Functional characterization of a short neuropeptide F-related receptor in a lophotrochozoan, the mollusk Crassostrea gigas

International audience Members of the short neuropeptide F (sNPF) family of peptides and their cognate receptors play key roles in a variety of physiological processes in arthropods. In silico screening of GigasDatabase, a specific expressed sequence tag database from the Pacific oyster Crassostrea...

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Published in:Journal of Experimental Biology
Main Authors: Bigot, Laetitia, Beets, Isabel, Dubos, Marie-Pierre, Boudry, Pierre, Schoofs, Liliane, Favrel, Pascal
Other Authors: Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), ANR-08-GENM-0041,Gametogenes,Génomiques de la gamétogénèse chez l'huître creuse Crassostrea gigas(2008)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2014
Subjects:
ACL
Online Access:https://hal.science/hal-02548665
https://doi.org/10.1242/jeb.104067
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spelling ftanrparis:oai:HAL:hal-02548665v1 2024-04-21T08:00:34+00:00 Functional characterization of a short neuropeptide F-related receptor in a lophotrochozoan, the mollusk Crassostrea gigas Bigot, Laetitia Beets, Isabel Dubos, Marie-Pierre Boudry, Pierre Schoofs, Liliane Favrel, Pascal Biologie des Organismes et Ecosystèmes Aquatiques (BOREA) Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) ANR-08-GENM-0041,Gametogenes,Génomiques de la gamétogénèse chez l'huître creuse Crassostrea gigas(2008) 2014 https://hal.science/hal-02548665 https://doi.org/10.1242/jeb.104067 en eng HAL CCSD The Company of Biologists info:eu-repo/semantics/altIdentifier/doi/10.1242/jeb.104067 hal-02548665 https://hal.science/hal-02548665 doi:10.1242/jeb.104067 ISSN: 0022-0949 EISSN: 1477-9145 Journal of Experimental Biology https://hal.science/hal-02548665 Journal of Experimental Biology, 2014, 217 (16), pp.2974--2982. ⟨10.1242/jeb.104067⟩ ACL Crassostrea gigas Energy metabolism Oyster Reproduction sNPF Starvation [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2014 ftanrparis https://doi.org/10.1242/jeb.104067 2024-03-26T18:18:59Z International audience Members of the short neuropeptide F (sNPF) family of peptides and their cognate receptors play key roles in a variety of physiological processes in arthropods. In silico screening of GigasDatabase, a specific expressed sequence tag database from the Pacific oyster Crassostrea gigas, resulted in the identification of a receptor (Cg-sNPFR-like) phylogenetically closely related to sNPF receptors (sNPFRs) of insects. A reverse endocrinology approach was undertaken to identify the peptide ligand(s) of this orphan receptor. Though structurally distinct from insect sNPFs, three RFamide peptides derived from the same precursor, i.e. GSLFRFamide, SSLFRFamide and GALFRFamide, specifically activate the receptor in a dose-dependent manner, with respective EC50 values (half-maximal effective concentrations) of 1.1, 2.1 and 4.1 mu mol l(-1). We found that both Cg-sNPFR-like receptor and LFRFamide encoding transcripts are expressed in the oyster central nervous system and in other tissues as well, albeit at lower levels. Mass spectrometry analysis confirmed the wide distribution of LFRFamide mature peptides in several central and peripheral tissues. The Cg-sNPFR-like receptor was more abundantly expressed in ganglia of females than of males, and upregulated in starved oysters. In the gonad area, highest receptor gene expression occurred at the start of gametogenesis, when storage activity is maximal. Our results suggest that signaling of LFRFamide peptides through the Cg-sNPFR-like receptor might play a role in the coordination of nutrition, energy storage and metabolism in C. gigas, possibly by promoting storage at the expense of reproduction. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Portail HAL-ANR (Agence Nationale de la Recherche) Journal of Experimental Biology
institution Open Polar
collection Portail HAL-ANR (Agence Nationale de la Recherche)
op_collection_id ftanrparis
language English
topic ACL
Crassostrea gigas
Energy metabolism
Oyster
Reproduction
sNPF
Starvation
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
spellingShingle ACL
Crassostrea gigas
Energy metabolism
