HN-NCA heteronuclear TOCSY-NH experiment for 1HN and 15N sequential correlations in (13C, 15N) labelled intrinsically disordered proteins

Journal of Biomolecular NMR

Volumn 63, Issue 2, 2015, Pages 201-212

  Wiedemann, Christoph ^a,c   Goradia, Nishit ^a   Häfner, Sabine ^a   Herbst, Christian ^a,b   Görlach, Matthias ^a   Ohlenschläger, Oliver ^a   Ramachandran, Ramadurai ^a  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b UBON RATCHATHANI UNIVERSITY   (Thailand)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Heteronuclear cross polarisation; Intrinsically disordered protein region; NMR spectroscopy; Non uniform sampling; Sequential resonance assignment

Indexed keywords

ALPHA SYNUCLEIN; AMIDE; AMINO ACID; CARBON 13; INTRINSICALLY DISORDERED PROTEIN; NITROGEN 15; PROTON;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; CORRELATION ANALYSIS; CROSS COUPLING REACTION; HETERONUCLEAR NUCLEAR MAGNETIC RESONANCE; HN NCA HETERONUCLEAR TOCSY NH; INFORMATION PROCESSING; ISOTOPE LABELING; MAGNETISM; NITROGEN NUCLEAR MAGNETIC RESONANCE; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTON NUCLEAR MAGNETIC RESONANCE; SIMULATION; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE; PROCEDURES;

INTRINSICALLY DISORDERED PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR;

EID: 84942988252     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-015-9976-x     Document Type: Article

References (72)

