Bombyx prothoracicostatic peptides activate the sex peptide receptor to regulate ecdysteroid biosynthesis

Abstract

Insect molting and metamorphosis are induced by steroid hormones named ecdysteroids, whose production is regulated by various neuropeptides. We cloned the gene and analyzed the expression of the prothoracicostatic peptide, a unique neuropeptide shown to suppress the production of ecdysteroids in the prothoracic gland of the silkworm, Bombyx mori. We also characterized a Bombyx G proteincoupled receptor, which has previously been identified as an ortholog of the Drosophila sex peptide receptor, as a functional prothoracicostatic peptide receptor. This receptor responded specifically to the prothoracicostatic peptides when examined using a heterologous expression system. The receptor was highly expressed in the prothoracic gland on the day before each larval and pupal ecdysis, when prothoracicostatic peptides are synthesized at a high level in the epiproctodeal glands. These results suggest that the sex peptide receptor functions as a prothoracicostatic peptide receptor in Bombyx and that the peripheral neurosecretory cells as well as the central neuroendocrine system play stage-specific roles in regulating ecdysteroidogenesis.Bombyx mori | G protein-coupled receptor | neuropeptides | steroidogenesis

MIPs are ancestral ligands for the sex peptide receptor

“…2B), as has also been found for activation of Bombyx SPR by Bombyx MIPs (13). In contrast, and as previously reported (5), Drosophila SP activates Aedes SPR with approximately 100-fold lower potency (Fig.…”

“…MIPs have been shown to suppress the spontaneous contractions of the hindgut and the oviduct, leading to their designation as myoinhibitory peptides (15,22). In B. mori, MIPs have also been found to suppress ecdysteroid production in the prothoracic gland and accordingly have also been named PTSPs (13,16). The conserved physiological functions of the MIPs, however, remain obscure.…”

“…We followed two approaches in parallel. First, we took a candidate approach, based on the identification of myoinhibitory peptides (MIPs) as ligands for SPR in Bombyx mori (13). Second, we attempted to identify ligands in fractionated extracts of Aedes whole bodies (for results, see SI Text).…”

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

“…Whether this occurs at the level of signalling, however, is not clear as the delay in the response could require higher amounts of SP to compensate for its degradation in the haemolymph. A puzzling discovery has been that SPR can bind MIPs in Drosophila and activate the receptor in cell culture, but injection of MIPs neither induces the SP response nor do MIPs act antagonistically to inhibit the SP response [19,40]. SPR is evolutionarily well conserved and functions in other insects also with ligands seemingly different from SP [19,40].…”

“…Despite the highly specific behavioural response, however, SPR is broadly expressed in the nervous system and the oviduct. SPR also binds myoinhibitory peptides (MIPs) with high affinity, which do not induce the SP-mediated postmating switch [17][18][19]. It therefore appears that SPR has additional functions.…”