A reduced dimensionality NMR pulse sequence and an efficient protocol for unambiguous assignment in intrinsically disordered proteins

Journal of Biomolecular NMR

Volumn 59, Issue 3, 2014, Pages 199-210

  Reddy, Jithender G ^a   Hosur, Ramakrishna V ^a,b  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b UNIVERSITY OF MUMBAI   (India)

Author keywords

Backbone resonance assignment; Check points; Intrinsically disordered proteins; Multidimensional NMR spectroscopy; Reduced dimensionality

Indexed keywords

ALPHA SYNUCLEIN; AMIDE; CARBON 13; INTRINSICALLY DISORDERED PROTEIN; NITROGEN 15; CARBON; NITROGEN; UBIQUITIN;

ARTICLE; ATOM; CONTROLLED STUDY; DISPERSION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REDUCED DIMENSIONALITY; BIOLOGICAL MODEL; CHEMISTRY; PH; PROCEDURES; PROTEIN FOLDING; PROTEOMICS;

ALPHA-SYNUCLEIN; CARBON ISOTOPES; HYDROGEN-ION CONCENTRATION; INTRINSICALLY DISORDERED PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, BIOLOGICAL; NITROGEN ISOTOPES; PROTEIN FOLDING; PROTEOMICS; UBIQUITIN;

EID: 84904044244     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-014-9839-x     Document Type: Article

References (65)

