Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates
Since its discovery in mammals as a key-hormone in reproduction and metabolism, leptin has been identified in an increasing number of tetrapods and teleosts. Tetrapods possess only one leptin gene, while most teleosts possess two leptin genes, as a result of the teleost third whole genome duplicatio...
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ftpubmed:oai:pubmedcentral.nih.gov:4422726 2023-05-15T16:08:41+02:00 Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates Morini, Marina Pasquier, Jérémy Dirks, Ron van den Thillart, Guido Tomkiewicz, Jonna Rousseau, Karine Dufour, Sylvie Lafont, Anne-Gaëlle 2015-05-06 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4422726/ http://www.ncbi.nlm.nih.gov/pubmed/25946034 https://doi.org/10.1371/journal.pone.0126008 en eng Public Library of Science http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4422726/ http://www.ncbi.nlm.nih.gov/pubmed/25946034 http://dx.doi.org/10.1371/journal.pone.0126008 http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited CC-BY Research Article Text 2015 ftpubmed https://doi.org/10.1371/journal.pone.0126008 2015-05-17T00:08:27Z Since its discovery in mammals as a key-hormone in reproduction and metabolism, leptin has been identified in an increasing number of tetrapods and teleosts. Tetrapods possess only one leptin gene, while most teleosts possess two leptin genes, as a result of the teleost third whole genome duplication event (3R). Leptin acts through a specific receptor (LEPR). In the European and Japanese eels, we identified two leptin genes, and for the first time in vertebrates, two LEPR genes. Synteny analyses indicated that eel LEPRa and LEPRb result from teleost 3R. LEPRb seems to have been lost in the teleost lineage shortly after the elopomorph divergence. Quantitative PCRs revealed a wide distribution of leptins and LEPRs in the European eel, including tissues involved in metabolism and reproduction. Noticeably, leptin1 was expressed in fat tissue, while leptin2 in the liver, reflecting subfunctionalization. Four-month fasting had no impact on the expression of leptins and LEPRs in control European eels. This might be related to the remarkable adaptation of silver eel metabolism to long-term fasting throughout the reproductive oceanic migration. In contrast, sexual maturation induced differential increases in the expression of leptins and LEPRs in the BPG-liver axis. Leptin2 was strikingly upregulated in the liver, the central organ of the reproductive metabolic challenge in teleosts. LEPRs were differentially regulated during sexual maturation, which may have contributed to the conservation of the duplicated LEPRs in this species. This suggests an ancient and positive role of the leptin system in the vertebrate reproductive function. This study brings new insights on the evolutionary history of the leptin system in vertebrates. Among extant vertebrates, the eel represents a unique case of duplicated leptins and leptin receptors as a result of 3R. Text European eel PubMed Central (PMC) PLOS ONE 10 5 e0126008 |
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Research Article Morini, Marina Pasquier, Jérémy Dirks, Ron van den Thillart, Guido Tomkiewicz, Jonna Rousseau, Karine Dufour, Sylvie Lafont, Anne-Gaëlle Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates |
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Research Article |
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Since its discovery in mammals as a key-hormone in reproduction and metabolism, leptin has been identified in an increasing number of tetrapods and teleosts. Tetrapods possess only one leptin gene, while most teleosts possess two leptin genes, as a result of the teleost third whole genome duplication event (3R). Leptin acts through a specific receptor (LEPR). In the European and Japanese eels, we identified two leptin genes, and for the first time in vertebrates, two LEPR genes. Synteny analyses indicated that eel LEPRa and LEPRb result from teleost 3R. LEPRb seems to have been lost in the teleost lineage shortly after the elopomorph divergence. Quantitative PCRs revealed a wide distribution of leptins and LEPRs in the European eel, including tissues involved in metabolism and reproduction. Noticeably, leptin1 was expressed in fat tissue, while leptin2 in the liver, reflecting subfunctionalization. Four-month fasting had no impact on the expression of leptins and LEPRs in control European eels. This might be related to the remarkable adaptation of silver eel metabolism to long-term fasting throughout the reproductive oceanic migration. In contrast, sexual maturation induced differential increases in the expression of leptins and LEPRs in the BPG-liver axis. Leptin2 was strikingly upregulated in the liver, the central organ of the reproductive metabolic challenge in teleosts. LEPRs were differentially regulated during sexual maturation, which may have contributed to the conservation of the duplicated LEPRs in this species. This suggests an ancient and positive role of the leptin system in the vertebrate reproductive function. This study brings new insights on the evolutionary history of the leptin system in vertebrates. Among extant vertebrates, the eel represents a unique case of duplicated leptins and leptin receptors as a result of 3R. |
format |
Text |
author |
Morini, Marina Pasquier, Jérémy Dirks, Ron van den Thillart, Guido Tomkiewicz, Jonna Rousseau, Karine Dufour, Sylvie Lafont, Anne-Gaëlle |
author_facet |
Morini, Marina Pasquier, Jérémy Dirks, Ron van den Thillart, Guido Tomkiewicz, Jonna Rousseau, Karine Dufour, Sylvie Lafont, Anne-Gaëlle |
author_sort |
Morini, Marina |
title |
Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates |
title_short |
Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates |
title_full |
Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates |
title_fullStr |
Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates |
title_full_unstemmed |
Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates |
title_sort |
duplicated leptin receptors in two species of eel bring new insights into the evolution of the leptin system in vertebrates |
publisher |
Public Library of Science |
publishDate |
2015 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4422726/ http://www.ncbi.nlm.nih.gov/pubmed/25946034 https://doi.org/10.1371/journal.pone.0126008 |
genre |
European eel |
genre_facet |
European eel |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4422726/ http://www.ncbi.nlm.nih.gov/pubmed/25946034 http://dx.doi.org/10.1371/journal.pone.0126008 |
op_rights |
http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited |
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CC-BY |
op_doi |
https://doi.org/10.1371/journal.pone.0126008 |
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PLOS ONE |
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10 |
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5 |
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e0126008 |
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