Oyster
Reproduction
sNPF
Starvation
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Bigot, Laetitia
Beets, Isabel
Dubos, Marie-Pierre
Boudry, Pierre
Schoofs, Liliane
Favrel, Pascal
Functional characterization of a short neuropeptide F-related receptor in a lophotrochozoan, the mollusk Crassostrea gigas
topic_facet ACL
Crassostrea gigas
Energy metabolism
Oyster
Reproduction
sNPF
Starvation
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
description International audience Members of the short neuropeptide F (sNPF) family of peptides and their cognate receptors play key roles in a variety of physiological processes in arthropods. In silico screening of GigasDatabase, a specific expressed sequence tag database from the Pacific oyster Crassostrea gigas, resulted in the identification of a receptor (Cg-sNPFR-like) phylogenetically closely related to sNPF receptors (sNPFRs) of insects. A reverse endocrinology approach was undertaken to identify the peptide ligand(s) of this orphan receptor. Though structurally distinct from insect sNPFs, three RFamide peptides derived from the same precursor, i.e. GSLFRFamide, SSLFRFamide and GALFRFamide, specifically activate the receptor in a dose-dependent manner, with respective EC50 values (half-maximal effective concentrations) of 1.1, 2.1 and 4.1 mu mol l(-1). We found that both Cg-sNPFR-like receptor and LFRFamide encoding transcripts are expressed in the oyster central nervous system and in other tissues as well, albeit at lower levels. Mass spectrometry analysis confirmed the wide distribution of LFRFamide mature peptides in several central and peripheral tissues. The Cg-sNPFR-like receptor was more abundantly expressed in ganglia of females than of males, and upregulated in starved oysters. In the gonad area, highest receptor gene expression occurred at the start of gametogenesis, when storage activity is maximal. Our results suggest that signaling of LFRFamide peptides through the Cg-sNPFR-like receptor might play a role in the coordination of nutrition, energy storage and metabolism in C. gigas, possibly by promoting storage at the expense of reproduction.
author2 Biologie des Organismes et Ecosystèmes Aquatiques (BOREA)
Université de Caen Normandie (UNICAEN)
Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)
Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR)
Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM)
Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)
ANR-08-GENM-0041,Gametogenes,Génomiques de la gamétogénèse chez l'huître creuse Crassostrea gigas(2008)
format Article in Journal/Newspaper
author Bigot, Laetitia
Beets, Isabel
Dubos, Marie-Pierre
Boudry, Pierre
Schoofs, Liliane
Favrel, Pascal
author_facet Bigot, Laetitia
Beets, Isabel
Dubos, Marie-Pierre
Boudry, Pierre
Schoofs, Liliane
Favrel, Pascal
author_sort Bigot, Laetitia
title Functional characterization of a short neuropeptide F-related receptor in a lophotrochozoan, the mollusk Crassostrea gigas
title_short Functional characterization of a short neuropeptide F-related receptor in a lophotrochozoan, the mollusk Crassostrea gigas
title_full Functional characterization of a short neuropeptide F-related receptor in a lophotrochozoan, the mollusk Crassostrea gigas
title_fullStr Functional characterization of a short neuropeptide F-related receptor in a lophotrochozoan, the mollusk Crassostrea gigas
title_full_unstemmed Functional characterization of a short neuropeptide F-related receptor in a lophotrochozoan, the mollusk Crassostrea gigas
title_sort functional characterization of a short neuropeptide f-related receptor in a lophotrochozoan, the mollusk crassostrea gigas
publisher HAL CCSD
publishDate 2014
url https://hal.science/hal-02548665
https://doi.org/10.1242/jeb.104067
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source ISSN: 0022-0949
EISSN: 1477-9145
Journal of Experimental Biology
https://hal.science/hal-02548665
Journal of Experimental Biology, 2014, 217 (16), pp.2974--2982. ⟨10.1242/jeb.104067⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1242/jeb.104067
hal-02548665
https://hal.science/hal-02548665
doi:10.1242/jeb.104067
op_doi https://doi.org/10.1242/jeb.104067
container_title Journal of Experimental Biology
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