The Folding Pathway of an FF domain: Characterization of an On-pathway Intermediate State Under Folding Conditions by 15N, 13Cα and 13C-methyl Relaxation Dispersion and 1H/2H-exchange NMR Spectroscopy

Journal of Molecular Biology

Volumn 372, Issue 2, 2007, Pages 497-512

  Korzhnev, Dmitry M ^a   Religa, Tomasz L ^b   Lundström, Patrik ^a   Fersht, Alan R ^b   Kay, Lewis E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MRC CENTRE FOR PROTEIN ENGINEERING   (United Kingdom)

Author keywords

chemical exchange; CPMG; folding kinetics; NMR; relaxation dispersion

Indexed keywords

MUTANT PROTEIN; PROTEIN FBP11; PROTEIN HYPA; UNCLASSIFIED DRUG; UREA;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; HYDROPHOBICITY; KINETICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; TEMPERATURE DEPENDENCE; THERMODYNAMICS; WILD TYPE;

EID: 34547935214     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.06.012     Document Type: Article

References (78)

1. Daggett V., and Fersht A. The present view of the mechanism of protein folding. Nature Rev. Mol. Cell Biol. 4 (2003) 497-502
2. Oliveberg M., and Wolynes P.G. The experimental survey of protein-folding energy landscapes. Quart. Rev. Biophys. 38 (2005) 245-288
3. Fersht A.R., Matouschek A., and Serrano L. The folding of an enzyme .1. 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. Matouschek A., Kellis J.T., Serrano L., and Fersht A.R. Mapping the transition-state and pathway of protein folding by protein engineering. Nature 340 (1989) 122-126
6. Brockwell D.J., and Radford S.E. Intermediates: ubiquitous species on folding energy landscapes?. Curr. Opin. Struct. Biol. 17 (2007) 30-37
7. Roder H., and Colon W. Kinetic role of early intermediates in protein folding. Curr. Opin. Struct. Biol. 7 (1997) 15-28
8. Religa T.L., Markson J.S., Mayor U., Freund S.M.V., and Fersht A.R. Solution structure of a protein denatured state and folding intermediate. Nature 437 (2005) 1053-1056
9. Dobson C.M. Protein folding and misfolding. Nature 426 (2003) 884-890
10. 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
11. 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 characterized by relaxation dispersion NMR. Nature 430 (2004) 586-590
12. Neudecker P., Zarrine-Afsar A., Choy W.Y., Muhandiram D.R., Davidson A.R., and Kay L.E. 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. J. Mol. Biol. 363 (2006) 958-976
13. Choy W.Y., Zhou Z., Bai Y.W., and Kay L.E. An N15 NMR spin relaxation dispersion study of the folding of a pair of engineered mutants of apocytochrome b(562). J. Am. Chem. Soc. 127 (2005) 5066-5072
14. Grey M.J., Tang Y.F., Alexov E., McKnight C.J., Raleigh D.P., and Palmer A.G. Characterizing a partially folded intermediate of the villin headpiece domain under non-denaturing conditions: contribution of His41 to the pH-dependent stability of the N-terminal subdomain. J. Mol. Biol. 355 (2006) 1078-1094
15. Zeeb M., and Balbach J. NMR spectroscopic characterization of millisecond protein folding by transverse relaxation dispersion measurements. J. Am. Chem. Soc. 127 (2005) 13207-13212
16. Kay L.E. NMR studies of protein structure and dynamics. J. Magn. Reson. 173 (2005) 193-207
17. Mittermaier A., and Kay L.E. New tools provide new insights in NMR studies of protein dynamics. Science 312 (2006) 224-228
18. Palmer A.G. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 104 (2004) 3623-3640
19. Palmer A.G., Kroenke C.D., and Loria J.P. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Nuclear Magnetic Resonance of Biological Macromolecules, Pt B vol. 339 (2001), Academic Press Inc, San Diego 204-238
20. 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
21. 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
22. Viguera A.R., Martinez J.C., Filimonov V.V., Mateo P.L., and Serrano L. Thermodynamic and kinetic analysis of the SH3 domain of spectrin shows a 2-state folding transition. Biochemistry 33 (1994) 2142-2150
23. 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
24. Filimonov V.V., Azuaga A.I., Viguera A.R., Serrano L., and Mateo P.L. A thermodynamic analysis of a family of small globular proteins: SH3 domains. Biophys. Chem. 77 (1999) 195-208
25. Grantcharova V.P., and Baker D. Folding dynamics of the src SH3 domain. Biochemistry 36 (1997) 15685-15692
