Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family

International audience Deorphanization of GPR54 receptor a decade ago led to the characterization of the kisspeptin receptor (Kissr) in mammalsand the discovery of its major role in the brain control of reproduction. While a single gene encodes for Kissr in eutherianmammals including human, other ve...

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Published in:PLoS ONE
Main Authors: Pasquier, Jérémy, Lafont, Anne-Gaëlle, Jeng, Shan-Ru, Morini, Marina, Dirks, Ron, van den Thillart, Guido, Tomkiewicz, Jonna, Tostivint, Hervé, Chang, Ching-Fong, Rousseau, Karine, Dufour, Sylvie
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), Institut de recherche en santé, environnement et travail (Irset), Université d'Angers (UA)-Université de Rennes (UR)-École des Hautes Études en Santé Publique EHESP (EHESP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ), Universitat Politècnica de València = Universitad Politecnica de Valencia = Polytechnic University of Valencia (UPV), Universiteit Leiden = Leiden University, DTU Aqua, National Institute of Aquatic Resources, Danmarks Tekniske Universitet = Technical University of Denmark (DTU), Neuroendocrinologie cellulaire et moléculaire, Université de Rouen Normandie (UNIROUEN), Normandie Université (NU)-Normandie Université (NU)-Institut National de la Santé et de la Recherche Médicale (INSERM), National Taiwan Ocean University (NTOU), ANR-08-BLAN-0173,Puberteel,Neuroendocrine control of eel puberty.(2008)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2012
Subjects:
Online Access:https://mnhn.hal.science/mnhn-02861073
https://mnhn.hal.science/mnhn-02861073/document
https://mnhn.hal.science/mnhn-02861073/file/pone.0048931.pdf
https://doi.org/10.1371/journal.pone.0048931
id ftanrparis:oai:HAL:mnhn-02861073v1
record_format openpolar
institution Open Polar
collection Portail HAL-ANR (Agence Nationale de la Recherche)
op_collection_id ftanrparis
language English
topic [SDV]Life Sciences [q-bio]
spellingShingle [SDV]Life Sciences [q-bio]
Pasquier, Jérémy
Lafont, Anne-Gaëlle
Jeng, Shan-Ru
Morini, Marina
Dirks, Ron
van den Thillart, Guido
Tomkiewicz, Jonna
Tostivint, Hervé
Chang, Ching-Fong
Rousseau, Karine
Dufour, Sylvie
Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family
topic_facet [SDV]Life Sciences [q-bio]
description International audience Deorphanization of GPR54 receptor a decade ago led to the characterization of the kisspeptin receptor (Kissr) in mammalsand the discovery of its major role in the brain control of reproduction. While a single gene encodes for Kissr in eutherianmammals including human, other vertebrates present a variable number of Kissr genes, from none in birds, one or two inteleosts, to three in an amphibian, xenopus. In order to get more insight into the evolution of Kissr gene family, weinvestigated the presence of Kissr in osteichthyans of key-phylogenetical positions: the coelacanth, a representative of earlysarcopterygians, the spotted gar, a non-teleost actinopterygian, and the European eel, a member of an early group ofteleosts (elopomorphs). We report the occurrence of three Kissr for the first time in a teleost, the eel. As measured byquantitative RT-PCR, the three eel Kissr were differentially expressed in the brain-pituitary-gonadal axis, and differentiallyregulated in experimentally matured eels, as compared to prepubertal controls. Subfunctionalisation, as shown by thesedifferences in tissue distribution and regulation, may have represented significant evolutionary constraints for theconservation of multiple Kissr paralogs in this species. Furthermore, we identified four Kissr in both coelacanth and spottedgar genomes, providing the first evidence for the presence of four Kissr in vertebrates. Phylogenetic and syntenic analysessupported the existence of four Kissr paralogs in osteichthyans and allowed to propose a clarified nomenclature of Kissr(Kissr-1 to -4) based on these paralogs. Syntenic analysis suggested that the four Kissr paralogs arose through the tworounds of whole genome duplication (1R and 2R) in early vertebrates, followed by multiple gene loss events in theactinopterygian and sarcopterygian lineages. Due to gene loss there was no impact of the teleost-specific whole genomeduplication (3R) on the number of Kissr paralogs in current teleosts.
