Diffusion in two-component lipid membranes--a fluorescence correlation spectroscopy and monte carlo simulation study.

Using fluorescence correlation spectroscopy, calorimetry, and Monte Carlo simulations, we studied diffusion processes in two-component membranes close to the chain melting transition. The aim is to describe complex diffusion behavior in lipid systems in which gel and fluid domains coexist. Diffusion processes in gel membranes are significantly slower than in fluid membranes. Diffusion processes in mixed phase regions are therefore expected to be complex. Due to statistical fluctuations the gel-fluid domain patterns are not uniform in space and time. No models for such diffusion processes are available. In this article, which is both experimental and theoretical, we investigated the diffusion in DMPC-DSPC lipid mixtures as a function of temperature and composition. We then modeled the fluorescence correlation spectroscopy experiment using Monte Carlo simulations to analyze the diffusion process. It is shown that the simulations yield a very good description of the experimental diffusion processes, and that predicted autocorrelation profiles are superimposable with the experimental curves. We believe that this study adds to the discussion on the physical nature of rafts found in biomembranes.

[1]  I. Vattulainen,et al.  Simulation study of lateral diffusion in lipid-sterol bilayer mixtures , 2001 .

[2]  A. Kusumi,et al.  Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. , 1993, Biophysical journal.

[3]  H. Mcconnell,et al.  Stripe Phases in Lipid Monolayers near a Miscibility Critical Point , 1999 .

[4]  Kai Simons,et al.  Lipid rafts and signal transduction , 2000, Nature Reviews Molecular Cell Biology.

[5]  R. Rigler,et al.  Molecular interactions of peptides with phospholipid vesicle membranes as studied by fluorescence correlation spectroscopy. , 2000, Chemistry and physics of lipids.

[6]  M. Saxton,et al.  Lateral diffusion in an archipelago. Effects of impermeable patches on diffusion in a cell membrane. , 1982, Biophysical journal.

[7]  Helmut Grubmüller,et al.  Effect of sodium chloride on a lipid bilayer. , 2003, Biophysical journal.

[8]  G. Schütz,et al.  Single-molecule anisotropy imaging. , 1999, Biophysical journal.

[9]  P. Chong,et al.  Geometrical properties of gel and fluid clusters in DMPC/DSPC bilayers: Monte Carlo simulation approach using a two-state model. , 2001, Biophysical journal.

[10]  T. E. Thompson,et al.  Translational diffusion and fluid domain connectivity in a two-component, two-phase phospholipid bilayer. , 1989, Biophysical journal.

[11]  T. Schäffer,et al.  Analyzing heat capacity profiles of peptide-containing membranes: cluster formation of gramicidin A. , 2003, Biophysical journal.

[12]  P. Mazur On the theory of brownian motion , 1959 .

[13]  E. Ikonen,et al.  Functional rafts in cell membranes , 1997, Nature.

[14]  T. James,et al.  Lateral diffusion of the phospholipid molecule in dipalmitoylphosphatidylcholine bilayers. An investigation using nuclear spin--lattice relaxation in the rotating frame. , 1978, Biochemistry.

[15]  K. Simons,et al.  The differential miscibility of lipids as the basis for the formation of functional membrane rafts. , 1998, Biochimica et biophysica acta.

[16]  M. Angelova,et al.  Preparation of giant vesicles by external AC electric fields. Kinetics and applications , 1992 .

[17]  W. van Osdol,et al.  Relaxation dynamics of the gel to liquid-crystalline transition of phosphatidylcholine bilayers. Effects of chainlength and vesicle size. , 1991, Biophysical journal.

[18]  R. Rigler,et al.  The standard deviation in fluorescence correlation spectroscopy. , 2001, Biophysical journal.

[19]  T. Heimburg,et al.  Domain Size and Fluctuations at Domain Interfaces in Lipid Mixtures , 2005 .

[20]  T. Heimburg,et al.  Histogram method to obtain heat capacities in lipid monolayers, curved bilayers, and membranes containing peptides. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[21]  J. Korlach,et al.  Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  P. Saffman,et al.  Brownian motion in biological membranes. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[23]  O. Mouritsen Self-assembly and organization of lipid-protein membranes , 1998 .

[24]  M. Edidin The state of lipid rafts: from model membranes to cells. , 2003, Annual review of biophysics and biomolecular structure.

[25]  E. Sackmann,et al.  On two-dimensional passive random walk in lipid bilayers and fluid pathways in biomembranes , 1979, The Journal of Membrane Biology.

[26]  G. A. Blab,et al.  Single-molecule imaging of l-type Ca(2+) channels in live cells. , 2001, Biophysical journal.