26. 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
27. Northey J.G.B., Maxwell K.L., and Davidson A.R. Protein folding kinetics beyond the phi value: using multiple amino acid substitutions to investigate the structure of the SH3 domain folding transition state. J. Mol. Biol. 320 (2002) 389-402
28. Bezsonova I., Korzhnev D.M., Prosser R.S., Forman-Kay J.D., and Kay L.E. Hydration and packing along the folding pathway of a pair of SH3 domains by pressure dependent NMR. Biochemistry 45 (2006) 4711-4719
29. Mittermaier A., Korzhnev D.M., and Kay L.E. Side-chain interactions in the folding pathway of a Fyn SH3 domain mutant studied by relaxation dispersion NMR spectroscopy. Biochemistry 44 (2005) 15430-15436
30. Pawson T., and Gish G.D. SH2 and SH3 domains- from structure to function. Cell 71 (1992) 359-362
31. 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
32. Jemth P., Day R., Gianni S., Khan F., Allen M., Daggett V., and Fersht A.R. The structure of the major transition state for folding of an FF domain from experiment and simulation. J. Mol. Biol. 350 (2005) 363-378
33. Jemth P., Gianni S., Day R., Li B., Johnson C.M., Daggett V., and Fersht A.R. Demonstration of a low-energy on-pathway intermediate in a fast-folding protein by kinetics, protein engineering, and simulation. Proc. Natl Acad. Sci. USA 101 (2004) 6450-6455
34. Capaldi A.P., Kleanthous C., and Radford S.E. Im7 folding mechanism: misfolding on a path to the native state. Nature Struct. Biol. 9 (2002) 209-216
35. Wildes D., and Marqusee S. Hydrogen-exchange strategies applied to energetics of intermediate processes in protein folding. Energetics of Biological Macromolecules, Pt E vol. 380 (2004), Academic Press Inc, San Diego 328-349
36. Englander S.W. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 29 (2000) 213-238
37. Loria J.P., Rance M., and Palmer 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
38. Tollinger M., Skrynnikov N.R., Mulder F.A.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
39. Ishima R., and Torchia D.A. Extending the range of amide proton relaxation dispersion experiments in proteins using a constant-time relaxation-compensated CPMG approach. J. Biomol. NMR 25 (2003) 243-248
40. Orekhov V.Y., Korzhnev D.M., and Kay L.E. Double- and zero-quantum NMR relaxation dispersion experiments sampling millisecond time scale dynamics in proteins. J. Am. Chem. Soc. 126 (2004) 1886-1891
41. Korzhnev D.M., Kloiber K., and Kay L.E. Multiple-quantum relaxation dispersion NMR spectroscopy probing millisecond time-scale dynamics in proteins: theory and application. J. Am. Chem. Soc. 126 (2004) 7320-7329
42. Skrynnikov N.R., Mulder F.A.A., Hon B., Dahlquist F.W., and Kay L.E. 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 (2001) 4556-4566
43. Korzhnev D.M., Kloiber K., Kanelis V., Tugarinov V., and Kay L.E. Probing slow dynamics in high molecular weight proteins by methyl-TROSY NMR spectroscopy: application to a 723-residue enzyme. J. Am. Chem. Soc. 126 (2004) 3964-3973
44. Akke M., and Palmer A.G. Monitoring macromolecular motions on microsecond to millisecond time scales by R1rho-R1 constant relaxation time NMR spectroscopy. J. Am. Chem. Soc. 118 (1996) 911-912
45. Mulder F.A.A., de Graaf R.A., Kaptein R., and Boelens R. An off-resonance rotating frame relaxation experiment for the investigation of macromolecular dynamics using adiabatic rotations. J. Magn. Reson. 131 (1998) 351-357
46. Korzhnev D.M., Skrynnikov N.R., Millet O., Torchia D.A., and Kay L.E. An NMR experiment for the accurate measurement of heteronuclear spin-lock relaxation rates. J. Am. Chem. Soc. 124 (2002) 10743-10753
47. Korzhnev D.M., Orekhov V.Y., and Kay L.E. Off-resonance R1rho NMR studies of exchange dynamics in proteins with low spin-lock fields: an application to a fyn SH3 domain. J. Am. Chem. Soc. 127 (2005) 713-721
48. Igumenova T.I., and Palmer A.G. Off-resonance TROSY-selected R1rho experiment with improved sensitivity for medium- and high-molecular-weight proteins. J. Am. Chem. Soc. 128 (2006) 8110-8111
49. Lundström P., and Akke M. Off-resonance rotating-frame amide proton spin relaxation experiments measuring microsecond chemical exchange in proteins. J. Biomol. NMR 32 (2005) 163-173
