Quiroga Artigas, Gonzalo and Lapébie, Pascal and Leclère, Lucas and Bauknecht, Philipp and Uveira, Julie and Chevalier, Sandra and Jékely, Gáspár and Momose, Tsuyoshi and Houliston, Evelyn and Wolfner, Mariana Federica (2020) A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia. PLOS Biology, 18 (3). e3000614. ISSN 1545-7885
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Abstract
The reproductive hormones that trigger oocyte meiotic maturation and release from the ovary vary greatly between animal species. Identification of receptors for these maturation-inducing hormones (MIHs) and understanding how they initiate the largely conserved maturation process remain important challenges. In hydrozoan cnidarians including the jellyfish Clytia hemisphaerica, MIH comprises neuropeptides released from somatic cells of the gonad. We identified the receptor (MIHR) for these MIH neuropeptides in Clytia using cell culture–based “deorphanization” of candidate oocyte-expressed G protein–coupled receptors (GPCRs). MIHR mutant jellyfish generated using CRISPR-Cas9 editing had severe defects in gamete development or in spawning both in males and females. Female gonads, or oocytes isolated from MIHR mutants, failed to respond to synthetic MIH. Treatment with the cAMP analogue Br-cAMP to mimic cAMP rise at maturation onset rescued meiotic maturation and spawning. Injection of inhibitory antibodies to the alpha subunit of the Gs heterodimeric protein (GαS) into wild-type oocytes phenocopied the MIHR mutants. These results provide the molecular links between MIH stimulation and meiotic maturation initiation in hydrozoan oocytes. Molecular phylogeny grouped Clytia MIHR with a subset of bilaterian neuropeptide receptors, including neuropeptide Y, gonadotropin inhibitory hormone (GnIH), pyroglutamylated RFamide, and luqin, all upstream regulators of sexual reproduction. This identification and functional characterization of a cnidarian peptide GPCR advances our understanding of oocyte maturation initiation and sheds light on the evolution of neuropeptide-hormone systems.
Item Type: | Article |
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Subjects: | Eurolib Press > Biological Science |
Depositing User: | Managing Editor |
Date Deposited: | 02 Mar 2023 06:12 |
Last Modified: | 11 May 2024 08:38 |
URI: | http://info.submit4journal.com/id/eprint/1156 |