Periodic Obstacles Regulate Membrane Tension Propagation to Enable Localized Mechanotransduction

Abstract

Forces applied to cellular membranes lead to transient membrane tension gradients. The way membrane tension propagates away from the stimulus site into the membrane reservoir is a key property in cellular adaptation. However, it remains unclear how tension propagation in membranes is regulated and how it depends on the cell type. Here, we investigate plasma membrane tension propagation in cultured Caenorhabditis elegans mechanosensory neurons. We show that tension propagation travels quickly and is restricted to a particular distance in the neurites -- projections from the cell body of a neuron. A biophysical model of tension propagation suggests that periodic obstacle density and arrangement play key roles in controlling the propagation of mechanical information. Our experiments show that tension propagation is strongly dependent on the intact actin and microtubule cytoskeleton, whereas membrane lipid properties have minimal impact. In particular, the organization of the /{beta}-spectrin network and the MEC-2 stomatin condensates in periodic scaffold act as barriers to tension propagation, limiting the spread of tension. Our findings suggest that restricting membrane tension propagation in space and time enables precise localized signaling, allows a single neuron to process mechanical signals in multiple distinct domains, thus expanding its computational capacity.