1. 1H detection. Sci Rep 4:4490
2. Bermel W, Bertini I, Felli IC, Lee YM, 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
3. Bermel W, Bruix M, Felli IC, Kumar MVV, Pierattelli R, Serrano S (2013a) Improving the chemical shift dispersion of multidimensional NMR spectra of intrinsically disordered proteins. J Biomol NMR 55:231-237
4. 13C direct-detected NMR experiments for the automatic assignment of intrinsically disordered proteins. J Biomol NMR 57:353-361
5. 15N-labeled proteins. J Biomol NMR 9:94-100
6. 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
7. 15N-labelled proteins. J Biomol NMR 3:349-354
8. 13C detection to study intrinsically disordered proteins. J Magn Reson 241:115-125
9. Felli IC, Pierattelli R, Tompa P (2012) Intrinsically Disordered Proteins. In: Bertini I, McGreevy KS, Parigi G (eds) NMR of biomolecules: towards mechanistic systems biology, First Edition edn. Wiley-VCH Verlag & Co. KGaA, Weinheim, pp 137-152
10. Gil S, Hošek T, Solyom Z, Kümmerle R, Brutscher B, Pierattelli R, Felli IC (2013) NMR spectroscopic studies of intrinsically disordered proteins at near-physiological conditions. Angew Chem Int Ed Engl 52:11808-11812
11. Glaser SJ, Quant JJ (1996) Homonuclear and heteronuclear Hartmann-Hahn transfer in isotropic liquids. Adv Magn Reson 19:59-252
12. Goradia N, Wiedemann C, Herbst C, Görlach M, Heinemann SH, Ohlenschläger O, Ramachandran R (2015) An approach to NMR assignment of intrinsically disordered proteins. ChemPhysChem 16:739-746
13. 13C magnetization. J Magn Reson B 101:114-119
14. Hellman M, Tossavainen H, Rappu P, Heino J, Permi P (2011) Characterization of intrinsically disordered prostate associated gene (PAGE5) at single residue resolution by NMR spectroscopy. PLoS One 6:e26633
15. Hellman M, Piirainen H, Jaakola VP, Permi P (2014) Bridge over troubled proline: assignment of intrinsically disordered proteins using (HCA)CON(CAN)H and (HCA)N(CA)CO(N)H experiments concomitantly with HNCO and i(HCA)CO(CA)NH. J Biomol NMR 58:49-60
16. Hoyer W, Antony T, Cherny D, Heim G, Jovin TM, Subramaniam V (2002) Dependence of alpha-synuclein aggregate morphology on solution conditions. J Mol Biol 322:383-393
17. Hsu ST, Bertoncini CW, Dobson CM (2009) Use of protonless NMR spectroscopy to alleviate the loss of information resulting from exchange-broadening. J Am Chem Soc 131:7222-7223
18. Hyberts SG, Arthanari H, Robson SA, Wagner G (2014) Perspectives in magnetic resonance: NMR in the post-FFT era. J Magn Reson 241:60-73
19. Ikegami T, Sato S, Wälchli M, Kyogoku Y, Shirakawa M (1997) An efficient HN(CA)NH pluse scheme for triple-resonance 4D correlation of sequential amide protons and nitrogens-15 in deuterated proteins. J Magn Reson 124:214-217
20. Isaksson L, Mayzel M, Saline M, Pedersen A, Rosenlöw 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
21. Jaravine V, Ibraghimov I, Orekhov VY (2006) Removal of a time barrier for high-resolution multi-dimensional NMR spectroscopy. Nat Methods 3:605-607
22. Jensen MR, Ruigrok RW, Blackledge M (2013) Describing intrinsically disordered proteins at atomic resolution by NMR. Curr Opin Struct Biol 23:426-435
23. Kazimierczuk K, Orekhov VY (2011) Accelerated NMR spectroscopy by using compressed sensing. Angew Chem Int Ed Engl 50:5556-5559
24. Kirschstein A, Herbst C, Riedel K, Carella M, Leppert J, Ohlenschläger O, Görlach M, Ramachandran R (2008a) Broadband homonuclear TOCSY with amplitude and phase-modulated RF mixing schemes. J Biomol NMR 40:227-237
25. Kirschstein A, Herbst C, Riedel K, Carella M, Leppert J, Ohlenschläger O, Görlach M, Ramachandran R (2008b) Heteronuclear J cross-polarisation in liquids using amplitude and phase modulated mixing sequences. J Biomol NMR 40:277-283
26. Konrat R (2014) NMR contributions to structural dynamics studies of intrinsically disordered proteins. J Magn Reson 241:74-85
27. Kosol S, Contreras-Martos S, Cedeño C, Tompa P (2013) Structural characterization of intrinsically disordered proteins by NMR spectroscopy. Molecules 18:10802-10828
28. 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
29. Logan TM, Olejniczak ET, Xu RX, Fesik SW (1992) Side chain and backbone assignments in isotropically labeled proteins from two heteronuclear triple resonance experiments. FEBS Lett 314:413-418
30. Luan T, Jaravine V, Yee A, Arrowsmith CH, Orekhov VY (2005) Optimization of resolution and sensitivity of 4D NOESY using multidimensional decomposition. J Biomol NMR 33:1-14
31. Lyons BA, Montelione GT (1993) An HCCNH triple-resonance experiment using carbon-13 isotropic mixing for correlating backbone amide and side-chain aliphatic resonances in isotopically enriched proteins. J Magn Reson B 101:206-209
32. Maciejewski MW, Mobli M, Schuyler AD, Stern AS, Hoch JC (2012) Data sampling in multidimensional NMR: fundamentals and strategies. Top Curr Chem 316:49-77
33. Mäntylahti 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
34. Mäntylahti 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
35. Motáčková V, Nováček J, Zawadzka-Kazimierczuk A, Kazimierczuk K, Žídek L, Šanderová H, Krásný L, Koźmiński W, Sklenář 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. Narayanan RL, Dürr UH, Bibow S, Biernat J, Mandelkow E, Zweckstetter M (2010) Automatic assignment of the intrinsically disordered protein Tau with 441-residues. J Am Chem Soc 132:11906-11907
37. NCα-selective HCBCANCO experiments for the sequential assignment and chemical shift analysis of intrinsically disordered proteins. J Biomol NMR 53:139-148
38. Nováček J, Janda L, Dopitová R, Židek L, Sklenář V (2013) 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 56:291-301
39. Nováček J, Židek L, Sklenář V (2014) Toward optimal-resolution NMR of intrinsically disordered proteins. J Magn Reson 241:41-52
