Transcriptional regulation of insect steroid hormone biosynthesis and its role in controlling timing of molting and metamorphosis

Abstract

The developmental transition from juvenile to adult is often accompanied by many systemic changes in morphology, metabolism, and reproduction. Curiously, both mammalian puberty and insect metamorphosis are triggered by a pulse of steroid hormones, which can harmonize gene expression profiles in the body and thus orchestrate drastic biological changes. However, understanding of how the timing of steroid hormone biosynthesis is regulated at the molecular level is poor. The principal insect steroid hormone, ecdysteroid, is biosynthesized from dietary cholesterol in the specialized endocrine organ called the prothoracic gland. The periodic pulses of ecdysteroid titers determine the timing of molting and metamorphosis. To date, at least nine families of ecdysteroidogenic enzyme genes have been identified. Expression levels of these genes correlate well with ecdysteroid titers, indicating that the transcriptional regulatory network plays a critical role in regulating the ecdysteroid biosynthesis pathway. In this article, we summarize the transcriptional regulation of ecdysteroid biosynthesis. We first describe the development of prothoracic gland cells during Drosophila embryogenesis, and then provide an overview of the transcription factors that act in ecdysteroid biosynthesis and signaling. We also discuss the external signaling pathways that target these transcriptional regulators. Furthermore, we describe conserved and/or diverse aspects of steroid hormone biosynthesis in insect species as well as vertebrates.

Green tea proanthocyanidins cause impairment of hormone-regulated larval development and reproductive fitness via repression of juvenile hormone acid methyltransferase, insulin-like peptide and cytochrome P450 genes in Anopheles gambiae sensu stricto

“…sinensis PA-rich fractions, differential gene expression profiles were assessed by RT-qPCR. Transcriptional regulation of growth, development and reproduction in insects represent a crosslink between metabolic and hormonal networks [33, 66, 67]. Plant compounds with insect growth regulatory effects have been reported to antagonize the effects of endogenous hormones by dysregulating their biosynthesis, secretion, and binding to their receptors [68, 69].…”

Activated Ras/JNK driven Dilp8 in imaginal discs adversely affects organismal homeostasis during early pupal stage inDrosophila, a new checkpoint for development

“…The ptth transcript levels were slightly reduced in larval brain, but were nearly absent in pupal brain of sev-GAL4>UAS-Ras1 V12 hsrω-RNAi individuals (Fig 7F). This is significant since Ptth hormone from brain triggers the prothoracic gland to produce ecdysone (Rewitz et al, 2009;Niwa and Niwa, 2016) and thus such low level of ptth transcripts ( Fig 7F) indicates absence of this triggering mechanism in individuals with high Ras activity in the eye discs.…”

“…Ectopic expression of activated Ras or certain other transgenes like UAS-rpr or UAStak 1 in wing discs also elevated Dilp8 levels in early pupae and resulted in their death. High Dilp8 reduced prothoracicotrophic hormone (Ptth) production in brain, leading to reduced activity of genes involved in ecdysone biosynthesis in prothoracic gland, the seat of ecdysone hormone production (Rewitz et al, 2009;Niwa and Niwa, 2016). Insufficient systemic ecdysone hormone during the critical early pupal stage hampered normal development, causing breakdown of organismal homeostasis and consequent death.…”

Activated Ras/JNK driven Dilp8 in imaginal discs adversely affects organismal homeostasis during early pupal stage in Drosophila, a new checkpoint for development

“…Ectopic expression of activated Ras or certain other transgenes like UAS‐rpr or UAS‐tak 1 in wing discs also elevated Dilp8 levels in early pupae and resulted in their death. High Dilp8 reduced prothoracicotrophic hormone (Ptth) production in brain, leading to reduced activity of genes involved in ecdysone biosynthesis in prothoracic gland, the seat of ecdysone hormone production . Insufficient systemic ecdysone hormone during the critical early pupal stage hampered normal development, causing breakdown of organismal homeostasis and consequent death.…”

“…High Dilp8 reduced prothoracicotrophic hormone (Ptth) production in brain, leading to reduced activity of genes involved in ecdysone biosynthesis in prothoracic gland, the seat of ecdysone hormone production. 21,22 Insufficient systemic ecdysone hormone during the critical early pupal stage hampered normal development, causing breakdown of organismal homeostasis and consequent death. These results thus unravel the early pupal ecdysone surge 23 as a new checkpoint for Dilp8 action and explain the intriguing results noted in several other studies 13,14 that expression of certain transgenes by predominantly eye disc specific GAL4 drivers is associated with pupal lethality.…”