Distribution of Pico- and Nanosecond Motions in Disordered Proteins from Nuclear Spin Relaxation

Biophysical Journal

Volumn 109, Issue 5, 2015, Pages 988-999

  Khan, Shahid N ^a,b,c   Charlier, Cyril ^a,b,c   Augustyniak, Rafal ^a,b,c,e   Salvi, Nicola ^d,f   Déjean, Victoire ^a,b,c   Bodenhausen, Geoffrey ^a,b,c,d   Lequin, Olivier ^a,b,c   Pelupessy, Philippe ^a,b,c   Ferrage, Fabien ^a,b,c  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

^d INSTITUTE OF CHEMICAL SCIENCES AND ENGINEERING   (Switzerland)

^e UNIVERSITY OF TORONTO   (Canada)

^f INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTRINSICALLY DISORDERED PROTEIN;

CHEMISTRY; KINETICS; METABOLISM; MOVEMENT (PHYSIOLOGY); NUCLEAR MAGNETIC RESONANCE; PROTEIN SECONDARY STRUCTURE;

INTRINSICALLY DISORDERED PROTEINS; KINETICS; MOVEMENT; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY;

EID: 84940502229     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.06.069     Document Type: Article

References (68)

1. R. van der Lee, and M. Buljan M.M. Babu Classification of intrinsically disordered regions and proteins Chem. Rev. 114 2014 6589 6631
2. H.J. Dyson, and P.E. Wright Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6 2005 197 208
3. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochim. Biophys. Acta 1804 2010 1231 1264
4. A.K. Dunker, and J.D. Lawson Z. Obradovic Intrinsically disordered protein J. Mol. Graph. Model. 19 2001 26 59
5. M.R. Jensen, and P.R.L. Markwick M. Blackledge Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using NMR dipolar couplings Structure 17 2009 1169 1185
6. M.R. Jensen, and M. Zweckstetter M. Blackledge Exploring free-energy landscapes of intrinsically disordered proteins at atomic resolution using NMR spectroscopy Chem. Rev. 114 2014 6632 6660
7. J.A. Marsh, and J.D. Forman-Kay Structure and disorder in an unfolded state under nondenaturing conditions from ensemble models consistent with a large number of experimental restraints J. Mol. Biol. 391 2009 359 374
8. P. Tompa On the supertertiary structure of proteins Nat. Chem. Biol. 8 2012 597 600
9. K. Lindorff-Larsen, and N. Trbovic D.E. Shaw Structure and dynamics of an unfolded protein examined by molecular dynamics simulation J. Am. Chem. Soc. 134 2012 3787 3791
10. A. Mittermaier, and L.E. Kay New tools provide new insights in NMR studies of protein dynamics Science 312 2006 224 228
11. A.G. Palmer 3rd NMR characterization of the dynamics of biomacromolecules Chem. Rev. 104 2004 3623 3640
12. A.G. Palmer 3rd Chemical exchange in biomacromolecules: past, present, and future J. Magn. Reson. 241 2014 3 17
13. J.W. Peng, and G. Wagner Mapping of spectral density-functions using heteronuclear NMR relaxation measurements J. Magn. Reson. 98 1992 308 332
14. G. Lipari, and A. Szabo 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
15. B. Halle The physical basis of model-free analysis of NMR relaxation data from proteins and complex fluids J. Chem. Phys. 131 2009 224507
16. G.M. Clore, and A. Szabo A.M. Gronenborn Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins J. Am. Chem. Soc. 112 1990 4989 4991
17. D. Eliezer Biophysical characterization of intrinsically disordered proteins Curr. Opin. Struct. Biol. 19 2009 23 30
18. M.R. Jensen, R.W.H. Ruigrok, and M. Blackledge Describing intrinsically disordered proteins at atomic resolution by NMR Curr. Opin. Struct. Biol. 23 2013 426 435
19. R. Konrat NMR contributions to structural dynamics studies of intrinsically disordered proteins J. Magn. Reson. 241 2014 74 85
20. P. Kadeřávek, and V. Zapletal L. Žídek Spectral density mapping protocols for analysis of molecular motions in disordered proteins J. Biomol. NMR 58 2014 193 207
21. R. Bussell Jr., and D. Eliezer Residual structure and dynamics in Parkinson's disease-associated mutants of α-synuclein J. Biol. Chem. 276 2001 45996 46003
22. K. Houben, and L. Blanchard D. Marion Intrinsic dynamics of the partly unstructured PX domain from the Sendai virus RNA polymerase cofactor P Biophys. J. 93 2007 2830 2844