1. Astrof NS, Lyon CE, Griffin RG (2001) Triple Resonance Solid State NMR Experiments with Reduced Dimensionality Evolution Periods. J Magn Reson 152:303-307
2. Atreya HS, Eletsky A, Szyperski T (2005) Resonance assignment of proteins with high shift degeneracy based on 5D spectral information encoded in G2FT NMR experiments. J Am Chem Soc 127:4554-4555
3. Bagai I, Ragsdale SW, Zuiderweg ERP (2011) Pseudo-4D triple resonance experiments to resolve HN overlap in the backbone assignment of unfolded proteins. J Biomol NMR 49:69-74
4. Bartels C, Güntert P, Billeter M, Wüthrich K (1997) GARANT-a general algorithm for resonance assignment of multidimensional nuclear magnetic resonance spectra. J Comput Chem 18:139-149
5. Bermel W, Bertini I, Felli IC, Lee Y-M, Luchinat C, Pierattelli R (2006) Protonless NMR Experiments for Sequence-Specific Assignment of Backbone Nuclei in Unfolded Proteins. J Am Chem Soc 128:3918-3919
6. Bermel W, Felli IC, Kümmerle R, Pierattelli R (2008) 13C Direct-detection biomolecular NMR. Concepts Magn Reson Part A 32:183-200
7. Bermel W, Bertini I, Felli I, Gonnelli L, Koźmiński W, Piai A, Pierattelli R, Stanek J (2012) Speeding up sequence specific assignment of IDPs. J Biomol NMR 53:293-301
8. Bermel W, Bruix M, Felli I, Kumar MV, Pierattelli R, Serrano S (2013a) Improving the chemical shift dispersion of multidimensional NMR spectra of intrinsically disordered proteins. J Biomol NMR 55:231-237
9. Bermel W, Felli I, Gonnelli L, Koźmiński W, Piai A, Pierattelli R, Zawadzka-Kazimierczuk A (2013b) High-dimensionality 13C direct-detected NMR experiments for the automatic assignment of intrinsically disordered proteins. J Biomol NMR 57:353-361
10. Bertini I, Felli IC, Kümmerle R, Moskau D, Pierattelli R (2003) 13C-13C NOESY: an attractive alternative for studying large macromolecules. J Am Chem Soc 126:464-465
11. Bertini I, Jiménez B, Pierattelli R, Wedd AG, Xiao Z (2008) Protonless 13C direct detection NMR: characterization of the 37 kDa trimeric protein CutA1. Proteins Struct Funct Bioinf 70:1196-1205
12. Billeter M, Orekhov V (2012) Novel sampling approaches in higher dimensional NMR. Springer, New York
13. Bracken C, Palmer AG 3rd, Cavanagh J (1997) (H)N(COCA)NH and HN(COCA)NH experiments for 1H-15 N backbone assignments in 13C/15 N-labeled proteins. J Biomol NMR 9:94-100
14. Bruschweiler R, Zhang F (2004) Covariance nuclear magnetic resonance spectroscopy. J Chem Phys 120:5253-5260
15. Brutscher B, Cordier F, Simorre J-P, Caffrey M, Marion D (1995) High-resolution 3D HNCOCA experiment applied to a 28 kDa paramagnetic protein. J Biomol NMR 5:202-206
16. Chandra K, Jaipuria G, Shet D, Atreya HS (2012) Efficient sequential assignments in proteins with reduced dimensionality 3D HN(CA)NH. J Biomol NMR 52:115-126
17. Chatterjee A, Bhavesh NS, Panchal SC, Hosur RV (2002) A novel protocol based on HN(C)N for rapid resonance assignment in (N-15, C-13) labeled proteins: implications to structural genomics. Biochem Biophys Res Commun 293:427-432
18. Chen JH, De Angelis AA, Mandelshtam VA, Shaka AJ (2003) Progress on the two-dimensional filter diagonalization method. An efficient doubling scheme for two-dimensional constant-time NMR. J Magn Reson 162:74-89
19. Dyson HJ, Wright PE (2001) Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states. NMR Biol Macromol Pt B 339:258-270
20. Dyson HJ, Wright PE (2004) Unfolded proteins and protein folding studied by NMR. Chem Rev 104:3607-3622
21. Eliezer D (2006) Characterizing residual structure in disordered protein states using nuclear magnetic resonance. In: Bai Y, Nussinov R (eds) Protein folding protocols. Humana Press, New York, pp 49-67
22. Emsley L, Bodenhausen G (1990) Gaussian pulse cascades: new analytical functions for rectangular selective inversion and in-phase excitation in NMR. Chem Phys Lett 165:469-476
23. Felli IC, Pierattelli R (2012) Recent progress in NMR spectroscopy: toward the study of intrinsically disordered proteins of increasing size and complexity. IUBMB Life 64:473-481
24. Fiorito F, Hiller S, Wider G, Wüthrich K (2006) Automated resonance assignment of proteins: 6D APSY-NMR. J Biomol NMR 35:27-37
25. Frueh DP, Arthanari H, Koglin A, Walsh CT, Wagner G (2009) A double TROSY hNCAnH experiment for efficient assignment of large and challenging proteins. J Am Chem Soc 131:12880-12881
26. Ghosh D, Mondal M, Mohite GM, Singh PK, Ranjan P, Anoop A, Ghosh S, Jha NN, Kumar A, Maji SK (2013) The Parkinson's disease-associated H50Q mutation accelerates α-synuclein aggregation in vitro. Biochemistry 52:6925-6927
27. Grzesiek S, Anglister J, Ren H, Bax A (1993) Carbon-13 line narrowing by deuterium decoupling in deuterium/carbon-13/nitrogen-15 enriched proteins. Application to triple resonance 4D J connectivity of sequential amides. J Am Chem Soc 115:4369-4370
28. Hiller S, Fiorito F, Wuthrich K, Wider G (2005) Automated projection spectroscopy (APSY). Proc Natl Acad Sci USA 102:10876-10881
29. Hoch JC, Stern AS (2001) Maximum entropy reconstruction, spectrum analysis and deconvolution in multidimensional nuclear magnetic resonance. NMR Biol Macromol Pt A 338:159-178
30. Isaksson L, Mayzel M, Saline M, Pedersen A, Rosenlow J, Brutscher B, Karlsson BG, Orekhov VY (2013) Highly efficient NMR assignment of intrinsically disordered proteins: application to B- and T cell receptor domains. PLoS ONE 8:e62947
31. Jaravine V, Ibraghimov I, Orekhov VY (2006) Removal of a time barrier for high-resolution multidimensional NMR spectroscopy. Nat Methods 3:605-607
32. Kang L, Janowska MK, Moriarty GM, Baum J (2013) Mechanistic insight into the relationship between N-terminal acetylation of α-synuclein and fibril formation rates by NMR and fluorescence. PLoS ONE 8:e75018
