Side-chain interactions in the folding pathway of a Fyn SH3 domain mutant studied by relaxation dispersion NMR spectroscopy

Biochemistry

Volumn 44, Issue 47, 2005, Pages 15430-15436

  Mittermaier, Anthony ^a   Korzhnev, Dmitry M ^a,b   Kay, Lewis E ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DISPERSIONS; NUCLEAR MAGNETIC RESONANCE; REACTION KINETICS; RELAXATION PROCESSES; THERMODYNAMICS;

CHEMICAL SHIFTS; INTERMEDIATE-FOLDED TRANSITION STATES; NMR RELAXATION DISPERSION; PROTEIN FOLDING;

PROTEINS;

METHYL GROUP; MUTANT PROTEIN; PROTEIN KINASE FYN; PROTEIN SH3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANALYTIC METHOD; ARTICLE; BETA SHEET; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXY TERMINAL SEQUENCE; ENERGY TRANSFER; EQUILIBRIUM CONSTANT; HYDROPHOBICITY; KINETICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; THERMODYNAMICS;

ANIMALS; CHICKENS; HYDROPHOBICITY; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTO-ONCOGENE PROTEINS C-FYN; SRC HOMOLOGY DOMAINS;

EID: 28244494171     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051771o     Document Type: Article

References (37)

