Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family
Deorphanization of GPR54 receptor a decade ago led to the characterization of the kisspeptin receptor (Kissr) in mammals and the discovery of its major role in the brain control of reproduction. While a single gene encodes for Kissr in eutherian mammals including human, other vertebrates present a v...
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ftpubmed:oai:pubmedcentral.nih.gov:3502363 2023-05-15T16:08:42+02:00 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 2012-11-20 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3502363 http://www.ncbi.nlm.nih.gov/pubmed/23185286 https://doi.org/10.1371/journal.pone.0048931 en eng Public Library of Science http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3502363 http://www.ncbi.nlm.nih.gov/pubmed/23185286 http://dx.doi.org/10.1371/journal.pone.0048931 This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. CC-BY Research Article Text 2012 ftpubmed https://doi.org/10.1371/journal.pone.0048931 2013-09-04T16:09:03Z Deorphanization of GPR54 receptor a decade ago led to the characterization of the kisspeptin receptor (Kissr) in mammals and the discovery of its major role in the brain control of reproduction. While a single gene encodes for Kissr in eutherian mammals including human, other vertebrates present a variable number of Kissr genes, from none in birds, one or two in teleosts, to three in an amphibian, xenopus. In order to get more insight into the evolution of Kissr gene family, we investigated the presence of Kissr in osteichthyans of key-phylogenetical positions: the coelacanth, a representative of early sarcopterygians, the spotted gar, a non-teleost actinopterygian, and the European eel, a member of an early group of teleosts (elopomorphs). We report the occurrence of three Kissr for the first time in a teleost, the eel. As measured by quantitative RT-PCR, the three eel Kissr were differentially expressed in the brain-pituitary-gonadal axis, and differentially regulated in experimentally matured eels, as compared to prepubertal controls. Subfunctionalisation, as shown by these differences in tissue distribution and regulation, may have represented significant evolutionary constraints for the conservation of multiple Kissr paralogs in this species. Furthermore, we identified four Kissr in both coelacanth and spotted gar genomes, providing the first evidence for the presence of four Kissr in vertebrates. Phylogenetic and syntenic analyses supported 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 two rounds of whole genome duplication (1R and 2R) in early vertebrates, followed by multiple gene loss events in the actinopterygian and sarcopterygian lineages. Due to gene loss there was no impact of the teleost-specific whole genome duplication (3R) on the number of Kissr paralogs in current teleosts. Text European eel PubMed Central (PMC) Gar’ ENVELOPE(162.014,162.014,57.140,57.140) PLoS ONE 7 11 e48931 |
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PubMed Central (PMC) |
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English |
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Research Article |
spellingShingle |
Research Article 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 |
Research Article |
description |
Deorphanization of GPR54 receptor a decade ago led to the characterization of the kisspeptin receptor (Kissr) in mammals and the discovery of its major role in the brain control of reproduction. While a single gene encodes for Kissr in eutherian mammals including human, other vertebrates present a variable number of Kissr genes, from none in birds, one or two in teleosts, to three in an amphibian, xenopus. In order to get more insight into the evolution of Kissr gene family, we investigated the presence of Kissr in osteichthyans of key-phylogenetical positions: the coelacanth, a representative of early sarcopterygians, the spotted gar, a non-teleost actinopterygian, and the European eel, a member of an early group of teleosts (elopomorphs). We report the occurrence of three Kissr for the first time in a teleost, the eel. As measured by quantitative RT-PCR, the three eel Kissr were differentially expressed in the brain-pituitary-gonadal axis, and differentially regulated in experimentally matured eels, as compared to prepubertal controls. Subfunctionalisation, as shown by these differences in tissue distribution and regulation, may have represented significant evolutionary constraints for the conservation of multiple Kissr paralogs in this species. Furthermore, we identified four Kissr in both coelacanth and spotted gar genomes, providing the first evidence for the presence of four Kissr in vertebrates. Phylogenetic and syntenic analyses supported 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 two rounds of whole genome duplication (1R and 2R) in early vertebrates, followed by multiple gene loss events in the actinopterygian and sarcopterygian lineages. Due to gene loss there was no impact of the teleost-specific whole genome duplication (3R) on the number of Kissr paralogs in current teleosts. |
format |
Text |
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 |
Public Library of Science |
publishDate |
2012 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3502363 http://www.ncbi.nlm.nih.gov/pubmed/23185286 https://doi.org/10.1371/journal.pone.0048931 |
long_lat |
ENVELOPE(162.014,162.014,57.140,57.140) |
geographic |
Gar’ |
geographic_facet |
Gar’ |
genre |
European eel |
genre_facet |
European eel |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3502363 http://www.ncbi.nlm.nih.gov/pubmed/23185286 http://dx.doi.org/10.1371/journal.pone.0048931 |
op_rights |
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1371/journal.pone.0048931 |
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PLoS ONE |
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7 |
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11 |
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e48931 |
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