Influence of cholesterol on dynamics of dimyristoylphosphatidylcholine bilayers as studied by deuterium NMR relaxation

Investigation of the deuterium (2H) nuclear magnetic resonance (NMR) relaxation rates of lipid bilayers containing cholesterol can yield new insights regarding its role in membrane function and dynamics. Spin-lattice (R1Z) and quadrupolar order (R1Q) 2H NMR relaxation rates were measured at 46.1 and 76.8 MHz for macroscopically oriented bilayers of 1,2-diperdeuteriomyristoyl-sn-glycero-3-phosphocholine (DMPC-d54) containing cholesterol (1/1 molar ratio) in the liquid-ordered phase at 40 °C. The data for various segmental positions along the DMPC-d54 acyl chain were simultaneously fitted to a composite membrane deformation model, including fast segmental motions which preaverage the coupling tensor along the lipid acyl chain, slow molecular reorientations, and small-amplitude collective fluctuations. In contrast to pure DMPC-d54 in the liquid-crystalline (Lα) phase, for the DMPC-d54:cholesterol (1/1) system a linear square-law functional dependence of the relaxation rates on the order parameter (quadrupola...

[1]  T. Alam,et al.  Angular anisotropy of 2H NMR spectral densities in phospholipid bilayers containing cholesterol , 1992 .

[2]  M. Bloom,et al.  The evolution of membranes , 1988 .

[3]  M. F. Brown,et al.  Theory of spin‐lattice relaxation in lipid bilayers and biological membranes. 2H and 14N quadrupolar relaxation , 1982 .

[4]  J. Seelig,et al.  Influence of cholesterol on the polar region of phosphatidylcholine and phosphatidylethanolamine bilayers. , 1978, Biochemistry.

[5]  S. Chan,et al.  Cholesterol-phospholipid interaction in membranes. 1. Cholestane spin-label studies of phase behavior of cholesterol-phospholipid liposomes. , 1982, Biochemistry.

[6]  R. Blinc,et al.  Proton spin–lattice relaxation in smectic TBBA , 1975 .

[7]  M. Rance,et al.  Effects of cholesterol on the orientational order of unsaturated lipids in the membranes of acholeplasma laidlawii. A 2H-NMR study. , 1982, Biochimica et biophysica acta.

[8]  H. Mantsch,et al.  Angular dependence of 2H NMR relaxation rates in lipid bilayers , 1988 .

[9]  Michael F. Brown,et al.  ANISOTROPIC NUCLEAR SPIN RELAXATION OF CHOLESTEROL IN PHOSPHOLIPID BILAYERS , 1990 .

[10]  D. Torchia,et al.  Spin-lattice relaxation in solids , 1982 .

[11]  M. Klein,et al.  Constant pressure and temperature molecular dynamics simulation of a fully hydrated liquid crystal phase dipalmitoylphosphatidylcholine bilayer. , 1995, Biophysical journal.

[12]  J. Freed.  Stochastic‐molecular theory of spin–relaxation for liquid crystals , 1977 .

[13]  R. Ghosh,et al.  The interaction of cholesterol with bilayers of phosphatidylethanolamine , 1982 .

[14]  James H. Davis,et al.  Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry. , 1990, Biochemistry.

[15]  H. Jarrell,et al.  Determination of conformational properties of glycolipid head groups by 2H NMR of oriented multibilayers. , 1987, Biochemistry.

[16]  K. Gawrisch,et al.  Effects of ethanol on lipid bilayers containing cholesterol, gangliosides, and sphingomyelin. , 1995, Biochemistry.

[17]  P. Yeagle,et al.  Cholesterol dynamics in membranes. , 1990, Biophysical journal.

[18]  M. Bloom,et al.  Relationships between lipid membrane area, hydrophobic thickness, and acyl-chain orientational order. The effects of cholesterol. , 1990, Biophysical journal.

[19]  Göran Lindblom,et al.  NMR Studies of translational diffusion in lyotropic liquid crystals and lipid membranes , 1994 .

[20]  R. Mendelsohn,et al.  Effects of cholesterol on conformational disorder in dipalmitoylphosphatidylcholine bilayers. A quantitative IR study of the depth dependence. , 1990, Biochemistry.

[21]  Y. K. Levine,et al.  Reorientational dynamics in lipid vesicles and liposomes studied with ESR: effects of hydration, curvature and unsaturation. , 1989, Biochimica et biophysica acta.

[22]  B. Halle.  Deuterium NMR relaxation in phospholipid bilayers: toward a consistent molecular interpretation , 1991 .

[23]  G. Karlström,et al.  Phase equilibria in the phosphatidylcholine-cholesterol system. , 1987, Biochimica et biophysica acta.

[24]  M. F. Brown,et al.  Deuterium Relaxation and Molecular Dynamics in Lipid Bilayers , 1979 .

