Nonlinear conductance, rectification and mechanosensitive channel formation of lipid membranes

TL;DR

This study explores how lipid membranes exhibit nonlinear conductance and rectification due to electrostrictive effects and spontaneous polarization, revealing mechanisms for channel-like conduction and voltage gating in biological membranes.

Contribution

It introduces a theoretical framework modeling electrostrictive effects and spontaneous polarization to explain nonlinear conductance and rectification in lipid membranes, supported by experimental measurements.

Findings

Lipid membranes show nonlinear I-V profiles with outward rectification.

Conductance involves leak currents and voltage-gated pore opening.

Negative differential conductance observed in certain voltage regimes.

Abstract

There is mounting evidence that lipid bilayers display conductive properties. However, when interpreting the electrical response of biological membranes to voltage changes, they are commonly considered as inert insulators. However, lipid bilayers under voltage-clamp conditions do not only display current traces with discrete conduction-steps indistinguishable from those attributed to the presence of protein channels. In current-voltage (I-V) plots they may also display outward rectification, i.e., voltage-gating. Surprisingly, this has even been observed in chemically symmetric lipid bilayers. Here, we investigate this phenomenon using a theoretical framework that models the electrostrictive effect of voltage on lipid membranes in the presence of a spontaneous polarization, which can be recognized by a voltage offset in electrical measurements. It can arise from an asymmetry of the membrane, for example from a nonzero spontaneous curvature of the membrane. This curvature can be caused by voltage via the flexoelectric effect, or by hydrostatic pressure differences across the membrane. Here, we describe I-V relations for lipid membranes formed at the tip of patch pipettes situated close to an aqueous surface. We measured at different depths relative to air/water surface, resulting in different pressure gradients across the membrane. Both linear and nonlinear I-V profiles were observed. Nonlinear conduction consistently takes the form of outward rectified currents. We explain the conductance properties by two mechanisms: One leak current with constant conductance without pores, and a second process that is due to voltage-gated pore opening correlating with the appearance of channel-like conduction steps. In some instances, these nonlinear I-V relations display a voltage regime in which dI/dV is negative. This has also been previously observed in the presence of sodium channels. ...