Non-muscle myosin II regulates presynaptic actin assemblies and neuronal mechanobiology inDrosophila

Neuromuscular junctions (NMJs) are evolutionarily ancient, specialized contacts between neurons and muscles. They endure mechanical strain from muscle contractions throughout life, but cellular mechanisms for managing this stress remain unclear. Here we identify a novel actomyosin structure atDrosophilalarval NMJs, consisting of a long-lived, low-turnover presynaptic actin core that co-localizes with non-muscle myosin II (NMII). This core is likely to have contractile properties, as manipulating neuronal NMII levels or activity disrupts its organization. Intriguingly, depleting neuronal NMII triggered changes in postsynaptic muscle NMII levels and organization near synapses, suggesting transsynaptic propagation of actomyosin rearrangements. We also found reduced levels of Integrin adhesion receptors both pre- and postsynaptically upon NMII knockdown, indicating disrupted neuron-muscle connections. Mechanical severing of axons caused similar actin core fragmentation and Integrin loss to NMII depletion, suggesting this structure responds to tension. Our findings reveal a presynaptic actomyosin assembly that maintains mechanical continuity between neurons and muscle, possibly facilitating mechanotransduction at the NMJ via Integrin-mediated adhesion.