Toward optimal-resolution NMR of intrinsically disordered proteins

Journal of Magnetic Resonance

Volumn 241, Issue 1, 2014, Pages 41-52

  Nováček, Jiří ^a   Žídek, Lukáš ^a   Sklenář, Vladimír ^a  

^a MASARYK UNIVERSITY   (Czech Republic)

Author keywords

IDPRs; IDPs; Multi dimensional NMR; Non uniform sampling; NUS; PRE; RDC; RNAP subunit

Indexed keywords

NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

IDPRS; IDPS; MULTIDIMENSIONAL NMR; NONUNIFORM SAMPLING; NUS; PRE; RDC;

PROTEINS;

PROTEIN;

ALGORITHM; ANIMAL; ARTICLE; CHEMISTRY; HUMAN; IDPRS; IDPS; METHODOLOGY; MULTI-DIMENSIONAL NMR; NON-UNIFORM SAMPLING; NUCLEAR MAGNETIC RESONANCE; NUS; PRE; PROTEIN CONFORMATION; RDC; RNAP Δ-SUBUNIT;

IDPRS; IDPS; MULTI-DIMENSIONAL NMR; NON-UNIFORM SAMPLING; NUS; PRE; RDC; RNAP Δ-SUBUNIT;

ALGORITHMS; ANIMALS; HUMANS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS;

EID: 84896942605     PISSN: 10907807     EISSN: 10960856     Source Type: Journal    
DOI: 10.1016/j.jmr.2013.12.008     Document Type: Article

References (75)