[25]  J R Brookeman,et al.  High‐resolution H NMR spectral signature from human atheroma , 1988, Magnetic resonance in medicine.

[26]  M. Bloom,et al.  Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective , 1991, Quarterly Reviews of Biophysics.

[27]  E. Oldfield,et al.  Spectroscopic studies of specifically deuterium labeled membrane systems. Nuclear magnetic resonance investigation of the effects of cholesterol in model systems. , 1978, Biochemistry.

[28]  G. Lindblom,et al.  Effect of cholesterol in membranes. Pulsed nuclear magnetic resonance measurements of lipid lateral diffusion. , 1981, Biochemistry.

[29]  Theodore P. Trouard,et al.  Lipid bilayer dynamics from simultaneous analysis of orientation and frequency dependence of deuterium spin-lattice and quadrupolar order relaxation , 1998 .

[30]  E. Jakobsson,et al.  Incorporation of surface tension into molecular dynamics simulation of an interface: a fluid phase lipid bilayer membrane. , 1995, Biophysical journal.

[31]  P. R. Bevington,et al.  Data Reduction and Error Analysis for the Physical Sciences , 1969 .

[32]  E. Dufourc,et al.  A detailed analysis of the motions of cholesterol in biological membranes by 2H-NMR relaxation. , 1986, Chemistry and physics of lipids.

[33]  E. Oldfield,et al.  Deuterium nuclear magnetic resonance investigation of the dipalmitoyl lecithin-cholesterol-water system. , 1977, Journal of the American Chemical Society.

[34]  J. Rubenstein,et al.  Lateral diffusion in binary mixtures of cholesterol and phosphatidylcholines. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[35]  R M Venable,et al.  Molecular dynamics simulations of a lipid bilayer and of hexadecane: an investigation of membrane fluidity. , 1993, Science.

[36]  B. Litman,et al.  Rhodopsin-phospholipid interactions: dependence of rate of the meta I to meta II transition on the level of associated disk phospholipid. , 1981, Biochemistry.

[37]  R. Thurmond,et al.  Deuterium NMR study of intermolecular interactions in lamellar phases containing palmitoyllysophosphatidylcholine , 1992 .

[38]  D. Golan,et al.  Use of a fluorescent cholesterol derivative to measure lateral mobility of cholesterol in membranes. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[39]  M. Bloom,et al.  Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains , 1976 .

[40]  H. Duwe,et al.  Bending elasticity and thermal excitations of lipid bilayer vesicles: Modulation by solutes , 1990 .

[41]  E. Dufourc,et al.  Structural and dynamical details of cholesterol-lipid interaction as revealed by deuterium NMR , 1984 .

[42]  A. Szabó.  Theory of fluorescence depolarization in macromolecules and membranes , 1984 .

[43]  J. Mason,et al.  A method for the synthesis of isomerically pure saturated mixed-chain phosphatidylcholines. , 1981, Analytical biochemistry.

[44]  G. Gröbner,et al.  Collective lipid motions in bilayer membranes studied by transverse deuteron spin relaxation , 1991 .

[45]  P. Meier,et al.  Multipulse dynamic NMR of liquid crystal polymers , 1985 .

[46]  A. Nevzorov,et al.  Dynamics of lipid bilayers from comparative analysis of 2H and 13C nuclear magnetic resonance relaxation data as a function of frequency and temperature , 1997 .

[47]  R. Demel,et al.  The properties of polyunsaturated lecithins in monolayers and liposomes and the interactions of these lecithins with cholesterol , 1972 .

[48]  B. Cornell,et al.  The effect of cholesterol and gramicidin A′ on the carbonyl groups of dimyristoylphosphatidylcholine dispersions , 1983 .

[49]  K. Müller,et al.  Orientation-dependent deuteron spin-lattice relaxation times in bilayer membranes: Characterization of the overall lipid motion , 1990 .

[50]  P. Meier,et al.  Multipulse dynamic nuclear magnetic resonance of phospholipid membranes , 1986 .

[51]  G. Gröbner,et al.  Deuteron nuclear magnetic resonance study of the dynamic organization of phospholipid/cholesterol bilayer membranes: molecular properties and viscoelastic behavior. , 1992, Biochemistry.

[52]  J. Freed,et al.  Dynamics of phosphatidylcholine-cholesterol mixed model membranes in the liquid crystalline state. , 1990, Biophysical journal.

[53]  P. Meier,et al.  Proton spin relaxation dispersion studies of phospholipid membranes , 1988 .

[54]  H. Jarrell,et al.  Use of a comprehensive approach to molecular dynamics in ordered lipid systems: cholesterol reorientation in oriented lipid bilayers. A deuterium NMR relaxation case study , 1990 .

[55]  Robin K. Harris,et al.  Encyclopedia of nuclear magnetic resonance , 1996 .

