Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1998 Jan;74(1):319–327. doi: 10.1016/S0006-3495(98)77789-6

Permeation of halide anions through phospholipid bilayers occurs by the solubility-diffusion mechanism.

S Paula 1, A G Volkov 1, D W Deamer 1
PMCID: PMC1299384  PMID: 9449332

Abstract

Two alternative mechanisms are frequently used to describe ionic permeation of lipid bilayers. In the first, ions partition into the hydrophobic phase and then diffuse across (the solubility-diffusion mechanism). The second mechanism assumes that ions traverse the bilayer through transient hydrophilic defects caused by thermal fluctuations (the pore mechanism). The theoretical predictions made by both models were tested for halide anions by measuring the permeability coefficients for chloride, bromide, and iodide as a function of bilayer thickness, ionic radius, and sign of charge. To vary the bilayer thickness systematically, liposomes were prepared from monounsaturated phosphatidylcholines (PC) with chain lengths between 16 and 24 carbon atoms. The fluorescent dye MQAE (N-(ethoxycarbonylmethyl)-6-methoxyquinolinium bromide) served as an indicator for halide concentration inside the liposomes and was used to follow the kinetics of halide flux across the bilayer membranes. The observed permeability coefficients ranged from 10(-9) to 10(-7) cm/s and increased as the bilayer thickness was reduced. Bromide was found to permeate approximately six times faster than chloride through bilayers of identical thickness, and iodide permeated three to four times faster than bromide. The dependence of the halide permeability coefficients on bilayer thickness and on ionic size were consistent with permeation of hydrated ions by a solubility-diffusion mechanism rather than through transient pores. Halide permeation therefore differs from that of a monovalent cation such as potassium, which has been accounted for by a combination of the two mechanisms depending on bilayer thickness.

Full Text

The Full Text of this article is available as a PDF (101.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Deamer D. W., Nichols J. W. Proton flux mechanisms in model and biological membranes. J Membr Biol. 1989 Feb;107(2):91–103. doi: 10.1007/BF01871715. [DOI] [PubMed] [Google Scholar]
  2. Dilger J. P., McLaughlin S. G., McIntosh T. J., Simon S. A. The dielectric constant of phospholipid bilayers and the permeability of membranes to ions. Science. 1979 Dec 7;206(4423):1196–1198. doi: 10.1126/science.228394. [DOI] [PubMed] [Google Scholar]
  3. Elamrani K., Blume A. Effect of the lipid phase transition on the kinetics of H+/OH- diffusion across phosphatidic acid bilayers. Biochim Biophys Acta. 1983 Jan 5;727(1):22–30. doi: 10.1016/0005-2736(83)90364-4. [DOI] [PubMed] [Google Scholar]
  4. Flewelling R. F., Hubbell W. L. Hydrophobic ion interactions with membranes. Thermodynamic analysis of tetraphenylphosphonium binding to vesicles. Biophys J. 1986 Feb;49(2):531–540. doi: 10.1016/S0006-3495(86)83663-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Flewelling R. F., Hubbell W. L. The membrane dipole potential in a total membrane potential model. Applications to hydrophobic ion interactions with membranes. Biophys J. 1986 Feb;49(2):541–552. doi: 10.1016/S0006-3495(86)83664-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Franklin J. C., Cafiso D. S. Internal electrostatic potentials in bilayers: measuring and controlling dipole potentials in lipid vesicles. Biophys J. 1993 Jul;65(1):289–299. doi: 10.1016/S0006-3495(93)81051-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gutknecht J., Graves J. S., Tosteson D. C. Electrically silent anion transport through lipid bilayer membranes containing a long-chain secondary amine. J Gen Physiol. 1978 Mar;71(3):269–284. doi: 10.1085/jgp.71.3.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hauser H., Oldani D., Phillips M. C. Mechanism of ion escape from phosphatidylcholine and phosphatidylserine single bilayer vesicles. Biochemistry. 1973 Oct 23;12(22):4507–4517. doi: 10.1021/bi00746a032. [DOI] [PubMed] [Google Scholar]
  9. Lewis B. A., Engelman D. M. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J Mol Biol. 1983 May 15;166(2):211–217. doi: 10.1016/s0022-2836(83)80007-2. [DOI] [PubMed] [Google Scholar]
  10. Nagle J. F., Scott H. L., Jr Lateral compressibility of lipid mono- and bilayers. Theory of membrane permeability. Biochim Biophys Acta. 1978 Nov 2;513(2):236–243. doi: 10.1016/0005-2736(78)90176-1. [DOI] [PubMed] [Google Scholar]
  11. Neumcke B., Läuger P. Nonlinear electrical effects in lipid bilayer membranes. II. Integration of the generalized Nernst-Planck equations. Biophys J. 1969 Sep;9(9):1160–1170. doi: 10.1016/S0006-3495(69)86443-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Nicholls P., Miller N. Chloride diffusion from liposomes. Biochim Biophys Acta. 1974 Jul 31;356(2):184–198. doi: 10.1016/0005-2736(74)90282-x. [DOI] [PubMed] [Google Scholar]
  13. Parsegian A. Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems. Nature. 1969 Mar 1;221(5183):844–846. doi: 10.1038/221844a0. [DOI] [PubMed] [Google Scholar]
  14. Paula S., Volkov A. G., Van Hoek A. N., Haines T. H., Deamer D. W. Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J. 1996 Jan;70(1):339–348. doi: 10.1016/S0006-3495(96)79575-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Small D. M. Phase equilibria and structure of dry and hydrated egg lecithin. J Lipid Res. 1967 Nov;8(6):551–557. [PubMed] [Google Scholar]
  16. Toyoshima Y., Thompson T. E. Chloride flux in bilayer membranes: chloride permeability in aqueous dispersions of single-walled, bilayer vesicles. Biochemistry. 1975 Apr 8;14(7):1525–1531. doi: 10.1021/bi00678a028. [DOI] [PubMed] [Google Scholar]
  17. Verkman A. S. Development and biological applications of chloride-sensitive fluorescent indicators. Am J Physiol. 1990 Sep;259(3 Pt 1):C375–C388. doi: 10.1152/ajpcell.1990.259.3.C375. [DOI] [PubMed] [Google Scholar]
  18. Verkman A. S., Sellers M. C., Chao A. C., Leung T., Ketcham R. Synthesis and characterization of improved chloride-sensitive fluorescent indicators for biological applications. Anal Biochem. 1989 May 1;178(2):355–361. doi: 10.1016/0003-2697(89)90652-0. [DOI] [PubMed] [Google Scholar]
  19. Verkman A. S., Takla R., Sefton B., Basbaum C., Widdicombe J. H. Quantitative fluorescence measurement of chloride transport mechanisms in phospholipid vesicles. Biochemistry. 1989 May 16;28(10):4240–4244. doi: 10.1021/bi00436a018. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES