Abstract
In this chapter we describe the use of solid state nuclear magnetic spectroscopy to study the structure of lyotropic phases and lipid model membranes and show its ability to probe, site specifically, at a sub-Ångstrom resolution. Here, we demonstrate the immense versatility of the technique and its ability to provide information on the different liquid crystalline phases present. A multinuclear for example 31P, 1H, and 13C approach is able to elucidate both the structure and dynamics over a wide variety of timescales. This coupled with a non-perturbing label 2H is able to provide information such as the order parameters for a wide variety of different liquid phases.
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References
Merz KM, Roux B (1996) Biological membranes: a molecular perspective from computation and experiment. Birkhäuser, Boston
Yeagle PL (2011) The structure of biological membranes, 3rd edn. CRC, Boca Raton
Stillwell W (2013) An introduction to biological membranes: from bilayers to rafts. Elsevier Science, London
Auger M (2000) Biological membrane structure by solid-state NMR. Curr Issues Mol Biol 2:119–124
Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572
Marsh D (2010) Liquid-ordered phases induced by cholesterol: a compendium of binary phase diagrams. Biochim Biophys Acta 1798:688–699
Ohvo-Rekila H, Ramstedt B, Leppimaki P, Slotte JP (2002) Cholesterol interactions with phospholipids in membranes. Prog Lipid Res 41:66–97
Ramamoorthy A, Lee D-K, Santos JS, Henzler-Wildman KA (2008) Nitrogen-14 solid-state NMR spectroscopy of aligned phospholipid bilayers to probe peptide-lipid interaction and oligomerization of membrane associated peptides. J Am Chem Soc 130:11023–11029
Lindstrom F, Williamson PTF, Grobner G (2005) Molecular insight into the electrostatic membrane surface potential by N-14/P-31 MAS NMR spectroscopy: nociceptin-lipid association. J Am Chem Soc 127:6610–6616
Rothgeb TM, Oldfield E (1981) N-14 nuclear magnetic-resonance spectroscopy as a probe of lipid bilayer headgroup structure. J Biol Chem 256:6004–6009
Faure C, Bonakdar L, Dufourc EJ (1997) Determination of DMPC hydration in the L(alpha) and L(beta′) phases by H-2 solid state NMR of D2O. FEBS Lett 405:263–266
Burnell EE, Cullis PR, Dekruijff B (1980) Effects of tumbling and lateral diffusion on phosphatidylcholine model membrane P-31-NMR lineshapes. Biochim Biophys Acta 603:63–69
Ando I, Naito A, Saito H (2006) Solid state NMR spectroscopy for biopolymers: principles and applications. Springer, Dordrecht
Ramamoorthy A (2005) NMR spectroscopy of biological solids. CRC, New YOrk
Das N, Murray DT, Cross TA (2013) Lipid bilayer preparations of membrane proteins for oriented and magic-angle spinning solid-state NMR samples. Nat Protocols 8:2256–2270
Katsaras J (1997) Highly aligned lipid membrane systems in the physiologically relevant “excess water” condition. Biophys J 73:2924–2929
Diller A, Loudet C, Aussenac F, Raffard G, Fournier S, Laguerre M et al (2009) Bicelles: a natural ‘molecular goniometer’ for structural, dynamical and topological studies of molecules in membranes. Biochimie 91:744–751
Park SH, Loudet C, Marassi FM, Dufourc EJ, Opella SJ (2008) Solid-state NMR spectroscopy of a membrane protein in biphenyl phospholipid bicelles with the bilayer normal parallel to the magnetic field. J Magn Reson 193:133–138
Cardon TB, Dave PC, Lorigan GA (2005) Magnetically aligned phospholipid bilayers with large q ratios stabilize magnetic alignment with high order in the gel and L-alpha phases. Langmuir 21:4291–4298
