Signaling Pathways That Regulate the Crustacean Molting Gland.

Donald L. Mykles

doi:10.3389/fendo.2021.674711

Abstract

A pair of Y-organs (YOs) are the molting glands of decapod crustaceans. They synthesize and secrete steroid molting hormones (ecdysteroids) and their activity is controlled by external and internal signals. The YO transitions through four physiological states over the molt cycle, which are mediated by molt-inhibiting hormone (MIH; basal state), mechanistic Target of Rapamycin Complex 1 (mTORC1; activated state), Transforming Growth Factor-β (TGFβ)/Activin (committed state), and ecdysteroid (repressed state) signaling pathways. MIH, produced in the eyestalk X-organ/sinus gland complex, inhibits the synthesis of ecdysteroids. A model for MIH signaling is organized into a cAMP/Ca2+-dependent triggering phase and a nitric oxide/cGMP-dependent summation phase, which maintains the YO in the basal state during intermolt. A reduction in MIH release triggers YO activation, which requires mTORC1-dependent protein synthesis, followed by mTORC1-dependent gene expression. TGFβ/Activin signaling is required for YO commitment in mid-premolt. The YO transcriptome has 878 unique contigs assigned to 23 KEGG signaling pathways, 478 of which are differentially expressed over the molt cycle. Ninety-nine contigs encode G protein-coupled receptors (GPCRs), 65 of which bind a variety of neuropeptides and biogenic amines. Among these are putative receptors for MIH/crustacean hyperglycemic hormone neuropeptides, corazonin, relaxin, serotonin, octopamine, dopamine, allatostatins, Bursicon, ecdysis-triggering hormone (ETH), CCHamide, FMRFamide, and proctolin. Contigs encoding receptor tyrosine kinase insulin-like receptor, epidermal growth factor (EGF) receptor, and fibroblast growth factor (FGF) receptor and ligands EGF and FGF suggest that the YO is positively regulated by insulin-like peptides and growth factors. Future research should focus on the interactions of signaling pathways that integrate physiological status with environmental cues for molt control.

Highlights

The progression of decapod crustaceans through the molt cycle depends on ecdysteroids synthesized by the Y-organ [YO; reviewed in [1]]
This review presents the current knowledge of the signaling pathways that control ecdysteroid synthesis by the YO and identifies areas for future research
The neuropeptides molt-inhibiting hormone (MIH) and crustacean hyperglycemic hormone (CHH) are the only known ligands identified for YOs in crustaceans [2, 50, 55, 189, 190]

Summary

INTRODUCTION

The progression of decapod crustaceans through the molt cycle depends on ecdysteroids synthesized by the Y-organ [YO; reviewed in [1]]. The transition of the YO from the activated to the committed state is mediated by transforming growth factor beta (TGFb)/Activin signaling, as SB431542, an inhibitor of Activin receptor signal transduction, prevents progression of animals from early premolt to midpremolt (stage D1; Figure 1) [15]. Most of the 478 differentially-expressed genes assigned to signal transduction pathways are downregulated to their lowest levels during the postmolt stage [21] Among these are critical components of the MIH, mTORC1, and TGFb/Activin signaling pathways [21]. These data suggest that the YO is not inhibited by MIH during postmolt and that repression of the YO involves transcriptional regulation that prevents premature reactivation of the YO until exoskeleton synthesis and calcification are completed [2]. It includes relevant research on signaling mechanisms that control the insect prothoracic gland

G PROTEIN-COUPLED RECEPTORMEDIATED SIGNALING

CONCLUSIONS AND FUTURE RESEARCH