New approaches to the dynamic interpretation and prediction of NMR relaxation data from proteins

Current Opinion in Structural Biology

Volumn 13, Issue 2, 2003, Pages 175-183

  Brüschweiler, Rafael ^a  

^a CLARK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

AMINO ACID SEQUENCE; ANALYTIC METHOD; CORRELATION ANALYSIS; METHODOLOGY; MOLECULAR DYNAMICS; MOTION; NUCLEAR MAGNETIC RESONANCE; PREDICTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; REVIEW; SEPARATION TECHNIQUE;

EID: 0037398803     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(03)00036-8     Document Type: Review

References (67)

1. Ernst RR, Bodenhausen G, Wokaun A: Principles of Nuclear Magnetic Resonance in One and Two Dimensions. Oxford: Clarendon Press; 1987.
2. Cavanagh J, Fairbrother WJ, Palmer AG III, Skelton NJ: Protein NMR Spectroscopy: Principles and Practice. San Diego: Academic Press; 1996.
3. Abragam A: Principles of Nuclear Magnetism. Oxford: Oxford University Press; 1961.
4. Brutscher B. Principles and applications of cross-correlated relaxation in biomolecules. Concepts in Magnetic Resonance. 12:2000;207-229.
5. Palmer A.G. III, Kroenke C.D., Loria J.P. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol. 339:2001;204-238.
6. Woessner D.E. Nuclear magnetic dipole-dipole relaxation in molecules with internal motion. J. Chem. Phys. 42:1965;1855-1859.
7. Daragan V.A., Mayo K.H. Motional model analyses of protein and peptide dynamics using and NMR relaxation. Prog. NMR Spectrosc. 31:1997;63-105.
8. Chang S.L., Tjandra N. Analysis of NMR relaxation data of biomolecules with slow domain motions using wobble-in-a-cone approximation. J. Am. Chem. Soc. 123:2001;11484-11485.
9. Vugmeyster L., Trott O., McKnight C.J., Raleigh D.P., Palmer A.G. III Temperature-dependent dynamics of the villin headpiece helical subdomain, an unusually small thermostable protein. J. Mol. Biol. 320:2002;841-854.
10. Bremi T., Brüschweiler R. Locally anisotropic internal polypeptide backbone dynamics by NMR relaxation. J. Am. Chem. Soc. 119:1997;6672-6673.
11. Bremi T., Brüschweiler R., Ernst R.R. A protocol for the interpretation of side-chain dynamics based on NMR relaxation: application to phenylalanines of antamanide. J. Am. Chem. Soc. 119:1997;4272-4284.
12. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104:1982;4546-4559.
13. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104:1982;4559-4570.
14. 15N nuclear magnetic relaxation of proteins J. Am. Chem. Soc. 112:1990;4989-4991.
15. Case D.A. Molecular dynamics and NMR spin relaxation in proteins. Acc. Chem. Res. 35:2002;325-331 A comprehensive review on the status of MD simulations for the prediction of NMR relaxation parameters of proteins.
16. Spyracopoulos L., Sykes B.D. Thermodynamic insights into proteins from NMR spin relaxation studies. Curr. Opin. Struct. Biol. 11:2001;555-559.
17. 13C O) NMR relaxation and computational molecular dynamics Biochemistry. 41:2002;2655-2666.
18. 2H NMR relaxation methods Biochemistry. 40:2001;9560-9569.
19. 2H NMR relaxation studies of R. capsulatus ferrocytochrome c2 Biochemistry. 40:2001;6559-6569.
20. Liu W., Flynn P.F., Fuentes E.J., Kranz J.K., McCormick M., Wand A.J. Main chain and side chain dynamics of oxidized flavodoxin from Cyanobacterium anabaena. Biochemistry. 40:2001;14744-14753.
21. 13C longitudinal and transverse relaxation rates measured in the same protein sample J. Am. Chem. Soc. 123:2001;6164-6171.
22. Ishima R., Louis J.M., Torchia D.A. Characterization of two hydrophobic methyl clusters in HIV-1 protease by NMR spin relaxation in solution. J. Mol. Biol. 305:2001;515-521.
23. Finerty P., Muhandiram R., Forman-Kay J. Side-chain dynamics of the SAP SH2 domain correlate with a binding hot spot and a region with conformational plasticity. J. Mol. Biol. 322:2002;605-620.
24. 2D methyl sidechains of two different proteins. Because the spectral density function is sampled at only three frequencies, the self-consistency of the relaxation data could be thoroughly established.