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)
Institut de recherche en santé, environnement et travail (Irset)
Université d'Angers (UA)-Université de Rennes (UR)-École des Hautes Études en Santé Publique EHESP (EHESP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique )
Universitat Politècnica de València = Universitad Politecnica de Valencia = Polytechnic University of Valencia (UPV)
Universiteit Leiden = Leiden University
DTU Aqua, National Institute of Aquatic Resources
Danmarks Tekniske Universitet = Technical University of Denmark (DTU)
Neuroendocrinologie cellulaire et moléculaire
Université de Rouen Normandie (UNIROUEN)
Normandie Université (NU)-Normandie Université (NU)-Institut National de la Santé et de la Recherche Médicale (INSERM)
National Taiwan Ocean University (NTOU)
ANR-08-BLAN-0173,Puberteel,Neuroendocrine control of eel puberty.(2008)
format Article in Journal/Newspaper
author Pasquier, Jérémy
Lafont, Anne-Gaëlle
Jeng, Shan-Ru
Morini, Marina
Dirks, Ron
van den Thillart, Guido
Tomkiewicz, Jonna
Tostivint, Hervé
Chang, Ching-Fong
Rousseau, Karine
Dufour, Sylvie
author_facet Pasquier, Jérémy
Lafont, Anne-Gaëlle
Jeng, Shan-Ru
Morini, Marina
Dirks, Ron
van den Thillart, Guido
Tomkiewicz, Jonna
Tostivint, Hervé
Chang, Ching-Fong
Rousseau, Karine
Dufour, Sylvie
author_sort Pasquier, Jérémy
title Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family
title_short Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family
title_full Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family
title_fullStr Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family
title_full_unstemmed Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family
title_sort multiple kisspeptin receptors in early osteichthyans provide new insights into the evolution of this receptor family
publisher HAL CCSD
publishDate 2012
url https://mnhn.hal.science/mnhn-02861073
https://mnhn.hal.science/mnhn-02861073/document
https://mnhn.hal.science/mnhn-02861073/file/pone.0048931.pdf
https://doi.org/10.1371/journal.pone.0048931
genre European eel
genre_facet European eel
op_source ISSN: 1932-6203
EISSN: 1932-6203
PLoS ONE
https://mnhn.hal.science/mnhn-02861073
PLoS ONE, 2012, 7 (11), pp.e48931. ⟨10.1371/journal.pone.0048931⟩
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container_title PLoS ONE
container_volume 7
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spelling ftanrparis:oai:HAL:mnhn-02861073v1 2024-04-21T08:01:41+00:00 Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family Pasquier, Jérémy Lafont, Anne-Gaëlle Jeng, Shan-Ru Morini, Marina Dirks, Ron van den Thillart, Guido Tomkiewicz, Jonna Tostivint, Hervé Chang, Ching-Fong Rousseau, Karine Dufour, Sylvie 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) Institut de recherche en santé, environnement et travail (Irset) Université d'Angers (UA)-Université de Rennes (UR)-École des Hautes Études en Santé Publique EHESP (EHESP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ) Universitat Politècnica de València = Universitad Politecnica de Valencia = Polytechnic University of Valencia (UPV) Universiteit Leiden = Leiden University DTU Aqua, National Institute of Aquatic Resources Danmarks Tekniske Universitet = Technical University of Denmark (DTU) Neuroendocrinologie cellulaire et moléculaire Université de Rouen Normandie (UNIROUEN) Normandie Université (NU)-Normandie Université (NU)-Institut National de la Santé et de la Recherche Médicale (INSERM) National Taiwan Ocean University (NTOU) ANR-08-BLAN-0173,Puberteel,Neuroendocrine control of eel puberty.(2008) 2012-11-20 https://mnhn.hal.science/mnhn-02861073 https://mnhn.hal.science/mnhn-02861073/document https://mnhn.hal.science/mnhn-02861073/file/pone.0048931.pdf https://doi.org/10.1371/journal.pone.0048931 en eng HAL CCSD Public Library of Science info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0048931 mnhn-02861073 https://mnhn.hal.science/mnhn-02861073 https://mnhn.hal.science/mnhn-02861073/document https://mnhn.hal.science/mnhn-02861073/file/pone.0048931.pdf doi:10.1371/journal.pone.0048931 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1932-6203 EISSN: 1932-6203 PLoS ONE https://mnhn.hal.science/mnhn-02861073 PLoS ONE, 2012, 7 (11), pp.e48931. ⟨10.1371/journal.pone.0048931⟩ [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2012 ftanrparis https://doi.org/10.1371/journal.pone.0048931 2024-03-26T18:17:47Z International audience Deorphanization of GPR54 receptor a decade ago led to the characterization of the kisspeptin receptor (Kissr) in mammalsand the discovery of its major role in the brain control of reproduction. While a single gene encodes for Kissr in eutherianmammals including human, other vertebrates present a variable number of Kissr genes, from none in birds, one or two inteleosts, to three in an amphibian, xenopus. In order to get more insight into the evolution of Kissr gene family, weinvestigated the presence of Kissr in osteichthyans of key-phylogenetical positions: the coelacanth, a representative of earlysarcopterygians, the spotted gar, a non-teleost actinopterygian, and the European eel, a member of an early group ofteleosts (elopomorphs). We report the occurrence of three Kissr for the first time in a teleost, the eel. As measured byquantitative RT-PCR, the three eel Kissr were differentially expressed in the brain-pituitary-gonadal axis, and differentiallyregulated in experimentally matured eels, as compared to prepubertal controls. Subfunctionalisation, as shown by thesedifferences in tissue distribution and regulation, may have represented significant evolutionary constraints for theconservation of multiple Kissr paralogs in this species. Furthermore, we identified four Kissr in both coelacanth and spottedgar genomes, providing the first evidence for the presence of four Kissr in vertebrates. Phylogenetic and syntenic analysessupported the existence of four Kissr paralogs in osteichthyans and allowed to propose a clarified nomenclature of Kissr(Kissr-1 to -4) based on these paralogs. Syntenic analysis suggested that the four Kissr paralogs arose through the tworounds of whole genome duplication (1R and 2R) in early vertebrates, followed by multiple gene loss events in theactinopterygian and sarcopterygian lineages. Due to gene loss there was no impact of the teleost-specific whole genomeduplication (3R) on the number of Kissr paralogs in current teleosts. Article in Journal/Newspaper European eel Portail HAL-ANR (Agence Nationale de la Recherche) PLoS ONE 7 11 e48931