Downhill versus Barrier-Limited Folding of BBL 2: Mechanistic Insights from Kinetics of Folding Monitored by Independent Tryptophan Probes

Journal of Molecular Biology

Volumn 387, Issue 4, 2009, Pages 975-985

  Neuweiler, Hannes ^a,b   Sharpe, Timothy D ^a,b   Johnson, Christopher M ^a,b   Teufel, Daniel P ^a,b   Ferguson, Neil ^a,b   Fersht, Alan R ^a,b  

^a MRC CENTRE FOR PROTEIN ENGINEERING   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

barrier limited folding; peripheral subunit binding domain; temperature jump spectroscopy; tryptophan fluorescence; ultrafast protein folding

Indexed keywords

BBL 2 PROTEIN; PROTEIN DERIVATIVE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONFORMATION; CONTROLLED STUDY; DENATURATION; EQUILIBRIUM CONSTANT; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; INTROSPECTION; KINETICS; MONITORING; MUTANT; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; TEMPERATURE; THERMODYNAMICS;

EID: 62649174053     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.12.056     Document Type: Article

References (43)

1. Allen M.D., Broadhurst R.W., Solomon R.G., and Perham R.N. Interaction of the E2 and E3 components of the pyruvate dehydrogenase multienzyme complex of Bacillus stearothermophilus. Use of a truncated protein domain in NMR spectroscopy. FEBS J. 272 (2005) 259-268
2. Kalia Y.N., Brocklehurst S.M., Hipps D.S., Appella E., Sakaguchi K., and Perham R.N. The high-resolution structure of the peripheral subunit-binding domain of dihydrolipoamide acetyltransferase from the pyruvate dehydrogenase multienzyme complex of Bacillus stearothermophilus. J. Mol. Biol. 230 (1993) 323-341
3. Robien M.A., Clore G.M., Omichinski J.G., Perham R.N., Appella E., Sakaguchi K., and Gronenborn A.M. Three-dimensional solution structure of the E3-binding domain of the dihydrolipoamide succinyltransferase core from the 2-oxoglutarate dehydrogenase multienzyme complex of Escherichia coli. Biochemistry 31 (1992) 3463-3471
4. Frank R.A., Pratap J.V., Pei X.Y., Perham R.N., and Luisi B.F. The molecular origins of specificity in the assembly of a multienzyme complex. Structure 13 (2005) 1119-1130
5. Mande S.S., Sarfaty S., Allen M.D., Perham R.N., and Hol W.G. Protein-protein interactions in the pyruvate dehydrogenase multienzyme complex: dihydrolipoamide dehydrogenase complexed with the binding domain of dihydrolipoamide acetyltransferase. Structure 4 (1996) 277-286
6. Ferguson N., Day R., Johnson C.M., Allen M.D., Daggett V., and Fersht A.R. Simulation and experiment at high temperatures: ultrafast folding of a thermophilic protein by nucleation-condensation. J. Mol. Biol. 347 (2005) 855-870
7. Ferguson N., Sharpe T.D., Johnson C.M., and Fersht A.R. The transition state for folding of a peripheral subunit-binding domain contains robust and ionic-strength dependent characteristics. J. Mol. Biol. 356 (2006) 1237-1247
8. Ferguson N., Sharpe T.D., Schartau P.J., Sato S., Allen M.D., Johnson C.M., et al. Ultra-fast barrier-limited folding in the peripheral subunit-binding domain family. J. Mol. Biol. 353 (2005) 427-446
9. Sharpe T.D., Ferguson N., Johnson C.M., and Fersht A.R. Conservation of transition state structure in fast folding peripheral subunit-binding domains. J. Mol. Biol. 383 (2008) 224-237
10. Spector S., and Raleigh D.P. Submillisecond folding of the peripheral subunit-binding domain. J. Mol. Biol. 293 (1999) 763-768
11. Jackson S.E., and Fersht A.R. Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry 30 (1991) 10428-10435
12. Bai Y. Hidden intermediates and levinthal paradox in the folding of small proteins. Biochem. Biophys. Res. Commun. 305 (2003) 785-788
13. Daggett V., and Fersht A. The present view of the mechanism of protein folding. Nat. Rev., Mol. Cell Biol. 4 (2003) 497-502
14. Garcia-Mira M.M., Sadqi M., Fischer N., Sanchez-Ruiz J.M., and Munoz V. Experimental identification of downhill protein folding. Science 298 (2002) 2191-2195
15. Naganathan A.N., Perez-Jimenez R., Sanchez-Ruiz J.M., and Munoz V. Robustness of downhill folding: guidelines for the analysis of equilibrium folding experiments on small proteins. Biochemistry 44 (2005) 7435-7449
