Periodic Obstacles Regulate Membrane Tension Propagation to Enable Localized Mechanotransduction

Forces applied to cellular membranes lead to transient membrane tension gradients. The manner in which membrane tension propagates away from the stimulus into the membrane reservoir has emerged as a key property in cellular adaptation, mechanotransduction, and thus organismal physiology. However, it remains unclear whether tension propagation in membranes is actively regulated or is a passive property and how it depends on the cell type. Here, we combined membrane nanorheology with time-shared optical traps and mathematical modeling to investigate plasma membrane tension propagation in cultured Caenorhabditis elegans mechanosensory neurons using a dual tether extrusion assay. Our results showed that, surprisingly, the propagation of tension was restricted to ~30 μm in the neurites and traveled quickly, at speeds exceeding 120 μm/s. Although membrane lipid properties had minimal impact, tension propagation strongly relied on the intact actin and microtubule cytoskeleton. In particular, the organization of the α/β spectrin network and the MEC-2 stomatin condensates acted as barriers, limiting the spread of tension. A biophysical model for tension propagation suggests that obstacle density and arrangement play a key role in controlling the propagation of mechanical information. Our findings suggest that restricting membrane tension propagation in space and time enables precise localized signaling. This localization may facilitate the recruitment of mechanosensitive ion channels and allow a single neuron to process mechanical signals in multiple distinct domains, thus expanding its computational capacity.