Identification of a Collapsed Intermediate with Non-native Long-range Interactions on the Folding Pathway of a Pair of Fyn SH3 Domain Mutants by NMR Relaxation Dispersion Spectroscopy

Journal of Molecular Biology

Volumn 363, Issue 5, 2006, Pages 958-976

  Neudecker, Philipp ^a   Zarrine Afsar, Arash ^a   Choy, Wing Yiu ^a   Muhandiram, D Ranjith ^a   Davidson, Alan R ^a   Kay, Lewis E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

chemical exchange; CPMG NMR relaxation dispersion; Fyn SH3 domain; protein folding; stopped flow kinetics

Indexed keywords

GLYCINE; PROTEIN KINASE FYN; PROTEIN SH3;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXY TERMINAL SEQUENCE; HEAT TREATMENT; LOW TEMPERATURE; MOLECULAR MODEL; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE; THERMODYNAMICS; VALIDATION STUDY;

EID: 33750004434     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.08.047     Document Type: Article

References (55)

1. Fersht A. Structure and Mechanism in Protein Science (1999), Freeman, New York
2. Plaxco K.W., Guijarro J.I., Morton C.J., Pitkeathly M., Campbell I.D., and Dobson C.M. The folding kinetics and thermodynamics of the Fyn-SH3 domain. Biochemistry 37 (1998) 2529-2537
3. Maxwell K.L., and Davidson A.R. Mutagenesis of a buried polar interaction in an SH3 domain: Sequence conservation provides the best prediction of stability effects. Biochemistry 37 (1998) 16172-16182
4. Martinez J.C., and Serrano L. The folding transition state between SH3 domains is conformationally restricted and evolutionarily conserved. Nature Struct. Biol. 6 (1999) 1010-1016
5. 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 domain folding. Nature Struct. Biol. 6 (1999) 1016-1024
6. Northey J.G.B., Di Nardo A.A., and Davidson A.R. Hydrophobic core packing in the SH3 domain folding transition state. Nature Struct. Biol. 9 (2002) 126-130
7. Korzhnev D.M., Salvatella X., Vendruscolo M., Di Nardo A.A., Davidson A.R., Dobson C.M., and Kay L.E. Low-populated folding intermediates of Fyn SH3 characterised by relaxation dispersion NMR. Nature 430 (2004) 586-590
8. Korzhnev D.M., Neudecker P., Mittermaier A., Orekhov V.Y., and Kay L.E. Multiple-site exchange in proteins studied with a suite of six NMR relaxation dispersion experiments: An application to the folding of a Fyn SH3 domain mutant. J. Am. Chem. Soc. 127 (2005) 15602-15611
9. Mittermaier A., Korzhnev D.M., and Kay L.E. Side-chain interactions in the folding pathway of a Fyn SH3 domain mutant studied by NMR relaxation dispersion NMR spectroscopy. Biochemistry 44 (2005) 15430-15436
10. Bezsonova I., Korzhnev D.M., Prosser R.S., Forman-Kay J.D., and Kay L.E. Hydration and packing along the folding pathway of SH3 domains by pressure-dependent NMR. Biochemistry 45 (2006) 4711-4719
11. Korzhnev D.M., Neudecker P., Zarrine-Afsar A., Davidson A.R., and Kay L.E. Abp1p and Fyn SH3 Domains Fold through Similar Low-Populated Intermediate States. Biochemistry 45 (2006) 10175-10183
12. Noble M.E.M., Musacchio A., Saraste M., Courtneidge S.A., and Wierenga R.K. Crystal structure of the SH3 domain in human Fyn; comparison of the three-dimensional structures of SH3 domains in tyrosine kinases and spectrin. EMBO J. 12 (1993) 2617-2624
13. Capaldi A.P., and Radford S.E. Kinetic studies of β-sheet protein folding. Curr. Opin. Struct. Biol. 8 (1998) 86-92
14. Morton C.J., Pugh D.J.R., Brown E.L.J., Kahmann J.D., Renzoni D.A.C., and Campbell I.D. Solution structure and peptide binding of the SH3 domain from human Fyn. Structure 4 (1996) 705-714
15. Wüthrich K. NMR of Proteins and Nucleic Acids (1986), Wiley, New York
16. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 5 (1995) 67-81
17. Palmer III A.G., Kroenke C.D., and Loria J.P. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol. 339 (2001) 204-238
18. Neudecker P., Korzhnev D.M., and Kay L.E. Assessment of the effects of increased relaxation dispersion data on the extraction of 3-site exchange parameters characterizing the unfolding of an SH3 domain. J. Biomol. NMR 34 (2006) 129-135
19. Skrynnikov N.R., Dahlquist F.W., and Kay L.E. Reconstructing NMR spectra of "Invisible" excited protein states using HSQC and HMQC experiments. J. Am. Chem. Soc. 124 (2002) 12352-12360
20. Wishart D.S., and Case D.A. Use of chemical shifts in macromolecular structure determination. Methods Enzymol. 338 (2001) 3-34
21. Schwarzinger S., Kroon G.J.A., Foss T.R., Chung J., Wright P.E., and Dyson H.J. Sequence-dependent correction of random coil NMR chemical shifts. J. Am. Chem. Soc. 123 (2001) 2970-2978
22. Eyring H. The activated complex and the absolute rate of chemical reactions. Chem. Rev. 17 (1935) 65-77
23. Hagen S.J., Hofrichter J., Szabo A., and Eaton W.A. Diffusion-limited contact formation in unfolded cytochrome c: Estimating the maximum rate of protein folding. Proc. Natl. Acad. Sci. USA 93 (1996) 11615-11617