25. ••] for the B1 domain of peptostreptococcal protein L at four different magnetic field strengths and visualized using a spectral density mapping procedure. For almost 90% of the methyl groups, a two-parameter model-free analysis [12] works well, whereas for the rest, slower timescale motions are relaxation active too, presumably reflecting jumps between rotameric states.
26. Woessner D.E. Nuclear spin relaxation in ellipsoids undergoing rotational Brownian motion. J. Chem. Phys. 37:1962;647-654.
27. Korzhnev D.M., Billeter M., Arseniev A.S., Orekhov V.Y. NMR studies of Brownian tumbling and internal motions in proteins. Prog. NMR Spectrosc. 38:2001;197-266.
28. Brüschweiler R., Liao X., Wright P.E. Long-range motional restrictions in a multidomain zinc-finger protein from anisotropic tumbling. Science. 268:1995;886-889.
29. α nuclear spin relaxation J. Biomol. NMR. 9:1997;287-298.
30. Ghose R., Fushman D., Cowburn D. Determination of the rotational diffusion tensor of macromolecules in solution from NMR relaxation data with a combination of exact and approximate methods - application to the determination of interdomain orientation in multidomain proteins. J. Magn. Reson. 149:2001;204-217.
31. Andrec M., Inman K.G., Weber D.J., Levy R.M., Montelione G. A Bayesian statistical method for the detection and quantification of rotational diffusion anisotropy from NMR relaxation data. J. Magn. Reson. 146:2000;66-80.
32. 15N NMR relaxation in Abl SH(32) Biochemistry. 38:1999;10225-10230.
33. Prestegard J.H., Kishore A.I. Partial alignment of biomolecules: an aid to NMR characterization. Curr. Opin. Chem. Biol. 5:2001;584-590.
34. Hwang P.M., Skrynnikov N.R., Kay L.E. Domain orientation in beta-cyclodextrin-loaded maltose binding protein: diffusion anisotropy measurements confirm the results of a dipolar coupling study. J. Biomol. NMR. 20:2001;83-88.
35. 15N NMR relaxation J. Am. Chem. Soc. 117:1995;12562-12566.
36. Osborne M.J., Wright P.E. Anisotropic rotational diffusion in model-free analysis for a ternary DHFR complex. J. Biomol. NMR. 19:2001;209-230.
37. Blackledge M., Cordier F., Dosset P., Marion D. Precision and uncertainty in the characterization of rotational diffusion from heteronuclear relaxation data. J. Am. Chem. Soc. 120:1998;4538-4539.
38. Dosset P., Hus J.-C., Blackledge M., Marion D. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR. 16:2000;23-28.
39. Pawley N.H., Gans J.D., Nicholson L.K. Factors determining the reliable description of global tumbling parameters in solution NMR. J. Biomol. NMR. 24:2002;215-229 A numerical analysis is presented of various sources of error on the accuracy of the fitting of global tumbling parameters from NMR relaxation data. It is found that, even in cases in which the N-H vector distribution is highly anisotropic, accurate tumbling parameters can be derived.
40. Garcia de la Torre J., Huertas M.L., Carrasco B. HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations. J. Magn. Reson. 147:2000;138-146.
41. 2 ratios. Assuming static structures, a hydrodynamic bead radius distribution ranging between 2.8 Å and 3.8 Å with an average of 3.3 Å was obtained. Deviant protein behavior is discussed in terms of protein aggregation, mobility or an inadequate structural model.
42. Akerud T., Thulin E., Van Etten R.L., Akke M. Intramolecular dynamics of low molecular weight protein tyrosine phosphatase in monomer-dimer equilibrium studied by NMR: a model for changes in dynamics upon target binding. J. Mol. Biol. 322:2002;137-152.
43. La Penna G., Mormino M., Pioli F., Perico A., Fioravanti R., Gruschus J.M., Ferretti J.A. Smoluchowski dynamics of the vnd/NK-2 homeodomain from Drosophila melanogaster: first-order mode-coupling approximation. Biopolymers. 49:1999;235-254.
44. La Penna G., Fausti S., Perico A., Ferretti J.A. Smoluchowski dynamics of the vnd/NK-2 homeodomain from Drosophila melanogaster: second-order maximum correlation approximation. Biopolymers. 54:2000;89-103.
45. 15N NMR relaxation in proteins J. Am. Chem. Soc. 123:2001;3055-3063.
46. 15N NMR relaxation J. Mol. Biol. 315:2002;155-170.
47. 15N spin relaxation Biochemistry. 41:2002;6271-6281.
48. Peng J.W., Wagner G. Mapping of spectral densities of N-H bond motions in eglin c using heteronuclear relaxation experiments. Biochemistry. 31:1992;8571-8586.