[56]  E. Hahn,et al.  Pulsed magnetic resonance : NMR, ESR, and optics : a recognition of E.L. Hahn , 1992 .

[57]  A determination of individual spectral densities in a smectic liquid crystal from angle dependent nuclear spin relaxation measurements , 1983 .

[58]  G. R. Luckhurst,et al.  The Molecular physics of liquid crystals , 1979 .

[59]  H. Kutchai,et al.  Effects of cholesterol on acyl chain dynamics in multilamellar vesicles of various phosphatidylcholines. , 1983, Biochimica et biophysica acta.

[60]  Nuclear Magnetic Resonance of Liquid Crystals , 1994 .

[61]  C. Wade,et al.  Lipid lateral diffusion by pulsed nuclear magnetic resonance. , 1979, Biochemistry.

[62]  M. Bloom,et al.  Orientation dependence of 2H nuclear magnetic resonance spin‐lattice relaxation in phospholipid and phospholipid:cholesterol systems , 1994 .

[63]  H. Carr,et al.  The Principles of Nuclear Magnetism , 1961 .

[64]  H. Mcconnell,et al.  Lateral diffusion in inhomogeneous membranes. Model membranes containing cholesterol. , 1980, Biophysical journal.

[65]  W. Hubbell,et al.  Molecular motion in spin-labeled phospholipids and membranes. , 1971, Journal of the American Chemical Society.

[66]  J. Pirs,et al.  Theory for spin-lattice relaxation in nematic liquid crystals , 1976 .

[67]  H. Mcconnell,et al.  Phase equilibria in binary mixtures of phosphatidylcholine and cholesterol. , 1981, Biochemistry.

[68]  Terry R. Stouch,et al.  The limiting behavior of water hydrating a phospholipid monolayer: A computer simulation study , 1993 .

[69]  T. Alam,et al.  Angular dependence of deuterium spin‐lattice relaxation rates of macroscopically oriented dilauroylphosphatidylcholine in the liquid‐crystalline state , 1994 .

[70]  R. Griffin,et al.  Carbon-13 and deuterium nuclear magnetic resonance study of the interaction of cholesterol with phosphatidylethanolamine. , 1982, Biochemistry.

[71]  P. Pincus.  Nuclear relaxation in a nematic liquid crystal , 1969 .

[72]  T. McIntosh.  The effect of cholesterol on the structure of phosphatidylcholine bilayers. , 1978, Biochimica et biophysica acta.

[73]  E. Olejniczak,et al.  Anisotropic 2H-nuclear magnetic resonance spin-lattice relaxation in cerebroside- and phospholipid-cholesterol bilayer membranes. , 1988, Biophysical journal.

[74]  J. Brainard,et al.  Theory for nuclear magnetic relaxation of probes in anisotropic systems: application of cholesterol in phospholipid vesicles. , 1981, Biochemistry.

[75]  E. Evans,et al.  Thermomechanical and transition properties of dimyristoylphosphatidylcholine/cholesterol bilayers. , 1988, Biochemistry.

[76]  J. Seelig,et al.  Structural dynamics in phospholipid bilayers from deuterium spin–lattice relaxation time measurements , 1979 .

[77]  S. Wimperis.  Broadband and narrowband composite excitation sequences , 1990 .

[78]  B. Halle,et al.  Orientational correlations and spin relaxation in lamellar fluid membrane phases , 1997 .

[79]  O. Söderman,et al.  Orientational anisotropy of nuclear spin relaxation in phospholipid membranes , 1990 .

[80]  M. Straume,et al.  Modulation of metarhodopsin formation by cholesterol-induced ordering of bilayer lipids. , 1990, Biochemistry.

[81]  I. Smith,et al.  A deuterium nuclear magnetic resonance study of the condensing effect of cholesterol on egg phosphatidylcholine bilayer membranes. I. Perdeuterated fatty acid probes. , 1976, Chemistry and physics of lipids.

[82]  G. Bodenhausen,et al.  Phase-shifted pulse sequence for measurement of spin-lattice relaxation in complex spin systems: an improvement , 1980 .

[83]  G. Hoatson.  Broadband composite excitation sequences for creating quadrupolar order in 2H NMR , 1991 .

[84]  G. Moro,et al.  Calculation of ESR spectra and related Fokker–Planck forms by the use of the Lanczos algorithm , 1981 .

[85]  Benoît Roux,et al.  Biological membranes : a molecular perspective from computation and experiment , 1996 .

[86]  K. Dill,et al.  Frequency dependence of NMR spin lattice relaxation in bilayer membranes , 1984 .

[87]  I. Smith,et al.  The molecular dynamics of cholesterol in bilayer membranes: A deuterium NMR study , 1981 .

[88]  H. Lécuyer,et al.  Structure of aqueous mixtures of lecithin and cholesterol. , 1969, Journal of molecular biology.