Regulation of insect steroid hormone biosynthesis by innervating peptidergic neurons

Abstract

In insects, steroid hormones named ecdysteroids elicit molting and metamorphosis. The prothoracic gland (PG) is a predominant source of ecdysteroids, where their biosynthesis (ecdysteroidogenesis) is regulated by several neuropeptides. Here, we report that FMRFamide-related peptides (FaRPs) regulate ecdysteroidogenesis through direct innervation of the PG in the silkworm Bombyx mori. We purified a previously uncharacterized Bombyx FaRP, DPSFIRFamide, and identified the corresponding Bombyx FMRFamide gene (Bommo-FMRFamide, BRFa), which encodes three additional FaRPs. All BRFa peptides suppressed ecdysteroidogenesis in the PG by reducing cAMP production by means of the receptor for Bommomyosuppressin, another FaRP we have previously shown to act as a prothoracicostatic factor. BRFa is predominantly expressed in neurosecretory cells of thoracic ganglia, and the neurons in the prothoracic ganglion innervate the PG to supply all four peptides to the gland surface. Electrophysiological recordings during development confirmed the increased firing activity of BRFa neurons in stages with low PG activity and decreased ecdysteroid levels in the hemolymph. To our knowledge, this study provides the first report of peptides controlling ecdysteroidogenesis by direct innervation.ecdysteroid ͉ FMRFamide-related peptides ͉ metamorphosis ͉ molting ͉ prothoracic gland

Differential Regulation of Ecdysteroidogenic P450 Gene Expression in the Silkworm,Bombyx mori

“…BRFa repressed PTTH-induced transcription of P450 genes in the PG Since BRFa inhibits ecdysteroidogenesis in the presence of PTTH, 13) it was important to determine the opposing effects of these two factors on the expression of ecdysteroidogenic P450 enzymes in the PG. As described previously, PTTH significantly upregulated the transcript levels of spo, phm, and dib in the shortterm PG culture, with the effect on dib most prominent (Fig.…”

“…In contrast, the expression of phm increased long before the rise in the PTTH titer, and was repressed after the onset of wandering, possibly reflecting the sensitivity of this gene to BRFa. In fact, the overall expression profile of phm is a mirror image of the firing profile of BRFa neurons, 13) suggesting the importance of neural input in the regulation of phm expression.…”

“…Tel: +81-4-7136-3622; Fax: +81-4-7136-3623; E-mail: kataoka@k.u-tokyo.ac.jp Abbreviations: PG, prothoracic gland; PTTH, prothoracicotropic hormone; BRFa, Bommo-FMRFamide; JH, juvenile hormone; spo, spook; phm, phantom; dib, disembodied; sad, shadow; CA, corpus allatum/corpora allata regulators is Bommo-FMRFamide (BRFa), a neural regulator of ecdysteroidogenesis that counteracts the prothoracicotropic activity of PTTH in the silkworm, Bombyx mori. 13) Juvenile hormone (JH) has also been reported to suppress the gland during the early stages of the last instar larvae in B. mori. [14][15][16] In this study, we found that BRFa and JH also modulate the expression of certain P450 genes in the PG of B. mori.…”

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

“…There is also growing evidence that the central neuroendocrine system exerts a prothoracicostatic effect in addition to the tropic effect, thus generating a timely fluctuation of the ecdysteroid titer in the hemolymph during insect development. We previously identified three prothoracicostatic factors: prothoracicostatic peptide (PTSP) (5), bommo-myosuppressin (BMS) (6), and bommo-FMRFamides (BRFas) (7) in Bombyx. PTSP belongs to the W(X) 6 Wamide peptide family, which shares a -W(X) 6 Wamide C-terminal sequence motif.…”

Neural control of steroid hormone biosynthesis during development in the fruit fly <i>Drosophila melanogaster</i>

“…While PTTH neurons are the only neurons in D. melanogaster that have been reported to project to the PG (McBrayer et al, 2007;Siegmund and Korge, 2001), different types of PG-innervating neurons have been reported in other insects, such as the silkworm B. mori (Tanaka, 2011;Yamanaka et al, 2006;Yokoyama, 1956), the cabbage moth Mamestra brassicae (Okajima and Watanabe, 1989) and the American cockroach Periplaneta americana (Richter and Bohm, 1997). The electrophysiological activities of these neurons correlate with the ecdysteroid titer, suggesting that these neurons stimulate the PG with tropic or static factors.…”