Hydration and packing along the folding pathway of SH3 domains by pressure-dependent NMR

Biochemistry

Volumn 45, Issue 15, 2006, Pages 4711-4719

  Bezsonova, Irina ^a,b   Korzhnev, Dmitry M ^a,c   Prosser, R Scott ^a   Forman Kay, Julie D ^b,c   Kay, Lewis E ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DISPERSION (WAVES); HYDRATION; MAGNETIZATION; NUCLEAR MAGNETIC RESONANCE; RATE CONSTANTS; SPECTROSCOPIC ANALYSIS;

NMR SPIN RELAXATION TECHNIQUES; PARTIAL MOLAR VOLUMES; TWO-STATE MECHANISM;

SULFUR COMPOUNDS;

ADAPTOR PROTEIN; MUTANT PROTEIN; NITROGEN 15; PROTEIN DRK; PROTEIN KINASE FYN; PROTEIN SH3; UNCLASSIFIED DRUG;

ARTICLE; DROSOPHILA; EQUILIBRIUM CONSTANT; HYDRATION; MAGNETIC FIELD; MATHEMATICAL MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRESSURE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTON NUCLEAR MAGNETIC RESONANCE; THERMODYNAMICS; VOLUMETRY;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; HYDROPHOBICITY; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTO-ONCOGENE PROTEINS C-FYN; SENSITIVITY AND SPECIFICITY; SRC HOMOLOGY DOMAINS; THERMODYNAMICS;

EID: 33645954277     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060177r     Document Type: Article

References (48)