[27]  M. Saxton,et al.  Lateral diffusion in a mixture of mobile and immobile particles. A Monte Carlo study. , 1990, Biophysical journal.

[28]  T. Heimburg,et al.  Relaxation kinetics of lipid membranes and its relation to the heat capacity. , 2002, Biophysical journal.

[29]  T. E. Thompson,et al.  Monte Carlo simulation of two-component bilayers: DMPC/DSPC mixtures. , 1999, Biophysical journal.

[30]  J. Tabony,et al.  Quasielastic neutron scattering measurements of fast local translational diffusion of lipid molecules in phospholipid bilayers. , 1991, Biochimica et biophysica acta.

[31]  D. Brown,et al.  Functions of lipid rafts in biological membranes. , 1998, Annual review of cell and developmental biology.

[32]  W. Webb,et al.  Molecular dynamics in living cells observed by fluorescence correlation spectroscopy with one- and two-photon excitation. , 1999, Biophysical journal.

[33]  M. Saxton,et al.  Lateral diffusion in an archipelago. Single-particle diffusion. , 1993, Biophysical journal.

[34]  S. Singer,et al.  The Fluid Mosaic Model of the Structure of Cell Membranes , 1972, Science.

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

[36]  M. Saxton,et al.  Single-particle tracking: effects of corrals. , 1995, Biophysical journal.

[37]  W. Steubing,et al.  Zur Theorie der Brownschen Bewegung , 1908 .

[38]  Kai Simons,et al.  Lipid Domain Structure of the Plasma Membrane Revealed by Patching of Membrane Components , 1998, The Journal of cell biology.

[39]  J. Korlach,et al.  Fluorescence correlation spectroscopy with single-molecule sensitivity on cell and model membranes. , 1999, Cytometry.

[40]  D. Bruns,et al.  SNAREs are concentrated in cholesterol‐dependent clusters that define docking and fusion sites for exocytosis , 2001, The EMBO journal.

[41]  K. Jacobson,et al.  Single-particle tracking: applications to membrane dynamics. , 1997, Annual review of biophysics and biomolecular structure.

[42]  A. Einstein Über die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen [AdP 17, 549 (1905)] , 2005, Annalen der Physik.

[43]  Werner Baumgartner,et al.  Characterization of Photophysics and Mobility of Single Molecules in a Fluid Lipid Membrane , 1995 .

[44]  W. van Osdol,et al.  Measuring the kinetics of membrane phase transitions. , 1989, Journal of biochemical and biophysical methods.

[45]  R. Rigler,et al.  Fluorescence correlation spectroscopy with high count rate and low background: analysis of translational diffusion , 1993, European Biophysics Journal.

[46]  J. Lakowicz Topics in fluorescence spectroscopy , 2002 .

[47]  T. Bjørnholm,et al.  Nanometre-scale structure of fluid lipid membranes , 2000 .

[48]  H Schindler,et al.  Single-molecule microscopy on model membranes reveals anomalous diffusion. , 1997, Biophysical journal.

[49]  T. Bjørnholm,et al.  Critical phenomena: Fluctuations caught in the act , 2000, Nature.

[50]  G. Feigenson,et al.  Ternary phase diagram of dipalmitoyl-PC/dilauroyl-PC/cholesterol: nanoscopic domain formation driven by cholesterol. , 2001, Biophysical journal.

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

[52]  W. Webb,et al.  Thermodynamic Fluctuations in a Reacting System-Measurement by Fluorescence Correlation Spectroscopy , 1972 .

[53]  Michael J. Saxton,et al.  Chapter 8 Lateral Diffusion of Lipids and Proteins , 1999 .

[54]  E. Sackmann,et al.  Molecular dynamics of lipid bilayers studied by incoherent quasi-elastic neutron scattering , 1992 .

[55]  N. Thompson,et al.  Fluorescence Correlation Spectroscopy , 2002 .

[56]  I. Sugár,et al.  Monte Carlo simulations of membranes: phase transition of small unilamellar dipalmitoylphosphatidylcholine vesicles. , 1994, Methods in enzymology.

[57]  M. Sperotto,et al.  Theory of protein-induced lateral phase separation in lipid membranes , 1989, Cell Biophysics.

[58]  P. L’Ecuyer,et al.  Random Numbers , 2001 .

[59]  K. Jørgensen,et al.  Nonequilibrium Lipid Domain Growth in the Gel−Fluid Two-Phase Region of a DC16PC−DC22PC Lipid Mixture Investigated by Monte Carlo Computer Simulation, FT-IR, and Fluorescence Spectroscopy , 2000 .

