Ion-induced defect permeation of lipid membranes

Igor Vorobyov, Timothy E. Olson, Jung H. Kim, Roger E. Koeppe, Olaf S. Andersen, Toby W. Allen

Research output: Contribution to journalArticle

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Abstract

We have explored the mechanisms of uncatalyzed membrane ion permeation using atomistic simulations and electrophysiological recordings. The solubility-diffusion mechanism of membrane charge transport has prevailed since the 1960s, despite inconsistencies in experimental observations and its lack of consideration for the flexible response of lipid bilayers. We show that direct lipid bilayer translocation of alkali metal cations, Cl-, and a charged arginine side chain analog occurs via an ion-induced defect mechanism. Contrary to some previous suggestions, the arginine analog experiences a large free-energy barrier, very similar to those for Na+, K+, and Cl-. Our simulations reveal that membrane perturbations, due to the movement of an ion, are central for explaining the permeation process, leading to both free-energy and diffusion-coefficient profiles that show little dependence on ion chemistry and charge, despite wide-ranging hydration energies and the membrane's dipole potential. The results yield membrane permeabilities that are in semiquantitative agreement with experiments in terms of both magnitude and selectivity. We conclude that ion-induced defect-mediated permeation may compete with transient pores as the dominant mechanism of uncatalyzed ion permeation, providing new understanding for the actions of a range of membrane-active peptides and proteins.

Original languageEnglish (US)
Pages (from-to)586-597
Number of pages12
JournalBiophysical Journal
Volume106
Issue number3
DOIs
StatePublished - Feb 4 2014

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Membrane Lipids
Ions
Membranes
Lipid Bilayers
Arginine
Alkali Metals
Membrane Potentials
Solubility
Cations
Permeability
Peptides
Proteins

ASJC Scopus subject areas

  • Biophysics

Cite this

Vorobyov, I., Olson, T. E., Kim, J. H., Koeppe, R. E., Andersen, O. S., & Allen, T. W. (2014). Ion-induced defect permeation of lipid membranes. Biophysical Journal, 106(3), 586-597. https://doi.org/10.1016/j.bpj.2013.12.027

Ion-induced defect permeation of lipid membranes. / Vorobyov, Igor; Olson, Timothy E.; Kim, Jung H.; Koeppe, Roger E.; Andersen, Olaf S.; Allen, Toby W.

In: Biophysical Journal, Vol. 106, No. 3, 04.02.2014, p. 586-597.

Research output: Contribution to journalArticle

Vorobyov, I, Olson, TE, Kim, JH, Koeppe, RE, Andersen, OS & Allen, TW 2014, 'Ion-induced defect permeation of lipid membranes', Biophysical Journal, vol. 106, no. 3, pp. 586-597. https://doi.org/10.1016/j.bpj.2013.12.027
Vorobyov I, Olson TE, Kim JH, Koeppe RE, Andersen OS, Allen TW. Ion-induced defect permeation of lipid membranes. Biophysical Journal. 2014 Feb 4;106(3):586-597. https://doi.org/10.1016/j.bpj.2013.12.027
Vorobyov, Igor ; Olson, Timothy E. ; Kim, Jung H. ; Koeppe, Roger E. ; Andersen, Olaf S. ; Allen, Toby W. / Ion-induced defect permeation of lipid membranes. In: Biophysical Journal. 2014 ; Vol. 106, No. 3. pp. 586-597.
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