1. Fersht, A. (1999) Structure and Mechanism in Protein Science, W. H. Freeman and Co., New York.
2. Dinner, A. R., Sali, A., Smith, L. J., Dobson, C. M., and Karplus, M. (2000) Understanding protein folding via free-energy surfaces from theory and experiment, Trends Biochem. Sci. 25, 331-9.
3. Dyson, H. J., and Wright, P. E. (2002) Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance, Adv. Protein Chem. 62, 311-40.
4. Shortle, D. (1996) Structural analysis of non-native states of proteins by NMR methods, Curr. Opin. Struct. Biol. 6, 24-30.
5. Plaxco, K. W., and Baker, D. (1998) Limited internal friction in the rate-limiting step of a two-state protein folding reaction, Proc. Natl. Acad. Sci. U.S.A. 95, 13591-6.
6. Chalikian, T. V. (2003) Volumetric properties of proteins, Annu. Rev. Biophys. Biomol. Struct. 32, 207-35.
7. Taulier, N., and Chalikian, T. V. (2002) Compressibility of protein transitions, Biochim. Biophys. Acta 1595, 48-70.
8. Silva, J. L., and Weber, G. (1993) Pressure stability of proteins, Annu. Rev. Phys. Chem. 44, 89-113.
9. Sarvazyan, A. P. (1991) Ultrasonic velocimetry of biological compounds, Annu. Rev. Biophys. Biophys. Chem. 20, 321-42.
10. Prehoda, K. E., Mooberry, E. S., and Markley, J. L. (1998) Pressure denaturation of proteins: Evaluation of compressibility effects, Biochemistry 37, 5785-90.
11. 562 examined by the dependence of hydrogen exchange on hydrostatic pressure, Biochemistry 37, 9877-83.
12. Akasaka, K. (2003) Highly fluctuating protein structures revealed by variable-pressure nuclear magnetic resonance, Biochemistry 42, 10875-85.
13. Pappenberger, G., Saudan, C., Becker, M., Merbach, A. E., and Kiefhaber, T. (2000) Denaturant-induced movement of the transition state of protein folding revealed by high-pressure stopped-flow measurements, Proc. Natl. Acad. Sci. U.S.A. 97, 17-22.
14. Taulier, N., Beletskaya, I. V., and Chalikian, T. V. (2005) Compressibility changes accompanying conformational transitions of apomyoglobin, Biopolymers 79, 218-29.
15. Zhang, O., and Forman-Kay, J. D. (1995) Structural characterization of folded and unfolded states of an SH3 domain in equilibrium in aqueous buffer, Biochemistry 34, 6784-94.
16. Tollinger, M., Skrynnikov, N. R., Mulder, F. A. 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, 11341-52.
17. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium, J. Biomol. NMR 4, 727-34.
18. a values in protein folding transition state ensembles by NMR spectroscopy, J. Am. Chem. Soc. 127, 8904-5.
19. 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, 586-90.
20. Korzhnev, D. M., Neudecker, P., Mittermaier, A., Orekhov, V. Y., and Kay, L. E. (2005) 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, 15602-11.
21. 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, 204-38.
22. Bezsonova, I., Singer, A., Choy, W. Y., Tollinger, M., and Forman-Kay, J. D. (2005) Structural comparison of the unstable drkN SH3 domain and a stable mutant, Biochemistry 44, 15550-60.
23. Korzhnev, D. M., Ibraghimov, I. V., Billeter, M., and Orekhov, V. Y. (2001) MUNIN: Application of three-way decomposition to the analysis of heteronuclear NMR relaxation data, J. Biomol. NMR 21, 263-8.
24. Orekhov, V. Y., Ibraghimov, I. V., and Billeter, M. (2001) MUNIN: A new approach to multi-dimensional NMR spectra interpretation, J. Biomol. NMR 20, 49-60.
25. Press, W. H., Flannery, B. P., Teukolsky, S. A., and Vetterling, W. T. (1988) Numerical Recipes in C, Cambridge University Press, Cambridge, U.K.
26. Hagen, S. J., Hofrichter, J., Szabo, A., and Eaton, W. A. (1996) Diffusion-limited contact formation in unfolded cytochrome c: Estimating the maximum rate of protein folding, Proc. Natl. Acad. Sci. U.S.A. 93, 11615-7.
27. Mittermaier, A., Korzhnev, D. M., and Kay, L. E. (2005) Side-chain interactions in the folding pathway of a Fyn SH3 domain mutant studied by relaxation dispersion NMR spectroscopy, Biochemistry 44, 15430-6.
28. Korzhnev, D. M., Bezsonova, I., Evanics, F., Taulier, N., Zhou, Z., Bai, Y., Chalikian, T. V., Prosser, R. S., and Kay, L. E. (2006) Probing the transition state ensemble of a protein folding reaction by pressure dependent NMR relaxation dispersion, J. Am. Chem. Soc. (in press).
29. Loria, J. P., Rance, M., and Palmer, A. G. (1999) A relaxation compensated CPMG sequence for characterizing chemical exchange, J. Am. Chem. Soc. 121, 2331-2.
30. Ishima, R., and Torchia, D. (2003) Extending the range of amide proton relaxation dispersion experiments in proteins using a constant-time relaxation-compensated CPMG approach, J. Biomol. NMR 25, 243-8.
31. Jacob, M. H., Saudan, C., Holtermann, G., Martin, A., Perl, D., Merbach, A. E., and Schmid, F. X. (2002) Water contributes actively to the rapid crossing of a protein unfolding barrier, J. Mol. Biol. 318, 837-45.
32. Vidugiris, G. J., Markley, J. L., and Royer, C. A. (1995) Evidence for a molten globule-like transition state in protein folding from determination of activation volumes, Biochemistry 34, 4909-12.
33. Woenckhaus, J., Kohling, R., Thiyagarajan, P., Littrell, K. C., Seifert, S., Royer, C. A., and Winter, R. (2001) Pressure-jump small-angle X-ray scattering detected kinetics of staphylococcal nuclease folding, Biophys. J. 80, 1518-23.
34. Chalikian, T. V., and Filfil, R. (2003) How large are the volume changes accompanying protein transitions and binding? Biophys. Chem. 104, 489-99.
35. Chalikian, T. V., and Bresiauer, K. J. (1996) On volume changes accompanying conformational transitions of biopolymers, Biopolymers 39, 619-26.
36. Silva, J. L., Foguel, D., and Royer, C. A. (2001) Pressure provides new insights into protein folding, dynamics and structure, Trends Biochem. Sci. 26, 612-8.
37. Gerstein, M., Tsai, J., and Levitt, M. (1995) The volume of atoms on the protein surface: Calculated from simulation, using Voronoi polyhedra, J. Mol. Biol. 249, 955-66.
38. Northey, J. G. B., Di Nardo, A. A., and Davidson, A. R. (2002) Hydrophobic core packing in the SH3 domain folding transition state, Nat. Struct. Biol. 9, 126-30.
39. Plaxco, K. W., Guijarro, J. I., Morton, C. J., Pitkeuthly, M., Campbell, I., and Dobson, C. M. (1998) The folding kinetics and thermodynamics of the Fyn-SH3 domain, Biochemistry 37, 2529-37.
40. Shea, J. E., Onuchic, J. N., and Brooks, C. L., III (2002) Probing the folding free energy landscape of the Src-SH3 protein domain, Proc. Natl. Acad. Sci. U.S.A. 99, 16064-8.
41. Guo, W., Lampoudi, S., and Shea, J. E. (2003) Posttransition state desolvation of the hydrophobic core of the src-SH3 protein domain, Biophys. J. 85, 61-9.
42. Mok, Y. K., Kay, C. M., Kay, L. E., and Forman-Kay, J. D. (1999) NOE data demonstrating a compact unfolded state for an SH3 domain under non-denaturing conditions, J. Mol. Biol. 289, 619-38.
43. 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, 8687-95.
44. Crowhurst, K. A., Tollinger, M., and Forman-Kay, J. D. (2002) Cooperative interactions and a non-native buried Trp in the unfolded state of an SH3 domain, J. Mol. Biol. 322, 163-78.
45. Choy, W. Y., and Forman-Kay, J. D. (2001) Calculation of ensembles of structures representing the unfolded state of an SH3 domain, J. Mol. Biol. 308, 1011-32.
46. 13C dipole-dipole cross-correlated spin relaxation as a probe of dynamics in unfolded proteins: Application to the drkN SH3 domain, J. Am. Chem. Soc. 121, 3555-6.
47. Mok, Y. K., Elisseeva, E. L., Davidson, A. R., and Forman-Kay, J. D. (2001) Dramatic stabilization of an SH3 domain by a single substitution: Roles of the folded and unfolded states, J. Mol. Biol. 307, 913-28.
48. Noble, M. E., Musacchio, 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, 2617-24.