Emergence of a cholecystokinin/sulfakinin signalling system in Lophotrochozoa
International audience Chordate gastrin/cholecystokinin (G/CCK) and ecdysozoan sulfakinin (SK) signalling systems represent divergent evolutionary scenarios of a common ancestral signalling system. The present article investigates for the first time the evolution of the CCK/SK signalling system in a...
Published in: | Scientific Reports |
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ftsorbonneuniv:oai:HAL:hal-01927201v1 2024-09-15T18:03:16+00:00 Emergence of a cholecystokinin/sulfakinin signalling system in Lophotrochozoa Schwartz, Julie Dubos, Marie-Pierre Pasquier, Jeremy Zatylny-Gaudin, Céline 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) ANR-14-CE02-0020,NEMO,Neuropeptides d'organismes marins(2014) 2018-12 https://hal.sorbonne-universite.fr/hal-01927201 https://hal.sorbonne-universite.fr/hal-01927201/document https://hal.sorbonne-universite.fr/hal-01927201/file/s41598-018-34700-4.pdf https://doi.org/10.1038/s41598-018-34700-4 en eng HAL CCSD Nature Publishing Group info:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-018-34700-4 hal-01927201 https://hal.sorbonne-universite.fr/hal-01927201 https://hal.sorbonne-universite.fr/hal-01927201/document https://hal.sorbonne-universite.fr/hal-01927201/file/s41598-018-34700-4.pdf doi:10.1038/s41598-018-34700-4 info:eu-repo/semantics/OpenAccess ISSN: 2045-2322 EISSN: 2045-2322 Scientific Reports https://hal.sorbonne-universite.fr/hal-01927201 Scientific Reports, 2018, 8 (1), pp.16424. ⟨10.1038/s41598-018-34700-4⟩ [SDV]Life Sciences [q-bio] [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology info:eu-repo/semantics/article Journal articles 2018 ftsorbonneuniv https://doi.org/10.1038/s41598-018-34700-4 2024-07-25T23:48:05Z International audience Chordate gastrin/cholecystokinin (G/CCK) and ecdysozoan sulfakinin (SK) signalling systems represent divergent evolutionary scenarios of a common ancestral signalling system. The present article investigates for the first time the evolution of the CCK/SK signalling system in a member of the Lophotrochozoa, the second clade of protostome animals. We identified two G protein-coupled receptors (GPCR) in the oyster Crassostrea gigas (Mollusca), phylogenetically related to chordate CCK receptors (CCKR) and to ecdysozoan sulfakinin receptors (SKR). These receptors, Cragi-CCKR1 and Cragi-CCKR2, were characterised functionally using a cell-based assay. We identified di- and mono-sulphated forms of oyster Cragi-CCK1 (pEGAWDY(SO3H)DY(SO3H)GLGGGRF-NH2) as the potent endogenous agonists for these receptors. The Cragi-CCK genes were expressed in the visceral ganglia of the nervous system. The Cragi-CCKR1 gene was expressed in a variety of tissues, while Cragi-CCKR2 gene expression was more restricted to nervous tissues. An in vitro bioassay revealed that different forms of Cragi-CCK1 decreased the frequency of the spontaneous contractions of oyster hindgut. Expression analyses in oysters with contrasted nutritional statuses or in the course of their reproductive cycle highlighted the plausible role of Cragi-CCK signalling in the regulation of feeding and its possible involvement in the coordination of nutrition and energy storage in the gonad. This study confirms the early origin of the CCK/SK signalling system from the common bilaterian ancestor and delivers new insights into its structural and functional evolution in the lophotrochozoan lineage. Article in Journal/Newspaper Crassostrea gigas HAL Sorbonne Université Scientific Reports 8 1 |
institution |
Open Polar |
collection |
HAL Sorbonne Université |
op_collection_id |
ftsorbonneuniv |
language |
English |
topic |
[SDV]Life Sciences [q-bio] [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology |
spellingShingle |
