Φ-Analysis at the Experimental Limits: Mechanism of β-Hairpin Formation

Journal of Molecular Biology

Volumn 360, Issue 4, 2006, Pages 865-881

  Petrovich, Miriana ^a   Jonsson, Amanda L ^b,c   Ferguson, Neil ^a   Daggett, Valerie ^b,c   Fersht, Alan R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

computer simulation; protein folding; two state; ultrafast

Indexed keywords

BETA HAIRPIN PEPTIDE; BINDING PROTEIN; FORMIN BINDING PROTEIN 28; GUANIDINE; PEPTIDE; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; DENATURATION; ENERGY; HYDROGEN BOND; MOLECULAR DYNAMICS; MUTATION; POLARIZATION; PRIORITY JOURNAL; PROTEIN FOLDING; REPRODUCIBILITY; SIMULATION; TEMPERATURE;

EID: 33745606942     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.05.050     Document Type: Article

References (43)

1. Fersht A.R., and Daggett V. Protein folding and unfolding at atomic resolution. Cell 108 (2002) 573-582
2. Fersht A.R., Leatherbarrow R.J., and Wells T.C.N. Quantitative analysis of structure-activity relationships in engineered proteins by linear free-energy relationships. Nature 322 (1986) 284-286
3. Fersht A.R., Matouschek A., and Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224 (1992) 771-782
4. Fersht A.R., and Sato S. Phi-value analysis and the nature of protein-folding transition states. Proc. Natl Acad. Sci. USA 101 (2004) 7976-7981
5. Chan D.C., Bedford M.T., and Leder P. Formin binding proteins bear WWP/WW domains that bind proline-rich peptides and functionally resemble SH3 domains. EMBO J. 15 (1996) 1045-1054
6. Macias M.J., Gervais V., Civera C., and Oschkinat H. Structural analysis of WW domains and design of a WW prototype. Nature Struct. Biol. 7 (2000) 375-379
7. Andre B., and Springael J.Y. WWP, a new amino acid motif present in single or multiple copies in various proteins including dystrophin and the SH3-binding Yes-associated protein YAP65. Biochem. Biophys. Res. Commun. 205 (1994) 1201-1205
8. Bork P., and Sudol M. The WW domain: a signalling site in dystrophin?. Trends Biochem. Sci. 19 (1994) 531-533
9. Sudol M., and Hunter T. New wrinkles for an old domain. Cell 103 (2000) 1001-1004
10. Macias M.J., Hyvonen M., Baraldi E., Schultz J., Sudol M., Saraste M., and Oschkinat H. Structure of the WW domain of a kinase-associated protein complexed with a proline-rich peptide. Nature 382 (1996) 646-649
11. Koepf E.K., Petrassi H.M., Sudol M., and Kelly J.W. WW: an isolated three-stranded antiparallel beta-sheet domain that unfolds and refolds reversibly; evidence for a structured hydrophobic cluster in urea and GdnHCl and a disordered thermal unfolded state. Protein Sci. 8 (1999) 841-853
12. Crane J.C., Koepf E.K., Kelly J.W., and Gruebele M. Mapping the transition state of the WW domain beta-sheet. J. Mol. Biol. 298 (2000) 222-283
13. 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
14. Ferguson N., Pires J.R., Toepert F., Johnson C.M., Pan Y.P., Volkmer-Engert R., et al. Using flexible loop mimetics to extend phi-value analysis to secondary structure interactions. Proc. Natl Acad. Sci. USA 98 (2001) 13008-13013
15. Jager M., Nguyen H., Crane J.C., Kelly J.W., and Gruebele M. The folding mechanism of a beta-sheet: the WW domain. J. Mol. Biol. 311 (2001) 373-393
16. Jiang X., Kowalski J., and Kelly J.W. Increasing protein stability using a rational approach combining sequence homology and structural alignment: stabilizing the WW domain. Protein Sci. 10 (2001) 1454-1465
17. Kaul R., Angeles A.R., Jager M., Powers E.T., and Kelly J.W. Incorporating beta-turns and a turn mimetic out of context in loop 1 of the WW domain affords cooperatively folded beta-sheets. J. Am. Chem. Soc. 123 (2001) 5206-5212
18. Ferguson N., Berriman J., Petrovich M., Sharpe T.D., Finch J.T., and Fersht A.R. Rapid amyloid fiber formation from the fast-folding WW domain FBP28. Proc. Natl Acad. Sci. USA 100 (2003) 9814-9819
19. Deechongkit S., Nguyen H., Jager M., Powers E.T., Gruebele M., and Kelly J.W. β-Sheet folding mechanisms from perturbation kinetics. Curr. Opin. Struct. Biol. 2006 (2006) 1-8
