Articles | Volume 4, issue 1
https://doi.org/10.5194/mr-4-115-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/mr-4-115-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Time-domain proton-detected local-field NMR for molecular structure determination in complex lipid membranes
Anika Wurl
NMR group, Institute for Physics, Martin Luther University Halle–Wittenberg, Halle (Saale), Germany
Kay Saalwächter
NMR group, Institute for Physics, Martin Luther University Halle–Wittenberg, Halle (Saale), Germany
Tiago Mendes Ferreira
CORRESPONDING AUTHOR
NMR group, Institute for Physics, Martin Luther University Halle–Wittenberg, Halle (Saale), Germany
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Nail Fatkullin, Ivan Brekotkin, and Kay Saalwächter
Magn. Reson., 6, 1–14, https://doi.org/10.5194/mr-6-1-2025, https://doi.org/10.5194/mr-6-1-2025, 2025
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We believe that, in addition to nontrivial theoretical interest, the proposed work offers experimenters a reliable time interval in which the experimentally measured signal allows for a relatively simple interpretation uncomplicated by contributions from three-particle dynamical correlations of having spin nuclei in condensed matter.
Günter Hempel, Ricardo Kurz, Silvia Paasch, Kay Saalwächter, and Eike Brunner
Magn. Reson., 5, 1–20, https://doi.org/10.5194/mr-5-1-2024, https://doi.org/10.5194/mr-5-1-2024, 2024
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Investigations of metal–organic frameworks are presented. This substance class is of interest for applications in gas storage (hydrogen, methane), separation, catalysis, and sensor technology. The properties of the material depend on the mobility of alkyl or alkyloxy side chains. We have determined that the side-chain methylene groups move highly anisotropically with a relatively short correlation time. Furthermore, we could improve the analysis procedure for the experiment used here.
Günter Hempel, Paul Sotta, Didier R. Long, and Kay Saalwächter
Magn. Reson., 2, 589–606, https://doi.org/10.5194/mr-2-589-2021, https://doi.org/10.5194/mr-2-589-2021, 2021
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We develop an exact analytical description of spinning sideband intensities in magic-angle spinning NMR, e.g., for 13C CSA. This can be used in spectral fitting to obtain tensor parameters and plays out its advantage in the analysis of orientation effects in non-isotropic samples. We present an improved approach to process data obtained with the simple syncMAS experiment, which is powerful but not very popular due to the as yet not very transparent and difficult data analysis.
Alexey Krushelnitsky and Kay Saalwächter
Magn. Reson., 1, 247–259, https://doi.org/10.5194/mr-1-247-2020, https://doi.org/10.5194/mr-1-247-2020, 2020
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This work presents systematic methodological study of one of the types of the nuclear magnetic resonance experiments that enables study of molecular dynamics on a millisecond timescale. A modification of a standard experiment was suggested that excludes possible artefacts and distortions. It has been demonstrated that the standard experiment reveals slow overall motion of proteins in a rigid crystal lattice, whereas the artefact-free experimental setup demonstrates that the proteins are rigid.
Related subject area
Field: Solid-state NMR | Topic: Applications – small molecules
EPR study of NO radicals encased in modified open C60 fullerenes
Klaus-Peter Dinse, Tatsuhisa Kato, Shota Hasegawa, Yoshifumi Hashikawa, Yasujiro Murata, and Robert Bittl
Magn. Reson., 1, 197–207, https://doi.org/10.5194/mr-1-197-2020, https://doi.org/10.5194/mr-1-197-2020, 2020
Short summary
Short summary
The stable, two-atomic radical NO, which is an important biophysical messenger, was studied with magnetic resonance methods. Caused by its specific electronic configuration, it has sensor properties: its magnetic moment sensitively depends on its environment and restricted mobility therein. The interaction with solvents or solid phases can thus be quantified. Encapsulating the radical in the nearly spherical cage of modified C60 fullerenes is a perfect situation to study this effect.
