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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Published in:PLoS ONE
Main Authors: Jérémy Pasquier, Anne-Gaëlle Lafont, Shan-Ru Jeng, Marina Morini, Ron Dirks, Guido van den Thillart, Jonna Tomkiewicz, Hervé Tostivint, Ching-Fong Chang, Karine Rousseau, Sylvie Dufour
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2012
Subjects:
R
Q
Online Access:https://doi.org/10.1371/journal.pone.0048931
https://doaj.org/article/7e03c4233d214acc8ffc72659267e905
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spelling ftdoajarticles:oai:doaj.org/article:7e03c4233d214acc8ffc72659267e905 2023-05-15T16:08:42+02:00 Multiple kisspeptin receptors in early osteichthyans provide new insights into the evolution of this receptor family. Jérémy Pasquier Anne-Gaëlle Lafont Shan-Ru Jeng Marina Morini Ron Dirks Guido van den Thillart Jonna Tomkiewicz Hervé Tostivint Ching-Fong Chang Karine Rousseau Sylvie Dufour 2012-01-01T00:00:00Z https://doi.org/10.1371/journal.pone.0048931 https://doaj.org/article/7e03c4233d214acc8ffc72659267e905 EN eng Public Library of Science (PLoS) http://europepmc.org/articles/PMC3502363?pdf=render https://doaj.org/toc/1932-6203 1932-6203 doi:10.1371/journal.pone.0048931 https://doaj.org/article/7e03c4233d214acc8ffc72659267e905 PLoS ONE, Vol 7, Iss 11, p e48931 (2012) Medicine R Science Q article 2012 ftdoajarticles https://doi.org/10.1371/journal.pone.0048931 2022-12-30T23:06:35Z 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. Article in Journal/Newspaper European eel Directory of Open Access Journals: DOAJ Articles Gar’ ENVELOPE(162.014,162.014,57.140,57.140) PLoS ONE 7 11 e48931
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Jérémy Pasquier
Anne-Gaëlle Lafont
Shan-Ru Jeng
Marina Morini
Ron Dirks
Guido van den Thillart
Jonna Tomkiewicz
Hervé Tostivint
Ching-Fong Chang
Karine Rousseau
Sylvie Dufour
Multiple kisspeptin receptors in early osteichthyans provide new insights into the evolution of this receptor family.
topic_facet Medicine
R
Science
Q
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 Article in Journal/Newspaper
author Jérémy Pasquier
Anne-Gaëlle Lafont
Shan-Ru Jeng
Marina Morini
Ron Dirks
Guido van den Thillart
Jonna Tomkiewicz
Hervé Tostivint
Ching-Fong Chang
Karine Rousseau
Sylvie Dufour
author_facet Jérémy Pasquier
Anne-Gaëlle Lafont
Shan-Ru Jeng
Marina Morini
Ron Dirks
Guido van den Thillart
Jonna Tomkiewicz
Hervé Tostivint
Ching-Fong Chang
Karine Rousseau
Sylvie Dufour
author_sort Jérémy Pasquier
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 (PLoS)
publishDate 2012
url https://doi.org/10.1371/journal.pone.0048931
https://doaj.org/article/7e03c4233d214acc8ffc72659267e905
long_lat ENVELOPE(162.014,162.014,57.140,57.140)
geographic Gar’
geographic_facet Gar’
genre European eel
genre_facet European eel
op_source PLoS ONE, Vol 7, Iss 11, p e48931 (2012)
op_relation http://europepmc.org/articles/PMC3502363?pdf=render
https://doaj.org/toc/1932-6203
1932-6203
doi:10.1371/journal.pone.0048931
https://doaj.org/article/7e03c4233d214acc8ffc72659267e905
op_doi https://doi.org/10.1371/journal.pone.0048931
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