20. Deechongkit S., Nguyen H., Powers E.T., Dawson P.E., Gruebele M., and Kelly J.W. Context-dependent contributions of backbone hydrogen bonding to beta-sheet folding energetics. Nature 430 (2004) 101-105
21. Jackson S.E., and Fersht A.R. Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry 30 (1991) 10428-10435
22. Clarke J., and Fersht A.R. Engineered disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation. Biochemistry 32 (1993) 4322-4329
23. Jackson S.E., and Fersht A.R. Folding of chymotrypsin inhibitor 2. 2. Influence of proline isomerization on the folding kinetics and thermodynamic characterization of the transition state of folding. Biochemistry 30 (1991) 10436-10443
24. Sato S., Religa T.L., and Fersht A.R. Phi-Analysis of the folding of the B domain of Protein A using multiple optical probes. J. Mol. Biol. (2006) accompanying article. doi:10.1016/j.jmb.2006.05.051
25. Day R., and Daggett V. Ensemble versus single-molecule protein unfolding. Proc. Natl Acad. Sci. USA 102 (2005) 13445-13450
26. Li A.J., and Daggett V. Characterization of the transition-state of protein unfolding by use of uolecular-dynamics-chymotrypsin inhibitor-2. Proc. Natl Acad. Sci. USA 91 (1994) 10430-10434
27. Li A.J., and Daggett V. Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations. J. Mol. Biol. 257 (1996) 412-429
28. Daggett V., Li A.J., Itzhaki L.S., Otzen D.E., and Fersht A.R. Structure of the transition state for folding of a protein derived from experiment and simulation. J. Mol. Biol. 257 (1996) 430-440
29. Gianni S., Guydosh N.R., Khan F., Caldas T.D., Mayor U., White G.W.N., et al. Unifying features in protein-folding mechanisms. Proc. Natl Acad. Sci. USA 100 (2003) 13286-13291
30. 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
31. Nguyen H., Jager M., Moretto A., Gruebele M., and Kelly J.W. Tuning the free-energy landscape of a WW domain by temperature, mutation, and truncation. Proc. Natl Acad. Sci. USA 100 (2003) 3948-3953
32. Karanicolas J., and Brooks III C.L. The structural basis for biphasic kinetics in the folding of the WW domain from a formin-binding protein: lessons for protein design?. Proc. Natl Acad. Sci. USA 100 (2003) 3954-3959
33. Munoz V., Henry E.R., Hofrichter J., and Eaton W.A. A statistical mechanical model for beta-hairpin kinetics. Proc. Natl Acad. Sci. USA 95 (1998) 5872-5879
34. Dinner A.R., Lazaridis T., and Karplus M. Understanding beta-hairpin formation. Proc. Natl Acad. Sci. USA 96 (1999) 9068-9073
35. Olsen K.A., Fesinmeyer R.M., Stewart J.M., and Andersen N.H. Hairpin folding rates reflect mutations within and remote from the turn region. Proc. Natl Acad. Sci. USA 102 (2005) 15483-15487
36. Gill S.C., and von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182 (1989) 319-326
37. Levitt M., Hirshberg M., Sharon R., and Daggett V. Potential-energy function and parameters for simulations of the molecular-dynamics of proteins and nucleic-acids in solution. Comput. Phys. Commun. 91 (1995) 215-231
38. Levitt M., Hirshberg M., Sharon R., Laidig K.E., and Daggett V. Calibration and testing of a water model for simulation of the molecular dynamics of proteins and nucleic acids in solution. J. Phys. Chem.ser. B 101 (1997) 5051-5061
39. Kell G.S. Precise representation of volume properties of water at one atmosphere. J. Chem. Eng. Data 12 (1967) 66-68
40. Beck D.A.C., and Daggett V. Methods for molecular dynamics simulations of protein folding/unfolding in solution. Methods 34 (2004) 112-120
41. Beck D.A.C., Alonso D.O.V., and Daggett V. ilmm, in lucem. Molecular Mechanics (2005), University of Washington, Seattle
42. Armen R.S., Bernard B.M., Day R., Alonso D.O.V., and Daggett V. Characterization of a possible amyloidogenic precursor in glutamine-repeat neurodegenerative diseases. Proc. Natl Acad. Sci. USA 102 (2005) 13433-13438
43. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera- a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612