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A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia
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 cha...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7053711/ https://www.ncbi.nlm.nih.gov/pubmed/32126082 http://dx.doi.org/10.1371/journal.pbio.3000614 |
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author | Quiroga Artigas, Gonzalo Lapébie, Pascal Leclère, Lucas Bauknecht, Philipp Uveira, Julie Chevalier, Sandra Jékely, Gáspár Momose, Tsuyoshi Houliston, Evelyn |
author_facet | Quiroga Artigas, Gonzalo Lapébie, Pascal Leclère, Lucas Bauknecht, Philipp Uveira, Julie Chevalier, Sandra Jékely, Gáspár Momose, Tsuyoshi Houliston, Evelyn |
author_sort | Quiroga Artigas, Gonzalo |
collection | PubMed |
description | 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 G(s) heterodimeric protein (Gα(S)) 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. |
format | Online Article Text |
id | pubmed-7053711 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-70537112020-03-12 A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia Quiroga Artigas, Gonzalo Lapébie, Pascal Leclère, Lucas Bauknecht, Philipp Uveira, Julie Chevalier, Sandra Jékely, Gáspár Momose, Tsuyoshi Houliston, Evelyn PLoS Biol Research Article 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 G(s) heterodimeric protein (Gα(S)) 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. Public Library of Science 2020-03-03 /pmc/articles/PMC7053711/ /pubmed/32126082 http://dx.doi.org/10.1371/journal.pbio.3000614 Text en © 2020 Quiroga Artigas et al http://creativecommons.org/licenses/by/4.0/ 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 the original author and source are credited. |
spellingShingle | Research Article Quiroga Artigas, Gonzalo Lapébie, Pascal Leclère, Lucas Bauknecht, Philipp Uveira, Julie Chevalier, Sandra Jékely, Gáspár Momose, Tsuyoshi Houliston, Evelyn A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia |
title | A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia |
title_full | A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia |
title_fullStr | A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia |
title_full_unstemmed | A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia |
title_short | A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia |
title_sort | g protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish clytia |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7053711/ https://www.ncbi.nlm.nih.gov/pubmed/32126082 http://dx.doi.org/10.1371/journal.pbio.3000614 |
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