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Pulsatile Gating of Giant Vesicles Containing Macromolecular Crowding Agents Induced by Colligative Nonideality
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posted on 2018-01-05, 19:55 authored by Wan-Chih Su, Douglas L. Gettel, Morgan Chabanon, Padmini Rangamani, Atul N. ParikhThe ability of large
macromolecules to exhibit nontrivial deviations
in colligative properties of their aqueous solutions is well-appreciated
in polymer physics. Here, we show that this colligative nonideality
subjects giant lipid vesicles containing inert macromolecular crowding
agents to osmotic pressure differentials when bathed in small-molecule
osmolytes at comparable concentrations. The ensuing influx of water
across the semipermeable membrane induces characteristic swell-burst
cycles: here, cyclical and damped oscillations in size, tension, and
membrane phase separation occur en route to equilibration.
Mediated by synchronized formation of transient pores, these cycles
orchestrate pulsewise ejection of macromolecules from the vesicular
interior reducing the osmotic differential in a stepwise manner. These
experimental findings are fully corroborated by a theoretical model
derived by explicitly incorporating the contributions of the solution
viscosity, solute diffusivity, and the colligative nonideality of
the osmotic pressure in a previously reported continuum description.
Simulations based on this model account for the differences in the
details of the noncolligatively induced swell-burst cycles, including
numbers and periods of the repeating cycles, as well as pore lifetimes.
Taken together, our observations recapitulate behaviors of vesicles
and red blood cells experiencing sudden osmotic shocks due to large
(hundreds of osmolars) differences in the concentrations of small
molecule osmolytes and link intravesicular macromolecular crowding
with membrane remodeling. They further suggest that any tendency for
spontaneous overcrowding in single giant vesicles is opposed by osmotic
stresses and requires independent specific interactions, such as associative
chemical interactions or those between the crowders and the membrane
boundary.