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Determination of methyl order parameters using solid state NMR under off magic angle spinning

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Abstract

Quantification of dipolar couplings in biological solids is important for the understanding of dynamic processes. Under Magic Angle Spinning (MAS), order parameters are normally obtained by recoupling of anisotropic interactions involving the application of radio frequency pulses. We have recently shown that amide backbone order parameters can be estimated accurately in a spin-echo experiment in case the rotor spinning angle is slightly mis-calibrated. In this work, we apply this method to determine methyl order parameters in a deuterated sample of the SH3 domain of chicken α-spectrin in which the methyl containing side chains valine and leucine are selectively protonated.

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References

  • Agarwal V, Xue Y, Reif B, Skrynnikov NR (2008) Protein side-chain dynamics as observed by solution- and solid-state NMR spectroscopy: a similarity revealed. J Am Chem Soc 130:16611–16621

    Article  Google Scholar 

  • Andrew ER, Bradbury A, Eades RG (1958) Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182:1659

    Article  ADS  Google Scholar 

  • Andrew ER, Bradbury A, Eades RG (1959) Removal of dipolar broadening of nuclear magnetic resonance spectra of solids by specimen rotation. Nature 183:1802

    Article  ADS  Google Scholar 

  • Asami S, Reif B (2013) Proton-detected solid-state NMR at aliphatic sites: applications to crystalline systems. Acc Chem Res 46:2089–2097

    Article  Google Scholar 

  • Asami S, Porter JR, Lange OF, Reif B (2015) Access to Cα backbone dynamics of biological solids by 13C T1 relaxation and molecular dynamics simulation. J Am Chem Soc 137:1094–1100

    Article  Google Scholar 

  • Batchelder LS, Sullivan CE, Jelinski LW, Torchia DA (1982) Characterization of leucine side-chain reorientation in collagen-fibrils by solid-state 2H NMR. Proc Natl Acad Sci USA 79:386–389

    Article  ADS  Google Scholar 

  • Chevelkov V, Rehbein K, Diehl A, Reif B (2006) Ultra-high resolution in proton solid-state NMR at high levels of deuteration. Angew Chem Int Ed 45:3878–3881

    Article  Google Scholar 

  • Chevelkov V, Diehl A, Reif B (2008) Measurement of N15-T1 relaxation rates in a perdeuterated protein by magic angle spinning solid-state nuclear magnetic resonance spectroscopy. J Chem Phys 128:052316

    Article  ADS  Google Scholar 

  • Chevelkov V, Fink U, Reif B (2009a) Accurate determination of order parameters from 1H, 15N dipolar couplings in MAS solid-state NMR experiments. J Am Chem Soc 131:14018–14022

    Article  Google Scholar 

  • Chevelkov V, Fink U, Reif B (2009b) Quantitative analysis of backbone motion in proteins using MAS solid-state NMR spectroscopy. J Biomol NMR 45:197–206

    Article  Google Scholar 

  • Chevelkov V, Xue Y, Linser R, Skrynnikov NR, Reif B (2010) Comparison of solid-state dipolar couplings and solution relaxation data provides insight into protein backbone dynamics. J Am Chem Soc 132:5015–5017

    Article  Google Scholar 

  • Clore GM, Szabo A, Bax A, Kay LE, Driscoll PC, Gronenborn AM (1990) Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J Am Chem Soc 112:4989–4991

    Article  Google Scholar 

  • Cole HBR, Torchia DA (1991) An NMR study of the backbone dynamics of staphylococcal nuclease in the crystalline state. Chem Phys 158:271–281

    Article  Google Scholar 

  • Cole HB, Sparks SW, Torchia DA (1988) Comparison of the solution and crystal structures of staphylococcal nuclease with 13C and 15N chemical shifts used as structural fingerprints. Proc Natl Acad Sci USA 85:6362–6365

    Article  ADS  Google Scholar 

  • Gans P, Hamelin O, Sounier R, Ayala I, Durá MA, Amero CD, Noirclerc-Savoye M, Franzetti B, Plevin MJ, Boisbouvier J (2010) Stereospecific isotopic labeling of methyl groups for nmr spectroscopic studies of high-molecular-weight proteins. Angew Chem 122:2002–2006

    Article  Google Scholar 

  • Giraud N, Böckmann A, Lesage A, Penin F, Blackledge M, Emsley L (2004) Site-specific backbone dynamics from a crystalline protein by solid-state NMR spectroscopy. J Am Chem Soc 126:11422–11423

    Article  Google Scholar 

  • Hou G, Lu X, Vega AJ, Polenova T (2014) Accurate measurement of heteronuclear dipolar couplings by phase-alternating R-symmetry (PARS) sequences in magic angle spinning NMR spectroscopy. J Chem Phys 141:104202

    Article  ADS  Google Scholar 

  • Jelinski LW, Sullivan CE, Torchia DA (1980) 2H NMR study of molecular motion in collagen fibrils. Nature 284:531–534

    Article  ADS  Google Scholar 

  • Levitt MH (2007) Symmetry-based pulse sequences in magic-angle spinning solid-state NMR. Wiley, New York