Seelig J (1978) P-31 nuclear magnetic-resonance and head group structure of phospholipids in membranes. Biochim Biophys Acta 515:105–140
Gorenstein DG (ed) (1984) Phosphorus-31 NMR principles and applications. Academic, Orlando
Dufourc EJ, Mayer C, Stohrer J, Althoff G, Kothe G (1992) Dynamics of phosphate head groups in biomembranes—comprehensive analysis using P-31 nuclear-magnetic-resonance lineshape and relaxation-time measurements. Biophys J 61:42–57
Dufourc EJ, Mayer C, Stohrer J, Kothe G (1992) P-31 and H-1-nmr pulse sequences to measure lineshapes, T1z and T2e relaxation-times in biological-membranes. J Chim Phys Phys Chim Biol 89:243–252
Picard F, Paquet MJ, Levesque J, Belanger A, Auger M (1999) P-31 NMR first spectral moment study of the partial magnetic orientation of phospholipid membranes. Biophys J 77:888–902
Clarke JA (2005) Solid state NMR investigations of phospholipid/cholesterol interactions in model membranes. Thesis, Imperial College London, London
Clarke JA, Seddon JM, Law RV (2009) Cholesterol containing model membranes studied by multinuclear solid state NMR spectroscopy. Soft Matter 5:369–378
Polozov IV, Gawrisch K (2004) Domains in binary SOPC/POPE lipid mixtures studied by pulsed field gradient H-1 MAS NMR. Biophys J 87:1741–1751
Polozov IV, Gawrisch K (2006) Characterization of the liquid-ordered state by proton MAS NMR. Biophys J 90:2051–2061
Forbes J, Husted C, Oldfield E (1988) High-field, high-resolution proton magic-angle sample-spinning nuclear magnetic-resonance spectroscopic studies of gel and liquid-crystalline lipid bilayers and the effects of cholesterol. J Am Chem Soc 110:1059–1065
Chen ZJ, Stark RE (1996) Evaluating spin diffusion in MAS-NOESY spectra of phospholipid multibilayers. Solid State Nucl Magn Reson 7:239–246
Feller SE, Huster D, Gawrisch K (1999) Interpretation of NOESY cross-relaxation rates from molecular dynamics simulation of a lipid bilayer. J Am Chem Soc 121:8963–8964
Clarke JA, Heron AJ, Seddon JM, Law RV (2006) The diversity of the liquid ordered (L-o) phase of phosphatidylcholine/cholesterol membranes: a variable temperature multinuclear solid-state NMR and X-ray diffraction study. Biophys J 90:2383–2393
Tonelli AE, Schilling FC (1981) C-13 Nmr chemical-shifts and the microstructure of polymers. Acc Chem Res 14:233–238
Ishikawa S, Ando I (1992) Structural studies of dimyristoylphosphatidylcholine and distearoylphosphatidylcholine in the crystalline and liquid-crystalline states by variable-temperature solid-state high-resolution C-13 Nmr-spectroscopy. J Mol Struct 271:57–73
Davis JH (1979) Deuterium magnetic-resonance study of the gel and liquid-crystalline phases of dipalmitoyl phosphatidylcholine. Biophys J 27:339–358
Davis JH (1983) The description of membrane lipid conformation, order and dynamics by H-2-Nmr. Biochim Biophys Acta 737:117–171
Seelig J (1977) Deuterium magnetic-resonance—theory and application to lipid-membranes. Q Rev Biophys 10:353–418
Bechinger B, Seelig J (1991) Conformational-changes of the phosphatidylcholine headgroup due to membrane dehydration—a H-2-Nmr study. Chem Phys Lipids 58:1–5
Brown MF, Nevzorov AA (1999) H-2-NMR in liquid crystals and membranes. Coll Surf A Physicochem Eng Aspects 158:281–298
Grelard A, Loudet C, Diller A, Dufourc EJ (2010) NMR spectroscopy of lipid bilayers. Methods Mol Biol (Clifton, NJ) 654:341–59
Vist MR, Davis JH (1990) Phase-equilibria of cholesterol dipalmitoylphosphatidylcholine mixtures—H-2 nuclear magnetic-resonance and differential scanning calorimetry. Biochemistry 29:451–464
Veatch SL, Polozov IV, Gawrisch K, Keller SL (2004) Liquid domains in vesicles investigated by NMR and fluorescence microscopy. Biophys J 86:2910–2922
