M. Gruebele. 2004. Detection-dependent kinetics as a probe of folding landscape microstructure. J. Am. Chem. Soc. In press.
67. Yang, W. Y., and M. Gruebele. 2003. Folding at the speed limit. Nature. 423:193-197.
68. 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.
69. Zhu, Y., D. O. V. Alonso, K. Maki, C.-Y. Huang, S. J. Lahr, V. Daggett, H. Roder, W. F. DeGrado, and F. Gai. 2003. Ultrafast folding of alpha-3-D, a de novo designed three-helix bundle protein. Proc. Natl. Acad. Sci. USA. 100:15486-15491.
70. Zwanzig, R. 1988. Diffusion in a rough potential. Proc. Natl. Acad. Sci. USA. 85:2029-2030.