Advertisement

Journal of Biomolecular NMR

, Volume 61, Issue 2, pp 151–160 | Cite as

Perspectives for sensitivity enhancement in proton-detected solid-state NMR of highly deuterated proteins by preserving water magnetization

  • Veniamin ChevelkovEmail author
  • ShengQi Xiang
  • Karin Giller
  • Stefan Becker
  • Adam Lange
  • Bernd Reif
Article

Abstract

In this work, we show how the water flip-back approach that is widely employed in solution-state NMR can be adapted to proton-detected MAS solid-state NMR of highly deuterated proteins. The scheme allows to enhance the sensitivity of the experiment by decreasing the recovery time of the proton longitudinal magnetization. The method relies on polarization transfer from non-saturated water to the protein during the inter-scan delay.

Keywords

Magic angle spinning (MAS) solid-state NMR Perdeuteration Sensitivity enchancement Protein water interaction 

Notes

Acknowledgments

We thank Brigitta Angerstein for expert technical assistance. This work was supported by the Max Planck Society, the Leibniz-Gemeinschaft, and the DFG (Emmy Noether Fellowship to A.L). A.L. and S.X. acknowledge funding from the CRC803 (DFG).

Supplementary material

10858_2015_9902_MOESM1_ESM.doc (1.7 mb)
Supplementary material 1 (DOC 1781 kb)
10858_2015_9902_MOESM2_ESM.pdf (18 kb)
Supplementary material 2 (PDF 17 kb)
10858_2015_9902_MOESM3_ESM.pdf (14 kb)
Supplementary material 3 (PDF 14 kb)

