Skip to main content
Log in

Continuum theory of lipid bilayer electrostatics

  • Regular Article
  • Published:
The European Physical Journal E Aims and scope Submit manuscript

Abstract

In order to address the concerns about the applicability of the continuum theory of lipid bilayers, we generalize it by including a film with uniaxial dielectric properties representing the polar head groups of the lipid molecules. As a function of the in-plane dielectric constant \( \kappa_{{\Vert}}^{}\) of this film, we encounter a sequence of different phases. For low values of \( \kappa_{{\Vert}}^{}\) , transmembrane pores have aqueous cores, ions are repelled by the bilayer, and the ion permeability of the bilayer is independent of the ion radius as in the existing theory. For increasing \( \kappa_{{\Vert}}^{}\) , a threshold is reached --of the order of the dielectric constant of water-- beyond which ions are attracted to the lipid bilayer by generic polarization attraction, transmembrane pores collapse, and the ion permeability becomes sensitively dependent on the ion radius, results that are more consistent with experimental and numerical studies of the interaction of ions with neutral lipid bilayers. At even higher values of \( \kappa_{{\Vert}}^{}\) , the ion/pore complexes are predicted to condense in the form of extended arrays. The generalized continuum theory can be tested quantitatively by studies of the ion permeability as a function of salt concentration and co-surfactant concentration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. A. Parsegian, Nature 221, 844 (1969); J.P. Dilger, S.G.A. McLaughlin, T.J. McIntosh, S.A. Simon, Science, 206, 1196 (1979).

    Article  ADS  Google Scholar 

  2. Continuum theory overestimates the Born barrier for small ions because it does not properly include the energy cost associated with the loss of the hydration shell when an ion is placed in a lipid environment.

  3. A. Finkelstein, Water Movement Through Lipid Bilayers, Pores, and Plasma Membranes: Theory and Reality (Wiley Interscience, New York, 1987).

    Google Scholar 

  4. R. Benz, P. Läuger, Biochem. Biophys. Acta 468, 245 (1977).

    Article  Google Scholar 

  5. H. Hauser, D. Oldani, M.C. Phillips, Biochemistry. 12, 4507 (1973).

    Article  Google Scholar 

  6. C. Taupin, M. Dvolaitzky, C. Sauterey, Biochemistry, 14, 4771 (1975); J.F. Nagle, H.L. Scott, Biochim. Biophys. Acta 513, 236 (1978).

    Article  Google Scholar 

  7. S. Paula, A.G. Volkov, A.N. Van Hoek, T.H. Haines, D.W. Deamer, Biophys. J. 70, 339 (1996).

    Article  Google Scholar 

  8. F. Bordi, C. Cametti, A. Naglieri, Biophys. J. 74, 1358 (1998).

    Article  ADS  Google Scholar 

  9. M. Pavlin, D. Miklav, Bioelectrochemistry. Epub (2008).

  10. V. Knecht, S.J. Marrink, Biophys. J. 92, 4254 (2007).

    Article  ADS  Google Scholar 

  11. A.A. Gurtovenko, O.I. Onike, J. Anwar, Langmuir. 24, 9656 (2008).

    Article  Google Scholar 

  12. A charge q in an aqueous medium with dielectric constant ϰ W near a dielectric slab with dielectric constant ϰ L is subject to a repulsive image-charge interaction with an effective image-charge q(κ Wϰ L / ϰ L+ϰ W).

  13. S.A. Tatulian, Eur. J. Biochem. 170, 413 (1987); the binding energy follows a Hofmeister Series (e.g., monovalent anions bind to DPPC with binding affinities that can be ordered as NO3− < I < SCN < ClO4−).

    Article  Google Scholar 

  14. L.J. Lis, V.A. Parsegian, R.P. Rand, Biochemistry. 20, 1761 (1981); L.J. Lis, W.T. Lis, V.A. Parsegian, R.P. Rand, Biochemistry 20, 1771 (1981).

