Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates
International audience 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...
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ftsorbonneuniv:oai:HAL:hal-02995677v1 2024-09-15T18:05:15+00:00 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-Gaelle 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) ZF-screens Universiteit Leiden = Leiden University Danmarks Tekniske Universitet = Technical University of Denmark (DTU) ANR-08-BLAN-0173,Puberteel,Neuroendocrine control of eel puberty.(2008) 2015-05-06 https://hal.science/hal-02995677 https://hal.science/hal-02995677/document https://hal.science/hal-02995677/file/pone.0126008.pdf https://doi.org/10.1371/journal.pone.0126008 en eng HAL CCSD Public Library of Science info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0126008 hal-02995677 https://hal.science/hal-02995677 https://hal.science/hal-02995677/document https://hal.science/hal-02995677/file/pone.0126008.pdf doi:10.1371/journal.pone.0126008 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1932-6203 EISSN: 1932-6203 PLoS ONE https://hal.science/hal-02995677 PLoS ONE, 2015, 10 (5), pp.e0126008. ⟨10.1371/journal.pone.0126008⟩ Eel leptin and LEPR sequence files are available from the EMBL Nucleotide Sequence database (accession numbers LN558789 LN558790 LN558791 LN558792) [SDV.BDD]Life Sciences [q-bio]/Development Biology info:eu-repo/semantics/article Journal articles 2015 ftsorbonneuniv https://doi.org/10.1371/journal.pone.0126008 2024-07-25T23:47:56Z International audience 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. Article in Journal/Newspaper European eel HAL Sorbonne Université PLOS ONE 10 5 e0126008 |
institution |
Open Polar |
collection |
HAL Sorbonne Université |
op_collection_id |
ftsorbonneuniv |
language |
English |
topic |
Eel leptin and LEPR sequence files are available from the EMBL Nucleotide Sequence database (accession numbers LN558789 LN558790 LN558791 LN558792) [SDV.BDD]Life Sciences [q-bio]/Development Biology |
spellingShingle |
Eel leptin and LEPR sequence files are available from the EMBL Nucleotide Sequence database (accession numbers LN558789 LN558790 LN558791 LN558792) [SDV.BDD]Life Sciences [q-bio]/Development Biology Morini, Marina Pasquier, Jérémy Dirks, Ron van den Thillart, Guido Tomkiewicz, Jonna Rousseau, Karine Dufour, Sylvie Lafont, Anne-Gaelle Duplicated Leptin Receptors in Two Species of Eel Bring New Insights into the Evolution of the Leptin System in Vertebrates |
topic_facet |
Eel leptin and LEPR sequence files are available from the EMBL Nucleotide Sequence database (accession numbers LN558789 LN558790 LN558791 LN558792) [SDV.BDD]Life Sciences [q-bio]/Development Biology |
description |
International audience 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. |
author2 |
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) ZF-screens Universiteit Leiden = Leiden University Danmarks Tekniske Universitet = Technical University of Denmark (DTU) ANR-08-BLAN-0173,Puberteel,Neuroendocrine control of eel puberty.(2008) |
format |
Article in Journal/Newspaper |
author |
Morini, Marina Pasquier, Jérémy Dirks, Ron van den Thillart, Guido Tomkiewicz, Jonna Rousseau, Karine Dufour, Sylvie Lafont, Anne-Gaelle |
author_facet |
Morini, Marina Pasquier, Jérémy Dirks, Ron van den Thillart, Guido Tomkiewicz, Jonna Rousseau, Karine Dufour, Sylvie Lafont, Anne-Gaelle |
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 |
HAL CCSD |
publishDate |
2015 |
url |
https://hal.science/hal-02995677 https://hal.science/hal-02995677/document https://hal.science/hal-02995677/file/pone.0126008.pdf https://doi.org/10.1371/journal.pone.0126008 |
genre |
European eel |
genre_facet |
European eel |
op_source |
ISSN: 1932-6203 EISSN: 1932-6203 PLoS ONE https://hal.science/hal-02995677 PLoS ONE, 2015, 10 (5), pp.e0126008. ⟨10.1371/journal.pone.0126008⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0126008 hal-02995677 https://hal.science/hal-02995677 https://hal.science/hal-02995677/document https://hal.science/hal-02995677/file/pone.0126008.pdf doi:10.1371/journal.pone.0126008 |
op_rights |
http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1371/journal.pone.0126008 |
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PLOS ONE |
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10 |
container_issue |
5 |
container_start_page |
e0126008 |
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