NOMPC-dependent mechanotransduction shapes the dendrite of proprioceptive neurons

Abstract

Animal locomotion depends on proprioceptive feedback which is generated by mechanosensory neurons. We recently demonstrated that the evolutionarily conserved stumble (stum) gene is essential for mechanical transduction in a group of proprioceptive neurons in Drosophila leg joints. A specialized dendritic ending of the stum-expressing neurons is stretched by changes in joint position, suggesting that the dendritic site is specifically tuned for joint proprioception. Here, we show that the stum-expressing neurons express the mechanosensory channel NOMPC. In nompC mutants responses to joint position were abolished, indicating that NOMPC is the mechanosensitive channel in stum-expressing neurons. The NOMPC protein had a similar subcellular distribution as STUM, being located specifically at the dendritic site that is stretched by joint motions, thus validating that this site is a specialized sensory compartment. In the absence of NOMPC the sensory portion of the dendrite was misshapen, generating membrane protrusions. Thus, we have shown that mechanical responsiveness at a specialized dendritic site is essential for determination of the fine dendritic structure. The abnormal morphology at the sensory compartment of non-active neurons suggests that the dendrite samples for a responsive anchoring site and stabilizes the structure that elicits the effective mechanotransduction.