Abstract
The nanomechanics of lipid membranes regulates a large number of cellular functions. However, the molecular mechanisms underlying the plastic rupture of individual bilayers remain elusive. This study uses force clamp spectroscopy to capture the force-dependent dynamics of membrane failure on a model diphytanoylphosphatidylcholine multilayer stack, which is devoid of surface effects. The obtained kinetic measurements demonstrate that the rupture of an individual lipid bilayer, occurring in the bilayer parallel plane, is a stochastic process that follows a log-normal distribution, compatible with a pore formation mechanism. Furthermore, the vertical individual force-clamp trajectories, occurring in the bilayer orthogonal bilayer plane, reveal that rupturing process occurs through distinct intermediate mechanical transition states that can be ascribed to the fine chemical composition of the hydrated phospholipid moiety. Altogether, these results provide a first description of unanticipated complexity in the energy landscape governing the mechanically induced bilayer rupture process.
Highlights
The cell membrane, mainly composed of lipid moieties, is an extraordinary robust system that needs to preserve its physical integrity while withstanding chemical, electrical, and mechanical perturbations
This study uses force clamp spectroscopy to capture the force-dependent dynamics of membrane failure on a model diphytanoylphosphatidylcholine multilayer stack, which is devoid of surface effects
Using a novel multibilayer stack approach that avoids the large mechanical effect of the stiff supporting substrate, our experiments using force-clamp spectroscopy provide direct evidence that the membrane rupture reaction occurs through a multistep process in two orthogonal planes
Summary
The nanomechanics of lipid membranes regulates a large number of cellular functions. the molecular mechanisms underlying the plastic rupture of individual bilayers remain elusive. The obtained kinetic measurements demonstrate that the rupture of an individual lipid bilayer, occurring in the bilayer parallel plane, is a stochastic process that follows a log-normal distribution, compatible with a pore formation mechanism. The vertical individual force-clamp trajectories, occurring in the bilayer orthogonal bilayer plane, reveal that rupturing process occurs through distinct intermediate mechanical transition states that can be ascribed to the fine chemical composition of the hydrated phospholipid moiety. These results provide a first description of unanticipated complexity in the energy landscape governing the mechanically induced bilayer rupture process
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