Rapid propagation of membrane tension at a presynaptic terminal

Abstract

Many cellular activities, such as cell migration1, cell division2,3, signaling4,5, infection6, phagocytosis7 and exo-endocytosis8-11, generate membrane tension gradients that in turn regulate them12. Moreover, membrane flows, which are driven by tension gradients, can limit exo-endocytosis coupling in space and time, as net membrane flow from exocytic to endocytic sites is required to maintain membrane homeostasis13. However, there is controversy over how rapidly plasma membrane flows can relax tension gradients; contrary to the common view12,14,15, recent work showed membrane tension does not equilibrate in several cell types16. Here we show membrane tension can propagate rapidly or slowly, spanning orders of magnitude in speed, depending on cell type. In a neuronal terminal specialized for rapid synaptic vesicle turnover and where exo-endocytosis events occur at distinct loci, membrane tension equilibrates within seconds. By contrast, membrane tension does not propagate in neuroendocrine adrenal chromaffin cells secreting catecholamines. Thus, slow membrane flow and tension equilibration may confine exo- and exocytosis to the same loci17. Stimulation of exocytosis causes a rapid, global decrease in the synaptic terminal membrane tension, which recovers slowly due to endocytosis. Our results demonstrate membrane tension propagates rapidly at neuronal terminals and varies during synaptic activity, likely contributing to exo-endocytosis coupling.