title: Duplicated leptin receptors in two species of eel bring new insights into the evolution of the leptin system in vertebrates.
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.
authors.affiliation: Muséum National d'Histoire Naturelle, Sorbonne Universités, Research Unit BOREA, Biology of Aquatic Organisms and Ecosystems, CNRS 7208, IRD207, UPMC, UCBN, Paris, France.
authors.forename: Marina
authors.initials: M
authors.lastname: Morini
authors.affiliation: Muséum National d'Histoire Naturelle, Sorbonne Universités, Research Unit BOREA, Biology of Aquatic Organisms and Ecosystems, CNRS 7208, IRD207, UPMC, UCBN, Paris, France.
authors.forename: Jérémy
authors.initials: J
authors.lastname: Pasquier
authors.affiliation: ZF-screens B.V., Leiden, The Netherlands.
authors.forename: Ron
authors.initials: R
authors.lastname: Dirks
authors.affiliation: ZF-screens B.V., Leiden, The Netherlands; Institute of Biology, Leiden University, Leiden, The Netherlands.
authors.forename: Guido
authors.initials: G
authors.lastname: van den Thillart
authors.affiliation: Technical University of Denmark, National Institute of Aquatic Resources, Charlottenlund, Denmark.
authors.forename: Jonna
authors.initials: J
authors.lastname: Tomkiewicz
authors.affiliation: Muséum National d'Histoire Naturelle, Sorbonne Universités, Research Unit BOREA, Biology of Aquatic Organisms and Ecosystems, CNRS 7208, IRD207, UPMC, UCBN, Paris, France.
authors.forename: Karine
authors.initials: K
authors.lastname: Rousseau
authors.affiliation: Muséum National d'Histoire Naturelle, Sorbonne Universités, Research Unit BOREA, Biology of Aquatic Organisms and Ecosystems, CNRS 7208, IRD207, UPMC, UCBN, Paris, France.
authors.forename: Sylvie
authors.initials: S
authors.lastname: Dufour
authors.affiliation: Muséum National d'Histoire Naturelle, Sorbonne Universités, Research Unit BOREA, Biology of Aquatic Organisms and Ecosystems, CNRS 7208, IRD207, UPMC, UCBN, Paris, France.
authors.forename: Anne-Gaëlle
authors.initials: AG
authors.lastname: Lafont
mesh_terms: D000811:Anguilla / Q000145:classification / Q000235:genetics* / Q000502:physiology; D000818:Animals; D019143:Evolution, Molecular; D005260:Female; D005399:Fishes / Q000235:genetics; D020440:Gene Duplication; D020738:Leptin / Q000235:genetics*; D008297:Male; D010802:Phylogeny; D054411:Receptors, Leptin / Q000235:genetics*; D012741:Sexual Maturation / Q000235:genetics; D013045:Species Specificity; D026801:Synteny; D014018:Tissue Distribution
chemical_list: D020738:Leptin; D054411:Receptors, Leptin