Two cGMP-dependent protein kinases have opposing effects on molt-inhibiting hormone regulation of Y-organ ecdysteroidogenesis

Talia B Head; Jorge L Pérez-Moreno; Tomer Ventura; David S Durica; Donald L Mykles

doi:10.1242/jeb.249739

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Two cGMP-dependent protein kinases have opposing effects on molt-inhibiting hormone regulation of Y-organ ecdysteroidogenesis

Journal article

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Two cGMP-dependent protein kinases have opposing effects on molt-inhibiting hormone regulation of Y-organ ecdysteroidogenesis

Talia B Head, Jorge L Pérez-Moreno, Tomer Ventura, David S Durica and Donald L Mykles

Journal of Experimental Biology, Vol.228(5), pp.1-17

2025

DOI: https://doi.org/10.1242/jeb.249739

PMID: 39850985

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Abstract

Crustacea

Ecdysteroid

Molt-inhibiting hormone (MIH)

Molting

cGMP-dependent protein kinase/protein kinase G (PKG)

Y-organ

Decapod crustaceans regulate molting through steroid molting hormones, ecdysteroids, synthesized by the molting gland (Y-organ, YO). Molt-inhibiting hormone (MIH), a neuropeptide synthesized and secreted by the eyestalk ganglia, negatively regulates YO ecdysteroidogenesis. MIH signaling is mediated by cyclic nucleotide second messengers. cGMP-dependent protein kinase (PKG) is the presumed effector of MIH signaling by inhibiting mechanistic Target of Rapamycin Complex 1 (mTORC1)-dependent ecdysteroidogenesis. Phylogenetic analysis of PKG contiguous sequences in CrusTome as well as 35 additional species in NCBI RefSeq, identified 206 PKG1 sequences in 108 species and 59 PKG2 sequences in 53 species. These included four PKG1α splice variants in the N-terminal region that were unique to decapods, as well as PKG1β and PKG2 homologs. In vitro assays using YOs from the blackback land crab (Gecarcinus lateralis) and green shore crab (Carcinus maenas) determined the effects of MIH±PKG inhibitors on ecdysteroid secretion. A general PKG inhibitor, Rp-8-Br-PET-cGMPS, countered the effects of MIH, as ecdysteroid secretion increased in PKG-inhibited YOs compared to C. maenas YOs incubated with MIH alone. By contrast, a PKG2-specific inhibitor, AP-C5 (4-[4-(1H-Imidazol-1-yl)phenyl]-N-2-propyn-1-yl-2-pyrimidinamine), enhanced the effects of MIH, as ecdysteroid secretion decreased in G. lateralis and C. maenas YOs incubated with AP-C5 and MIH compared to YOs incubated with MIH alone. These data suggest that both PKG1 and PKG2 are activated by MIH, but have opposing effects on mTORC1-dependent ecdysteroidogenesis. A model is proposed in which the dominant role of PKG1 is countered by PKG2, resulting in low ecdysteroid production by the basal YO during intermolt.

Details

Title: Two cGMP-dependent protein kinases have opposing effects on molt-inhibiting hormone regulation of Y-organ ecdysteroidogenesis
Authors: Talia B Head (Corresponding Author) - Colorado State University
Jorge L Pérez-Moreno - Colorado State University
Tomer Ventura - University of the Sunshine Coast, Queensland, Centre for Bioinnovation
David S Durica - University of Oklahoma
Donald L Mykles - Colorado State University
Publication details: Journal of Experimental Biology, Vol.228(5), pp.1-17
Publisher: The Company of Biologists Ltd.
Date published: 2025
DOI: 10.1242/jeb.249739
ISSN: 1477-9145
PMID: 39850985
Copyright note: © 2025. Published by The Company of Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
Data Availability: Fasta files of all sequences and alignments presented in this study, sequence metadata, raw data from in vitro YO assays, and sanger sequencing have been deposited on Dryad: https://doi.org/10.5061/dryad.1g1jwsv7b. Table S1, Table S2, and PhyloPic credits are available in the supplementary PDF.
Grant note: This work was supported by the National Science Foundation to DM (IOS-1922701) and DD (IOS-1922755); a Graduate Student Travel Fellowship to TH from the Society for Integrative and Comparative Biology; and a Graduate Studies Fellowship to TH from The Crustacean Society.
Organisation Unit: School of Science, Technology and Engineering; Centre for Bioinnovation
Language: English
Record Identifier: 991097746102621
Output Type: Journal article

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