Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates
Identifieur interne : 000004 ( France/Analysis ); précédent : 000003; suivant : 000005Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates
Auteurs : Marina Morini [France] ; Jérémy Pasquier [France] ; Ron Dirks [Pays-Bas] ; Guido Van Den Thillart [Pays-Bas] ; Jonna Tomkiewicz [Danemark] ; Karine Rousseau [France] ; Sylvie Dufour [France] ; Anne-Gaëlle Lafont [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2015.
Abstract
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.
Url:
DOI: 10.1371/journal.pone.0126008
PubMed: 25946034
PubMed Central: 4422726
Affiliations:
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PMC:4422726Le document en format XML
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Organisms and Ecosystems, CNRS 7208, IRD207, UPMC, UCBN, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Muséum National d'Histoire Naturelle, Sorbonne Universités, Research Unit BOREA, Biology of Aquatic Organisms and Ecosystems, CNRS 7208, IRD207, UPMC, UCBN, Paris</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>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.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zhang, Y" uniqKey="Zhang Y">Y Zhang</name></author><author><name sortKey="Proenca, R" uniqKey="Proenca R">R Proenca</name></author><author><name sortKey="Maffei, M" uniqKey="Maffei M">M Maffei</name></author><author><name sortKey="Barone, M" uniqKey="Barone M">M Barone</name></author><author><name sortKey="Leopold, L" uniqKey="Leopold L">L Leopold</name></author><author><name sortKey="Friedman, Jm" uniqKey="Friedman J">JM Friedman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Huising, Mo" uniqKey="Huising M">MO Huising</name></author><author><name sortKey="Kruiswijk, Cp" uniqKey="Kruiswijk C">CP Kruiswijk</name></author><author><name sortKey="Flik, G" uniqKey="Flik G">G 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Gg" uniqKey="Li G">GG Li</name></author><author><name sortKey="Liang, Xf" uniqKey="Liang X">XF Liang</name></author><author><name sortKey="Xie, Q" uniqKey="Xie Q">Q Xie</name></author><author><name sortKey="Li, G" uniqKey="Li G">G Li</name></author><author><name sortKey="Yu, Y" uniqKey="Yu Y">Y Yu</name></author><author><name sortKey="Lai, K" uniqKey="Lai K">K Lai</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Danemark</li><li>France</li><li>Pays-Bas</li></country></list><tree><country name="France"><noRegion><name sortKey="Morini, Marina" sort="Morini, Marina" uniqKey="Morini M" first="Marina" last="Morini">Marina Morini</name></noRegion><name sortKey="Dufour, Sylvie" sort="Dufour, Sylvie" uniqKey="Dufour S" first="Sylvie" last="Dufour">Sylvie Dufour</name><name sortKey="Lafont, Anne Gaelle" sort="Lafont, Anne Gaelle" uniqKey="Lafont A" first="Anne-Gaëlle" last="Lafont">Anne-Gaëlle Lafont</name><name sortKey="Pasquier, Jeremy" sort="Pasquier, Jeremy" uniqKey="Pasquier J" first="Jérémy" last="Pasquier">Jérémy Pasquier</name><name sortKey="Rousseau, Karine" sort="Rousseau, Karine" uniqKey="Rousseau K" first="Karine" last="Rousseau">Karine Rousseau</name></country><country name="Pays-Bas"><noRegion><name sortKey="Dirks, Ron" sort="Dirks, Ron" uniqKey="Dirks R" first="Ron" last="Dirks">Ron Dirks</name></noRegion><name sortKey="Van Den Thillart, Guido" sort="Van Den Thillart, Guido" uniqKey="Van Den Thillart G" first="Guido" last="Van Den Thillart">Guido Van Den Thillart</name><name sortKey="Van Den Thillart, Guido" sort="Van Den Thillart, Guido" uniqKey="Van Den Thillart G" first="Guido" last="Van Den Thillart">Guido Van Den Thillart</name></country><country name="Danemark"><noRegion><name sortKey="Tomkiewicz, Jonna" sort="Tomkiewicz, Jonna" uniqKey="Tomkiewicz J" first="Jonna" last="Tomkiewicz">Jonna Tomkiewicz</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix 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