On two-dimensional passive random walk in lipid bilayers and fluid pathways in biomembranes

SummaryThe lateral mobility of pyrene, pyrene decanoic acid, and 1-palmitoyl-2-pyrene decanoyl-phosphatidyl choline (pyrene lecithin) in lipid bilayers is determined by the excimer formation technique. This method is applied to vesicles of lecithins differing in chain length and in the degree of saturation of the hydrocarbon chains. These values are compared with results in cephalins of different chain length and in dipalmitoyl phosphatidic acid at variable pH. The influence of cholesterol is investigated. The results are analyzed in terms of the Montroll model of two-dimensional random walk. The jump frequency of the probe molecule within the lipid lattice is obtained. The advantage of this measure of transport in lipid layers is that it does not involve lipid lattice parameters.The main results of the present work are: (i) The lateral mobility of a given solute molecule in lamellae of saturated lecithins is independent of hydrocarbon chain length and rather a universal function of temperature. (ii) In unsaturated dioleyl lecithin the amphiphatic molecules have lateral mobilities of the same size as in saturated lipids. The jump frequency of pyrene, however, is by a factor of two larger in the unsaturated lecithin. (iii) The jump frequencies in phosphatidyl ethanolamines are about equal to those in lecithins. (iv) In phosphatidic acid layers the hopping frequencies depend on the chargers of the head groups of both the lipids and the probes. (v) Cholesterol strongly reduces the jump frequency in fluid layers. (vi) The lateral mobility in biological membranes is comparable to that in artificial lipid bilayers.The experimental results are discussed in terms of the free volume model of diffusion in fluids. Good agreement with the predictions made from this model is found. A striking result is the observation of a tilt in dioleyl-lecithin bilayer membranes from the hopping frequencies of pyrene and pyrene lecithin. A tilt angle of ϕ-17° is estimated.

[1]  G M Edelman,et al.  Surface modulation in cell recognition and cell growth. , 1976, Science.

[2]  David Turnbull,et al.  Molecular Transport in Liquids and Glasses , 1959 .

[3]  M. Raff,et al.  Redistribution and pinocytosis of lymphocyte surface immunoglobulin molecules induced by anti-immunoglobulin antibody. , 1971, Nature: New biology.

[4]  J. Behr,et al.  Methods for probing lateral diffusion of membrane components: triplet—triplet annihilation and triplet—triplet energy transfer , 1974 .

[5]  W. Webb,et al.  Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. , 1976, Biophysical journal.

[6]  K. Jacobson,et al.  Lateral diffusion in phospholipid multibilayers measured by fluorescence recovery after photobleaching. , 1977, Biochemistry.

[7]  H. Träuble,et al.  The movement of molecules across lipid membranes: A molecular theory , 1971, The Journal of Membrane Biology.

[8]  E. Sackmann,et al.  Local measurement of lateral motion in erythrocyte membranes by photobleaching technique. , 1980, Biochimica et biophysica acta.

[9]  Th. Förster,et al.  Untersuchungen zum Konzentrationsumschlag der Fluoreszenz des Pyrens , 1965 .

[10]  E. Sackmann,et al.  Lateral diffusion, protein mobility, and phase transitions in Escherichia coli membranes. A spin label study. , 1973, Biochemistry.

[11]  E. Sackmann,et al.  Polymorphism of phospholipid monolayers , 1978 .

[12]  GEOFFREY TAYLOR,et al.  Aeronautics before 1919 , 1971, Nature.

[13]  I. H. Munro,et al.  'Excimer’ fluorescence II. Lifetime studies of pyrene solutions , 1963, Proceedings of the Royal Society of London. Series A. Mathematical and Physical Sciences.

[14]  P. Fahey,et al.  Lateral diffusion in planar lipid bilayers. , 1977, Science.

[15]  E. Sackmann,et al.  Chemically induced phase separation in mixed vesicles containing phosphatidic acid. An optical study. , 1975, Journal of the American Chemical Society.

[16]  W. Webb,et al.  Diffusion and patching of macromolecules on planar lipid bilayer membranes. , 1977, Biochemistry.

[17]  DONOR FLUORESCENCE AS A PROBE OF ENERGY TRANSFER*,† , 1968, Photochemistry and photobiology.

[18]  E. Sackmann,et al.  Studies of the crystalline-liquid crystalline phase transition of lipid model membranes. I. Use of spin labels and optical probes as indicators of the phase transition. , 1972, Journal of the American Chemical Society.

[19]  C. Scandella,et al.  Rapid lateral diffusion of phospholipids in rabbit sarcoplasmic reticulum. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[20]  E. Sackmann,et al.  Studies of the crystalline-liquid crystalline phase transition of lipid model membranes. 3. Structure of a steroid-lecithin system below and above the lipid-phase transition. , 1972, Journal of the American Chemical Society.

[21]  G. Entine,et al.  Lateral Diffusion of Visual Pigment in Photoreceptor Disk Membranes , 1974, Science.

[22]  E. Montroll Random walks on lattices , 1969 .

[23]  D. Marsh An interacting spin label study of lateral expansion in dipalmitoyllecithin-cholesterol bilayers. , 1974, Biochimica et biophysica acta.

[24]  E. Sackmann,et al.  Lateral diffusion in the hydrophobic region of membranes: use of pyrene excimers as optical probes. , 1974, Biochimica et biophysica acta.

[25]  E. Sackmann,et al.  Spin labels as enzyme substrates. Heterogeneous lipid distribution in liver microsomal membranes. , 1973, Biochimica et biophysica acta.

[26]  H. Möhwald,et al.  Monitoring the location profile of fluorophores in phosphatidylcholine bilayers by the use or paramagnetic quenching. , 1979, Biochimica et biophysica acta.

[27]  A. Keith,et al.  Viscosity of Cellular Protoplasm , 1974, Science.

[28]  Elliott W. Montroll,et al.  Random Walks on Lattices. III. Calculation of First‐Passage Times with Application to Exciton Trapping on Photosynthetic Units , 1969 .

[29]  P. Devaux,et al.  Lateral diffusion in spin-labeled phosphatidylcholine multilayers. , 1972, Journal of the American Chemical Society.

[30]  E. Sackmann On the Application of Excimers as Optical Probes in Membrane Research , 1976 .

[31]  R. Peters,et al.  A microfluorimetric study of translational diffusion in erythrocyte membranes. , 1974, Biochimica et biophysica acta.

[32]  H. Galla,et al.  Transversal mobility in bilayer membrane vesicles: Use of pyrene lecithin as optical probe , 1979 .