Cited articles
Aisenbrey, C., Salnikov, E., and Bechinger, B.: Solid-State NMR Investigations
of the MHC II Transmembrane Domains: Topological Equilibria and Lipid
Interactions, J. Mem. Biol., 252, 371–384,
https://doi.org/10.1007/s00232-019-00071-8, 2019. a
Andersson, J. M., Grey, C., Larsson, M., Ferreira, T. M., and Sparr, E.: Effect
of cholesterol on the molecular structure and transitions in a clinical-grade
lung surfactant extract, P. Natl. Acad. Sci. USA, 114, E3592–E3601,
https://doi.org/10.1073/pnas.1701239114, 2017. a
Asami, S. and Reif, B.: Comparative Study of REDOR and CPPI Derived Order
Parameters by 1H-Detected MAS NMR and MD Simulations, J. Phys. Chem. B, 121,
8719–8730, https://doi.org/10.1021/acs.jpcb.7b06812, 2017. a
Bacle, A., Buslaev, P., Garcia-Fandino, R., Favela-Rosales, F., Ferreira, T.,
Fuchs, P., Gushchin, I., Javanainen, M., Kiirikki, A., Madsen, J., Melcr, J.,
Milán Rodríguez, P., Miettinen, M., Ollila, O., Papadopoulos, C., Peón,
A., Piggot, T., Piñeiro, A., and Virtanen, S.: Inverse Conformational
Selection in Lipid–Protein Binding, J. Am. Chem. Soc., 143,
13701–13709, https://doi.org/10.1021/jacs.1c05549, 2021. a, b, c
Bechinger, B. and Seelig, J.: Conformational changes of the phosphatidylcholine
headgroup due to membrane dehydration. A 2H-NMR study, Chemistry and Physics
of Lipids, 58, 1–5, https://doi.org/10.1016/0009-3084(91)90105-K,
1991. a, b
Bärenwald, R., Achilles, A., Lange, F., Ferreira, T. M., and Saalwächter, K.:
Applications of Solid-State NMR Spectroscopy for the Study of Lipid Membranes
with Polyphilic Guest (Macro)Molecules, Polymers, 8, 439,
https://doi.org/10.3390/polym8120439, 2016. a
Cady, S., Goodman, C., Tatko, C., DeGrado, W., and Hong, M.: Determining the
Orientation of Uniaxially Rotating Membrane Proteins Using Unoriented
Samples: A 2H, 13C, and 15N Solid-State NMR Investigation of the Dynamics
and Orientation of a Transmembrane Helical Bundle, J. Am. Chem. Soc., 129,
5719–5729, https://doi.org/10.1021/ja070305e, 2007. a
Cheng, Y.: Membrane protein structural biology in the era of single particle
cryo-EM, Curr. Opin. Struct. Biol., 52, 58–63,
https://doi.org/10.1016/j.sbi.2018.08.008, 2018. a
Chevelkov, V., Fink, U., and Reif, B.: Accurate Determination of Order
Parameters from 1H,15N Dipolar Couplings in MAS Solid-State NMR Experiments,
J. Am. Chem. Soc., 131, 14018–14022, https://doi.org/10.1021/ja902649u, 2009. a
Davis, J.: The description of membrane lipid conformation, order and dynamics
by 2H-NMR, Biochimica et Biophysica Acta (BBA) – Reviews on Biomembranes,
737, 117–171, https://doi.org/10.1016/0304-4157(83)90015-1, 1983. a
Davis, J. H., Clair, J. J., and Juhasz, J.: Phase equilibria in
DOPC/DPPC-d62/cholesterol mixtures, Biophys. J., 96, 521–539,
https://doi.org/10.1016/j.bpj.2008.09.042, 2009. a
De Paëpe, G.: Dipolar Recoupling in Magic Angle Spinning Solid-State Nuclear
Magnetic Resonance, Annu. Rev. Phys. Chem., 63, 661–684,
https://doi.org/10.1146/annurev-physchem-032511-143726, 2012. a, b
deAzevedo, E., Saalwachter, K., Pascui, O., de Souza, A., Bonagamba, T., and
Reichert, D.: Intermediate motions as studied by solid-state separated local
field NMR experiments, J. Chem. Phys., 128, 104505,
https://doi.org/10.1063/1.2831798, 2008. a
Dvinskikh, S., Castro, V., and Sandström, D.: Efficient solid-state NMR
methods for measuring heteronuclear dipolar couplings in unoriented lipid
membrane systems, Phys. Chem. Chem. Phys., 7, 607–613,
https://doi.org/10.1039/b418131j, 2005. a, b, c, d
Ferreira, T. M., Coreta-Gomes, F., Ollila, O. H. S., Moreno, M. J., Vaz, W.
