Inter-layer slide and stress relaxation in a bilayer fluid membrane in the patch-clamp setting

TL;DR

This paper develops a thermodynamic theory of stress relaxation in bilayer membranes under patch-clamp conditions, explaining experimental adaptation of mechanosensitive channels through lipid redistribution and stress dynamics.

Contribution

It introduces a novel model of lateral stress relaxation in bilayer membranes that accounts for channel adaptation and estimates relevant timescales consistent with experiments.

Findings

Lipid transfer reduces local stress, facilitating adaptation.

Stress relaxation triggers channel closing, explaining adaptation.

Estimated adaptation times are seconds, matching experimental data.

Abstract

Protein mechanosensitive channels (MS) are activated by tension transmitted through the lipid bilayer. We propose a theory of lateral stress relaxation in a bilayer lipid membrane exposed to external pressure pulse in the patch-clamp experimental setting. It is shown that transfer of lipid molecules into a strained region is thermodynamically advantageous due to local decrease of the stress. Considered stress relaxation mechanism may explain recent experimental observations (Davidson and Martinac 2003) of adaptation of MscL, bacterial mechanosensitive channel of large conductance, to sustained membrane stretch. Lateral stress relaxation in the monolayer, which controls the gating of MscL, triggers thermally activated transition of the open channels back to the closed state ("adaptation"). We evaluate the contribution of the hydrophobic mismatch between MS channel and lipid bilayer to the energy barrier separating open and closed states. Then, using the MscL thermodynamic model (Sukharev et. al, 1999), we estimate characteristic adaptation times at room temperature to be of the order of seconds, well in the range of the experimental data (Davidson and Martinac 2003). Estimated propagation time of the initial channel-opening stress over the whole membrane is 4-5 orders of magnitude shorter.