33. Kazimierczuk K, Zawadzka A, Kozminski W, Zhukov I (2006) Random sampling of evolution time space and Fourier transform processing. J Biomol NMR 36:157-168
34. Keller R (2004) Optimizing the process of nuclear magnetic resonance spectrum analysis and computer aided resonance assignment. In CANTINA, Verlag, Goldau, Switzerland. Swiss Federal Institute of Technology Zurich, Switzerland
35. Korzhnev DM, Ibraghimov IV, Billeter M, Orekhov VY (2001) MUNIN: application of three-way decomposition to the analysis of heteronuclear NMR relaxation data. J Biomol NMR 21:263-268
36. Kosol S, Contreras-Martos S, Cedeño C, Tompa P (2013) Structural characterization of intrinsically disordered proteins by NMR spectroscopy. Molecules 18:10802-10828
37. Kragelj J, Ozenne V, Blackledge M, Jensen MR (2013) Conformational propensities of intrinsically disordered proteins from NMR chemical shifts. ChemPhysChem 14:3034-3045
38. Kumar D (2013a) Reduced dimensionality (4,3)D-hnCOCANH experiment: an efficient backbone assignment tool for NMR studies of proteins. J Struct Funct Genom 14:109-118
39. Kumar D (2013b) Reduced dimensionality tailored HN(C)N experiments for facile backbone resonance assignment of proteins through unambiguous identification of sequential HSQC peaks. J Magn Reson 237:85-91
40. Kumar D, Paul S, Hosur RV (2010a) BEST-HNN and 2D (HN)NH experiments for rapid backbone assignment in proteins (vol 204, pp 111, 2010). J Magn Reson 207:173-174
41. Kumar D, Reddy JG, Hosur RV (2010b) hnCOcaNH and hncoCANH pulse sequences for rapid and unambiguous backbone assignment in (13C, 15 N) labeled proteins. J Magn Reson 206:134-138
42. Liu X, Yang D (2013) HN(CA)N and HN(COCA)N experiments for assignment of large disordered proteins. J Biomol NMR 57:83-89
43. Löhr F, Rüterjans H (1995) A new triple-resonance experiment for the sequential assignment of backbone resonances in proteins. J Biomol NMR 6:189-197
44. Mantylahti S, Aitio O, Hellman M, Permi P (2010) HA-detected experiments for the backbone assignment of intrinsically disordered proteins. J Biomol NMR 47:171-181
45. Mantylahti S, Hellman M, Permi P (2011) Extension of the HA-detection based approach: (HCA)CON(CA)H and (HCA)NCO(CA)H experiments for the main-chain assignment of intrinsically disordered proteins. J Biomol NMR 49:99-109
46. 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
47. Motackova V, Novacek J, Zawadzka-Kazimierczuk A, Kazimierczuk K, Zidek L, Anderova HS, 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
48. Mukrasch MD, Bibow S, Korukottu J, Jeganathan S, Biernat J, Griesinger C, Mandelkow E, Zweckstetter M (2009) Structural polymorphism of 441-residue tau at single residue resolution. PLoS Biol 7:e1000034
49. Panchal SC, Bhavesh NS, Hosur RV (2001) Improved 3D triple resonance experiments, HNN and HN(C)N, for HN and 15 N sequential correlations in (13C, 15 N) labeled proteins: application to unfolded proteins. J Biomol NMR 20:135-147
50. Permi P, Hellman M (2012) Alpha proton detection based backbone assignment of intrinsically disordered proteins. In: Uversky VN, Dunker AK (eds) Intrinsically disordered protein analysis. Humana Press, New York, pp 211-226
51. Piotto M, Saudek V, Sklenář V (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 2:661-665
52. Rao JN, Kim YE, Park LS, Ulmer TS (2009) Effect of pseudorepeat rearrangement on α-synuclein misfolding, vesicle binding, and micelle binding. J Mol Biol 390:516-529
53. Reddy JG, Hosur RV (2012) Reduced dimensionality (4,3)D-HN(C)NH for rapid assignment of 1H(N)-15 N HSQC peaks in proteins: an analytical tool for protein folding, proteomics, and drug discovery programs. Anal Chem 84:10404-10410
54. Rout MK, Mishra P, Atreya HS, Hosur RV (2012) Reduced dimensionality 3D HNCAN for unambiguous HN, CA and N assignment in proteins. J Magn Reson 216:161-168
55. Rovnyak D, Frueh DP, Sastry M, Sun Z-YJ, Stern AS, Hoch JC, Wagner G (2004) Accelerated acquisition of high resolution triple-resonance spectra using non-uniform sampling and maximum entropy reconstruction. J Magn Reson 170:15-21
56. Schmieder P, Stern A, Wagner G, Hoch J (1993) Application of nonlinear sampling schemes to COSY-type spectra. J Biomol NMR 3:569-576
57. Serber Z, Richter C, Dötsch V (2001) Carbon-detected NMR experiments to investigate structure and dynamics of biological macromolecules. ChemBioChem 2:247-251
58. Shaka AJ, Keeler J, Frenkiel T, Freeman R (1983) An improved sequence for broadband decoupling: WALTZ-16. J Magn Reson 52:335-338
59. Shaka AJ, Barker PB, Freeman R (1985) Computer-optimized decoupling scheme for wideband applications and low-level operation. J Magn Reson 64:547-552
60. Sun ZY, Frueh DP, Selenko P, Hoch JC, Wagner G (2005) Fast assignment of 15 N-HSQC peaks using high-resolution 3D HNcocaNH experiments with non-uniform sampling. J Biomol NMR 33:43-50
61. Szyperski T, Wider G, Bushweller JH, Wuethrich K (1993) Reduced dimensionality in triple-resonance NMR experiments. J Am Chem Soc 115:9307-9308
62. Szyperski T, Yeh DC, Sukumaran DK, Moseley HNB, Montelione GT (2002) Reduced-dimensionality NMR spectroscopy for high-throughput protein resonance assignment. Proc Natl Acad Sci USA 99:8009-8014
63. Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, Lin J, Livny M, Mading S, Maziuk D, Miller Z, Nakatani E, Schulte CF, Tolmie DE, Kent Wenger R, Yao H, Markley JL (2008) BioMagResBank. Nucleic Acids Res 36:D402-D408
64. Wu K-P, Baum J (2011) Backbone assignment and dynamics of human α-synuclein in viscous 2 M glucose solution. Biomol NMR Assign 5:43-46
65. Zhang SM, Gorenstein DG (2002) Design of Bloch-Siegert phase-shift self-compensated pulses for HCN triple-resonance experiments. Chem Phys Lett 362:278-284