Improving the chemical shift dispersion of multidimensional NMR spectra of intrinsically disordered proteins

Journal of Biomolecular NMR

Volumn 55, Issue 3, 2013, Pages 231-237

  Bermel, Wolfgang ^a   Bruix, Marta ^b   Felli, Isabella C ^c   Kumar M V , Vasantha ^c   Pierattelli, Roberta ^c   Serrano, Soraya ^b  

^a BRUKER BIOSPIN GMBH   (Germany)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

13C direct detection; 13C NMR; Chemical shift; IDP; Intrinsically disordered proteins; NMR; Secondary structure

Indexed keywords

CARBON 13; INTRINSICALLY DISORDERED PROTEIN; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

ADIABATICITY; ARTICLE; DISPERSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

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

EID: 84877921301     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-013-9704-3     Document Type: Article

References (61)

1. Bermel W, Bertini I, Duma L, Emsley L, Felli IC, Pierattelli R, Vasos PR (2005a) Complete assignment of heteronuclear protein resonances by protonless NMR spectroscopy. Angew Chem Int Ed 44:3089-3092
2. Bermel W, Bertini I, Felli IC, Pierattelli R, Vasos PR (2005b) A selective experiment for the sequential protein backbone assignment from 3D heteronuclear spectra. J Magn Reson 172:324-328
3. Bermel W, Bertini I, Felli IC, Lee Y-M, Luchinat C, Pierattelli R (2006a) Protonless NMR experiments for sequence-specific assignment of backbone nuclei in unfolded proteins. J Am Chem Soc 128:3918-3919
4. 13C-detected protonless NMR spectroscopy of proteins in solution. Progr NMR Spectrosc 48:25-45
5. α direct-detection in protonless NMR. J Magn Reson 188:301-310
6. 13C direct-detection biomolecular NMR. Concepts Magn Reson 32A:183-200
7. Bermel W, Bertini I, Csizmok V, Felli IC, Pierattelli R, Tompa P (2009a) H-start for exclusively heteronuclear NMR spectroscopy: the case of intrinsically disordered proteins. J Magn Reson 198:275-281
8. 13C direct detection NMR experiments. J Am Chem Soc 131:15339-15345
9. 13C direct-detected exclusively heteronuclear experiments to study intrinsically disordered proteins. Chem Bio Chem 13:2425-2432
10. Bermel W, Bertini I, Gonnelli L, Felli IC, Kozminski W, Piai A, Pierattelli R, Stanek J (2012b) Speeding up sequence specific assignment of IDPs. J Biomol NMR 53:293-301
11. Bertini I, Duma L, Felli IC, Fey M, Luchinat C, Pierattelli R, Vasos PR (2004) A heteronuclear direct detection NMR experiment for protein backbone assignment. Angew Chem Int Ed 43:2257-2259
12. 13C detected NMR experiments to determine key observables. ChemBioChem 12:2347-2352
13. Boehlen J-M, Bodenhausen G (1993) Experimental aspects of chirp NMR spectroscopy. J Magn Reson Ser A 102:293-301
14. Clark PJ, Evans FC (1954) Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35:445-453
15. De Simone A, Cavalli A, Hsu ST, Vranken W, Vendruscolo M (2009) Accurate random coil chemical shifts from an analysis of loop regions in native states of loop regions in native states of proteins. J Am Chem Soc 131:16332-16333
16. Duma L, Hediger S, Lesage A, Emsley L (2003) Spin-state selection in solid-state NMR. J Magn Reson 164:187-195
17. Dunker AK, Silman I, Uversky VN, Sussman JL (2008) Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18:756-764
18. Dyson HJ, Wright PE (2001) Nuclear magnetic resonance methods for the elucidation of structure and dynamics in disordered states. Methods Enzymol 339:258-271
19. Dyson HJ, Wright PE (2004) Unfolded proteins and protein folding studied by NMR. Chem Rev 104:3607-3622
20. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6:197-208
21. 13C spectroscopy. J Biomol NMR 26:167-179
22. Eliezer D (2009) Biophysical characterization of intrinsically disordered proteins. Curr Opin Struct Biol 19:23-30
23. Emsley L, Bodenhausen G (1992) Optimization of shaped selective pulses for NMR using a quaternion description of their overall propagators. J Magn Reson 97:135-148
24. 13C direct detection NMR. In: McGreevy KS, Parigi G, Bertini I (eds) NMR of biomolecules. Wiley, Newyork, pp 433-442
25. Felli IC, Pierattelli R (2012b) Recent progress in NMR spectroscopy: toward the study of intrinsically disordered proteins of increasing size and complexity. IUBMB Life 64:473-481
26. Felli IC, Pierattelli R and Tompa P (2012) Intrinsically disordered proteins. In: Bertini I, McGreevy KS, Parigi G (eds) Wiley, Newyork, 137-152
27. Garner E, Cannon P, Romero P, Obradovic Z, Dunker AK (1998) Predicting disordered regions from aminoacid sequence: common themes despite differing structural characterization. Genome Inform 9:201-213
28. 15N NMR spectroscopy. J Mol Biol 288:705-723
29. Hsu ST, Bertoncini CW, Dobson CM (2009) Use of protonless NMR spectroscopy to alleviate the loss of information resulting from exchange to broadening. J Am Chem Soc 131:7222-7223
