Using relaxation dispersion NMR spectroscopy to determine structures of excited, invisible protein states

Journal of Biomolecular NMR

Volumn 41, Issue 3, 2008, Pages 113-120

  Hansen, D Flemming ^a   Vallurupalli, Pramodh ^a   Kay, Lewis E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

ANISOTROPY; ARTICLE; CONFORMATION; CONTROLLED STUDY; ENERGY; MOLECULE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

ANISOTROPY; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEINS; THERMODYNAMICS;

EID: 46949093335     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-008-9251-5     Document Type: Article

References (59)

1. Allerhand A, Gutowsky HS, Jonas J, Meinzer RA (1966) Nuclear magentic resonance methods for determining chemical-exchange rates. J Am Chem Soc 88:3185-3194
2. Bax A (2003) Weak alignment offers new NMR opportunities to study protein structure and dynamics. Protein Sci 12:1-16
3. Boehr DD, McElheny D, Dyson HJ, Wright PE (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313:1638-1642
4. Campbell I, Carver J, Dwek R, Nummelin A, Richards R (1971) Proton relaxation of methyl cynaide in presence of NI(II) ions, as studied by spin echo techniques. Mol Phys 20:913-917
5. Carr HY, Purcell EM (1954) Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 54:630-638
6. Carver JP, Richards RE (1972) A general two-site solution for the chemial exchange produced dependence of T2 upon the Carr-Purcell pulse separation. J Magn Reson 6:89-105
7. Cavalli A, Salvatella X, Dobson CM, Vendruscolo M (2007) Protein structure determination from NMR chemical shifts. Proc Natl Acad Sci USA 104:9615-9620
8. Clore GM, Driscoll PC, Wingfield PT, Gronenborn AM (1990) Analysis of backbone dynamics of Interleukin-1b using two-dimensional inverse detected heteronuclear 15N-1H NMR spectroscopy. Biochemistry 29:7387-7401
9. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homolgy. J Biomol NMR 13:289-302
10. Deverell C, Morgan RE, Strange JH (1970) Studies of chemical exchange by nuclear magnetic relaxation in the rotating frame. Mol Phys 18:553-559
11. Dittmer J, Bodenhausen G (2004) Evidence for slow motion in proteins by multiple refocusing of heteronuclear nitrogen/proton multiple quantum coherences in NMR. J Am Chem Soc 126:1314-1315
12. Drubin DG, Mulholland J, Zhu ZM, Botstein D (1990) Homology of a yeast actin-binding protein to signal transduction proteins and myosin-I. Nature 343:288-290
13. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, Skalicky JJ, Kay LE, Kern D (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117-121
14. Grey MJ, Wang CY, Palmer AG (2003) Disulfide bond isomerization in basic pancreatic trypsin inhibitor: Multisite chemical exchange quantified by CPMG relaxation dispersion and chemical shift modeling. J Am Chem Soc 125:14324-14335
15. 13Cα dipolar couplings of invisible protein states by spin-state selective relaxation dispersion NMR spectroscopy. J Am Chem Soc. doi: 10.1021/ja801005n
16. Hansen DF, Vallurupalli P, Lundstrom P, Neudecker P, Kay LE (2008b) Probing chemical shifts of invisible states of proteins with relaxation dispersion NMR spectroscopy: How well can we do? J Am Chem Soc 130:2667-2675
17. Haynes J, Garcia B, Stollar EJ, Rath A, Andrews BJ, Davidson AR (2007) The biologically relevant targets and binding affinity requirements for the function of the yeast actin-binding protein 1 SRC-homology 3 domain vary with genetic context. Genetics 176:193-208
18. 13C NMR spectroscopy of alanine methyl groups in detergent-solubilized M13 coat protein. Biochemistry 25:590-598
19. Henzler-Wildman KA, Thai V, Lei M, Ott M, Wolf-Watz M, Fenn T, Pozharski E, Wilson MA, Petsko GA, Karplus M, Hubner CG, Kern D (2007) Intrinsic motions along an enzymatic reaction trajectory. Nature 450:838-844
20. Hill RB, Bracken C, DeGrado WF, Palmer AG (2000) Molecular motions and protein folding: Characterization of the backbone dynamics and folding equilibrium of alpha D-2 using C-13 NMR spin relaxation. J Am Chem Soc 122:11610-11619
21. Igumenova TI, Brath U, Akke M, Palmer AG (2007) Characterization of chemical exchange using residual dipolar coupling. J Am Chem Soc 129:13396-13397
22. Ishima R, 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 25:243-248
23. Ishima R, Freedberg DI, Wang YX, Louis JM, Torchia DA (1999) Flap opening and dimer-interface flexibility in the free and inhibitor-bound HIV protease, and their implications for function. Structure Fold Des 7:1047-1055
24. Ishima R, Baber J, Louis JM, Torchia DA (2004) Carbonyl carbon transverse relaxation dispersion measurements and ms-micros timescale motion in a protein hydrogen bond network. J Biomol NMR 29:187-198
25. Jarymowycz V, Stone M (2006) Fast time scale dynamics of protein backbones: NMR relaxation methods, applications and functional consequences. Chem Rev 106:1624-1671
26. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28:8972-8979
27. Kloiber K, Konrat R (2000) Differential multiple-quantum relaxation arising from cross-correlated time-modulation of isotropic chemical shifts. J Biomol NMR 18:33-42
28. Korzhnev DM, Kay LE (2008) Probing invisible, low-populated states of protein molecules by relaxation dispersion NMR spectroscopy: An application to protein folding. Acc Chem Res 41:442-451
