Rupture of a Biomembrane under Dynamic Surface Tension

TL;DR

This paper develops a theoretical framework to describe membrane rupture under dynamic surface tension, successfully reproducing experimental observations and providing insights into rupture kinetics and membrane stability.

Contribution

The authors introduce a formal analytical model for membrane rupture under dynamic tension, incorporating pore formation and Brownian pore growth, applicable to various membrane disruption processes.

Findings

Simulations match experimental rupture data

Membrane lifetime depends on pore nucleation rate and tension loading

Model captures pore nucleation and growth dynamics

Abstract

How long a fluid membrane vesicle stressed with a steady ramp of micropipette last before rupture? Or conversely, how high the surface tension should be to rupture a membrane? To answer these challenging questions we have developed a theoretical framework that allows description and reproduction of Dynamic Tension Spectroscopy (DTS) observations. The kinetics of the membrane rupture under ramps of surface tension is described as a combination of initial pore formation followed by Brownian process of the pore radius crossing the time-dependent energy barrier. We present the formalism and derive (formal) analytical expression of the survival probability describing the fate of the membrane under DTS conditions. Using numerical simulations for the membrane prepared in an initial state with a given distribution of times for pore nucleation, we have studied the membrane lifetime (or inverse of rupture rate) and distribution of membrane surface tension at rupture as a function of membrane characteristics like pore nucleation rate, the energy barrier to failure and tension loading rate. It is found that simulations reproduce main features of the experimental data, particularly, the pore nucleation and pore size diffusion controlled limits of membrane rupture dynamics. This approach can also be applied to processes of permeation and pore opening in membranes (electroporation, membrane disruption by antimicrobial peptides, vesicle fusion).