References

  1. Akbey U et al (2010) Optimum levels of exchangeable protons in perdeuterated proteins for proton detection in MAS solid-state NMR spectroscopy. J Biomol NMR 46:67–73CrossRefGoogle Scholar
  2. Atreya HS, Szyperski T (2004) G-matrix Fourier transform NMR spectroscopy for complete protein resonance assignment. Proc Natl Acad Sci USA 101:9642–9647CrossRefADSGoogle Scholar
  3. Baldus M, Petkova AT, Herzfeld J, Griffin RG (1998) Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol Phys 95:1197–1207CrossRefADSGoogle Scholar
  4. Bennett AE, Rienstra CM, Griffiths JM, Zhen WG, Lansbury PT, Griffin RG (1998) Homonuclear radio frequency-driven recoupling in rotating solids. J Chem Phys 108:9463–9479CrossRefADSGoogle Scholar
  5. Boeckmann A et al (2009) Characterization of different water pools in solid-state NMR protein samples. J Biomol NMR 45:319–327CrossRefGoogle Scholar
  6. Chevelkov V et al (2003) H-1 detection in MAS solid-state NMR Spectroscopy of biomacromolecules employing pulsed field gradients for residual solvent suppression. J Am Chem Soc 125:7788–7789CrossRefGoogle Scholar
  7. Chevelkov V, Faelber K, Diehl A, Heinemann U, Oschkinat H, Reif B (2005) Detection of water molecules in a polycrystalline sample of a chicken a-spectrin SH3 domain. J Biomol NMR 31:295–310CrossRefGoogle Scholar
  8. Chevelkov V, Rehbein K, Diehl A, Reif B (2006) Ultrahigh resolution in proton solid-state NMR spectroscopy at high levels of deuteration. Angew Chem Int Ed 45:3878–3881CrossRefGoogle Scholar
  9. Chevelkov V, Fink U, Reif B (2009) Quantitative analysis of backbone motion in proteins using MAS solid-state NMR spectroscopy. J Biomol NMR 45:197–206CrossRefGoogle Scholar
  10. Chevelkov V, Giller K, Becker S, Lange A (2013) Efficient CO-CA transfer in highly deuterated proteins by band-selective homonuclear cross-polarization. J Magn Reson 230:205–211CrossRefADSGoogle Scholar
  11. Chevelkov V, Habenstein B, Loquet A, Giller K, Becker S, Lange A (2014) Proton-detected MAS NMR experiments based on dipolar transfers for backbone assignment of highly deuterated proteins. J Magn Reson 242:180–188CrossRefADSGoogle Scholar
  12. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPIPE—a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277–293CrossRefGoogle Scholar
  13. Emsley L, Bodenhausen G (1990) Gaussian pulse cascades—new analytical functions for rectangular selective inversion and in-phase excitation in NMR. Chem Phys Lett 165:469–476CrossRefADSGoogle Scholar
  14. Ernst RR, Bodenhausen G, Wokaun A (1987) Principles of nuclear magnetic resonance in one and two dimensions. Clarendon, OxfordGoogle Scholar
  15. Ganapathy S, Naito A, McDowell CA (1981) Paramagnetic doping as an aid in obtaining high-resolution C-13 NMR-spectra of biomolecules in the solid-state. J Am Chem Soc 103:6011–6015CrossRefGoogle Scholar
  16. Giffard M, Bardet M, Bersch B, Coves J, Hediger S (2009) Impact of selective excitation on carbon longitudinal relaxation: towards fast solid-state NMR techniques. J Magn Reson 200:153–160CrossRefADSGoogle Scholar
  17. Grzesiek S, Bax A (1993) The importance of not saturating H2O in protein nmr—application to sensitivity enhancement and NOE measurements. J Am Chem Soc 115:12593–12594CrossRefGoogle Scholar
  18. Helmus JJ, Surewicz K, Nadaud PS, Surewicz WK, Jaroniec CP (2008) Molecular conformation and dynamics of the Y145Stop variant of human prion protein. Proc Natl Acad Sci USA 105:6284–6289CrossRefADSGoogle Scholar
  19. Huber M, Hiller S, Schanda P, Ernst M, Bockmann A, Verel R, Meier BH (2011) A proton-detected 4D solid-state NMR experiment for protein structure determination. ChemPhysChem 12:915–918CrossRefGoogle Scholar
  20. Knight MJ et al (2011) Fast resonance assignment and fold determination of human superoxide dismutase by high-resolution proton-detected solid-state MAS NMR spectroscopy. Angew Chem Int Ed 50:11697–11701CrossRefGoogle Scholar
  21. Linser R, Chevelkov V, Diehl A, Reif B (2007) Sensitivity enhancement using paramagnetic relaxation in MAS solid-state NMR of perdeuterated proteins. J Magn Reson 189:209–216CrossRefADSGoogle Scholar
  22. Linser R, Bardiaux B, Higman V, Fink U, Reif B (2011) Structure calculation from unambiguous long-range amide and methyl (1)H-(1)H distance restraints for a microcrystalline protein with MAS solid-state NMR spectroscopy. J Am Chem Soc 133:5905–5912CrossRefGoogle Scholar
  23. Lopez JJ, Kaiser C, Asami S, Glaubitz C (2009) Higher sensitivity through selective (13)C excitation in solid-state NMR spectroscopy. J Am Chem Soc 131:15970–15971CrossRefGoogle Scholar
  24. Loquet A, Lv G, Giller K, Becker S, Lange A (2011) C-13 spin dilution for simplified and complete solid-state NMR resonance assignment of insoluble biological assemblies. J Am Chem Soc 133:4722–4725CrossRefGoogle Scholar