1. A.K. Dunker, J.D. Lawson, C.J. Brown, R.M. Williams, P. Romero, J.S. Oh, C.J. Oldfield, A.M. Campen, C.M. Ratliff, K.W. Hipps, J. Ausio, M.S. Nissen, R. Reeves, C. Kang, C.R. Kissinger, R.W. Bailey, M.D. Griswold, W. Chiu, E.C. Garner, and Z. Obradovic Intrinsically disordered protein J. Mol. Graphics Modell. 19 2001 26 59 (Pubitemid 32411501)
2. A.K. Dunker, Z. Obradovic, P. Romero, E.C. Garner, and C.J. Brown Intrinsic protein disorder in complete genomes Gen. Inform. Ser. Workshop Gen. Inform. 11 2000 161 171
3. C.B. Anfinsen Principles that govern folding of protein chains Science 181 1973 223 230
4. A.K. Dunker, C.J. Oldfield, J. Meng, P. Romero, J.Y. Yang, J.W. Chen, V. Vacic, Z. Obradovic, and V.N. Uversky The unfoldomics decade: an update on intrinsically disordered proteins BMC Genomics 9 2008 S1
5. P. Tompa Intrinsically disordered proteins: a 10-year recap Trends Biochem. Sci. 37 2012 509 516
6. V.N. Uversky A decade and a half of protein intrinsic disorder: biology still waits for physics Protein Sci. 22 2013 693 724
7. T. Mittag, and J.D. Forman-Kay Atomic-level characterization of disordered protein ensembles Curr. Opin. Struct. Biol. 17 2007 3 14 (Pubitemid 46240819)
8. M.R. Jensen, R.W. Ruigrok, and M. Blackledge Describing intrinsically disordered proteins at atomic resolution by NMR Curr. Opin. Struct. Biol. 23 2013 426 435
9. J.A. Marsh, V.K. Singh, Z. Jia, and J.D. Forman-Kay Sensitivity of secondary structure propensities to sequence differences between alpha- and gamma-synuclein: implications for fibrillation Protein Sci. 15 2006 2795 2804 (Pubitemid 44833760)
10. C. Camilloni, A. De Simone, W.F. Vranken, and M. Vendruscolo Determination of secondary structure populations in disordered states of proteins using nuclear magnetic resonance chemical shifts Biochemistry 51 2012 2224 2231
11. K. Tamiola, B. Acar, and F.A. Mulder Sequence-specific random coil chemical shifts of intrinsically disordered proteins J. Am. Chem. Soc. 132 2010 18000 18003
12. M. Kjaergaard, and F.M. Poulsen Sequence correction of random coil chemical shifts: correlation between neighbor correction factors and changes in the Ramachandran distribution J. Biomol. NMR 50 2011 157 165
13. J. Koehler, and J. Meiler Expanding the utility of NMR restraints with paramagnetic compounds: background and practical aspects Prog. Nucl. Magn. Reson. Spectrosc. 59 2011 360 389
14. M.D. Mukrasch, P. Markwick, J. Biernat, M. Bergen, P. Bernado, C. Griesinger, E. Mandelkow, M. Zweckstetter, and M. Blackledge Highly populated turn conformations in natively unfolded tau protein identified from residual dipolar couplings and molecular simulations J. Am. Chem. Soc. 129 2007 5235 5243 (Pubitemid 46651401)
15. P.R.L. Markwick, G. Bouvignies, and M. Blackledge Exploring multiple timescale motions in protein GB3 using accelerated molecular dynamics and NMR spectroscopy J. Am. Chem. Soc. 129 2007 4724 4730 (Pubitemid 46648771)
16. Y. Xue, I.S. Podkorytov, D.K. Rao, N. Benjamin, H.L. Sun, and N.R. Skrynnikov Paramagnetic relaxation enhancements in unfolded proteins: theory and application to drkN SH3 domain Protein Sci. 18 2009 1401 1424
17. A.K. Jha, A. Colubri, K.F. Freed, and T.R. Sosnick Statistical coil model of the unfolded state: resolving the reconciliation problem Proc. Natl. Acad. Sci. U.S.A. 102 2005 13099 13104 (Pubitemid 41324985)
18. L. Salmon, G. Nodet, V. Ozenne, G.W. Yin, M.R. Jensen, M. Zweckstetter, and M. Blackledge NMR characterization of long-range order in intrinsically disordered proteins J. Am. Chem. Soc. 132 2010 8407 8418
19. C. Bracken NMR spin relaxation methods for characterization of disorder and folding in proteins J. Mol. Graphics Modell. 19 2001 3 12 (Pubitemid 32411499)
20. R.B. Hill, C. Bracken, W.F. DeGrado, and A.G. Palmer 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 2000 11610 11619
21. D.M. Korzhnev, M. Billeter, A.S. Arseniev, and V.Y. Orekhov NMR studies of Brownian tumbling and internal motions in proteins Prog. Nucl. Magn. Reson. 38 2001 197 266 (Pubitemid 32263164)
22. 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
23. F. Ochsenbein, R. Guerois, J.M. Neumann, A. Sanson, E. Guittet, and C. van Heijenoort N-15 NMR relaxation as a probe for helical intrinsic propensity: the case of the unfolded D2 domain of annexin I J. Biomol. NMR 19 2001 3 18 (Pubitemid 32162237)
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 (Pubitemid 29453415)
