The Voltage-gated sodium channel in Drosophila, Para, localizes to dendrites as well as axons in mechanosensitive chordotonal neurons

Abstract

The fruit fly Drosophila melanogaster has provided important insights into how sensory information is transduced by Transient Receptor Potential (TRP) channels in the Peripheral Nervous System (PNS). However, TRP channels alone have not been able to completely model mechanosensitive transduction in mechanoreceptive chordotonal neurons (CN). Here we show that, in addition to TRP channels, the sole voltage-gated sodium channel (NaV) in Drosophila, Para, is localized to the dendrites of CNs. Para is localized to the distal tip of the dendrites in all CNs, from embryos to adults, and is colocalized with the mechanosensitive TRP channels No mechanoreceptor potential C (NompC) and Inactive/Nanchung (Iav/Nan). Para localization also demarcates spike initiation zones (SIZ) in axons and the dendritic localization of Para is indicative of a likely dendritic SIZ in fly CNs. Para is not present in the dendrites of other peripheral sensory neurons. In both multipolar and bipolar neurons in the PNS, Para is present in a proximal region of the axon, comparable to the axonal initial segment in vertebrates, 40-60m from the soma in multipolar neurons and 20-40m in bipolar neurons. Whole-cell reduction of para expression using RNAi in CNs of the adult Johnstons organ severely affects sound-evoked potentials. However, the duality of Para localization in the CN dendrites and axons identifies a need to develop resources to study compartment-specific roles of proteins that will enable us to better understand Paras role in mechanosensitive transduction. Significance StatementSeveral transient receptor potential (TRP) channels have been shown to localize to dendrites of Drosophila mechanosensitive chordotonal neurons (CN). Here, we show that the fly voltage-gated sodium channel, Para co-localizes with the TRP channels NompC and iav and a possible dendritic spike initiation zone (SIZ) in CN dendrites. This dendritic localization is unique to CNs, is not seen in other peripheral neurons, and may account for some aspects of mechanotransduction. Para also localizes to a SIZ at an axonal initial segment-like region, which is shared amongst many peripheral neurons.