50. Brath U., Akke M., Yang D.W., Kay L.E., and Mulder F.A.A. Functional dynamics of human FKBP12 revealed by methyl C-13 rotating frame relaxation dispersion NMR spectroscopy. J. Am. Chem. Soc. 128 (2006) 5718-5727
51. 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
52. 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
53. Carver J.P., and Richards R.E. A general two-site solution for the chemical exchange produced dependence of T2 upon the Carr-Pursell pulse seperation. J. Magn. Reson. 6 (1972) 89-105
54. Jen J. Chemical exchange and NMR T2 relaxation- multisite case. J. Magn. Reson. 30 (1978) 111-128
55. Fersht A. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (1999), W.H. Freeman, New York
56. 15N NMR chemical-shifts in proteins and secondary structure. J. Biomol. NMR 4 (1994) 341-348
57. Xu X.P., and Case D.A. Probing multiple effects on N15, C13 alpha, C13 beta, and C13′ chemical shifts in peptides using density functional theory. Biopolymers 65 (2002) 408-423
58. Spera S., and Bax A. Empirical correlation between protein backbone conformation and C-alpha and C-beta C13 nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc. 113 (1991) 5490-5492
59. Wishart D.S., and Sykes B.D. The C13 chemical shift index- a simple method for the identification of protein secondary structure using C13 chemical shift data. J. Biomol. NMR 4 (1994) 171-180
60. Wuthrich K. NMR of Proteins and Nucleic Acids (1986), Wiley, New York
61. Wishart D.S., Bigam C.G., Holm A., Hodges R.S., and Sykes B.D. H1, C13 and N15 random coil NMR chemical shifts of the common amino-acids .1. Investigations of nearest-neighbor effects. J. Biomol. NMR 5 (1995) 67-81
62. 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
63. Munoz V., and Serrano L. Development of the multiple sequence approximation within the AGADIR model of alpha-helix formation: comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers 41 (1997) 495-509
64. Zana R. Rate-determining step for helix propagation in helix-coil transition of polypeptides in solution. Biopolymers 14 (1975) 2425-2428
65. Thompson P.A., Eaton W.A., and Hofrichter J. Laser temperature jump study of the helix reversible arrow coil kinetics of an alanine peptide interpreted with a 'kinetic zipper' model. Biochemistry 36 (1997) 9200-9210
66. Korzhnev D.M., Orekhov V.Y., and Arseniev A.S. The effect of helix-coil transition on backbone N-15 NMR relaxation of isolated transmembrane segment (1-36)-bacteriorhodopsin. J. Biomol. NMR 14 (1999) 357-368
67. Johnson B.A., and Blevins R.A. NMR View- a computer-program for the visualization and analysis of NMR data. J. Biomol. NMR 4 (1994) 603-614
68. Lundström P., Teilum K., Carstensen T., Bezsonova I., Wiesner S., Hansen F., et al. Fractional 13C enrichment of isolated carbons using [1-13C]-or [2-13C]-glucose facilitates the accurate measurement of dynamics at backbone Ca and side-chain methyl positions in proteins. J. Biomol. NMR 38 (2007) 79-88
69. Lundström P., Vallurupalli P., Religa T., Dahlquist F.W., and Kay L.E. A single-quantum methyl relaxation dispersion experiment with improved sensitivity. J. Biomol. NMR 38 (2007) 199-212
70. McConnell H.M. Reaction rates by nuclear magnetic resonance. J. Chem. Phys. 28 (1958) 430-431
71. 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
72. Press W.H., Teukolsky S.A., Vetterling W.T., and Flannery B.P. Numerical recipes in C: The Art of Scientific Computing. 2nd, rev. edit (1997), Cambridge University Press, Cambridge
73. Efron B., and Gong G. A leisurely look at the bootstrap, the jackknife, and cross-validation. Am. Stat. 37 (1983) 36-48
74. 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
75. Bai Y.W., Milne J.S., Mayne L., and Englander S.W. Primary structure effects on peptide group hydrogen-exchange. Proteins: Struct. Funct. Genet. 17 (1993) 75-86
76. Connelly G.P., Bai Y.W., Jeng M.F., and Englander S.W. Isotope effects in peptide group hydrogen-exchange. Proteins: Struct. Funct. Genet. 17 (1993) 87-92
77. Englander S.W., Mayne L., Bai Y., and Sosnick T.R. Hydrogen exchange: the modern legacy of Linderstrom-Lang. Protein Sci. 6 (1997) 1101-1109
78. Allen M., Friedler A., Schon O., and Bycroft M. The structure of an FF domain from human HYPA/FBII. J. Mol. Biol. 323 (2002) 411-416