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Direct measurements of shear-induced nanoscale lipid dynamics and restructuring

Direct measurements of shear-induced nanoscale lipid dynamics and restructuring

Session

Stream 4 (AFM): Quantitative SPM for Biology, Biomedicine, and Bioinspired Technologies

Authors

Dr William Trewby (1), Prof. Kislon Voitchovsky (1)

Affiliations

1. Durham University

Keywords

Biolubrication, nano-rheology, membrane dynamics, lipid diffusion, AFM

Abstract text

Biological membranes perform a staggering array of functions in vivo, with their lipid molecules acting not just as passive structural components, but actively driving processes related to protein function, oncogenesis and disease signalling, and even intrinsic sensing capabilities [1–5]. The versatility of lipid bilayers originates from their fluidity and flexibility – that is, their dynamics – which allows molecular transport along and across them, membrane restructuring, and the ability to robustly sustain large shear forces, all with minimal energy cost. In-plane lipid motion, as well as the slowly-evolving hydration structures at their headgroups contributes to the strongly lubricating regimes observed in synovial joints which outperform artificial lubricants with friction coefficients as low as µ = 10^-5 [6,7]. Further, a bilayer’s fluidity and ability to restructure governs the motion of bound nanostructures and transport of proteins [8,9] as well as modulating mesoscale events such as the generation and detection of exosomes [4].

Despite the clear need for a holistic understanding of lipid dynamics, experimental techniques rarely have access to local membrane viscosity, frictional or diffusive coefficients over a broad range of timescales, relying instead upon either equilibrium fluctuations or experimentally friendly velocities that are typically two orders of magnitude too small for modelling real-life applications [9,10].

Here, we demonstrate the use of an atomic force microscope-based high-frequency shearing device to probe the dissipation and lubrication abilities of supported lipid membranes. We can access velocities ranging from hundreds of nms^-1 to mms^-1, easily capturing quasistatic (v_shear << lipid motion), glassy (v_shear >> lipid motion) and potential non-linear transitional regimes. Crucially, the technique does not require molecular labels and has contact areas of order ~nm², allowing for direct, local energetic measurements on the scale of single proteins. We explore the impact of membrane and buffer composition and unpick the complex interplay between lipid dynamics, headgroup hydration and experimental timescale. The results have important implications for our understanding of biolubrication, as well as dynamic membrane binding events.

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