Abstract
In living cells, mechanochemical coupling represents a dynamic means by which membrane components are spatially organized. An extra-ordinary example of such coupling involves curvature-dependent polar localization of chemically-distinct lipid domains at bacterial poles, which also undergo dramatic reequilibration upon subtle changes in their interfacial environment such as during sporulation. Here, we demonstrate that such interfacially-triggered mechanochemical coupling can be recapitulated in vitro by simultaneous, real-time introduction of mechanically-generated periodic curvatures and attendant strain-induced lateral forces in lipid bilayers supported on elastomeric substrates. In particular, we show that real-time wrinkling of the elastomeric substrate prompts a dynamic domain reorganization within the adhering bilayer, producing large, oriented liquid-ordered domains in regions of low curvature. Our results suggest a mechanism in which interfacial forces generated during surface wrinkling and the topographical deformation of the bilayer combine to facilitate dynamic reequilibration prompting the observed domain reorganization. We anticipate this curvature-generating model system will prove to be a simple and versatile tool for a broad range of studies of curvature-dependent dynamic reorganizations in membranes that are constrained by the interfacial elastic and dynamic frameworks such as the cell wall, glycocalyx, and cytoskeleton.
Highlights
An emerging tenet in membrane biophysics is that an interplay between compositional heterogeneity and membrane mechanics holds the key to linking organization with functions. [1] Lipids in biological membranes are not homogeneously dispersed: nonrandom co-distributions of lipids and proteins, spatial gradients of lipid concentrations, and compositionally differentiated domains are pervasive
Functional membrane heterogeneities are often linked to membrane mechanics by curvature and dynamics. [6,7] Curvatures in cellular membranes are modulated by a variety of intrinsic and extrinsic pathways
To prompt substrate-directed dynamic reequilibration in PDMS supported lipid bilayers, we begin with the fusion of small unilamellar vesicles (SUVs) onto stretched, hydrophilic PDMS elastomers
Summary
An emerging tenet in membrane biophysics is that an interplay between compositional heterogeneity and membrane mechanics holds the key to linking organization with functions. [1] Lipids in biological membranes are not homogeneously dispersed: nonrandom co-distributions of lipids and proteins, spatial gradients of lipid concentrations, and compositionally differentiated domains are pervasive. An emerging tenet in membrane biophysics is that an interplay between compositional heterogeneity and membrane mechanics holds the key to linking organization with functions. [3,4] Rather, domains form, reorganize, and break-up as an active response to a host of physical and chemical perturbations, spatially and temporally organizing lipids (and associated membrane proteins), thereby producing functional hot-spots for signaling and trafficking, within the membrane milieu. [6,7] Curvatures in cellular membranes are modulated by a variety of intrinsic and extrinsic pathways These include insertion (or generation) of curvature-sensitive lipids and membrane proteins, surface scaffolding by cytoskeletal (re)polymerization, intra- and extracellular forces due to osmotic gradients in the aqueous environment, protein-binding, and motor protein activity. By modulating the balance of these competing interactions, the repartitioning of the cardiolipin domains occurs at the septal plane due to changes in osmotic pressure, which reduces long-range elastic repulsions
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