Summary
Diffusion of small nonelectrolytes through planar lipid bilayer membranes (egg phosphatidylcholine-decane) was examined by correlating the permeability coefficients of 22 solutes with their partition coefficients between water and four organic solvents. High correlations were observed with hexadecane and olive oil (r=0.95 and 0.93), but not octanol and ether (r=0.75 and 0.74). Permeabilities of the seven smallest molecules (mol wt <50) (water, hydrofluoric acid, hydrochloric acid, ammonia, methylamine, formic acid and formamide) were 2- to 15-fold higher than the values predicted by the permeabilities of the larger molecules (50<mol wt<300). The “extra” permeabilities of the seven smallest molecules were not correlated with partition coefficients but were inversely correlated with molecular volumes. The larger solute permeabilities also decreased with increasing molecular volume, but the relationship was neither steep nor significant. The permeability pattern cannot be explained by the molecular volume dependence of partitioning into the bilayer or by the existence of transient aqueous pores. The molecular volume dependence of solute permeability suggests that the membrane barrier behaves more like a polymer than a liquid hydrocarbon. All the data are consistent with the “solubility-diffusion” model, which can explain both the hydrophobicity dependence and the molecular volume dependence of nonelectrolyte permeability.
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References
Amerongen, G.J. van 1964. Diffusion in elastomers.Rubber Chem. Technol. 37:1065–1152
Andersen, O.S. 1978. Permeability properties of unmodified lipid bilayer membranes.In: Membrane Transport in Biology. Vol. I, pp. 369–446. G. Giebisch, D.C. Tosteson, and H.H. Ussing, editors. Spring-Verlag, New York
Antonenko Y.N., Yaguzhinsky, L.S. 1982. Generation of potential in lipid bilayer membranes as a result of proton-transfer reactions in the unstirred layers.J. Bioenerg. Biomembr. 14:457–465
Antonenko, Y.N., Yaguzhinsky, L.S. 1984. The role of pH gradient in the unstirred layers in the transport of weak acids and bases through bilayer lipid membranes.Bioelectrochem. Bioenerg. 13:85–91
Benson, J.R., Hare, P.E. 1975.o-Phthalaldehyde: Fluorogenic detection of primary amines in the picomole ranges. Comparison with fluorescamine and ninhydrin.Proc. Natl. Acad. Sci. USA 72:619–622
Benz, R., McLaughlin, S. 1983. The molecular mechanism of action of the proton ionophore FCCP (carbonylcyanidep-trifluoromethoxyphenylhydrazone).Biophys. J. 41:381–398
Bindslev, N., Wright, E.M. 1976. Effect of temperature on non-electrolyte permeation across the toad urinary bladder.J. Membrane Biol. 29:265–288
Cohen, B.E. 1975a. The permeability of liposomes to nonelectrolytes: I. Activation energies for permeation.J. Membrane Biol. 20:205–234
Cohen, B.E. 1975b. The permeability of liposomes to nonelectrolytes: II. The effect of nystatin and gramicidin A.J. Membrane Biol. 20:235–268
Collander, R. 1949. The permeability of plant protoplasts to small molecules.Physiol. Plant. 2:300–311
Collander, R. 1954. The permeability ofNitella cells to nonelectrolytes.Physiol. Plant. 7:420–445
Diamond, J.M., Katz, Y. 1974. Interpretation of nonelectrolyte partition coefficients between dimyristoyl lecithin and water.J. Membrane Biol. 17:121–154
Diamond, J.M., Wright, E.M. 1969. Biological membranes: The physical basis of ion and nonelectrolyte selectivity.Annu. Rev. Physiol. 31:582–646
