Temperature-Dependent Hydrocarbon Chain Disorder in Phosphatidylcholine Bilayers Studied by Raman Spectroscopy.

Raman scattering of five phosphatidylcholines [1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine (POPC), 1,2-dihexadecanoyl-sn-glycero-3-phosphocholine (DPPC), 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC), 1,2-dilinoleoyl-sn-glycero-3-phosphocholine (DLPC), and 1,2-dilignoceroyl-sn-glycero-3-phosphocholine (PC24)] was studied in a wide temperature range. These phospholipid bilayers differ in the temperature of the gel-fluid transition Tm (from -57 to +80 °C) and in the number of unsaturated bonds. For all lipids, the temperature dependence of both asymmetrical methylene stretching and C-C stretching bands provides evidence that the disordering processes occur significantly below Tm. Temperature onset of the decrease of Raman intensity of the asymmetrical methylene stretching band is the same for unsaturated lipids (DLPC, POPC, and DOPC), which was interpreted as the importance of packing defects in the bilayers of these phospholipids. The chain conformational order was characterized by Raman intensity of the high-frequency C-C stretching mode. An approach was used where the Raman intensity of this mode serves as a measure of hydrocarbon chains in the ground conformational state. Temperature dependence of the chains in the ground conformational state was well described by a simple model with the ground and two excited states: the kinked state and the highly disordered, fluidlike state.

[1]  Application of finite-size scaling to the Pink model for lipid bilayers. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[2]  H. Mantsch,et al.  Polymorphic phase behaviour of phospholipid membranes studied by infrared spectroscopy. , 1984, Biochimica et biophysica acta.

[3]  A. Sum,et al.  Molecular studies of the gel to liquid-crystalline phase transition for fully hydrated DPPC and DPPE bilayers. , 2007, Biochimica et biophysica acta.

[4]  B P Gaber,et al.  On the quantitative interpretation of biomembrane structure by Raman spectroscopy. , 1977, Biochimica et biophysica acta.

[5]  T. Gutberlet,et al.  Hydration of the dienic lipid dioctadecadienoylphosphatidylcholine in the lamellar phase--an infrared linear dichroism and x-ray study on headgroup orientation, water ordering, and bilayer dimensions. , 1998, Biophysical journal.

[6]  D. Marsh,et al.  Time-resolved electron spin resonance studies of spin-labelled lipids in membranes. , 2006, Chemistry and physics of lipids.

[7]  I W Levin,et al.  Hydrocarbon chain disorder in lipid bilayers. Temperature dependent Raman spectra of 1,2-diacyl phosphatidylcholine-water gels. , 1977, Biochimica et biophysica acta.

[8]  J. Nagle,et al.  Lipid bilayers: thermodynamics, structure, fluctuations, and interactions. , 2004, Chemistry and physics of lipids.

[9]  E. Dufourc,et al.  Restatement of order parameters in biomembranes: calculation of C-C bond order parameters from C-D quadrupolar splittings. , 1995, Biophysical journal.

[10]  S. Kaneshina,et al.  Effect of unsaturated acyl chains on the thermotropic and barotropic phase transitions of phospholipid bilayer membranes , 1999 .

[11]  Y. Kadoma,et al.  A calorimetric study of the interaction of synthetic phospholipid liposomes with lipid-soluble small molecules used as dental materials and devices. , 1987, Journal of biomedical materials research.

[12]  B. Tenchov,et al.  Time-resolved x-ray diffraction and calorimetric studies at low scan rates: I. Fully hydrated dipalmitoylphosphatidylcholine (DPPC) and DPPC/water/ethanol phases. , 1989, Biophysical journal.

[13]  N. Surovtsev,et al.  Flexibility of phospholipids with saturated and unsaturated chains studied by Raman scattering: the effect of cholesterol on dynamical and phase transitions. , 2014, The Journal of chemical physics.

[14]  P. Meier,et al.  Chain configuration and flexibility gradient in phospholipid membranes. Comparison between spin-label electron spin resonance and deuteron nuclear magnetic resonance, and identification of new conformations. , 1989, Biophysical journal.

[15]  Joel M Harris,et al.  Detecting phase transitions in phosphatidylcholine vesicles by Raman microscopy and self-modeling curve resolution. , 2007, The journal of physical chemistry. B.

[16]  P. Davis,et al.  Differential scanning calorimetric studies of aqueous dispersions of mixtures of cholesterol with some mixed-acid and single-acid phosphatidylcholines , 1983 .

[17]  E. Bamberg,et al.  Raman spectroscopic investigation of the interaction of gramicidin A with dipalmitoyl phosphatidylcholine liposomes. , 1977, Biochimica et biophysica acta.