L. C., and Topgaard, D.: Cholesterol and POPC segmental order parameters in
lipid membranes: solid state 1HÐ13C NMR and MD simulation studies, Phys.
Chem. Chem. Phys., 15, 1976–1989, https://doi.org/10.1039/C2CP42738A, 2013. a, b
Fridolf, S., Hamid, M., Svenningsson, L., Skepö, M., Sparr, E., and Topgaard,
D.: Molecular dynamics simulations and solid-state nuclear magnetic resonance
spectroscopy measurements of C–H bond order parameters and effective
correlation times in a POPC-GM3 bilayer, Phys. Chem. Chem. Phys., 24,
25588–25601, https://doi.org/10.1039/D2CP02860C, 2022. a, b
Gally, H. U., Niederberger, W., and Seelig, J.: Conformation and motion of the
choline head group in bilayers of dipalmitoyl-3-sn-phosphatidylcholine,
Biochemistry, 14, 3647–3652, https://doi.org/10.1021/bi00687a021, 1975. a
Gansmüller, A., Simorre, J.-P., and Hediger, S.: Windowed R-PDLF recoupling: A
flexible and reliable tool to characterize molecular dynamics, J. Mag.
Reson., 234, 154–164, https://doi.org/10.1016/j.jmr.2013.06.017, 2013. a, b, c
Gauto, D., Estrozi, L., Schwieters, C., Effantin, G., Macek, P., Sounier, R.,
Sivertsen, A., Schmidt, E., Kerfah, R., Mas, G., Colletier, J., Güntert, P.,
Favier, A., Schoehn, G., Schanda, P., and Boisbouvier, J.: Integrated NMR and
cryo-EM atomic-resolution structure determination of a half-megadalton enzyme
complex, Nat. Commun., 10, 2697, https://doi.org/10.1038/s41467-019-10490-9, 2019. a
Griffin, R.: Dipolar recoupling in MAS spectra of biological solids, Nat.
Struct. Biol., 5, 508–512, https://doi.org/10.1038/749, 1998. a
Gullion, T.: Introduction to rotational-echo, double-resonance NMR, Concepts
Magn. Reson., 10, 277–289,
https://doi.org/10.1002/(SICI)1099-0534(1998)10:5<277::AID-CMR1>3.0.CO;2-U,
1998. a, b
Hester, R., Ackerman, J., Neff, B., and Waugh, J.: Separated Local Field
Spectra in NMR: Determination of Structure of Solids, Phys. Rev. Lett., 36,
1081–1083, https://doi.org/10.1103/PhysRevLett.36.1081, 1976. a
Hou, G., Byeon, I., Ahn, J., Gronenborn, A., and Polenova, T.:
1H–13C/1H–15N Heteronuclear Dipolar Recoupling by R-Symmetry Sequences
Under Fast Magic Angle Spinning for Dynamics Analysis of Biological and
Organic Solids, J. Am. Chem Soc., 133, 18646–18655,
https://doi.org/10.1021/ja203771a, 2011. a
Jain, M., Mote, K., Hellwagner, J., Rajalakshmi, G., Ernst, M., Madhu, P., and
Agarwal, V.: Measuring strong one-bond dipolar couplings using REDOR in
magic-angle spinning solid-state NMR, J. Chem. Phys., 150, 134201,
https://doi.org/10.1063/1.5088100, 2019. a
Leftin, A. and Brown, M. F.: An NMR database for simulations of membrane
dynamics, Biochim. Biophys. Acta-Biomembr., 1808, 818–839,
https://doi.org/10.1016/j.bbamem.2010.11.027, 2011. a
Leftin, A., Molugu, T., Job, C., Beyer, K., and Brown, M.: Area per Lipid and
Cholesterol Interactions in Membranes from Separated Local-Field 13C NMR
Spectroscopy, Biophys. J., 107, 2274–2286,
https://doi.org/10.1016/j.bpj.2014.07.044, 2014. a
Levitt, M.: Symmetry-Based Pulse Sequences in Magic-Angle Spinning Solid-State
NMR, in: Encyclopedia of Nuclear Magnetic Resonance, Volume 9: Advances in NMR, edited by: Grant, D. M. and Harris, R. K., John Wiley and Sons, pp. 165–196,