30. Kjaergaard M, Poulsen FM (2011) Sequence correction of random coil chemical shifts: correlation between neighbor correction factors and changes in the Ramachandran distribution. J Biomol NMR 50:157-165
31. Kjaergaard M, Poulsen FM (2012) Disordered proteins studied by chemical shifts. Prog NMR Spectrosc 60:42-51
32. Marsh JA, Singh VK, Jia Z, Forman-Kay JD (2006) Sensitivity of secondary structural propensities to sequence differences between α-and γ-synuclein: implications for fibrillation. Protein Sci 15:2795-2804
33. Marsh JA, Dancheck B, Ragusa MJ, Allaire M, Forman-Kay JD, Peti W (2010) Structural diversity in free and bound states of intrinsically disordered protein phosphatase 1 regulators. Structure 18:1094-1103
34. Mittag T, Forman-Kay J (2007) Atomic-level characterization of disordered protein ensembles. Curr Opin Struct Biol 17:3-14
35. Motackova V, Novacek J, Zawadzka-Kazimierczuk A, Kazimierczuk K, Zidek L, Sanderová H, Krasny L, Kozminski W, Sklenar V (2010) Strategy for complete NMR assignment of disordered proteins with highly repetitive sequences based on resolution-enhanced 5D experiments. J Biomol NMR 48:169-177
36. Mukrasch MD, Bibow S, Korukottu J, Jeganathan S, Biernat J, Griesinger C, Mendelkow E, Zweckstetter M (2009) Structural polimorphism of 441-residue tau at single residue resolution. PLoS Biol 7:e34
37. 13C-detected experiments for backbone assignment of unstructured proteins with a very low signal dispersion. J Biomol NMR 50:1-11
38. Novacek J, Haba NY, Chill JH, Zidek L, Sklenar V (2012) 4D Non-uniformly sampled HCBCACON and (1) J[NC (α)]-selective HCBCANCO experiments for the sequential assignment and chemical shift analysis of intrinsically disordered proteins. J Biomol NMR 53:139-148
39. 13C-direct detected spectroscopy of intrinsically disordered proteins in solution. J Magn Reson 200:354-358
40. Pérez Y, Gairi M, Pons M, Bernadó P (2009) Structural characterization of the natively unfolded N-terminal domain of human c-Src kinase: insights into the role of phosphorylation of the unique domain. J Mol Biol 391:136-148
41. 13C-direct detected NMR experiments for the sequential J-based resonance assignment of RNA oligonucleotides. J Biomol NMR 47:259-269
42. Romero P, Obradovic Z, Kissinger CR, Villafranca JE, Garner E, Guillot S, Dunker AK (1998) Thousands of proteins likely to have long disordered regions. Pac Symp Biocomputing 3:437-448
43. Schwalbe H, Fiebig KM, Buck M, Jones JA, Grimshaw SB, Spencer A, Glaser SJ, Smith LJ, Dobson CM (1997) Structural and dynamical properties of a denatured protein. Heteronuclear 3D NMR experiments and theoretical simulations of lysozyme in 8 M urea. Biochem 36:8977-8991
44. Schwarzinger S, Kroon GJA, Foss TR, Chung J, Wright PE, Dyson HJ (2001) Sequence-dependent correction of random coil NMR chemical shifts. J Am Chem Soc 123:2970-2978
45. Serber Z, Richter C, Moskau D, Boehlen J-M, Gerfin T, Marek D, Haeberli M, Baselgia L, Laukien F, Stern AS, Hoch JC, Dötsch V (2000) New carbon-detected protein NMR experiments using cryoprobes. J Am Chem Soc 122:3554-3555
46. Serber Z, Richter C, Dötsch V (2001) Carbon-detected NMR experiments to investigate structure and dynamics of biological macromolecules. ChemBioChem 2:247-251
47. Shaka AJ, Keeler J, Freeman R (1983) Evaluation of a new broadband decoupling sequence: WALTZ-16. J Magn Reson 53:313-340
48. Shaka AJ, Barker PB, Freeman R (1985) Computer-optimized decoupling scheme for wideband applications and low-level operation. J Magn Reson 64:547-552
49. Sickmeier M, Hamilton JA, LeGall T, Vacic V, Cortese MS, Tantos A, Szabo B, Tompa P, Chen J, Uversky VN, Obradovic Z, Dunker AK (2007) DisProt: the database of disordered proteins. Nucleic Acids Res 35:D786-D793
50. α direct-detection with applicability toward fast relaxing protein systems. J Am Chem Soc 130:17210-17211
51. α direct detection. J Am Chem Soc 132:2945-2951
52. α direct detection experiment for main chain resonance assignment, dihedral angle information and aminoacid type identification. J Biomol NMR 47:55-63
53. Tamiola K, Mulder FA (2012) Using NMR chemical shifts to calculate the propensity for structural order and disorder in proteins. Biochem Soc Trans 10:1014-1020
54. Tamiola K, Acar B, Mulder FAA (2010) Sequence-specific random coil chemical shifts of intrinsically disordered proteins. J Am Chem Soc 132:18000-18003
55. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527-533
56. Tompa P (2009) Structure and function of intrinsically disordered proteins. Taylor and Francis Group, Boca Raton, FL
57. Tompa P (2012) Intrinsically disordered proteins: a 10-year recap. Trends Biochem Sci
58. 13C residual dipolar coupling in uniformly deuterated proteins. J Am Chem Soc 126:2414-2420
59. 13C-detected experiments with proteins and oligonucleotides. J Biomol NMR 31:1-9
60. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J Biomol NMR 5:67-81
61. Wright PE, Dyson HJ (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 293:321-331