[60]  Lee,et al.  Finite-size scaling and Monte Carlo simulations of first-order phase transitions. , 1991, Physical review. B, Condensed matter.

[61]  Watt W. Webb,et al.  Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension , 2003, Nature.

[62]  M. Saxton,et al.  Anomalous subdiffusion in fluorescence photobleaching recovery: a Monte Carlo study. , 2001, Biophysical journal.

[63]  T. E. Thompson,et al.  Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis. , 1992, Biochemistry.

[64]  E Gratton,et al.  Two-photon fluorescence microscopy observation of shape changes at the phase transition in phospholipid giant unilamellar vesicles. , 1999, Biophysical journal.

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

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

[67]  Simon L. Peyton Jones,et al.  Haskell 98 Libraries: Random Numbers , 2003, J. Funct. Program..

[68]  K. Jacobson,et al.  Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis. , 1995, Biophysical journal.

[69]  E Gratton,et al.  A correlation between lipid domain shape and binary phospholipid mixture composition in free standing bilayers: A two-photon fluorescence microscopy study. , 2000, Biophysical journal.

[70]  M. Bloom,et al.  Mattress model of lipid-protein interactions in membranes. , 1984, Biophysical journal.

[71]  M. Saxton,et al.  Lateral diffusion in an archipelago. Dependence on tracer size. , 1993, Biophysical journal.

[72]  William H. Press,et al.  Numerical recipes in C , 2002 .

[73]  W. Vaz,et al.  Microscopic versus macroscopic diffusion in one-component fluid phase lipid bilayer membranes. , 1991, Biophysical journal.

[74]  O. G. Mouritsen,et al.  Micro-, nano- and meso-scale heterogeneity of lipid bilayers and its influence on macroscopic membrane properties. , 1995, Molecular membrane biology.

[75]  A. Shevchenko,et al.  Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[76]  E. Sackmann,et al.  Hydration dependence of chain dynamics and local diffusion in L-alpha-dipalmitoylphosphtidylcholine multilayers studied by incoherent quasi-elastic neutron scattering. , 1995, Biophysical journal.

[77]  G. Lindblom,et al.  Lateral diffusion of cholesterol and dimyristoylphosphatidylcholine in a lipid bilayer measured by pulsed field gradient NMR spectroscopy. , 2002, Biophysical journal.

[78]  M. Eigen,et al.  Sorting single molecules: application to diagnostics and evolutionary biotechnology. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[79]  M. Saxton Anomalous diffusion due to obstacles: a Monte Carlo study. , 1994, Biophysical journal.

[80]  W. K. Chan,et al.  Fast diffusion along defects and corrugations in phospholipid P beta, liquid crystals. , 1983, Biophysical journal.

[81]  E Gratton,et al.  Two photon fluorescence microscopy of coexisting lipid domains in giant unilamellar vesicles of binary phospholipid mixtures. , 2000, Biophysical journal.

[82]  H. Qian,et al.  Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. , 1991, Biophysical journal.

[83]  A. Lee,et al.  Lipid phase transitions and phase diagrams. I. Lipid phase transitions. , 1977, Biochimica et biophysica acta.

[84]  W. Webb,et al.  Focal volume optics and experimental artifacts in confocal fluorescence correlation spectroscopy. , 2002, Biophysical journal.

[85]  G. Schütz,et al.  Free Brownian motion of individual lipid molecules in biomembranes. , 1999, Biophysical journal.

[86]  T. E. Thompson,et al.  Fluid phase connectivity in an isomorphous, two-component, two-phase phosphatidylcholine bilayer. , 1990, Biophysical journal.

[87]  P. Gennes Book reviewPhysics of complex and supramolecular fluids: Edited by S. Safran and N. Clark. Wiley, New York, 1987. 720 pp. $49.95 , 1988 .

[88]  R. Glauber Time‐Dependent Statistics of the Ising Model , 1963 .

[89]  W. Vaz,et al.  Chapter 6 - Lateral Diffusion in Membranes , 1995 .

[90]  M. Saxton,et al.  Lateral diffusion in an archipelago. The effect of mobile obstacles. , 1987, Biophysical journal.

[91]  H Schindler,et al.  Imaging of single molecule diffusion. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[92]  T. E. Thompson,et al.  Lateral diffusion and percolation in two-phase, two-component lipid bilayers. Topology of the solid-phase domains in-plane and across the lipid bilayer. , 1992, Biochemistry.

[93]  T. Heimburg Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry. , 1998, Biochimica et biophysica acta.