https://doi.org/10.1002/9780470034590.emrstm0551, 2007. a
Lindon, J. and Ferrige, A.: Digitisation and data processing in Fourier
transform NMR, Prog. Nucl. Magn. Reson. Spectrosc., 14, 27–66,
https://doi.org/10.1016/0079-6565(80)80002-1, 1980. a
Löser, L., Saalwächter, K., and Ferreira, T.: Liquid-liquid phase
coexistence in lipid membranes observed by natural abundance 1H-13C
solid-state NMR, Phys. Chem. Chem. Phys., 20, 9751–9754,
https://doi.org/10.1039/C8CP01012A, 2018. a, b
Lu, X., Zhang, H., Lu, M., Vega, A. J., Hou, G., and Polenova, T.: Improving
dipolar recoupling for site-specific structural and dynamics studies in
biosolids NMR: windowed RN-symmetry sequences, Phys. Chem. Chem. Phys., 18,
4035–4044, https://doi.org/10.1039/C5CP07818K, 2016. a, b, c, d
Mandala, V., Williams, J., and Hong, M.: Structure and Dynamics of Membrane
Proteins from Solid-State NMR, Annu. Rev. Biophys., 47, 201–222,
https://doi.org/10.1146/annurev-biophys-070816-033712, 2018. a
Mandala, V., Loftis, A., Shcherbakov, A., Pentelute, B., and Hong, M.: Atomic
structures of closed and open influenza B M2 proton channel reveal the
conduction mechanism, Nat. Struct. Mol. Biol., 27, 160–167,
https://doi.org/10.1038/s41594-019-0371-2, 2020. a
Mendes Ferreira, T. and Wurl, A.: Simulation data and code used for the publication in Magn. Reson. “Time-domain proton-detected local-field NMR for molecular structure determination in complex lipid membranes” (v1.0.0), Zenodo [code/data], https://doi.org/10.5281/zenodo.7898743, 2023. a
Molugu, T., Lee, S., and Brown, M.: Concepts and Methods of Solid-State NMR
Spectroscopy Applied to Biomembranes, Chem. Rev., 117, 12087–12132,
https://doi.org/10.1021/acs.chemrev.6b00619, 2017. a
Nakai, T. and Terao, T.: Measurements of heteronuclear dipolar powder patterns
due only to directly bonded couplings, Magn. Reson. Chem., 30, 42–44,
https://doi.org/10.1002/mrc.1260300109, 1992. a
Nimerovsky, E. and Soutar, C.: A modification of γ-encoded RN symmetry pulses
for increasing the scaling factor and more accurate measurements of the
strong heteronuclear dipolar couplings, J. Magn. Reson., 319, 106827,
https://doi.org/10.1016/j.jmr.2020.106827, 2020. a
Nishimura, K., Fu, R., and Cross, T. A.: The Effect of RF Inhomogeneity on
Heteronuclear Dipolar Recoupling in Solid State NMR: Practical Performance of
SFAM and REDOR, J. Mag. Reson., 152, 227–233,
https://doi.org/10.1006/jmre.2001.2410, 2001. a
Norton, W. and Autilio, L.: The lipid composition of purified bovine brain
myelin, J. Neurochem., 13, 213–222,
https://doi.org/10.1111/j.1471-4159.1966.tb06794.x, 1966. a
Nowacka, A., Mohr, P., Norrman, J., Martin, R., and Topgaard, D.: Polarization
Transfer Solid-State NMR for Studying Surfactant Phase Behavior, Langmuir,
26, 16848–16856, https://doi.org/10.1021/la102935t, 2010. a
Nowacka, A., Bongartz, N., Ollila, O., Nylander, T., and Topgaard, D.: Signal
intensities in 1H–13C CP and INEPT MAS NMR of liquid crystals, J. Magn.
Reson., 230, 165–175, https://doi.org/10.1016/j.jmr.2013.02.016, 2013. a
Odedra, S. and Wimperis, S.: Imaging of the B1 distribution and background
signal in a MAS NMR probehead using inhomogeneous B0 and B1 fields, J. Mag.