    Book  Google Scholar 

  • Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 104:4546–4559

    Article  Google Scholar 

  • Mack JW, Torchia DA, Steinert PM (2002) Solid-state NMR studies of the dynamics and structure of mouse keratin intermediate filaments. Biochemistry 27:5418–5426

    Article  Google Scholar 

  • Munowitz MG, Griffin RG, Bodenhausen G, Huang TH (1981) Two-dimensional rotational spin-echo nuclear magnetic resonance in solids: correlation of chemical shift and dipolar interactions. J Am Chem Soc 103:2529–2533

    Article  Google Scholar 

  • Paluch P, Trébosc J, Nishiyama Y, Potrzebowski MJ, Malon M, Amoureux JP (2015) Theoretical study of CP-VC: a simple, robust and accurate MAS NMR method for analysis of dipolar C-H interactions under rotation speeds faster than ca. 60kHz. J Magn Reson 252:67–77

    Article  ADS  Google Scholar 

  • Pileio G, Guo Y, Pham TN, Griffin JM, Levitt MH, Brown SP (2007) Residual dipolar couplings by off-magic-angle spinning in solid-state nuclear magnetic resonance spectroscopy. J Am Chem Soc 129:10972–10973

    Article  Google Scholar 

  • Pileio G, Mamone S, Mollica G, Montesinos IM, Gansmüller A, Carravetta M, Brown SP, Levitt MH (2008) Estimation of internuclear couplings in the solid-state NMR of multiple-spin systems. Selective spin echoes and off-magic-angle sample spinning. Chem Phys Lett 456:116–121

    Article  ADS  Google Scholar 

  • Reif B, Xue Y, Agarwal V, Pavlova MS, Hologne M, Diehl A, Ryabov YE, Skrynnikov NR (2006) Protein side-chain dynamics observed by solution- and solid-state NMR: comparative analysis of methyl2h relaxation data. J Am Chem Soc 128:12354–12355

    Article  Google Scholar 

  • Sarkar R, Rodriguez Camargo DC, Pintacuda G, Reif B (2015) Restoring resolution in biological solid-state NMR under conditions of off-magic-angle spinning. J Phys Chem Lett 6:5040–5044

    Article  Google Scholar 

  • 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 132:15957–15967

    Article  Google Scholar 

  • Schanda P, Huber M, Boisbouvier J, Meier BH, Ernst M (2011a) Solid-state NMR measurements of asymmetric dipolar couplings provide insight into protein side-chain motion. Angew Chem Int Ed Engl 50:11005–11009

    Article  Google Scholar 

  • Schanda P, Meier BH, Ernst M (2011b) Accurate measurement of one-bond H-X heteronuclear dipolar couplings in MAS solid-state NMR. J Magn Reson 210:246–259

    Article  ADS  Google Scholar 

  • Smith AA, Testori E, Cadalbert R, Meier BH, Ernst M (2016) Characterization of fibril dynamics on three timescales by solid-state NMR. J Biomol NMR 65:171–191

    Article  Google Scholar 

  • Torchia DA, Szabo A (1982) Spin-lattice relaxation in solids. J Magn Reson 49:107–121

    ADS  Google Scholar 

  • Xue K, Mühlbauer M, Mamone S, Sarkar R, Reif B (2019) Accurate determination of 1H-15N dipolar couplings using inaccurate settings of the magic angle in solid state NMR. Angew Chem 131:4330–4334

    Article  Google Scholar 

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Acknowledgements

This work was performed in the framework of the SFB-1035 (Project B07; German Research Foundation, DFG). We acknowledge support from the Helmholtz-Gemeinschaft and the Deutsche Forschungsgemeinschaft (Grants Re1435). We are grateful to the Center for Integrated Protein Science Munich (CIPS-M) for financial support. We thank Dr. Sam Asami for stimulating discussions, and making the methyl REDOR order parameters for α-spectrin SH3 available for this study.

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Authors and Affiliations

  1. Helmholtz-Zentrum München (HMGU), Deutsches Forschungszentrum für Gesundheit und Umwelt, Ingolstädter Landstr. 1, 85764, Neuherberg, Germany

    Kai Xue, Benita Koch, Riddhiman Sarkar & Bernd Reif

  2. Munich Center for Integrated Protein Science (CIPS-M) at Department Chemie, Technische Universität München (TUM), Lichtenbergstr. 4, 85747, Garching, Germany

    Kai Xue, Benita Koch, Riddhiman Sarkar & Bernd Reif

  3. Max Planck Institute for Biophysical Chemistry, Göttingen, Germany

    Salvatore Mamone

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  1. Kai Xue
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  2. Salvatore Mamone
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  3. Benita Koch
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  4. Riddhiman Sarkar
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  5. Bernd Reif
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Correspondence to Riddhiman Sarkar or Bernd Reif.

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Xue, K., Mamone, S., Koch, B. et al. Determination of methyl order parameters using solid state NMR under off magic angle spinning. J Biomol NMR 73, 471–475 (2019). https://doi.org/10.1007/s10858-019-00253-5

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