49. 15N relaxation data exclusively J. Biomol. NMR. 6:1995;153-162.
50. Ishima R., Nagayama K. Quasi spectral density function analysis for N-15 nuclei in proteins. J. Mag. Reson. B. 108:1995;73-76.
51. Yao J., Chung J., Eliezer D., Wright P.E., Dyson H.J. NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding. Biochemistry. 40:2001;3561-3571.
52. 15N relaxation data, are nearly quantitatively explained in terms of the intrinsic properties of the amino acids and their sequence, including the sidechain volume and local hydrophobic clustering, using Equation 3.
53. Schwalbe H., Fiebig K.M., Buck M., Jones J.A., Grimshaw S.B., Spencer A., Glaser S.J., Smith L.J., Dobson C.M. Structural and dynamical properties of a denatured protein. Heteronuclear 3D NMR experiments and theoretical simulations of lysozyme in 8 M urea. Biochemistry. 36:1997;8977-8991.
54. Buevich A.V., Baum J. Dynamics of unfolded proteins: incorporation of distributions of correlation times in the model free analysis of NMR relaxation data. J. Am. Chem. Soc. 121:1999;8671-8672.
55. Buevich A.V., Shinde U.P., Inouye M., Baum J. Backbone dynamics of the natively unfolded pro-peptide of subtilisin by heteronuclear NMR relaxation studies. J. Biomol. NMR. 20:2001;233-249.
56. Brüschweiler R., Wright P.E. NMR order parameters of biomolecules - A new analytical representation and application to the Gaussian axial fluctuation model. J. Am. Chem. Soc. 116:1994;8426-8427.
57. 15N relaxation data at multiple magnetic fields from the folded native state and the partially folded A-state of ubiquitin are described in terms of the isotropic reorientational eigenmode dynamics (iRED) analysis. Adjustment of the correlation times of the ten largest eigenmodes yields good agreement between the model and the experiment.
58. Goodman J.L., Pagel M.D., Stone M.J. Relationships between protein structure and dynamics from a database of NMR-derived backbone order parameters. J. Mol. Biol. 295:2000;963-978.
59. Zhang F., Brüschweiler R. Contact model for the prediction of NMR N-H order parameters in globular proteins. J. Am. Chem. Soc. 124:2002;12654-12655 The analytical relationship Equation 5 is presented for the prediction of order parameters from a known protein structure For the proteins analyzed, the quality of the prediction does not significantly depend whether an X-ray or an NMR structure is used, provided that the X-ray structure is representative of the solution state and that the predictions are averaged over an ensemble of NMR structures.
60. Lienin S.F., Brüschweiler R. Characterization of collective and anisotropic reorientational protein dynamics. Phys. Rev. Lett. 84:2000;5439-5442.
61. Brüschweiler R., Case D.A. Collective NMR relaxation model applied to protein dynamics. Phys. Rev. Lett. 72:1994;940-943.
62. Kitao A., Wagner G. A space-time structure determination of human CD2 reveals the CD58-binding mode. Proc. Natl. Acad. Sci. USA. 97:2000;2064-2068.
63. Prompers J.J., Brüschweiler R. Reorientational eigenmode dynamics: a combined MD/NMR relaxation analysis method for flexible parts in globular proteins. J. Am. Chem. Soc. 123:2001;7305-7313.
64. 15N relaxation data from the wild type and two single amino acid mutants of the N-terminal RNA-binding domain of the human U1A protein, RBD1, have been analyzed in terms of the reorientational eigenmode dynamics formalism based on two 2.5 ns MD trajectories of each protein. Significant changes in the magnitude and extent of intradomain motional correlations are found for both mutants, which suggests that their weak RNA-binding properties are a consequence of their loss of collective dynamics.
65. Lienin S.F., Bremi T., Brutscher B., Brüschweiler R., Ernst R.R. Anisotropic intramolecular backbone dynamics of ubiquitin characterized by NMR relaxation and MD computer simulation. J. Am. Chem. Soc. 120:1998;9870-9879.
66. Vijay-Kumar S., Bugg C.E., Cook W.J. Structure of ubiquitin refined at 1.8 Å resolution. J. Mol. Biol. 194:1987;531-544.
67. Cornilescu G., Marquardt J.L., Ottiger M., Bax A. Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J. Am. Chem. Soc. 120:1998;6836-6837.