Dilger, J., McLaughlin, S. 1979. Proton transport through membranes induced by weak acids: A study of two substituted benzimidazoles.J. Membrane Biol. 46:359–384
Evans, D.F., Tominaga, T., Davis, H.T. 1981. Tracer diffusion in polyatomic liquids.J. Chem. Phys. 74:1298–1305
Fettiplace, R., Haydon, D.A. 1980. Water permeability of lipid membranes.Physiol. Rev. 60:510–550
Finkelstein, A. 1976a. Water and nonelectrolyte permeability of lipid bilayer membranes.J. Gen. Physiol. 68:127–135
Finkelstein, A. 1976b. Nature of the water permeability increase induced by antidiuretic hormone (ADH) in toad urinary bladder.J. Gen. Physiol. 68:137–143
Finkelstein, A. 1977. Reply to a comment on the water permeability through planar lipid bilayers.J. Gen. Physiol. 70:125–127
Gutknecht, J., Tosteson, D.C. 1973. Diffusion of weak acids through lipid bilayer membranes: Effects of chemical reactions in the aqueous unstirred layers.Science 182:1258–1261
Gutknecht, J., Walter, A. 1981a. Transport of protons and hydrochloric acid through lipid bilayer membranes.Biochim. Biophys. Acta 641:183–188
Gutknecht, J., Walter, A. 1981b. Hydrofluoric and nitric acid transport through lipid bilayer membranes.Biochim. Biophys. Acta 644:153–156
Gutknecht, J., Walter, A. 1981c. Histamine, theophylline and tryptamine transport through lipid bilayer membranes.Biochim. Biophys. Acta 649:149–154
Gutknecht, J., Walter, A. 1982. SCN− and HSCN transport through lipid bilayer membranes: A model for SCN− inhibition of gastric acid secretion.Biochim. Biophys. Acta 685:233–240
Hanai, T., Haydon, D.A. 1966. The permeability to water of bimolecular lipid membranes.J. Theoret. Biol. 11:370–382
Hayduk, W., Ioakimidis, S. 1976. Liquid diffusivities in normal paraffin solutions.J. Chem. Eng. Data 21:255–260
Hayduk, W., Laudie, H. 1974. Prediction of diffusion coefficients for nonelectrolytes in dilute aqueous solutions.Am. Inst. Chem. Eng. J. 20:611–615
Hung, G.W.C., Autian, J. 1972. Use of thermal gravimetric analysis in sorption studies: II. Evaluation of diffusivity and solubility of a series of aliphatic alcohols in polyurethan.J. Pharmaceut. Sci. 61:1094–1098
Kimmich, R., Peters, A., Spohn, K.H. 1981. Solubility of oxygen in lecithin bilayers and other hydrocarbon lamellae as a probe for free volume and transport properties.J. Membrane Sci. 9:313–336
Koroleff, F. 1969. Direct determination of ammonia in natural waters as indophenol blue.In: Information on Techniques and Methods for Seawater Analysis. International Council for the Exploration of the Sea. Interlab Report No. 3, pp. 19–22
Leo, A., Hansch, C., Elkins, D. 1971. Partition coefficients and their uses.Chem. Rev. 71:525–616
Lieb, W.R., Stein, W.D. 1969. Biological membranes behave as non-porous polymeric sheets with respect to the diffusion of nonelectrolytes.Nature (London) 224:240–243
Lieb, W.R., Stein, W.D. 1971. The molecular basis of simple diffusion within biological membranes.Curr. Top. Membr. Transp. 2:1–39
Macey, R. 1948. Partition coefficients of fifty compounds between olive oil and water.J. Ind. Hyg. Toxicol. 30:140–143
Miller, K.W., Hammond, L., Porter, E.G. 1977. The solubility of hydrocarbon gases in lipid bilayers.Chem. Phys. Lipids 20:229–241
Morrison, R.T., Boyd, R.N. 1973. Organic Chemistry. (3rd ed.) Allyn & Bacon, Boston
Mueller, P., Rudin, D.O. 1969. Translocators in bimolecular lipid membranes: Their role in dissipative and conservative bioenergy transductions.Curr. Top. Bioenerg. 3:157–249
Orbach, E., Finkelstein, A. 1980. The nonelectrolyte permeability of planar lipid bilayer membranes.J. Gen. Physiol. 75:427–436