[18]  P. F. Almeida,et al.  Simulation of the gel-fluid transition in a membrane composed of lipids with two connected acyl chains: application of a dimer-move step. , 1996, Biophysical journal.

[19]  S. P. Verma,et al.  Multiple thermotropic state transitions in erythrocyte membranes. A laser-Raman study of the CH-stretching and acoustical regions. , 1976, Biochimica et biophysica acta.

[20]  J. Villalaín.  Membranotropic effects of arbidol, a broad anti-viral molecule, on phospholipid model membranes. , 2010, The journal of physical chemistry. B.

[21]  R. Vink,et al.  Main transition in the Pink membrane model: finite-size scaling and the influence of surface roughness. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  D. Marsh,et al.  Dynamic chain conformations in dimyristoyl glycerol-dimyristoyl phosphatidylcholine mixtures. 2H-NMR studies. , 1996, Biophysical journal.

[23]  T. Heimburg.  A model for the lipid pretransition: coupling of ripple formation with the chain-melting transition. , 2000, Biophysical journal.

[24]  P. Knowles,et al.  Characterization of dimyristoylphosphatidylcholine vesicles and their dimensional changes through the phase transition: molecular control of membrane morphology. , 1978, Biochemistry.

[25]  R. McCreery,et al.  Raman Spectroscopy for Chemical Analysis: McCreery/Raman Spectroscopy , 2005 .

[26]  H. Mantsch,et al.  Effects of hydrostatic pressure on the molecular structure and endothermic phase transitions of phosphatidylcholine bilayers: a Raman scattering study. , 1985, Biochemistry.

[27]  N. Dencher,et al.  Interactions of Hydration Water and Biological Membranes Studied by Neutron Scattering , 1999 .

[28]  E. Goormaghtigh,et al.  Effect of the antibiotic azithromycin on thermotropic behavior of DOPC or DPPC bilayers. , 2006, Chemistry and physics of lipids.

[29]  D. Marsh,et al.  EPR studies on the influence of chain length on the segmental motion of spin-labelled fatty acids in dimyristoylphosphatidylcholine bilayers. , 1991, Biochimica et biophysica acta.

[30]  R. Meier.  Studying the length of trans conformational sequences in polyethylene using Raman spectroscopy: a computational study , 2002 .

[31]  P. Barton,et al.  Phase behavior of synthetic phosphatidylglycerols and binary mixtures with phosphatidylcholines in the presence and absence of calcium ions. , 1978, Biochemistry.

[32]  N. Surovtsev,et al.  On the low-temperature onset of molecular flexibility in lipid bilayers seen by Raman scattering. , 2008, The journal of physical chemistry. B.

[33]  G. Zerbi,et al.  Molecular flexibility of polymethylene molecules: A Raman spectroscopic study , 1988 .

[34]  G. P. Holland,et al.  Probing lipid-cholesterol interactions in DOPC/eSM/Chol and DOPC/DPPC/Chol model lipid rafts with DSC and (13)C solid-state NMR. , 2013, Biochimica et biophysica acta.

[35]  Alexander P. Lyubartsev,et al.  Derivation and Systematic Validation of a Refined All-Atom Force Field for Phosphatidylcholine Lipids , 2012, The journal of physical chemistry. B.

[36]  R. G. Snyder,et al.  IR spectroscopic study of the structure and phase behavior of long-chain diacylphosphatidylcholines in the gel state. , 1996, Biophysical journal.

[37]  J. Nagle,et al.  Structure of lipid bilayers. , 2000, Biochimica et biophysica acta.

[38]  D. Marsh,et al.  Binary phase diagram of hydrated dimyristoylglycerol-dimyristoylphosphatidylcholine mixtures. , 1992, Biophysical journal.

[39]  B. Sears,et al.  A calorimetry and deuterium NMR study of mixed model membranes of 1-palmitoyl-2-oleylphosphatidylcholine and saturated phosphatidylcholines. , 1985, Biochimica et biophysica acta.

[40]  Sterling A. Wheaten,et al.  Phase separation and fluctuations in mixtures of a saturated and an unsaturated phospholipid. , 2012, Biophysical journal.

[41]  K. Keough,et al.  Cholesterol does not remove the gel-liquid crystalline phase transition of phosphatidylcholines containing two polyenoic acyl chains. , 1991, Biochimica et biophysica acta.

[42]  K. Keough,et al.  Gel to liquid-crystalline transition temperatures of water dispersions of two pairs of positional isomers of unsaturated mixed-acid phosphatidylcholines. , 1981, Biochemistry.

[43]  D. Pink,et al.  Raman scattering in bilayers of saturated phosphatidylcholines. Experiment and theory. , 1980, Biochemistry.

