Counterion release in membrane-biopolymer interactions

Daniel Harries, Sylvio May*, Avinoam Ben-Shaul

*Corresponding author for this work

Research output: Contribution to journalReview articlepeer-review

39 Scopus citations

Abstract

When two oppositely charged macroions are brought into contact, a large fraction of the mobile counterions that previously surrounded each isolated macromolecule is released into the bulk solution, thereby increasing the counterions' translational entropy. The entropy gain associated with this counterion release mechanism is the driving force for various macroion binding processes, such as protein-membrane, protein-DNA, and DNA-membrane complexation. In this review we focus on the role of counterion release in the interaction between charged macromolecules and oppositely charged lipid membranes. The electrostatic interaction is generally coupled to other degrees of freedom of the membrane, or of the adsorbed macroion. Thus, for example, when a basic protein adsorbs onto a binary fluid membrane comprising anionic and neutral lipids then, in addition to the release of the mobile counterions to the bulk solution, the protein polarizes the membrane composition by attracting the charged lipids to its immediate vicinity. This process, which enhances the electrostatic attraction, is partly hampered by the concomitant loss of two-dimensional (2D) lipid mixing entropy, so that the resulting lipid distribution reflects the balance between these opposing tendencies. In membranes containing both monovalent and multivalent lipids, as is often the case with biological membranes, the peripheral protein preferentially interacts with (and thus immobilizes) the multivalent lipids, because a smaller number of these lipids are needed to neutralize its charge. The monovalent "counterlipids" are thus free to translate in the remaining area of the membrane. This entropy-driven counterlipid release mechanism in 2D is analogous to the extensively studied phenomenon of DNA condensation by polyvalent cations in 3D. Being self-assembled fluid aggregates, lipid bilayers can respond to interactions with peripheral or integral (whether charged or neutral) macromolecules in various ways. Of particular interest in this review is the interplay between electrostatic interactions, the lipid composition degrees of freedom mentioned above, and the membrane curvature elasticity, as will be discussed in some detail in the context of the thermodynamic stability and phase behavior of lipid-DNA complexes (also known as "lipoplexes") . This article is primarily theoretical, but the systems and phenomena considered are directly related to and motivated by specific experiments. The theoretical modeling is generally based on mean-field level approaches, specifically the Poisson-Boltzmann theory for electrostatic interactions, sometimes in conjunction with coarse grained computer simulations.

Original languageAmerican English
Pages (from-to)9268-9284
Number of pages17
JournalSoft Matter
Volume9
Issue number39
DOIs
StatePublished - 21 Oct 2013

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