40. Orekhov VY, Ibragimov I, Billeter M (2003) Optimizing resolution in multidimensional NMR by threeway decomposition. J Biomol NMR 27:165-173
41. Palmer MR, Wenrich BR, Stahlfeld P, Rovnyak D (2014) Performance tuning non-uniform sampling for sensitivity enhancement of signal-limited biological NMR. J Biomol NMR 58:303-314
42. 15N) labeled proteins: application to unfolded proteins. J Biomol NMR 20:135-147
43. Pantoja-Uceda D, Santoro J (2013) Direct correlation of consecutive C'-N groups in proteins: a method for the assignment of intrinsically disordered proteins. J Biomol NMR 57:57-63
44. 13C-detected experiments for the assignment of intrinsically disordered proteins. J Biomol NMR 59:43-50
45. Paramasivam S, Suiter CL, Hou G, Sun S, Palmer M, Hoch JC, Rovnyak D, Polenova T (2012) Enhanced sensitivity by nonuniform sampling enables multidimensional MAS NMR spectroscopy of protein assemblies. J Phys Chem B 116:7416-7427
46. Piai A, Hošek T, Gonnelli L, Zawadzka-Kazimierczuk A, Koźmiński W, Brutscher B, Bermel W, Pierattelli R, Felli IC (2014) "CON-CON" assignment strategy for highly flexible intrinsically disordered proteins. J Biomol NMR 60:209-218
47. Reddy JG, Hosur RV (2014) A reduced dimensionality NMR pulse sequence and an efficient protocol for unambiguous assignment in intrinsically disordered proteins. J Biomol NMR 59:199-210
48. Rezaei-Ghaleh N, Blackledge M, Zweckstetter M (2012) Intrinsically disordered proteins: from sequence and conformational properties toward drug discovery. ChemBioChem 13:930-950
49. Richardson JM, Clowes RT, Boucher W, Domaille PJ, Hardman CH, Keeler J, Laue ED (1993) The use of heteronuclear cross polarization to enhance the sensitivity of triple-resonance NMR experiments. Improved 4D HCNNH pulse sequences. J Magn Reson B 101:223-227
50. Rovnyak D, Sarcone M, Jiang Z (2011) Sensitivity enhancement for maximally resolved two-dimensional NMR by nonuniform sampling. Magn Reson Chem 49:483-491
51. Sahoo N, Goradia N, Ohlenschläger O, Schönherr R, Friedrich M, Plass W, Kappl R, Hoshi T, Heinemann SH (2013) Heme impairs the ball-and-chain inactivation of potassium channels. Proc Natl Acad Sci USA 110:E4036-E4044
52. Sahu D, Bastidas M, Showalter SA (2014) Generating NMR chemical shift assignments of intrinsically disordered proteins using carbon-detected NMR methods. Anal Biochem 449:17-25
53. Salmon L, Nodet G, Ozenne V, Yin G, Jensen MR, Zweckstetter M, Blackledge M (2010) NMR characterization of long-range order in intrinsically disordered proteins. J Am Chem Soc 132:8407-8418
54. Schulenburg C, Hilvert D (2013) Protein conformational disorder and enzyme catalysis. Top Curr Chem 337:41-67
55. 15N. J Biomol NMR 5:323-326
56. Sibille N, Bernadó P (2012) Structural characterization of intrinsically disordered proteins by the combined use of NMR and SAXS. Biochem Soc Trans 40:955-962
57. Skrabana R, Sevcik J, Novak M (2006) Intrinsically disordered proteins in the neurodegenerative processes: formation of tau protein paired helical filaments and their analysis. Cell Mol Neurobiol 26:1085-1097
58. Solyom Z, Schwarten M, Geist L, Konrat R, Willbold D, Brutscher B (2013) BEST-TROSY experiments for time-efficient sequential resonance assignment of large disordered proteins. J Biomol NMR 55:311-321
59. States DJ, Haberkorn RA, Ruben DJ (1982) A two-dimensional nuclear overhauser experiment with pure absorption phase in four quadrants. J Magn Reson 48:286-292
60. Szalainé Ágoston B, Kovács D, Tompa P, Perczel A (2011) Full backbone assignment and dynamics of the intrinsically disordered dehydrin ERD14. Biomol NMR Assign 5:189-193
61. Theillet FX, Binolfi A, Liokatis S, Verzini S, Selenko P (2011) Paramagnetic relaxation enhancement to improve sensitivity of fast NMR methods: application to intrinsically disordered proteins. J Biomol NMR 51:487-495
62. Tompa P (2011) Unstructural biology coming of age. Curr Opin Struct Biol 21:419-425
63. Tompa P (2012) Intrinsically disordered proteins: a 10-year recap. Trends Biochem Sci 37:509-516
64. 13C NOE spectroscopy using methyl-TROSY, sparce data acquisition, and multidimensional decomposition. J Am Chem Soc 127:2767-2775
65. Uversky VN, Oldfield CJ, Midic U, Xie H, Xue B, Vucetic S, Iakoucheva LM, Obradovic Z, Dunker AK (2009) Unfoldomics of human diseases: linking protein intrinsic disorder with diseases. BMC Genom 10(Suppl 1):S7
66. Waudby CA, Camilloni C, Fitzpatrick AW, Cabrita LD, Dobson CM, Vendruscolo M, Christodoulou J (2013) In-cell NMR characterization of the secondary structure populations of a disordered conformation of alpha-synuclein within E. coli cells. PLoS One 8:e72286
67. 13C-labelled proteins. J Biomol NMR 3:113-120
68. Wen J, Wu J, Zhou P (2011) Sparsely sampled high-resolution 4-D experiments for efficient backbone resonance assignment of disordered proteins. J Magn Reson 209:94-100
69. Wiedemann C, Bellstedt P, Kirschstein A, Häfner S, Herbst C, Görlach M, Ramachandran R (2014a) Sequential protein NMR assignments in the liquid state via sequential data acquisition. J Magn Reson 239:23-28
70. Wiedemann C, Bellstedt P, Herbst C, Görlach M, Ramachandran R (2014b) An approach to sequential NMR assignments of proteins: application to chemical shift restraint-based structure prediction. J Biomol NMR 59:211-217
71. Wiedemann C, Szambowska A, Häfner S, Ohlenschläger O, Gührs KH, Görlach M (2015) Structure and regulatory role of the C-terminal winged helix domain of the archaeal minichromosome maintenance complex. Nucleic Acids Res 43:2958-2967
72. Zawadzka-Kazimierczuk A, Koźmiński W, Šanderová H, Krásný L (2012) High dimensional and high resolution pulse sequences for backbone resonance assignment of intrinsically disordered proteins. J Biomol NMR 52:329-337