    Article  Google Scholar 

  15. R. Zidovetzki, A.W. Atiya, H. De Boeck, Membr. Biochem. 8, 177 (1989).

    Article  Google Scholar 

  16. J.R. Rydall, P.M. Macdonald, Biochemistry 31, 1092 (1992).

    Article  Google Scholar 

  17. J. Sachs et al., Biophys. J. 86, 3772 (2004).

    Article  ADS  Google Scholar 

  18. A. Raudino, D. Mauzerall, Biophys. J. 50, 441 (1986).

    Article  ADS  Google Scholar 

  19. H.A. Stern, S.E. Feller, J. Chem. Phys. 118, 3401 (2003).

    Article  ADS  Google Scholar 

  20. H. Nymeyer, H.X. Zhou, Biophys. J. 94, 1185 (2008).

    Article  Google Scholar 

  21. O.S. Andersen, Membrane Transport in Biology, edited by G. Giebish, Vol. I (Springer, New York, 1978), p. 349.

    Google Scholar 

  22. For a discussion: P. Shuskov et al., Langmuir 24, 4615 (2008).

    Article  Google Scholar 

  23. U. Kaatze et al., J. Phys. Chem. 89, 2565 (1989).

    Article  Google Scholar 

  24. P. Yeagle, Acc. Chem. Res. 11, 321 (1978).

    Article  Google Scholar 

  25. L. Hari, A.E. Mark, S.-J. Marrink, Biophys. J. 92, 4209 (2007).

    Article  Google Scholar 

  26. A.A. Gurtovenko, I. Vattulainen, J. Am. Chem. Soc. 127, 17570 (2005); Biophys. J. 92, 1878 (2007).

    Article  Google Scholar 

  27. NMR studies such as those of D.I. Semchyschyn, P.M. Macdonald, Magn. Res. Chem. 42, 89 (2004) indicate that charges imbedded in lipid bilayers can alter the angle between the head group and the layer normal. This is an important non-linear effect not included in the present description.

    Article  Google Scholar 

  28. This is obtained from the capacitive self-energy of a charged prolate ellipsoidal conductor given in L. Landau, E. Lifshitz, Electrodynamics of Continuous Media (Pergamom, Oxford, 1975), Eq. 4.18, and then relating this result to the self-energy of a charged spherical conductor placed in a uniaxial dielectric medium by simple scaling arguments.

    Google Scholar 

  29. Numerical simulations of cations associating with neutral lipid bilayers report a peak in the density profile at the water/lipid-head-group interface: A. Cordomi, O. Erdholm, J. Perez, J. Phys. Chem. 112, 1401 (2008).

    Google Scholar 

  30. W. Helfrich, Phys. Lett. A 50, 115 (1974).

    Article  ADS  Google Scholar 

  31. F.Y. Jiang, Y. Bouret, J.T. Kindt, Biophys. J. 87, 182 (2004).

    Article  ADS  Google Scholar 

  32. J. Zhang, A. Kamenev, B.I. Shklovskii, Phys. Rev. Lett. 95, 148101 (2005).

    Article  ADS  Google Scholar 

  33. A. Kamenev, J. Zhang, A.I. Larkin, B.I. Shklovskii, Physica A 359, 129 (2006).

    Article  ADS  Google Scholar 

  34. F.Y. Jiang, Y. Bouret, J.T. Kindt, Biophys. J. 87, 182 (2004).

    Article  ADS  Google Scholar 

  35. P.H. Puech, N. Borghi, E. Karatekin, F. Brochard-Wyart, Phys. Rev. Lett. 90, 128304 (2003).

    Article  ADS  Google Scholar 

  36. E.J. Mele, Am. J. Phys. 69, 557 (2001).

    Article  ADS  Google Scholar 

  37. B. Neumcke, P. Lauger, Biophys. J. 9, 1160 (1969).

    Article  ADS  Google Scholar 

  38. A.V. Finkelstein, D.N. Ivankov, A.M. Dykhne, http://eprintweb.org/S/authors/All/iv/Ivankov/5.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. F. Bruinsma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gerami, R., Bruinsma, R.F. Continuum theory of lipid bilayer electrostatics. Eur. Phys. J. E 30, 197–204 (2009). https://doi.org/10.1140/epje/i2009-10519-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1140/epje/i2009-10519-2

PACS

Navigation