Reson., 231, 95–99, https://doi.org/10.1016/j.jmr.2013.04.002, 2013. a
Park, S., Das, B., Casagrande, F., Tian, Y., Nothnagel, H., Chu, M., Kiefer,
H., Maier, K., De Angelis, A., Marassi, F., and Opella, S.: Structure of the
chemokine receptor CXCR1 in phospholipid bilayers, Nature, 491,
779–784, https://doi.org/10.1038/nature11580, 2012. a
Roux, M. and Bloom, M.: Calcium, magnesium, lithium, sodium, and potassium
distributions in the headgroup region of binary membranes of
phosphatidylcholine and phosphatidylserine as seen by deuterium NMR,
Biochemistry, 29, 7077–7089, https://doi.org/10.1021/bi00482a019, 1990. a, b, c
Schanda, P., Meier, B., and Ernst, M.: Accurate measurement of one-bond H–X
heteronuclear dipolar couplings in MAS solid-state NMR, J. Magn. Reson., 210,
246–259, https://doi.org/10.1016/j.jmr.2011.03.015, 2011. a, b, c, d
Schmidt-Rohr, K., Nanz, D., Emsley, L., and Pines, A.: NMR Measurement of
Resolved Heteronuclear Dipole Couplings in Liquid Crystals and Lipids, J.
Phys. Chem., 98, 6668–6670, https://doi.org/10.1021/j100078a002, 1994. a
Seelig, J.: Deuterium magnetic resonance: theory and application to lipid
membranes, Q. Rev. Biophys., 10, 353–418,
https://doi.org/10.1017/S0033583500002948, 1977.
a
Seelig, J. and Niederberger, W.: Deuterium-labeled lipids as structural probes
in liquid crystalline bilayers. Deuterium magnetic resonance study, J. Am.
Chem. Soc., 96, 2069–2072, https://doi.org/10.1021/ja00814a014, 1974. a
Strandberg, E. and Ulrich, A.: NMR methods for studying membrane-active
antimicrobial peptides, Concepts in Magnetic Resonance Part A, 23A, 89–120,
https://doi.org/10.1002/cmr.a.20024, 2004. a
Tošner, Z., Purea, A., Struppe, J. O., Wegner, S., Engelke, F., Glaser, S. J.,
and Reif, B.: Radiofrequency fields in MAS solid state NMR probes, J.
Magn. Reson., 284, 20–32,
https://doi.org/10.1016/j.jmr.2017.09.002, 2017. a, b, c
Ulrich, A. S. and Watts, A.: Molecular response of the lipid headgroup to
bilayer hydration monitored by 2H NMR, Biophys. J., 66, 1441–1449,
https://doi.org/10.1016/S0006-3495(94)80934-8, 1994. a, b
Umegawa, Y., Matsumori, N., and Murata, M.: Chapter Two – Recent Solid-State
NMR Studies of Hydrated Lipid Membranes, vol. 94 of Annual Reports on
NMR Spectroscopy, 41–72, Academic Press,
https://doi.org/10.1016/bs.arnmr.2017.12.003, 2018. a
Wu, M. and Lander, G.: How low can we go? Structure determination of small
biological complexes using single-particle cryo-EM, Curr. Opin. Struct.
Biol., 64, 9–16, https://doi.org/10.1016/j.sbi.2020.05.007, 2020. a
Xue, K., Nimerovsky, E., Tekwani Movellan, K., Becker, S., and Andreas, L.:
Backbone Torsion Angle Determination Using Proton Detected Magic-Angle
Spinning Nuclear Magnetic Resonance, J. Phys. Chem. Lett., 13, 18–24,
https://doi.org/10.1021/acs.jpclett.1c03267, 2022. a
Zerweck, J., Strandberg, E., Kukharenko, O., Reichert, J., Buerck, J.,
Wadhwani, P., and Ulrich, A.: Molecular mechanism of synergy between the
antimicrobial peptides PGLa and magainin 2, Sci. Rep., 7, 13153,
https://doi.org/10.1038/s41598-017-12599-7, 2017. a
Short summary
R-proton-detected local-field NMR is a powerful method to obtain structural information from biological membrane models. However, the conventional analysis of experiments, by using a Fourier transform in the indirect time-domain and reading-off splittings, is unsuitable to investigate complex systems. One then needs to model the experimental data. Fitting the experimental data with simulations that account for radiofrequency field inhomogeneity enables accurate modeling of R-PDLF data.
R-proton-detected local-field NMR is a powerful method to obtain structural information from...