23. B. Brutscher, R. Brüschweiler, and R.R. Ernst Backbone dynamics and structural characterization of the partially folded A state of ubiquitin by 1H, 13C, and 15N nuclear magnetic resonance spectroscopy Biochemistry 36 1997 13043 13053
24. A.V. Buevich, and J. Baum 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
25. A.V. Buevich, and U.P. Shinde J. Baum Backbone dynamics of the natively unfolded pro-peptide of subtilisin by heteronuclear NMR relaxation studies J. Biomol. NMR 20 2001 233 249
26. K. Modig, and F.M. Poulsen Model-independent interpretation of NMR relaxation data for unfolded proteins: the acid-denatured state of ACBP J. Biomol. NMR 42 2008 163 177
27. E. Sternin Use of inverse theory algorithms in the analysis of biomembrane NMR data Methods Mol. Biol. 400 2007 103 125
28. R.C. Aster, B. Borchers, and C.H. Thurber Parameter Estimation and Inverse Problems 2nd ed. 2012 Academic Press New York
29. I. Foucher, and M.L. Montesinos A. Trembleau Joint regulation of the MAP1B promoter by HNF3β/Foxa2 and Engrailed is the result of a highly conserved mechanism for direct interaction of homeoproteins and Fox transcription factors Development 130 2003 1867 1876
30. L.T.C. Peltenburg, and C. Murre Engrailed and Hox homeodomain proteins contain a related Pbx interaction motif that recognizes a common structure present in Pbx EMBO J. 15 1996 3385 3393
31. R. Augustyniak, and S. Balayssac O. Lequin 1H, 13C and 15N resonance assignment of a 114-residue fragment of Engrailed 2 homeoprotein, a partially disordered protein Biomol. NMR Assign. 5 2011 229 231
32. Y. Xue, and N.R. Skrynnikov Motion of a disordered polypeptide chain as studied by paramagnetic relaxation enhancements, 15N relaxation, and molecular dynamics simulations: how fast is segmental diffusion in denatured ubiquitin? J. Am. Chem. Soc. 133 2011 14614 14628
33. R. Augustyniak, and F. Ferrage G. Bodenhausen Methods to determine slow diffusion coefficients of biomolecules: applications to Engrailed 2, a partially disordered protein J. Biomol. NMR 50 2011 209 218
34. L.E. Kay, and L.K. Nicholson D.A. Torchia Pulse sequences for removal of the effects of cross-correlation between dipolar and chemical-shift anisotropy relaxation mechanism on the measurement of heteronuclear T1 and T2 values in proteins J. Magn. Reson. 97 1992 359 375
35. A.G. Palmer III, and N.J. Skelton M. Rance Suppression of the effects of cross-correlation between dipolar and anisotropic chemical-shift relaxation mechanisms in the measurement of spin spin relaxations rates Mol. Phys. 75 1992 699 711
36. F. Ferrage Protein dynamics by 15N nuclear magnetic relaxation Methods Mol. Biol. 831 2012 141 163
37. F. Ferrage, D. Cowburn, and R. Ghose Accurate sampling of high-frequency motions in proteins by steady-state 15N-1H nuclear Overhauser effect measurements in the presence of cross-correlated relaxation J. Am. Chem. Soc. 131 2009 6048 6049
38. F. Ferrage, and A. Reichel R. Ghose On the measurement of 15N-1H nuclear Overhauser effects. 2. Effects of the saturation scheme and water signal suppression J. Magn. Reson. 207 2010 294 303
39. P. Pelupessy, G.M. Espallargas, and G. Bodenhausen Symmetrical reconversion: measuring cross-correlation rates with enhanced accuracy J. Magn. Reson. 161 2003 258 264
40. P. Pelupessy, F. Ferrage, and G. Bodenhausen Accurate measurement of longitudinal cross-relaxation rates in nuclear magnetic resonance J. Chem. Phys. 126 2007 134508
41. L. Carlier, and S. Balayssac O. Lequin Investigation of homeodomain membrane translocation properties: insights from the structure determination of engrailed-2 homeodomain in aqueous and membrane-mimetic environments Biophys. J. 105 2013 667 678
42. Wolfram Research Wolfram Mathematica 2012 Wolfram Research Champaign, IL
43. J.A. Marsh, and V.K. Singh J.D. Forman-Kay Sensitivity of secondary structure propensities to sequence differences between α- and γ-synuclein: implications for fibrillation Protein Sci. 15 2006 2795 2804