Overton, E. 1899. Ueber die allgemeinen osmotischen Eigenschaften der Zelle, ihre vermutlichen Ursachen und ihre Bedeutung fur die Physiologie.Vierteljahrsschr. Naturforsch. Ges. Zuerich 44:88–135
Perry, J.H. (editor) 1963. Chemical Engineer's Handbook. (4th ed.) pp. 14–20. McGraw-Hill, New York
Petersen, D.C. 1983. The water permeability of the monoolein/triolein bilayer membrane.Biochim. Biophys. Acta 734:201–209
Rossi, C., Bianchi, E., Rossi, P. 1958. Mesures de diffusion dans le benzene.J. Chim. Phys. 55:97–101
Roth, M. 1971. Fluorescein reaction for amino acids.Anal. Chem. 43:880–882
Schatzberg, P. 1965. Diffusion of water through hydrocarbon liquids.J. Polym. Sci. Part C. 10:87–92
Schneider, F.L. 1964. Qualitative microanalysis: Cognition and recognition of carbon compounds. Academic Press, New York
Shalafi, R.I. 1981. Permeability for water and other polar molecules.In: Membrane Transport. S.L. Bonting and J.J.H.H.M. de Pont, editors. pp. 29–60. Elsevier/North-Holland Biomedical, New York
Simon, S.A., Gutknecht, J. 1980. Solubility of carbon dioxide in lipid bilayer membranes and organic solvents.Biochim. Biophys. Acta 596:352–358
Simon, S.A., Stone, W.L., Busto-Latorre P. 1977. A thermodynamic study of the partition ofn-hexane into phosphatidylcholine and phosphatidylcholine-cholesterol bilayers.Biochim. Biophys. Acta 468:378–388
Stein, W.D. 1981. Permeability for lipophilic molecules.In: Membrane Transport. S.L. Bonting and J.J.H.H.M. de Pont, editors. pp. 1–28. Elsevier/North-Holland Biomedical, New York
Strickland, J.D.H., Parsons, T.R. (editors) 1972. A Manual of Sea Water analysis. (2nd ed.) Bulletin No. 167. Fisheries Research Board of Canada, Ottawa
Subczynski, W.K., Hyde, J.S. 1984. Diffusion of oxygen in water and hydrocarbons using an electron spin resonance spinlabel technique.Biophys. J. 45:743–748
Sutherland, G.B.B.M. 1905. A dynamical theory of diffusion for nonelectrolytes and the molecular mass of albumin. Philos. Mag. (S. 6)9:781–785
Träuble, H. 1971. The movement of molecules across lipid membranes: A molecular theory.J. Membrane Biol. 4:193–208
Walter, A. 1981. Nonelectrolyte Permeability of Lipid Bilayer Membranes. Ph.D. Thesis. Duke University. University Microfilms, Ann Arbor, Michigan
Walter, A., Gutknecht, J. 1984. Monocarboxylic acid permeation through lipid bilayer membranes.J. Membrane Biol. 77:255–264
Walter, A., Hastings, D., Gutknecht, J. 1982. Weak acid permeability through lipid bilayer membranes: Role of chemical reactions in the unstirred layer.J. Gen. Physiol. 79:917–933
Weaver, J.C., Powell, K.T., Mintzer, R.A., Sloan, S.R., Ling, H. 1984. The diffusive permeability of bilayer membranes: The contribution of transient aqueous pores.Bioelectrochem. Bioenerg. 12:405–412
Wolosin, J.M., Ginsburg, H. 1975. The permeation of organic acids through lecithin bilayers: Resemblance to diffusion in polymers.Biochim. Biophys. Acta 389:20–33
Wolosin, J.M., Ginsburg, H., Lieb, W.R., Stein, W.D. 1978. Diffusion within egg lecithin bilayers resembles that within soft polymers.J. Gen. Physiol. 71:93–100
Wright, E.M., Bindslev, N. 1976. Thermodynamic analysis of nonelectrolyte permeation across the toad urinary bladder.J. Membrane Biol. 29:289–312
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Walter, A., Gutknecht, J. Permeability of small nonelectrolytes through lipid bilayer membranes. J. Membrain Biol. 90, 207–217 (1986). https://doi.org/10.1007/BF01870127
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DOI: https://doi.org/10.1007/BF01870127