16. Sadqi M., Fushman D., and Munoz V. Atom-by-atom analysis of global downhill protein folding. Nature 442 (2006) 317-321
17. Bryngelson J.D., Onuchic J.N., Socci N.D., and Wolynes P.G. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins 21 (1995) 167-195
18. Oliva F.Y., and Munoz V. A simple thermodynamic test to discriminate between two-state and downhill folding. J. Am. Chem. Soc. 126 (2004) 8596-8597
19. Ferguson N., Schartau P.J., Sharpe T.D., Sato S., and Fersht A.R. One-state downhill versus conventional protein folding. J. Mol. Biol. 344 (2004) 295-301
20. Cho S.S., Weinkam P., and Wolynes P.G. Origins of barriers and barrierless folding in BBL. Proc. Natl. Acad. Sci. USA 105 (2008) 118-123
21. Yu W., Chung K., Cheon M., Heo M., Han K.H., Ham S., and Chang I. Cooperative folding kinetics of BBL protein and peripheral subunit-binding domain homologues. Proc. Natl. Acad. Sci. USA 105 (2008) 2397-2402
22. Knott M., and Chan H.S. Criteria for downhill protein folding: calorimetry, chevron plot, kinetic relaxation, and single-molecule radius of gyration in chain models with subdued degrees of cooperativity. Proteins 65 (2006) 373-391
23. Zuo G., Wang J., and Wang W. Folding with downhill behavior and low cooperativity of proteins. Proteins 63 (2006) 165-173
24. Zhang J., Li W., Wang J., Qin M., and Wang W. All-atom replica exchange molecular simulation of protein BBL. Proteins 72 (2008) 1038-1047
25. Tanford C. Protein denaturation. Adv. Protein Chem. 23 (1968) 121-282
26. Myers J.K., Pace C.N., and Scholtz J.M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4 (1995) 2138-2148
27. Huang F., Sato S., Sharpe T.D., Ying L., and Fersht A.R. Distinguishing between cooperative and unimodal downhill protein folding. Proc. Natl Acad. Sci. USA 104 (2007) 123-127
28. a. J. Mol. Biol. 387 (2009) 986-992
29. Matouschek A., Otzen D.E., Itzhaki L.S., Jackson S.E., and Fersht A.R. Movement of the position of the transition state in protein folding. Biochemistry 34 (1995) 13656-13662
30. Kuwajima K. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins 6 (1989) 87-103
31. Ptitsyn O.B. Protein folding-hypotheses and experiments. J. Protein Chem. 6 (1987) 273-293
32. Griko Y.V., Freire E., and Privalov P.L. Energetics of the alpha-lactalbumin states: a calorimetric and statistical thermodynamic study. Biochemistry 33 (1994) 1889-1899
33. Griko Y.V., and Privalov P.L. Thermodynamic puzzle of apomyoglobin unfolding. J. Mol. Biol. 235 (1994) 1318-1325
34. Yutani K., Ogasahara K., and Kuwajima K. Absence of the thermal transition in apo-alpha-lactalbumin in the molten globule state. A study by differential scanning microcalorimetry. J. Mol. Biol. 228 (1992) 347-350
35. Ferguson N., Sharpe T.D., Johnson C.M., Schartau P.J., and Fersht A.R. Structural biology: analysis of 'downhill' protein folding. Nature 445 (2007) E14-E15 discussion E17-18
36. Sadqi M., Fushman D., and Munoz V. Structural biology-analysis of protein-folding cooperativity-reply. Nature 445 (2007) E17-E18
37. Zhou Z., and Bai Y. Structural biology: analysis of protein-folding cooperativity. Nature 445 (2007) E16-E17 discussion E17-18
38. Riddle D.S., Grantcharova V.P., Santiago J.V., Alm E., Ruczinski I., and Baker D. Experiment and theory highlight role of native state topology in SH3 folding. Nat. Struct. Biol. 6 (1999) 1016-1024
39. Schon O., Friedler A., Bycroft M., Freund S.M., and Fersht A.R. Molecular mechanism of the interaction between MDM2 and p53. J. Mol. Biol. 323 (2002) 491-501
40. Ferguson N., Johnson C.M., Macias M., Oschkinat H., and Fersht A. Ultrafast folding of WW domains without structured aromatic clusters in the denatured state. Proc. Natl Acad. Sci. USA 98 (2001) 13002-13007
41. Religa T.L., Johnson C.M., Vu D.M., Brewer S.H., Dyer R.B., and Fersht A.R. The helix-turn-helix motif as an ultrafast independently folding domain: the pathway of folding of Engrailed homeodomain. Proc. Natl Acad. Sci. USA 104 (2007) 9272-9277
42. Santoro M.M., and Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27 (1988) 8063-8068
43. Johnson C.M., and Fersht A.R. Protein stability as a function of denaturant concentration: the thermal stability of barnase in the presence of urea. Biochemistry 34 (1995) 6795-6804