Enhanced accuracy of kinetic information from CT-CPMG experiments by transverse rotating-frame spectroscopy

Journal of Biomolecular NMR

Volumn 57, Issue 1, 2013, Pages 73-82

  Ban, David ^a   Mazur, Adam ^a   G Carneiro, Marta ^a   Sabo, T Michael ^a   Giller, Karin ^a   Koharudin, Leonardus M I ^b   Becker, Stefan ^a   Gronenborn, Angela M ^b   Griesinger, Christian ^a   Lee, Donghan ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

CT CPMG; Kinetics; R1 ; Relaxation dispersion

Indexed keywords

AGGLUTININ; UBIQUITIN;

ACCURACY; ARTICLE; CONSTANT TIME CARR PURCELL MEIBOOM GILL RELAXATION DISPERSION; DISPERSION; KINETICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OSCILLATORIA; PRIORITY JOURNAL; RELAXATION TRAINING;

PLANKTOTHRIX AGARDHII;

BACTERIAL PROTEINS; KINETICS; LECTINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OSCILLATORIA; PROTEIN CONFORMATION; UBIQUITIN;

EID: 84883552917     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-013-9769-z     Document Type: Article

References (53)

1. Akke M, Liu J, Cavanagh J, Erickson HP, Palmer AG III (1998) Pervasive conformational fluctuations on microsecond time scales in a fibronectin type III domain. Nat Struct Biol 5:55-59
2. Allerhand A, Gutowsky HS (1964) Spin-echo studies of chemical exchange II. Closed formulas for two sites. J Chem Phys 42:1587-1599
3. Ban D et al (2011) Kinetics of conformational sampling in ubiquitin. Angew Chem Int Ed Engl 50:11437-11440
4. Ban D et al (2012) Exceeding the limit of dynamics studies on biomolecules using high spin-lock field strengths with a cryogenically cooled probehead. J Magn Reson 221:1-4
5. Bhabha G et al (2011) A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis. Science 332:234-238
6. Burnham KP, Anderson DR (2002) Model selection and multi-model inference. Springer, Berlin
7. Carr HY, Purcell EM (1954) Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 54:630-638
8. 2 upon the Carr-Purcell pulse separation. J Magn Reson 6:89-105
9. Chan DC, Kim PS (1998) HIV entry and its inhibition. Cell 93:681-684
10. 2 (CPMG) methods. J Magn Reson 104:266-275
11. Delaglio F et al (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293
12. Eisenmesser EZ et al (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117-121
13. Evenäs J, Malmendal A, Akke M (2001) Dynamics of the transition between open and closed conformations in a calmodulin C-terminal domain mutant. Structure 9:185-195
14. 15N NMR relaxation. Biochemistry 33:5984-6003
15. Grey MJ, Wang C, Palmer AG III (2003) Disulfide bond isomerization in basic pancreatic trypsin inhiptor: multisite chemical exchange quantified by CPMG relaxation dispersion and chemical shift modeling. J Am Chem Soc 125:14324-14335
16. 15N transverse relaxation: an NMR spectroscopy application to the study of a folding intermediate with pervasive chemical exchange. J Am Chem Soc 129:11468-11479
17. 15N NMR relaxation studies that probe protein backbone dynamics. Top Curr Chem 326:99-122
18. Ishima R, Torchia DA (1999) Estimating the time scale of chemical exchange of proteins from measurements of transverse relaxation rates in solution. J Biomol NMR 14:369-372
19. Ishima R, Torchia DA (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
20. Koharudin LM, Gronenborn AM (2011) Structural basis of the anti-HIV activity of the cyanobacterial Oscillatoria agardhii agglutinin. Structure 19:1170-1181
21. Koharudin LM, Furey W, Gronenborn AM (2011) Novel fold and carbohydrate specificity of the potent anti-HIV cyanobacterial lectin from Oscillatoria agardhii. J Biol Chem 286:1588-1597
22. Korzhnev DM et al (2004) Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 430:586-590
23. 1ρ NMR studies of exchange dynamics in proteins with low spin-lock fields: an application to a Fyn SH3 domain. J Am Chem Soc 127:713-721
24. Korzhnev DM, Bezsonova I, Lee S, Chalikian TV, Kay LE (2009) Alternate binding modes for a ubiquitin-SH3 domain interaction studied by NMR spectroscopy. J Mol Biol 386:391-405