[SDV]Life Sciences [q-bio] [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology Schwartz, Julie Dubos, Marie-Pierre Pasquier, Jeremy Zatylny-Gaudin, Céline Favrel, Pascal Emergence of a cholecystokinin/sulfakinin signalling system in Lophotrochozoa |
topic_facet |
[SDV]Life Sciences [q-bio] [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology |
description |
International audience Chordate gastrin/cholecystokinin (G/CCK) and ecdysozoan sulfakinin (SK) signalling systems represent divergent evolutionary scenarios of a common ancestral signalling system. The present article investigates for the first time the evolution of the CCK/SK signalling system in a member of the Lophotrochozoa, the second clade of protostome animals. We identified two G protein-coupled receptors (GPCR) in the oyster Crassostrea gigas (Mollusca), phylogenetically related to chordate CCK receptors (CCKR) and to ecdysozoan sulfakinin receptors (SKR). These receptors, Cragi-CCKR1 and Cragi-CCKR2, were characterised functionally using a cell-based assay. We identified di- and mono-sulphated forms of oyster Cragi-CCK1 (pEGAWDY(SO3H)DY(SO3H)GLGGGRF-NH2) as the potent endogenous agonists for these receptors. The Cragi-CCK genes were expressed in the visceral ganglia of the nervous system. The Cragi-CCKR1 gene was expressed in a variety of tissues, while Cragi-CCKR2 gene expression was more restricted to nervous tissues. An in vitro bioassay revealed that different forms of Cragi-CCK1 decreased the frequency of the spontaneous contractions of oyster hindgut. Expression analyses in oysters with contrasted nutritional statuses or in the course of their reproductive cycle highlighted the plausible role of Cragi-CCK signalling in the regulation of feeding and its possible involvement in the coordination of nutrition and energy storage in the gonad. This study confirms the early origin of the CCK/SK signalling system from the common bilaterian ancestor and delivers new insights into its structural and functional evolution in the lophotrochozoan lineage. |
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) ANR-14-CE02-0020,NEMO,Neuropeptides d'organismes marins(2014) |
format |
Article in Journal/Newspaper |
author |
Schwartz, Julie Dubos, Marie-Pierre Pasquier, Jeremy Zatylny-Gaudin, Céline Favrel, Pascal |
author_facet |
Schwartz, Julie Dubos, Marie-Pierre Pasquier, Jeremy Zatylny-Gaudin, Céline Favrel, Pascal |
author_sort |
Schwartz, Julie |
title |
Emergence of a cholecystokinin/sulfakinin signalling system in Lophotrochozoa |
title_short |
Emergence of a cholecystokinin/sulfakinin signalling system in Lophotrochozoa |
title_full |
Emergence of a cholecystokinin/sulfakinin signalling system in Lophotrochozoa |
title_fullStr |
Emergence of a cholecystokinin/sulfakinin signalling system in Lophotrochozoa |
title_full_unstemmed |
Emergence of a cholecystokinin/sulfakinin signalling system in Lophotrochozoa |
title_sort |
emergence of a cholecystokinin/sulfakinin signalling system in lophotrochozoa |
publisher |
HAL CCSD |
publishDate |
2018 |
url |
https://hal.sorbonne-universite.fr/hal-01927201 https://hal.sorbonne-universite.fr/hal-01927201/document https://hal.sorbonne-universite.fr/hal-01927201/file/s41598-018-34700-4.pdf https://doi.org/10.1038/s41598-018-34700-4 |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
ISSN: 2045-2322 EISSN: 2045-2322 Scientific Reports https://hal.sorbonne-universite.fr/hal-01927201 Scientific Reports, 2018, 8 (1), pp.16424. ⟨10.1038/s41598-018-34700-4⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-018-34700-4 hal-01927201 https://hal.sorbonne-universite.fr/hal-01927201 https://hal.sorbonne-universite.fr/hal-01927201/document https://hal.sorbonne-universite.fr/hal-01927201/file/s41598-018-34700-4.pdf doi:10.1038/s41598-018-34700-4 |
op_rights |
info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1038/s41598-018-34700-4 |
container_title |
Scientific Reports |
container_volume |
8 |
container_issue |
1 |
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1810440784812441600 |