Hubner W, Blume A (1990) H-2 Nmr-spectroscopy of oriented phospholipid-bilayers in the gel phase. J Phys Chem 94:7726–7730
Smith ICP, Butler KW, Tulloch AP, Davis JH, Bloom M (1979) Properties of gel state lipid in membranes of acholeplasma-laidlawii as observed by H-2 Nmr. FEBS Lett 100:57–61
Bloom M, Davis JH, Mackay AL (1981) Direct determination of the oriented sample nmr-spectrum from the powder spectrum for systems with local axial symmetry. Chem Phys Lett 80:198–202
Sternin E, Bloom M, Mackay AL (1983) De-Pake-Ing of Nmr-spectra. J Magn Reson 55:274–282
Schafer H, Madler B, Sternin E (1998) Determination of orientational order parameters from H-2 NMR spectra of magnetically partially oriented lipid bilayers. Biophys J 74:1007–1014
Jansson M, Thurmond RL, Trouard TP, Brown MF (1990) Magnetic alignment and orientational order of dipalmitoylphosphatidylcholine bilayers containing palmitoyllysophosphatidylcholine. Chem Phys Lipids 54:157–170
Nevzorov AA, Brown MF (1997) Dynamics of lipid bilayers from comparative analysis of H-2 and C-13 nuclear magnetic resonance relaxation data as a function of frequency and temperature. J Chem Phys 107:10288–10310
Sani M-A, Weber DK, Delaglio F, Separovic F, Gehman JD (2013) A practical implementation of de-Pake-ing via weighted Fourier transformation. Peer J 1:e30-e
Vermeer LS, de Groot BL, Reat V, Milon A, Czaplicki J (2007) Acyl chain order parameter profiles in phospholipid bilayers: computation from molecular dynamics simulations and comparison with H-2 NMR experiments. Eur Biophys J Biophys Lett 36:919–931
Heaton N, Reimer D, Kothe G (1992) Transverse deuteron spin relaxation in thermotropic liquid-crystal polymers—determination of viscoelastic properties. Chem Phys Lett 195:448–454
Jarrell HC, Smith ICP, Jovall PA, Mantsch HH, Siminovitch DJ (1988) Angular-dependence of H-2 Nmr relaxation rates in lipid bilayers. J Chem Phys 88:1260–1263
Jarrell HC, Jovall PA, Giziewicz JB, Turner LA, Smith ICP (1987) Determination of conformational properties of glycolipid head groups by H-2 Nmr of oriented multibilayers. Biochemistry 26:1805–1811
Stohrer J, Grobner G, Reimer D, Weisz K, Mayer C, Kothe G (1991) Collective lipid motions in bilayer-membranes studied by transverse deuteron spin relaxation. J Chem Phys 95:672–678
Nagle JF (1993) Area lipid of bilayers from Nmr. Biophys J 64:1476–1481
Petrache HI, Brown MF (2007) X-ray scattering and solid-state deuterium nuclear magnetic resonance probes of structural fluctuations in lipid membranes. In: Dopico AM (ed) Methods in molecular biology, vol 400. Humana, Totowa, pp 341–53
Sternin E, Schafer H, Polozov IV, Gawrisch K (2001) Simultaneous determination of orientational and order parameter distributions from NMR spectra of partially oriented model membranes. J Magn Reson 149:110–113
Brus J (2000) Heating of samples induced by fast magic-angle spinning. Solid State Nucl Magn Reson 16:151–160
Mellinger F, Wilhelm M, Spiess HW (1999) Calibration of H-1 NMR spin diffusion coefficients for mobile polymers through transverse relaxation measurements. Macromolecules 32:4686–4691
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Tyler, A.I.I., Clarke, J.A., Seddon, J.M., Law, R.V. (2015). Solid State NMR of Lipid Model Membranes. In: Owen, D. (eds) Methods in Membrane Lipids. Methods in Molecular Biology, vol 1232. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-1752-5_17
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DOI: https://doi.org/10.1007/978-1-4939-1752-5_17
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