25. A.V. Buevich, U.P. Shinde, M. Inouye, and J. Baum Backbone dynamics of the natively unfolded pro-peptide of subtilisin by heteronuclear NMR relaxation studies J. Biomol. NMR 20 2001 233 249 (Pubitemid 32747189)
26. W. Cao, C. Bracken, N.R. Kallenbach, and M. Lu Helix formation and the unfolded state of a 52-residue helical protein Protein Sci. 13 2004 177 189 (Pubitemid 38021152)
27. N.A. Farrow, O.W. Zhang, J.D. Forman-Kay, and L.E. Kay Characterization of the backbone dynamics of folded and denatured states of an SH3 domain Biochemistry 36 1997 2390 2402 (Pubitemid 27106631)
28. J. Yao, J. Chung, D. Eliezer, P.E. Wright, and H.J. Dyson 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 (Pubitemid 32242813)
29. P. Pelupessy, F. Ferrage, and G. Bodenhausen Accurate measurement of longitudinal cross-relaxation rates in nuclear magnetic resonance J. Chem. Phys. 126 2007
30. S. Kim, K.P. Wu, and J. Baum Fast hydrogen exchange affects N-15 relaxation measurements in intrinsically disordered proteins J. Biomol. NMR 55 2013 249 256
31. M. Sattler, J. Schleucher, and C. Griesinger Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients Prog. Nucl. Magn. Reson. Spectrosc. 34 1999 93 158 (Pubitemid 129595216)
32. T. Diercks, V. Truffault, M. Coles, and O. Millet Diagonal-free 3D/4D HN, HN-TROSY-NOESY-TROSY J. Am. Chem. Soc. 132 2010 2138 2139
33. D.P. Frueh, Z.Y. Sun, D.A. Vosburg, C.T. Walsh, J.C. Hoch, and G. Wagner Non-uniformly sampled double-TROSY hNcaNH experiments for NMR sequential assignments of large proteins J. Am. Chem. Soc. 128 2006 5757 5763 (Pubitemid 43724379)
34. 15N) labeled proteins: application to unfolded proteins J. Biomol. NMR 20 2001 135 147 (Pubitemid 32677757)
35. Z.-Y. Sun, D. Frueh, P. Selenko, J. Hoch, and G. Wagner Fast assignment of 15N-HSQC peaks using high-resolution 3D HNcocaNH experiments with non-uniform sampling J. Biomol. NMR 33 2005 43 50 (Pubitemid 41573968)
36. M.D. Mukrasch, S. Bibow, J. Korukottu, S. Jeganathan, J. Biernat, C. Griesinger, E. Mandelkow, and M. Zweckstetter Structural polymorphism of 441-residue tau at single residue resolution PLoS Biol. 7 2009 e34
37. D. Rovnyak, D.P. Frueh, M. Sastry, Z.-Y.J. Sun, A.S. Stern, J.C. Hoch, and G. Wagner Accelerated acquisition of high resolution triple-resonance spectra using non-uniform sampling and maximum entropy reconstruction J. Magn. Reson. 170 2004 15 21
38. V. Motáčková, J. Nováček, A. Zawadzka-Kazimierczuk, K. Kazimierczuk, L. Žídek, H. Šanderová, L. Krásný, W. Koźmiński, and V. Sklenář Strategy for complete NMR assignment of disordered proteins with highly repetitive sequences based on resolution-enhanced 5D experiments J. Biomol. NMR 48 2010 169 177
39. J. Barna, E. Laue, M. Mayger, J. Skilling, and S. Worrall Exponential sampling: an alternative method for sampling in two-dimensional NMR experiments J. Magn. Reson. 73 1987 69 77
40. M. Mobli, M.W. Maciejewski, A.D. Schuyler, A.S. Stern, and J.C. Hoch Sparse sampling methods in multidimensional NMR Phys. Chem. Chem. Phys. 14 2012 10835 10843
41. G. Bodenhausen, and R. Ernst The accordion experiment, a simple approach to three dimensional NMR spectroscopy J. Magn. Reson. 45 1981 367 373
42. E. Kupče, and R. Freeman Projection-reconstruction of three-dimensional NMR spectra J. Am. Chem. Soc. 125 2003 13958 13959 (Pubitemid 37420891)
43. T. Szyperski, G. Wider, J. Bushweller, and K. Wüthrich Reduced dimensionality in triple-resonance NMR experiments J. Am. Chem. Soc. 115 1993 9307 9308
44. S. Kim, and T. Szyperski GFT NMR, a new approach to rapidly obtain precise high-dimensional NMR spectra information J. Am. Chem. Soc. 125 2003 1385 1393 (Pubitemid 36159850)
45. A. Schuyler, M. Maciejewski, H. Arthanari, and J. Hoch Knowledge-based nonuniform sampling in multidimensional NMR J. Biomol. NMR 50 2011 247 262
46. S. Hiller, F. Fiorito, K. Wüthrich, and G. Wider Automated projection spectroscopy (APSY) Proc. Natl. Acad. Sci. U.S.A. 102 2005 10876 810881
47. S. Sibisi, J. Skilling, R.G. Brereton, E.D. Laue, and J. Staunton Maximum entropy signal processing in practical NMR spectroscopy Nature 311 1984 446 447
48. 1-norm reconstruction J. Magn. Reson. 188 2007 295 300 (Pubitemid 47562806)
49. R. Chylla, and J. Markley Theory and application of the maximum likelihood principle to NMR parameter estimation of multidimensional NMR data J. Biomol. NMR 5 1995 245 258
50. G.L. Bretthorst Nonuniform sampling: bandwidth and aliasing Concepts Magn. Reson. Part A 32A 2008 417 435
51. J.C.J. Barna, S.M. Tan, and E.D. Laue Use of CLEAN in conjunction with selective data sampling for 2-D NMR experiments J. Magn. Reson. 78 1988 327 332
