Membrane Remodeling by DNA Origami Nanorods: Experiments Exploring the Parameter Space for Vesicle Remodeling

Abstract

Inspired by the ability of cell membranes to alter their shape in response to bound particles, we report an experimental study of long, slender nanorods binding to lipid bilayer vesicles and altering the membrane shape. Our work illuminates the role of particle concentration, adhesion strength, and membrane tension in determining the membrane morphology. We combined giant unilamellar vesicles with oppositely charged nanorods, carefully tuning the adhesion strength, membrane tension, and particle concentration. With increasing adhesion strength, the primary behaviors observed were membrane deformation, vesicle−vesicle adhesion, and vesicle rupture. These behaviors were observed in welldefined regions in the parameter space with sharp transitions between them. We observed the deformation of the membrane resulting in tubulation, textured surfaces, and small and large lipid−particle aggregates. These responses are robust and repeatable and provide a new physical understanding of the dependence on the shape, binding affinity, and particle concentration in membrane remodeling. The design principles derived from these experiments may lead to new bioinspired membrane-based materials.

Membrane‐Mediated Self‐Organization of Rod‐Like DNA Origami on Supported Lipid Bilayers

“…Importantly, although SLBs do not allow for high-magnitude deformations on a solid support, nanometer-scale deformations are possible, due to the presence of a hydration layer between the support surface and the phospholipid headgroups (Note S1, Supporting Information). [49][50][51] Interestingly, while membrane-mediated interactions of elongated colloidal particles have been previously observed on free-standing lipid bilayers, [23,24] no evidence of membranemediated interactions has been reported for macromolecules and colloidal particles adsorbed on SLBs. [23,[52][53][54][55] A potential reason for that could be that all these experiments were carried out using cationic lipid bilayers strongly adhering to the oppositely charged mica surface via electrostatic attraction.…”

“…This results in a stronger interaction of the lipid bilayer with the DNA nanoparticles in comparison with the macromolecules and colloids used in previous studies, and thus allows one to achieve higher surface tension and observe a range of self-organization regimes, which so far has been only achieved in vesicles fully composed of cationic lipids. [24] Although some experiments on interactions of macromolecules with lipid membranes in the gel phase have been carried out previously, [55] these did not allow one to conclude on the existence of membrane-mediated interactions on gel-phase membranes. In these experiments, negatively charged macromolecules were directly electrostatically bound to cationic headgroups of lipid molecules residing in the bilayer.…”

“…[23] More recently, DNA origami needles have been observed to organize in a parallel fashion or form aster-like structures after adsorption to freestanding cationic lipid membranes. [24] Henceforth, to better understand the role of lipid membranes for the lateral self-organization of rigid colloidal particles, we set out to study the dynamic behavior of ensembles of rod-like DNA nanostructures of aspect ratio 7 (AR7) [25] (Figures S1 and S4, Supporting Information) adsorbed through Mg 2+ -mediated electrostatic interactions on the solid mica surface and more elastically responsive 1,2-distearoyl-sn-glycero-3-phosphocholine (DSPC) Organization of elongated particles into ordered phases on 2D surfaces and interfaces has been extensively studied during the last decades both theoretically and experimentally. For mutually repulsive particles on solid nondeformable substrates, the process is controlled only by the aspect ratio and the surface density of the adsorbed particles.…”

Molecular Cybernetics: Challenges toward Cellular Chemical Artificial Intelligence

“…Zuraw‐Weston et al reported a similar vesicle deformation triggered by the binding of DNA origami rods. [ 137 ]…”

“…DNA origami is often modified with lipid-membrane binding moieties and is used to directly but statically deform liposomes. [134][135][136][137] As early as 2014, Simmel et al reported rectangular DNA origami modified with cholesterol moieties. [134] They confirmed for the first time that such origami binds to the lipid membrane of GUVs.…”