25. Korzhnev DM, Religa TL, Banachewicz W, Fersht AR, Kay LE (2010) A transient and low-populated protein-folding intermediate at atomic resolution. Science 329:1312-1316
26. Kovrigin EL, Kempf JG, Grey MJ, Loria JP (2006) Faithful estimation of dynamics parameters from CPMG relaxation dispersion measurements. J Magn Reson 180:93-104
27. 15N chemical shift anisotropy relaxation interference: unambiguous determination of rotational diffusion tensors and chemical exchange effects in biological macromolecules. J Am Chem Soc 120:7905-7915
28. Lange OF et al (2008) Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320:1471-1475
29. Lee D, Hilty C, Wider G, Wüthrich K (2006) Effective rotational correlation times of proteins from NMR relaxation interference. J Magn Reson 178:72-76
30. Long D, Yang D (2010) Millisecond timescale dynamics of human liver fatty acid binding protein: testing of its relevance to the ligand entry process. Biophys J 98:3054-3061
31. Loria JP, Rance M, Palmer AG III (1999) A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J Am Chem Soc 121:2331-2332
32. Luz Z, Meiboom S (1963) Nuclear magnetic resonance study of the protolysis of trimethylammonium ion in aqueous solution-order of the reaction with respect to solvent. J Chem Phys 39:366-370
33. Marion D, Ikura M, Tschudin R, Bax A (1989) Rapid recording of 2D NMR spectra without phase cycling. Application to the study of hydrogen exchange in proteins. J Magn Reson 85:393-399
34. 1ρ rotating-frame relaxatin with weak radio-frequency fields. J Am Chem Soc 126:2247-2256
35. 1ρ relaxation experiments. Prot Sci 14:735-742
36. Mazur A, Hammesfahr B, Griesinger C, Kollmar M (2013) ShereKhan - calculating exchange parameters in relaxation dispersion data from CPMG experiments. Bioinformatics 29:1819-1820
37. McConnell HM (1958) Reaction rates by nuclear magnetic resonance. J Chem Phys 28:430-431
38. Meiboom S, Gill S (1958) Modified spin-echo method for measuring nuclear relaxation times. Rev Sci Inst 29:688-691
39. Millet O, Loria JP, Kroenke CD, Pons M, Palmer AG III (2000) The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J Am Chem Soc 122:2867-2877
40. Myint W, Ishima R (2009) Chemical exchange effects during refocusing pulses in constant-time CPMG relaxation dispersion experiments. J Biomol NMR 45:207-216
41. Neudecker P, Lundstrom P, Kay LE (2009) Relaxation dispersion NMR spectroscopy as a tool for detailed studies of protein folding. Biophys J 96:2045-2054
42. Palmer AG III (2004) NMR characterization of the dynamics of biomacromolecules. Chem Rev 104:3623-3640
43. Palmer AG III, Massi F (2006) Characterization of the dynamics of biomacromolecules using rotating-frame spin relaxation NMR spectroscopy. Chem Rev 106:1700-1719
44. Palmer AG III, Kroenke CD, Loria JP (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 339:204-238
45. 2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci USA 94:12366-12371
46. Shaka AJ, Keeler J, Frenkiel T, Freeman R (1983) An improved sequence for broadband decoupling: WALTZ-16. J Magn Reson 52:335-338
47. Skrynnikov NR, Mulder FA, Hon B, Dahlquist FW, Kay LE (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
48. Sugase K, Dyson HJ, Wright PE (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447:1021-1025
49. Tollinger M, Skrynnikov NR, Mulder FA, Forman-Kay JD, Kay LE (2001) Slow dynamics in folded and unfolded states of an SH3 domain. J Am Chem Soc 123:11341-11352
50. Vallurupalli P, Bouvignies G, Kay LE (2011) Increasing the exchange time-scale that can be probed by CPMG relaxation dispersion NMR. J Phys Chem B 115:14891-14900
51. Wang AC, Bax A (1993) Minimizing the effects of radio-frequency heating in multidimensional NMR experiments. J Biomol NMR 3:715-720
52. Wang C, Grey MJ, Palmer AG III (2001) CPMG sequences with enhanced sensitivity to chemical exchange. J Biomol NMR 21:361-366
53. 15N relaxation experiment. J Magn Reson 171:25-36