[44]  D. F. Wallach,et al.  Application of laser Raman and infrared spectroscopy to the analysis of membrane structure. , 1979, Biochimica et biophysica acta.

[45]  J M Sturtevant,et al.  Investigation of phase transitions of lipids and lipid mixtures by sensitivity differential scanning calorimetry. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[46]  J. Sturtevant,et al.  Thermodynamics of phospholipid-sucrose interactions. , 1984, Biophysical journal.

[47]  F. Schwarz.  Biological thermodynamic data for the calibration of differential scanning calorimeters: dynamic temperature data on the gel to liquid crystal phase transition of dialkylphosphatidylcholine in water suspensions , 1991 .

[48]  T. Heimburg,et al.  A Monte Carlo simulation study of protein-induced heat capacity changes and lipid-induced protein clustering. , 1996, Biophysical journal.

[49]  N. Ivanisenko,et al.  Low-temperature dynamical and structural properties of saturated and monounsaturated phospholipid bilayers revealed by Raman and spin-label EPR spectroscopy. , 2012, The journal of physical chemistry. B.

[50]  D. Fioretto,et al.  Infrared versus light scattering techniques to monitor the gel to liquid crystal phase transition in lipid membranes , 2015 .

[51]  R. Mendelsohn,et al.  Quantitative determination of conformational disorder in the acyl chains of phospholipid bilayers by infrared spectroscopy. , 1989, Biochemistry.

[52]  T. Heimburg,et al.  Enthalpy and volume changes in lipid membranes I. The proportionality of heat and volume changes in the lipid melting transition and its implication for the elastic constants. , 2001 .

[53]  K. Heremans,et al.  Reorientation of hydration water during the thermotropic main phase transition of 1-palmitoyl-2-oleolyl-sn-glycero-3-phosphocholine (POPC) bilayers at low degrees of hydration , 2013 .

[54]  H. Casal,et al.  Quantitative determination of hydrocarbon chain conformational order in bilayers of saturated phosphatidylcholines of various chain lengths by Fourier transform infrared spectroscopy. , 1990, Biochemistry.

[55]  M. Harrand.  Polarized Raman spectra of oriented dipalmitoylphosphatidylcholine (DPPC). I. Scattering activities of skeletal stretching and methylene vibrations of hydrocarbon chains , 1983 .

[56]  A. Blume.  Apparent molar heat capacities of phospholipids in aqueous dispersion. Effects of chain length and head group structure , 1983 .

[57]  Zachary D. Schultz,et al.  Vibrational spectroscopy of biomembranes. , 2011, Annual review of analytical chemistry.

[58]  P. Knowles,et al.  Evidence for phase boundary lipid. Permeability of Tempo-choline into dimyristoylphosphatidylcholine vesicles at the phase transition. , 1976, Biochemistry.

[59]  S. Kaneshina,et al.  Barotropic and thermotropic bilayer phase behavior of positional isomers of unsaturated mixed-chain phosphatidylcholines. , 2009, Biochimica et biophysica acta.

[60]  T. Lookman,et al.  Computer simulation of the main gel–fluid phase transition of lipid bilayers , 1983 .

[61]  K. Jørgensen,et al.  Freeze/thaw effects on lipid-bilayer vesicles investigated by differential scanning calorimetry. , 2003, Biochimica et biophysica acta.

[62]  Pierre-Yves Turpin,et al.  Interaction of phospholipid dispersions with water-soluble porphyrins as monitored by their Raman temperature profiles. , 2004, Chemistry and physics of lipids.

[63]  S. Bonora,et al.  DSC and Raman study on the interaction between polychlorinated biphenyls (PCB) and phospholipid liposomes , 2003 .

[64]  H. Amenitsch,et al.  Structural, dynamic and mechanical properties of POPC at low cholesterol concentration studied in pressure/temperature space , 2003, European Biophysics Journal.

[65]  H. Berendsen,et al.  Molecular dynamics simulation of a phospholipid membrane , 2004, European Biophysics Journal.

[66]  T. Bayerl,et al.  Phase transition behavior of single phosphatidylcholine bilayers on a solid spherical support studied by DSC, NMR and FT-IR. , 1992, Biophysical journal.

[67]  Guo,et al.  Phase behavior of pure lipid bilayers with mismatch interactions. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[68]  I W Levin,et al.  Two types of hydrocarbon chain interdigitation in sphingomyelin bilayers. , 1985, Biochemistry.

[69]  I. W. Levin,et al.  Vibrational Raman spectra of lipid systems containing amphotericin B. , 1977, Biochimica et biophysica acta.

[70]  John F. Nagle,et al.  Theory of the Main Lipid Bilayer Phase Transition , 1980 .