1. Levinthal, C. (1969) in Mossbauer spectroscopy in biological systems (de Brunner, J. T. P., and Munck, E., Eds.) pp 22-24. University of Illinois Press, Allerton House, Monticello, IL.
2. Burton, R. E., Busby, R. S., and Oas, T. G. (1998) ALASKA: A Mathematica package for two-state kinetic analysis of protein folding reactions, J. Biomol. NMR 11, 355-359.
3. Palmer, A. G., Kroenke, C. D., and Loria, J. P. (2001) NMR methods for quantifying microsecond-to-millisecond motions in biological macromolecules, Methods Enzymol. 339, 204-238.
4. Di Nardo, A. A., Korzhnev, D. M., Stogios, P. J., Zarrine-Afsar, A., Kay, L. E., and Davidson, A. R. (2004) Dramatic acceleration of protein folding by stabilization of a nonnative backbone conformation, Proc. Natl. Acad. Sci. U.S.A. 101, 7954-7959.
5. Korzhnev, D. M., Salvatella, X., Vendruscolo, M., Di Nardo, A. A., Davidson, A. R., Dobson, C. M., and Kay, L. E. (2004) Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR, Nature 430, 586-590.
6. Musacchio, A., Wilmanns, M., and Saraste, M. (1994) Structure and function of the SH3 domain, Prog. Biophys. Mol. Biol. 61, 283-297.
7. Filimonov, V. V., Azuaga, A. I., Viguera, A. R., Serrano, L., and Mateo, P. L. (1999) A thermodynamic analysis of a family of small globular proteins: SH3 domains, Biophys. Chem. 77, 195-208.
8. Capaldi, A. P., and Radford, S. E. (1998) Kinetic studies of β-sheet protein folding, Curr. Opin. Struct. Biol. 8, 86-92.
9. Northey, J. G. B., Maxwell, K. L., and Davidson, A. R. (2002) Protein folding kinetics beyond the φ value: Using multiple amino acid substitutions to investigate the structure of the SH3 domain folding transition state, J. Mol. Biol. 320, 389-402.
10. Turowski, M., Yamakawa, N., Meller, J., Kimata, K., Ikegami, T., Hosoya, K., Tanaka, N., and Thornton, E. R. (2003) Deuterium isotope effects on hydrophobic interactions: The importance of dispersion interactions in the hydrophobic phase, J. Am. Chem. Soc. 125, 13836-13849.
11. Maxwell, K. L., and Davidson, A. R. (1998) Mutagenesis of a buried polar interaction in an SH3 domain: Sequence conservation provides the best prediction of stability effects, Biochemistry 37, 16172-16182.
12. 2H-labeled proteins, J. Biomol. NMR 13, 369-374.
13. Crowhurst, K. A., and Forman-Kay, J. D. (2003) Aromatic and methyl NOEs highlight hydrophobic clustering in the unfolded state of an SH3 domain, Biochemistry 42, 8687-8695.
14. Loria, P. J., Rance, M., and Palmer, A. G. (1999) A relaxation- compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy, J. Am. Chem. Soc. 121, 2331-2332.
15. Tollinger, M., Skrynnikov, N. R., Mulder, F. A., Forman-Kay, J. D., and Kay, L. E. (2001) Slow dynamics in folded and unfolded states of an SH3 domain, J. Am. Chem. Soc 123, 11341-11352.
16. Ishima, R., and Torchia, D. A. (2003) Extending the range of amide proton relaxation dispersion experiments in proteins using a constant-time relaxation-compensated CPMG approach, J. Biomol. NMR 25, 243-248.
17. Orekhov, V. Y., Korzhnev, D. M., and Kay, L. E. (2004) Double- and zero-quantum NMR relaxation dispersion experiments sampling millisecond time scale dynamics in proteins, J. Am. Chem. Soc. 126, 1886-1891.
18. Korzhnev, D. M., Kloiber, K., and Kay, L. E. (2004) Multiple-quantum relaxation dispersion NMR spectroscopy probing millisecond time-scale dynamics in proteins: Theory and application, J. Am. Chem. Soc. 126, 7320-7329.
19. Skrynnikov, N. R., Mulder, F. A. A., Hon, B., Dahlquist, F. W., and Kay, L. E. (2001) Probing slow time scale dynamics at methyl-containing side chains in proteins by relaxation dispersion NMR measurements: Application to methionine residues in a cavity mutant of T4 lysozyme, J. Am. Chem. Soc. 123, 4556-4566.
20. Meiler, J. (2003) PROSHIFT: Protein chemical shift prediction using artificial neural networks, J. Biol. NMR 26, 25-37.
21. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects, J. Biomol. NMR 5, 67-81.
22. Brockwell, D., Yu, L., Cooper, S., McCleland, S., Cooper, A., Attwood, D., Gaskell, S. J., and Barber, J. (2001) Physicochemical consequences of the perdeuteriation of glutathione S-transferase from S. japonicum, Protein Sci. 10, 572-580.
23. Bartell, L. S., and Roskos, R. R. (1966) Isotope Effects on Molar Volume and Surface Tension: Simple Theoretical Model and Experimental Data for Hydrocarbons, J. Chem. Phys. 44, 457.
24. Bates, F. S., Fetters, L. J., and Wignall, G. D. (1988) Thermodynamics of Isotopic Polymer Mixtures: Poly(Vinylethylene) and Poly(Ethylethylene), Macromolecules 21, 1086-1094.
25. Armstrong, G. T., Brickwedde, F. G., and Scott, R. B. (1955) Vapor Pressures of the Methanes, J. Res. Natl. Bur. Stand. (U.S.) 55, 39-52.
26. Ptitsyn, O. B. (1995) Molten globule and protein folding, Adv. Protein Chem. 47, 83-229.
27. Redfield, C. (2004) Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins, Methods 34, 121-132.
28. Bai, P., Luo, L., and Peng, Z. Y. (2000) Side chain accessibility and dynamics in the molten globule state of α-lactalbumin: A F-19-NMR study, Biochemistry 39, 372-380.
29. Guo, W. H., Lampoudi, S., and Shea, J. E. (2004) Temperature dependence of the free energy landscape of the src-SH3 protein domain, Proteins: Struct., Funct., Bioinf. 55, 395-406.
30. Guo, W. H., Lampoudi, S., and Shea, J. E. (2003) Posttransition state desolvation of the hydrophobic core of the src-SH3 protein domain, Biophys. J. 85, 61-69.
31. Shea, J. E., Onuchic, J. N., and Brooks, C. L. (2002) Probing the folding free energy landscape of the src-SH3 protein domain, Proc. Natl. Acad. Sci. U.S.A. 99, 16064-16068.
32. Riddle, D. S., Grantcharova, V. P., Santiago, J. V., Alm, E., Ruczinski, I., and Baker, D. (1999) Experiment and theory highlight role of native state topology in SH3 folding, Nat. Struct. Biol. 6, 1016-1024.
33. Capaldi, A. P., Kleanthous, C., and Radford, S. E. (2002) Im7 folding mechanism: Misfolding on a path to the native state, Nat. Struct. Biol. 9, 209-216.
34. 562: Native fold with non-native hydrophobic interactions, J. Mol. Biol. 343, 1477-1485.
35. Canet, D., Lyon, C. E., Scheek, R. M., Robillard, G. T., Dobson, C. M., Hore, P. J., and van Nuland, N. A. J. (2003) 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, 397-407.
36. Noble, M. E., Mussachio, A., Saraste, M., Courtneidge, S. A., and Wierenga, R. K. (1993) 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, 2617-2624.
37. Alm, E., Morozov, A. V., Kortemme, T., and Baker, D. (2002) Simple physical models connect theory and experiment in protein folding kinetics, J. Mol. Biol. 322, 463-476.