44. F. Delaglio, and S. Grzesiek A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
45. H.J. Dyson, and P.E. Wright Unfolded proteins and protein folding studied by NMR Chem. Rev. 104 2004 3607 3622
46. A.M. Mandel, M. Akke, and A.G. Palmer 3rd Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme J. Mol. Biol. 246 1995 144 163
47. R. Cole, and J.P. Loria FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data J. Biomol. NMR 26 2003 203 213
48. D. Fushman, S. Cahill, and D. Cowburn The main-chain dynamics of the dynamin pleckstrin homology (PH) domain in solution: analysis of 15N relaxation with monomer/dimer equilibration J. Mol. Biol. 266 1997 173 194
49. P. Dosset, and J.C. Hus D. Marion Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data J. Biomol. NMR 16 2000 23 28
50. M. Bieri, E.J. d'Auvergne, and P.R. Gooley relaxGUI: a new software for fast and simple NMR relaxation data analysis and calculation of ps-ns and μs motion of proteins J. Biomol. NMR 50 2011 147 155
51. N.A. Farrow, and O. Zhang L.E. Kay Spectral density function mapping using 15N relaxation data exclusively J. Biomol. NMR 6 1995 153 162
52. R. Ishima, and K. Nagayama Protein backbone dynamics revealed by quasi spectral density function analysis of amide N-15 nuclei Biochemistry 34 1995 3162 3171
53. R.B. Hill, and C. Bracken A.G. Palmer Molecular motions and protein folding: Characterization of the backbone dynamics and folding equilibrium of α2D using 13C NMR spin relaxation J. Am. Chem. Soc. 122 2000 11610 11619
54. V. Ropars, and S. Bouguet-Bonnet C. Roumestand Unraveling protein dynamics through fast spectral density mapping J. Biomol. NMR 37 2007 159 177
55. C.D. Kroenke, and J.P. Loria A.G. Palmer III Longitudinal and transverse 1H-15N dipolar/15N chemical shift anisotropy relaxation interference: unambiguous determination of rotational diffusion tensors and chemical exchange effects in biological macromolecules J. Am. Chem. Soc. 120 1998 7905 7915
56. D.M. LeMaster Larmor frequency selective model free analysis of protein NMR relaxation J. Biomol. NMR 6 1995 366 374
57. Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle. Proc. 2nd Int. Symp. Information Theory. B. N. Petrov, and F. Csáki, editors. Akadémiai Kiadó, Budapest, Hungary. 267-281.
58. N. Sugiura Further analysis of data by Akaike's information criterion and finite corrections Commun. Stat. Theory Methods 7 1978 13 26
59. C.M. Hurvich, and C.L. Tsai Regression and time-series model selection in small samples Biometrika 76 1989 297 307
60. K.P. Burnham, and D.R. Anderson Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2002 Springer New York
61. V. Wong, D.A. Case, and A. Szabo Influence of the coupling of interdomain and overall motions on NMR relaxation Proc. Natl. Acad. Sci. USA 106 2009 11016 11021
62. J.J. Prompers, and R. Brüschweiler General framework for studying the dynamics of folded and nonfolded proteins by NMR relaxation spectroscopy and MD simulation J. Am. Chem. Soc. 124 2002 4522 4534
63. V. Calandrini, D. Abergel, and G.R. Kneller Fractional protein dynamics seen by nuclear magnetic resonance spectroscopy: relating molecular dynamics simulation and experiment J. Chem. Phys. 133 2010 145101
64. Y.E. Ryabov, and D. Fushman A model of interdomain mobility in a multidomain protein J. Am. Chem. Soc. 129 2007 3315 3327
65. G. Parigi, and N. Rezaei-Ghaleh C. Luchinat Long-range correlated dynamics in intrinsically disordered proteins J. Am. Chem. Soc. 136 2014 16201 16209
66. J.B. Hall, and D. Fushman Variability of the 15N chemical shielding tensors in the B3 domain of protein G from 15N relaxation measurements at several fields. Implications for backbone order parameters J. Am. Chem. Soc. 128 2006 7855 7870
67. C. Charlier, and S.N. Khan F. Ferrage Nanosecond time scale motions in proteins revealed by high-resolution NMR relaxometry J. Am. Chem. Soc. 135 2013 18665 18672
68. V. Ozenne, and F. Bauer M. Blackledge Flexible-meccano: a tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables Bioinformatics 28 2012 1463 1470