The Voltage-Gated Sodium Channel in Drosophila, Para, Localizes to Dendrites As Well As Axons in Mechanosensitive Chordotonal Neurons

Authors

Thomas A Ravenscroft
Ashleigh Jacobs
Mingxue Gu
Daniel F Eberl
Hugo J Bellen

Publication Date

6-1-2023

Journal

eNeuro

DOI

10.1523/ENEURO.0105-23.2023

PMID

37328295

PubMedCentral® Posted Date

6-27-2023

PubMedCentral® Full Text Version

Post-print

Published Open-Access

yes

Keywords

Animals, Action Potentials, Axons, Dendrites, Drosophila, Drosophila melanogaster, Sensory Receptor Cells, Transient Receptor Potential Channels, Voltage-Gated Sodium Channels, AIS, channel, mechanosensors, para, PNS, sodium

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 (CNs). 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 (SIZs) 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 (AIS) in vertebrates, 40–60 μm from the soma in multipolar neurons and 20–40 μm in bipolar neurons. Whole-cell reduction of para expression using RNAi in CNs of the adult Johnston’s organ (JO) severely affects sound-evoked potentials (SEPs). 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 Para’s role in mechanosensitive transduction.