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...

Full description

Bibliographic Details
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
Description
Summary: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.