29. Korzhnev DM, Kloiber K, Kanelis V, Tugarinov V, Kay LE (2004a) Probing slow dynamics in high molecular weight proteins by methyl-TROSY NMR spectroscopy: Application to a 723-residue enzyme. J Am Chem Soc 126:3964-3973
30. Korzhnev DM, Salvatella X, Vendruscolo M, Di Nardo AA, Davidson AR, Dobson CM, Kay LE (2004b) Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 430:586-590
31. Korzhnev DM, Neudecker P, Mittermaier A, Orekhov VY, Kay LE (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 127:15602-15611
32. Lindorff-Larsen K, Best RB, Depristo MA, Dobson CM, Vendruscolo M (2005) Simultaneous determination of protein structure and dynamics. Nature 433:128-132
33. Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic relaxation in macromolecules: 1. Theory and range of validity. J Am Chem Soc 104:4546-4559
34. Loria JP, Rance M, Palmer AG (1999) A relaxation compensated CPMG sequence for characterizing chemical exchange. J Am Chem Soc 121:2331-2332
35. Lundstrom P, Teilum K, Carstensen T, Bezsonova I, Wiesner S, Hansen DF, Religa TL, Akke M, Kay LE (2007) Fractional 13C enrichment of isolated carbons using [1-13C]- or [2-13C]-glucose facilitates the accurate measurement of dynamics at backbone Calpha and side-chain methyl positions in proteins. J Biomol NMR 38:199-212
36. McConnell HM (1958) Reaction rates by nuclear magnetic resonance. J Chem Phys 28:430-431
37. Meiboom S, Gill D (1958) Modified spin-echo method for measuring nuclear magnetic relaxation times. Rev Sci Instrum 29:688-691
38. Mulder FAA, Mittermaier A, Hon B, Dahlquist FW, Kay LE (2001) Studying excited states of protein by NMR spectroscopy. Nat Struct Biol 8:932-935
39. Palmer AG, Kroenke CD, Loria JP (2001) NMR methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 339:204-238
40. Palmer AG, Grey MJ, Wang C (2005) Solution NMR spin relaxation methods for characterizing chemical exchange in high-molecular-weight systems. Methods Enzymol 394:430-465
41. Peng JW, Wagner G (1992) Mapping of spectral density functions using heteronuclear NMR relaxation measurements. J Magn Reson 98:308-332
42. Prestegard JH, Mayer KL, Valafar H, Benison GC (2005) Determination of protein backbone structures from residual dipolar couplings. Methods Enzymol 394:175-209
43. Richarz R, Nagayama K, Wuthrich K (1980) Carbon-13 nuclear magnetic resonance relaxation studies of internal mobility of the polypeptide chain in basic pancreatic trypsin inhibitor and a selectively reduced analogue. Biochemistry 19:5189-5196
44. Shen Y, Lange O, Delaglio F, Rossi P, Aramini JM, Liu G, Eletsky A, Wu Y, Singarapu KK, Lemak A, Ignatchenko A, Arrowsmith CH, Szyperski T, Montelione GT, Baker D, Bax A (2008) Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci USA 105:4685-4690
45. Skrynnikov NR, Dahlquist FW, Kay LE (2002) Reconstructing NMR spectra of "invisible" excited protein states using HSQC and HMQC experiments. J Am Chem Soc 124:12352-12360
46. Sugase K, Dyson HJ, Wright PE (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447:1021-1024
47. 13C labeling of aromatic side chains in proteins for NMR relaxation measurements. J Am Chem Soc 128:2506-2507
48. Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111-1114
49. Tolkatchev D, Xu P, Ni F (2003) Probing kinetic landscape of transient peptide-protein interactions by use of peptide 15N NMR relaxation dispersion spectroscopy; Binding of an antithrombin peptide to human prothrombin. J Am Chem Soc 125:12432-12442
50. Tollinger M, Skrynnikov NR, Mulder FAA, Forman-Kay JD, Kay LE (2001) Slow dynamics in folded and unfolded states of an SH3 domain. J Am Chem Soc 123:11341-11352
51. Tollinger M, Kloiber K, Agoston B, Dorigoni C, Lichtenecker R, Schmid W, Konrat R (2006) An isolated helix persists in a sparsely populated form of KIX under native conditions. Biochemistry 45:8885-8893
52. Tolman JR, Flanagan JM, Kennedy MA, Prestegard JH (1995) Nuclear magnetic dipole interactions in field-oriented proteins: Information for structure determination in solution. Proc Natl Acad Sci USA 92:9279-9283
53. Vallurupalli P, Kay LE (2006) Complementarity of ensemble and single-molecule measures of protein motion: A relaxation dispersion NMR study of an enzyme complex. Proc Natl Acad Sci USA 103:11910-11915
54. Vallurupalli P, Hansen DF, Stollar EJ, Meirovitch E, Kay LE (2007) Measurement of bond vector orientations in invisible excited states of proteins. Proc Natl Acad Sci USA 104:18473-18477
55. Vallurupalli P, Hansen DF, Kay LE (2008a) Probing structure in invisible protein states with anisotropic NMR chemical shifts. J Am Chem Soc 130:2734-2735
56. Vallurupalli P, Hansen DF, Kay LE (2008b) Structures of excited protein states by relaxation dispersion NMR spectroscopy (submitted)
57. van Ingen H, Vuister GW, Wijmenga S, Tessari M (2006) CEESY: characterizing the conformation of unobservable protein states. J Am Chem Soc 128:3856-3857
58. Watt ED, Shimada H, Kovrigin EL, Loria JP (2007) The mechanism of rate-limiting motions in enzyme function. Proc Natl Acad Sci USA 104:11981-11986
59. Zeeb M, Balbach J (2005) NMR spectroscopic characterization of millisecond protein folding by transverse relaxation dispersion measurements. J Am Chem Soc 127:13207-13212