A Drosophila DEG/ENaC channel subunit is required for male response to female pheromones

Abstract

Odorants and pheromones as well as sweet-and bitter-tasting small molecules are perceived through activation of G proteincoupled chemosensory receptors. In contrast, gustatory detection of salty and sour tastes may involve direct gating of sodium channels of the DEG͞ENaC family by sodium and hydrogen ions, respectively. We have found that ppk25, a Drosophila melanogaster gene encoding a DEG͞ENaC channel subunit, is expressed at highest levels in the male appendages responsible for gustatory and olfactory detection of female pheromones: the legs, wings, and antennae. Mutations in the ppk25 gene reduce or even abolish male courtship response to females in the dark, conditions under which detection of female pheromones is an essential courtshipactivating sensory input. In contrast, the same mutations have no effect on other behaviors tested. Importantly, ppk25 mutant males that show no response to females in the dark execute all of the normal steps of courtship behavior in the presence of visible light, suggesting that ppk25 is required for activation of courtship behavior by chemosensory perception of female pheromones. Finally, a ppk25 mutant allele predicted to encode a truncated protein has dominant-negative properties, suggesting that the normal Ppk25 protein acts as part of a multiprotein complex. Together, these results indicate that ppk25 is necessary for response to female pheromones by D. melanogaster males, and suggest that members of the DEG͞ENaC family of genes play a wider role in chemical senses than previously suspected.courtship ͉ behavior ͉ olfaction ͉ taste A s in most other animals, pheromones play key roles in the regulation of sexual behaviors of Drosophila melanogaster (1-3). In particular, several pheromones modulate male courtship of the female, which involves a stereotyped series of behaviors. By analogy with olfactory and gustatory perception of organic molecules in both insects and vertebrates (4), perception of these pheromones most likely involves interactions with seven-transmembrane receptors and subsequent activation of a G protein-coupled signal transduction pathway. Indeed, a male-specific member of the seven-transmembrane gustatory receptor family has been identified as a putative receptor for female courtship-stimulating pheromones (5). In contrast, gustatory perception of hydrogen and sodium ions, perceived as sour and salty tastes, respectively, has been suggested to involve direct gating of sodium channels of the DEG͞ENaC family (6, 7). In support of this possibility, inactivation of ppk11 or ppk19, two Drosophila DEG͞ENaC subunit genes, results in loss of behavioral and electrophysiological responses to salt (8). Here we report the unexpected finding that another Drosophila DEG͞ENaC subunit gene, ppk25, is specifically required for male response to courtshipactivating female pheromones. This observation suggests that members of this protein family play more diverse roles in chemical senses than previously suspected. Experimental ProceduresMutant and Transgenic Flies. Deletio...

Eukaryotic operon-like transcription of functionally related genes in Drosophila

“…Consistent with this suggestion, CheB42a and llz showed a similar pattern of expression. Moreover, they both seem to be involved in male courtship behavior (5,30,31), and the two proteins interact (Y.B.-S. and M.J.W., unpublished data).…”

ENaCs and ASICs as therapeutic targets

“…ENaC is also a wellestablished member of the channel repertoire of the nasal epithelium, but this tissue is predominantly involved in fluid transport, and is widely used in CF-related studies as a model of the airway epithelium. To date, the only member of the Deg/ENaC family that has a direct role in olfaction is the Drosophila homolog pickpocket, which is thought to be involved in sensing of female pheromones by male flies (247).…”

Temperature-sensitive Mutant of the Caenorhabditis elegans Neurotoxic MEC-4(d) DEG/ENaC Channel Identifies a Site Required for Trafficking or Surface Maintenance

“…ASICs have been implicated in mechanosensation (7,8), pain sensation (9, 10), vascular (11) and visceral mechanotransduction (12), salt and sour taste (13,14), fear conditioning (15), and synaptic plasticity (16). Invertebrate channels of this superfamily (Caenorhabditis elegans degenerins, Aplysia FNaC, Drosophila pickpockets (PPKs)) are expressed in neurons, muscle, and epithelia and contribute to fluid clearance (17), thermosensation (18), taste (14), pheromone perception (19), touch sensation (reviewed in Ref. 20), proprioception (21,22), and locomotor rhythms (23).…”