52. D. Malmodin, and M. Billeter Multiway decomposition of NMR spectra with coupled evolution periods J. Am. Chem. Soc. 127 2005 13486 413487
53. K. Kazimierczuk, W. Koźmiński, and I. Zhukov Two-dimensional Fourier transform of arbitrarily sampled NMR data sets J. Magn. Reson. 179 2006 323 328
54. K. Kazimierczuk, A. Zawadzka, W. Koźmínski, and I. Zhukov Lineshapes and artifacts in Multidimensional Fourier Transform of arbitrary sampled NMR data sets J. Magn. Reson. 188 2007 344 356 (Pubitemid 47562815)
55. W. Bermel, M. Bruix, I.C. Felli, M.V.V. Kumar, R. Pierattelli, and S. Serrano Improving the chemical shift dispersion of multidimensional NMR spectra of intrinsically disordered proteins J. Biomol. NMR 55 2013 231 237
56. A. Zawadzka-Kazimierczuk, W. Koźmiński, H. Šanderová, and L. Krásný High dimensional and high resolution pulse sequences for backbone resonance assignment of intrinsically disordered proteins J. Biomol. NMR 52 2012 329 337
57. K. Kazimierczuk, A. Zawadzka-Kazimierczuk, and W. Koźmínski Non-uniform frequency domain for optimal exploitation of non-uniform sampling J. Magn. Reson. 205 2010 286 292
58. R. Narayanan, U. Durr, S. Bibow, J. Biernat, E. Mandelkow, and M. Zweckstetter Automatic assignment of the intrinsically disordered protein tau with 441-residues J. Am. Chem. Soc. 132 2010 11906 911907
59. N.W. Harbison, S. Bhattacharya, and D. Eliezer Assigning backbone NMR resonances for full length tau isoforms: efficient compromise between manual assignments and reduced dimensionality PLoS One 7 2012 e34679
60. W. Bermel, I. Bertini, I.C. Felli, M. Piccioli, and R. Pierattelli 13C-detected protonless NMR spectroscopy of proteins in solution Prog. Nucl. Magn. Reson. Spectrosc. 48 2006 25 45 (Pubitemid 44508624)
61. W. Bermel, I. Bertini, I.C. Felli, L. Gonnelli, W. Koźmiń ski, A. Piai, R. Pierattelli, and J. Stanek Speeding up sequence specific assignment of IDPs J. Biomol. NMR 53 2012 293 301
62. 1J(NC-alpha) selective HCBCANCO experiments for the sequential assignment and chemical shift analysis of intrinsically disordered proteins J. Biomol. NMR 53 2012 139 148
63. 13C-detected experiments for backbone assignment of unstructured proteins with a very low signal dispersion J. Biomol. NMR 50 2011 1 11
64. J. Nováček, L. Janda, R. Dopitová, L. Žídek, and V. Sklenář Efficient protocol for backbone and side-chain assignments of large, intrinsically disordered proteins: transient secondary structure analysis of 49.2 kDa microtubule associated protein 2c J. Biomol. NMR 56 2013 291 301
65. K. Pervushin, B. Vogeli, and A. Eletsky Longitudinal 1H relaxation optimization in TROSY NMR spectroscopy J. Am. Chem. Soc. 124 2002 12898 12902 (Pubitemid 35216013)
66. E. Lescop, P. Schanda, and B. Brutscher A set of BEST triple-resonance experiments for time-optimized protein resonance assignment J. Magn. Reson. 187 2007 163 169 (Pubitemid 46898871)
67. P. Schanda, and B. Brutscher Very fast two-dimensional NMR spectroscopy for real-time investigation of dynamic events in proteins on the time scale of seconds J. Am. Chem. Soc. 127 2005 8014 8015 (Pubitemid 40799646)
68. E. Babini, I. Bertini, F. Capozzi, I.C. Felli, M. Lelli, and C. Luchinat Direct carbon detection in paramagnetic metalloproteins to further exploit pseudocontact shift restraints J. Am. Chem. Soc. 126 2004 10496 10497 (Pubitemid 39129125)
69. 2H)-labeled proteins J. Biomol. NMR 17 2000 43 54 (Pubitemid 30434837)
70. 13C-alpha chemical shift anisotropy in proteins correlate with secondary structure J. Am. Chem. Soc. 119 1997 9576 9577 (Pubitemid 27460551)
71. R.M. Rasia, E. Lescop, J.F. Palatnik, J. Boisbouvier, and B. Brutscher Rapid measurement of residual dipolar couplings for fast fold elucidation of proteins J. Biomol. NMR 51 2011 369 378
72. J. Stanek, S. Saxena, L. Geist, R. Konrat, and W. Koźmiński Probing local backbone geometries in intrinsically disordered proteins by cross-correlated NMR relaxation Angew. Chem., Int. Ed. 52 2013 4604 4606
73. I. Bertini, I.C. Felli, L. Gonnelli, M.V.V. Kumar, and R. Pierattelli C-13 direct-detection biomolecular NMR spectroscopy in living cells Angew. Chem., Int. Ed. 50 2011 2339 2341
74. J.F. Bodart, J.M. Wieruszeski, L. Amniai, A. Leroy, I. Landrieu, A. Rousseau-Lescuyer, J.P. Vilain, and G. Lippens NMR observation of Tau in Xenopus oocytes J. Magn. Reson. 192 2008 252 257
75. A. Binolfi, F.X. Theillet, and P. Selenko Bacterial in-cell NMR of human alpha-synuclein: a disordered monomer by nature? Biochem. Soc. Trans. 40 2012 950 954