  25. Loquet A et al (2012) Atomic model of the type III secretion system needle. Nature 486:276–279ADSGoogle Scholar
  26. Lupulescu A, Frydman L (2011) Sensitizing solid state nuclear magnetic resonance of dilute nuclei by spin-diffusion assisted polarization transfers. J Chem Phys 135:134202. doi: 10.1063/1.3643116
  27. Mori S, Abeygunawardana C, Johnson MO, Vanzijl PCM (1995) Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J Magn Reson Ser B 108:94–98CrossRefGoogle Scholar
  28. Nadaud PS, Helmus JJ, Sengupta I, Jaroniec CP (2010) Rapid acquisition of multidimensional solid-state NMR spectra of proteins facilitated by covalently bound paramagnetic tags. J Am Chem Soc 132:9561–9563CrossRefGoogle Scholar
  29. Nielsen NC, Bildsoe H, Jakobsen HJ, Levitt MH (1994) Double-quantum homonuclear rotary resonance: efficient dipolar recovery in magic-angle spinning nuclear magnetic resonance. J Chem Phys 101:1805–1812CrossRefADSGoogle Scholar
  30. Orekhov VY, Ibraghimov I, Billeter M (2003) Optimizing resolution in multidimensional NMR by three-way decomposition. J Biomol NMR 27:165–173CrossRefGoogle Scholar
  31. Paulson EK, Morcombe CR, Gaponenko V, Dancheck B, Byrd RA, Zilm KW (2003) Sensitive high resolution inverse detection NMR spectroscopy of proteins in the solid state. J Am Chem Soc 125:15831–15836CrossRefGoogle Scholar
  32. Pervushin K, Vogeli B, Eletsky A (2002) Longitudinal H-1 relaxation optimization in TROSY NMR spectroscopy. J Am Chem Soc 124:12898–12902CrossRefGoogle Scholar
  33. Pines A, Waugh JS, Gibby MG (1972) Proton-enhanced nuclear induction spectroscopy—method for high-resolution NMR of dilute spins in solids. J Chem Phys 56:1776CrossRefADSGoogle Scholar
  34. Saito K, Martineau C, Fink G, Taulelle F (2011) Flip-back, an old trick to face highly contrasted relaxation times: application in the characterization of pharmaceutical mixtures by CPMAS NMR. Solid State Nucl Magn Reson 40:66–71CrossRefGoogle Scholar
  35. Schanda P, Brutscher B (2005) 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 127:8014–8015CrossRefGoogle Scholar
  36. Schanda P, Meier BH, Ernst M (2010) Quantitative analysis of protein backbone dynamics in microcrystalline ubiquitin by solid-state NMR spectroscopy. J Am Chem Soc 132:15957–15967CrossRefGoogle Scholar
  37. Shaka AJ, Keeler J, Frenkiel T, Freeman R (1983) An improved sequence for broad-band decoupling—WALTZ-16. J Magn Reson 52:335–338ADSGoogle Scholar
  38. Stonehouse J, Shaw GL, Keeler J, Laue ED (1994) Minimizing sensitivity losses in gradient-selected N-15-H-1 hsqc spectra of proteins. J Magn Reson Ser A 107:178–184CrossRefADSGoogle Scholar
  39. Tegenfeldt J, Haeberlen U (1979) Cross polarization in solids with flip-back of I-spin magnetization. J Magn Reson 36:453–457ADSGoogle Scholar
  40. Verel R, Ernst M, Meier BH (2001) Adiabatic dipolar recoupling in solid-state NMR: the DREAM scheme. J Magn Reson 150:81–99CrossRefADSGoogle Scholar
  41. Vranken WF et al (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59:687–696CrossRefGoogle Scholar
  42. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319:1523–1526CrossRefADSGoogle Scholar
  43. Wickramasinghe NP et al (2009) Nanomole-scale protein solid-state NMR by breaking intrinsic H-1 T-1 boundaries. Nat Methods 6:215–218CrossRefGoogle Scholar
  44. Yamamoto K, Xu JD, Kawulka KE, Vederas JC, Ramamoorthy A (2010) Use of a copper-chelated lipid speeds up NMR measurements from membrane proteins. J Am Chem Soc 132:6929–6931CrossRefGoogle Scholar
  45. Zhou DH, Rienstra CM (2008) High-performance solvent suppression for proton detected solid-state NMR. J Magn Reson 192:167–172CrossRefADSGoogle Scholar
  46. Zhou DH, Shah G, Cormos M, Mullen C, Sandoz D, Rienstra CM (2007a) Proton-detected solid-state NMR Spectroscopy of fully protonated proteins at 40 kHz magic-angle spinning. J Am Chem Soc 129:11791–11801CrossRefGoogle Scholar
  47. Zhou DH et al (2007b) Solid-rate protein-structure determination with proton-detected triple-resonance 3D magic-angle-spinning NMR spectroscopy. Angew Chem Int Ed 46:8380–8383CrossRefGoogle Scholar

Copyright information

© European Union 2015

Authors and Affiliations

  • Veniamin Chevelkov
    • 1
    • 2
    Email author
  • ShengQi Xiang
    • 1
  • Karin Giller
    • 1
  • Stefan Becker
    • 1
  • Adam Lange
    • 1
    • 2
    • 3
  • Bernd Reif
    • 4
    • 5
  1. 1.Max-Planck-Institut für biophysikalische Chemie (MPI-bpc)GoettingenGermany
  2. 2.Leibnizinstitut für Molekulare Pharmakologie (FMP)BerlinGermany
  3. 3.Institut für BiologieHumboldt Universität zu BerlinBerlinGermany
  4. 4.Munich Center for Integrated Protein Science (CIPS-M), Department ChemieTechnische Universität München (TUM)GarchingGermany
  5. 5.Helmholtz-Zentrum München (HMGU), Deutsches Forschungszentrum für Gesundheit und Umwelt (HMGU)NeuherbergGermany

Personalised recommendations