Curvature-Assisted Vesicle Explosion Under Light-Induced Asymmetric Oxidation.

Exposure of cell membranes to reactive oxygen species can cause oxidation of membrane lipids. Oxidized lipids undergo drastic conformational changes, compromising the mechanical integrity of the membrane and causing cell death. For giant unilamellar vesicles, a classic cell mimetic system, a range of mechanical responses under oxidative assault has been observed including formation of nanopores, transient micron-sized pores, and total sudden catastrophic collapse (i.e., explosion). However, the physical mechanism regarding how lipid oxidation causes vesicles to explode remains elusive. Here, with light-induced asymmetric oxidation experiments, the role of spontaneous curvature on vesicle instability and its link to the conformational changes of oxidized lipid products is systematically investigated. A comprehensive membrane model is proposed for pore-opening dynamics incorporating spontaneous curvature and membrane curling, which captures the experimental observations well. The kinetics of lipid oxidation are further characterized and how light-induced asymmetric oxidation generates spontaneous curvature in a non-monotonic temporal manner is rationalized. Using the framework, a phase diagram with an analytical criterion to predict transient pore formation or catastrophic vesicle collapse is provided. The work can shed light on understanding biomembrane stability under oxidative assault and strategizing release dynamics of vesicle-based drug delivery systems.

Correction: Light-triggered explosion of lipid vesicles.

Correction for 'Light-triggered explosion of lipid vesicles' by Vinit Kumar Malik et al., Soft Matter, 2020, DOI: 10.1039/d0sm01027h.

Light-triggered explosion of lipid vesicles.

Lipid vesicles have received considerable interest because of their applications to in vitro reductionist cell membrane models as well as therapeutic delivery vehicles. In these contexts, the mechanical response of vesicles in nonequilibrium environments plays a key role in determining the corresponding dynamics. A common understanding of the response of lipid vesicles upon exposure to a hypotonic solution is a characteristic pulsatile behavior. Recent experiments, however, have shown vesicles exploding under an osmotic shock generated by photo-reactions, yet the explanatory mechanism is unknown. Here we present a generalized biophysical model incorporating a stochastic account of membrane rupture to describe both swell-burst-reseal cycling and exploding dynamics. This model agrees well with experimental observations, and it unravels that the sudden osmotic shock strains the vesicle at an extreme rate, driving the vesicle into buckling instabilities responsible for membrane fragmentation, i.e. explosion. Our work not only advances the fundamental framework for non-equilibrium vesicle dynamics under osmotic stress, but also offers design guidelines for programmable vesicle-encapsulated substance release in therapeutic carriers.