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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 Wolfner, Mariana Federica

PLoS Biology, 2020-03, Vol.18 (3), p.e3000614-e3000614 [Periódico revisado por pares]

United States: Public Library of Science

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Título:
A G protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia
Autor: Quiroga Artigas, Gonzalo ; Lapébie, Pascal ; Leclère, Lucas ; Bauknecht, Philipp ; Uveira, Julie ; Chevalier, Sandra ; Jékely, Gáspár ; Momose, Tsuyoshi ; Houliston, Evelyn
Wolfner, Mariana Federica
Assuntos: Animal species ; Antibodies ; Biology and Life Sciences ; Candidates ; Cell culture ; Cell cycle ; Cellular Biology ; Characterization ; Clytia ; Clytia hemisphaerica ; Cnidaria ; Coupling (molecular) ; CRISPR ; Cyclic adenosine monophosphate ; Cyclic AMP ; Development Biology ; Developmental biology ; Experiments ; G protein-coupled receptors ; G proteins ; Gametocytes ; Gametogenesis ; Gonadotropins ; Gonads ; Hormones ; Laboratories ; Life Sciences ; Ligands ; Maturation ; Medicine and Health Sciences ; Meiosis ; Membrane proteins ; Mutants ; Neuropeptide receptors ; Neuropeptide Y ; Neuropeptides ; Oocytes ; Peptides ; Phylogenetics ; Phylogeny ; Physiology ; Pituitary (anterior) ; Proteins ; Receptors ; Regulators ; Reproduction (biology) ; Reproductive Biology ; Research and Analysis Methods ; Sexual reproduction ; Somatic cells ; Spawning ; Subcellular Processes ; Supervision ; Vertebrates
É parte de: PLoS Biology, 2020-03, Vol.18 (3), p.e3000614-e3000614
Notas: ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
PMCID: PMC7053711
The authors have declared that no competing interests exist.
Current address: The Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, Florida, United States of America
Descrição: 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.
Editor: United States: Public Library of Science
Idioma: Inglês

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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 Wolfner, Mariana Federica

United States: Public Library of Science

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