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...
Published in: | Journal of Experimental Biology |
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Main Authors: | , , , , , |
Other Authors: | , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2014
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Subjects: | |
Online Access: | https://hal.archives-ouvertes.fr/hal-02548665 https://doi.org/10.1242/jeb.104067 |
id |
ftccsdartic:oai:HAL:hal-02548665v1 |
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openpolar |
institution |
Open Polar |
collection |
Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) |
op_collection_id |
ftccsdartic |
language |
English |
topic |
Starvation sNPF ACL Crassostrea gigas Energy metabolism Oyster Reproduction [SDE.BE]Environmental Sciences/Biodiversity and Ecology |
spellingShingle |
Starvation sNPF ACL Crassostrea gigas Energy metabolism Oyster Reproduction [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 |
Starvation sNPF ACL Crassostrea gigas Energy metabolism Oyster Reproduction [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) Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU) 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 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 - Brest (IFREMER Centre de Bretagne) 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.archives-ouvertes.fr/hal-02548665 https://doi.org/10.1242/jeb.104067 |
geographic |
Pacific |
geographic_facet |
Pacific |
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.archives-ouvertes.fr/hal-02548665 Journal of Experimental Biology, The Company of Biologists, 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.archives-ouvertes.fr/hal-02548665 doi:10.1242/jeb.104067 |
op_doi |
https://doi.org/10.1242/jeb.104067 |
container_title |
Journal of Experimental Biology |
_version_ |
1766393524941488128 |
spelling |
ftccsdartic:oai:HAL:hal-02548665v1 2023-05-15T15:57:49+02:00 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) Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU) 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 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 - Brest (IFREMER Centre de Bretagne) 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.archives-ouvertes.fr/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.archives-ouvertes.fr/hal-02548665 doi:10.1242/jeb.104067 ISSN: 0022-0949 EISSN: 1477-9145 Journal of Experimental Biology https://hal.archives-ouvertes.fr/hal-02548665 Journal of Experimental Biology, The Company of Biologists, 2014, 217 (16), pp.2974--2982. ⟨10.1242/jeb.104067⟩ Starvation sNPF ACL Crassostrea gigas Energy metabolism Oyster Reproduction [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2014 ftccsdartic https://doi.org/10.1242/jeb.104067 2021-12-19T01:22:59Z 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 Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Pacific Journal of Experimental Biology |