24. Press W.H., Teukolsky S.A., Vetterling W.T., and Flannery B.P. Numerical Recipes in C. 2nd edit. (1992), Cambridge University Press, Cambridge
25. 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
26. Nölting B. Protein Folding Kinetics. 2nd edit. (2005), Springer, Berlin
27. Guo W., Lampoudi S., and Shea J.-E. Posttransition state desolvation of the hydrophobic core of the src-SH3 protein domain. Biophys. J. 85 (2003) 61-69
28. Plotkin S.S. Speeding protein folding beyond the Gō model: How a little frustration sometimes helps. Proteins: Struct. Funct. Genet. 45 (2001) 337-345
29. Treptow W.L., Barbosa M.A.A., Garcia L.G., and Pereira de Araújo A.F. Non-native interactions, effective contact order, and protein folding: A mutational investigation with the energetically frustrated hydrophobic model. Proteins: Struct. Funct. Genet. 49 (2002) 167-180
30. Li L., Mirny L.A., and Shakhnovich E.I. Kinetics, thermodynamics and evolution of non-native interactions in a protein folding nucleus. Nature Struct. Biol. 7 (2000) 336-342
31. Clementi C., and Plotkin S.S. The effects of nonnative interactions on protein folding rates: Theory and simulation. Protein Sci. 13 (2004) 1750-1766
32. Fan K., Wang J., and Wang W. Folding of lattice protein chains with modified Gō potential. Eur. Phys. J. B30 (2002) 381-391
33. Viguera A.R., Vega C., and Serrano L. Unspecific hydrophobic stabilization of folding transition states. Proc. Natl. Acad. Sci. USA 99 (2002) 5349-5354
34. Canet D., Lyon C.E., Scheek R.M., Robillard G.T., Dobson C.M., Hore P.J., and van Nuland N.A.J. Rapid formation of non-native contacts during the folding of HPr revealed by real-time photo-CIDNP NMR and stopped-flow fluorescence experiments. J. Mol. Biol. 330 (2003) 397-407
35. Di Nardo A.A., Korzhnev D.M., Stogios P.J., Zarrine-Afsar A., Kay L.E., and Davidson A.R. Dramatic acceleration of protein folding by stabilization of a nonnative backbone conformation. Proc. Natl. Acad. Sci. USA 101 (2004) 7954-7959
36. Friel C.T., Beddard G.S., and Radford S.E. Switching Two-state to Three-state Kinetics in the Helical Protein Im9 via the optimisation of stabilising non-native interactions by design. J. Mol. Biol. 342 (2004) 261-273
37. Cavanagh J., and Rance M. Suppression of cross-relaxation effects in TOCSY spectra via a modified DIPSI-2 mixing sequence. J. Magn. Reson. 96 (1992) 670-678
38. 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques. J. Biomol. NMR 4 (1994) 845-858
39. Marion D., Ikura M., Tschudin R., and Bax A. Rapid recording of 2D NMR spectra without phase cycling. Application to the study of hydrogen exchange in proteins. J. Magn. Reson. 85 (1989) 393-399
40. Kay L.E., Keifer P., and Saarinen T. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114 (1992) 10663-10665
41. Schleucher J., Sattler M., and Griesinger C. Coherence selection by gradients without signal attenuation: application to the three-dimensional HNCO experiment. Angew. Chem. Int. Ed. Engl. 32 (1993) 1489-1491
42. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
43. Johnson B.A., and Blevins R.A. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4 (1994) 603-614
44. Markley J.L., Bax A., Arata Y., Hilbers C.W., Kaptein R., Sykes B.D., et al. Recommendations for the presentation of NMR structures of proteins and nucleic acids (Recommendations 1998). Pure Appl. Chem. 70 (1998) 117-142
45. Loria J.P., Rance M., and Palmer III A.G. A Relaxation-Compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J. Am. Chem. Soc. 121 (1999) 2331-2332
46. Tollinger M., Skrynnikov N.R., Mulder F.A., Forman-Kay J.D., and Kay L.E. Slow Dynamics in Folded and Unfolded States of an SH3 Domain. J. Am. Chem. Soc. 123 (2001) 11341-11352
47. Orekhov V.Y., Ibraghimov I.V., and Billeter M. MUNIN: a new approach to multi-dimensional NMR spectra interpretation. J. Biomol. NMR 20 (2001) 49-60
48. Korzhnev D.M., Ibraghimov I.V., Billeter M., and Orekhov V.Y. MUNIN: Application of three-way decomposition to the analysis of heteronuclear NMR relaxation data. J. Biomol. NMR 21 (2001) 263-268
49. Ishima R., and Torchia D.A. Error estimation and global fitting in transverse-relaxation dispersion experiments to determine chemical-exchange parameters. J. Biomol. NMR 32 (2005) 41-54
50. McConnell H.M. Reaction rates by nuclear magnetic resonance. J. Chem. Phys. 28 (1958) 430-431
51. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24 (1991) 946-950
52. Merrit E.A., and Murphy M.E.P. Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallog. sect. D 50 (1994) 869-873
53. Guex M., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
54. Schwieters C.D., Kuszewski J.J., Tjandra N., and Clore G.M. The Xplor-NIH NMR molecular structure determination package. J. Mag. Reson. 160 (2003) 65-73
55. Brünger A.T. X-PLOR Version 3.1. A System for X-ray Crystallography and NMR. (1992), Yale University Press, New Haven