Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians

International audience Pituitary gonadotropins, FSH and LH, control gonad activity in vertebrates, via binding to their respective receptors, FSHR and LHR, members of GPCR superfamily. Until recently, it was accepted that gnathostomes possess a single FSHR and a single LHR, encoded by fshr and lhcgr...

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Published in:PLOS ONE
Main Authors: Maugars, Gersende, Dufour, Sylvie
Other Authors: 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)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2015
Subjects:
Online Access:https://hal.sorbonne-universite.fr/hal-01236229
https://hal.sorbonne-universite.fr/hal-01236229/document
https://hal.sorbonne-universite.fr/hal-01236229/file/journal.pone.0135184.pdf
https://doi.org/10.1371/journal.pone.0135184
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spelling ftsorbonneuniv:oai:HAL:hal-01236229v1 2023-12-17T10:29:53+01:00 Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians Maugars, Gersende Dufour, Sylvie 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) 2015-08-13 https://hal.sorbonne-universite.fr/hal-01236229 https://hal.sorbonne-universite.fr/hal-01236229/document https://hal.sorbonne-universite.fr/hal-01236229/file/journal.pone.0135184.pdf https://doi.org/10.1371/journal.pone.0135184 en eng HAL CCSD Public Library of Science info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0135184 hal-01236229 https://hal.sorbonne-universite.fr/hal-01236229 https://hal.sorbonne-universite.fr/hal-01236229/document https://hal.sorbonne-universite.fr/hal-01236229/file/journal.pone.0135184.pdf doi:10.1371/journal.pone.0135184 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1932-6203 EISSN: 1932-6203 PLoS ONE https://hal.sorbonne-universite.fr/hal-01236229 PLoS ONE, 2015, 10 (8), pp.e0135184. ⟨10.1371/journal.pone.0135184⟩ [SDV.EE.ECO]Life Sciences [q-bio]/Ecology environment/Ecosystems info:eu-repo/semantics/article Journal articles 2015 ftsorbonneuniv https://doi.org/10.1371/journal.pone.0135184 2023-11-21T23:55:06Z International audience Pituitary gonadotropins, FSH and LH, control gonad activity in vertebrates, via binding to their respective receptors, FSHR and LHR, members of GPCR superfamily. Until recently, it was accepted that gnathostomes possess a single FSHR and a single LHR, encoded by fshr and lhcgr genes. We reinvestigated this question, focusing on vertebrate species of key-phylogenetical positions. Genome analyses supported the presence of a single fshr and a single lhcgr in chondrichthyans, and in sarcopterygians including mammals, birds, amphibians and coelacanth. In contrast, we identified a single fshr but two lhgcr in basal tel-eosts, the eels. We further showed the coexistence of duplicated lhgcr in other actinoptery-gians, including a non-teleost, the gar, and other teleosts, e.g. Mexican tetra, platyfish, or tilapia. Phylogeny and synteny analyses supported the existence in actinopterygians of two lhgcr paralogs (lhgcr1/ lhgcr2), which do not result from the teleost-specific whole-genome duplication (3R), but likely from a local gene duplication that occurred early in the actinopter-ygian lineage. Due to gene losses, there was no impact of 3R on the number of gonadotro-pin receptors in extant teleosts. Additional gene losses during teleost radiation, led to a single lhgcr (lhgcr1 or lhgcr2) in some species, e.g. medaka and zebrafish. Sequence comparison highlighted divergences in the extracellular and intracellular domains of the duplicated lhgcr, suggesting differential properties such as ligand binding and activation mechanisms. Comparison of tissue distribution in the European eel, revealed that fshr and both lhgcr transcripts are expressed in the ovary and testis, but are differentially expressed in non-gonadal tissues such as brain or eye. Differences in structure-activity relationships and tissue expression may have contributed as selective drives in the conservation of the duplicated lhgcr. This study revises the evolutionary scenario and nomenclature of gonado-tropin receptors, and opens new ... Article in Journal/Newspaper European eel HAL Sorbonne Université Gar’ ENVELOPE(162.014,162.014,57.140,57.140) PLOS ONE 10 8 e0135184
institution Open Polar
collection HAL Sorbonne Université
op_collection_id ftsorbonneuniv
language English
topic [SDV.EE.ECO]Life Sciences [q-bio]/Ecology
environment/Ecosystems
spellingShingle [SDV.EE.ECO]Life Sciences [q-bio]/Ecology
environment/Ecosystems
Maugars, Gersende
Dufour, Sylvie
Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians
topic_facet [SDV.EE.ECO]Life Sciences [q-bio]/Ecology
environment/Ecosystems
description International audience Pituitary gonadotropins, FSH and LH, control gonad activity in vertebrates, via binding to their respective receptors, FSHR and LHR, members of GPCR superfamily. Until recently, it was accepted that gnathostomes possess a single FSHR and a single LHR, encoded by fshr and lhcgr genes. We reinvestigated this question, focusing on vertebrate species of key-phylogenetical positions. Genome analyses supported the presence of a single fshr and a single lhcgr in chondrichthyans, and in sarcopterygians including mammals, birds, amphibians and coelacanth. In contrast, we identified a single fshr but two lhgcr in basal tel-eosts, the eels. We further showed the coexistence of duplicated lhgcr in other actinoptery-gians, including a non-teleost, the gar, and other teleosts, e.g. Mexican tetra, platyfish, or tilapia. Phylogeny and synteny analyses supported the existence in actinopterygians of two lhgcr paralogs (lhgcr1/ lhgcr2), which do not result from the teleost-specific whole-genome duplication (3R), but likely from a local gene duplication that occurred early in the actinopter-ygian lineage. Due to gene losses, there was no impact of 3R on the number of gonadotro-pin receptors in extant teleosts. Additional gene losses during teleost radiation, led to a single lhgcr (lhgcr1 or lhgcr2) in some species, e.g. medaka and zebrafish. Sequence comparison highlighted divergences in the extracellular and intracellular domains of the duplicated lhgcr, suggesting differential properties such as ligand binding and activation mechanisms. Comparison of tissue distribution in the European eel, revealed that fshr and both lhgcr transcripts are expressed in the ovary and testis, but are differentially expressed in non-gonadal tissues such as brain or eye. Differences in structure-activity relationships and tissue expression may have contributed as selective drives in the conservation of the duplicated lhgcr. This study revises the evolutionary scenario and nomenclature of gonado-tropin receptors, and opens new ...
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)
format Article in Journal/Newspaper
author Maugars, Gersende
Dufour, Sylvie
author_facet Maugars, Gersende
Dufour, Sylvie
author_sort Maugars, Gersende
title Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians
title_short Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians
title_full Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians
title_fullStr Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians
title_full_unstemmed Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians
title_sort demonstration of the coexistence of duplicated lh receptors in teleosts, and their origin in ancestral actinopterygians
publisher HAL CCSD
publishDate 2015
url https://hal.sorbonne-universite.fr/hal-01236229
https://hal.sorbonne-universite.fr/hal-01236229/document
https://hal.sorbonne-universite.fr/hal-01236229/file/journal.pone.0135184.pdf
https://doi.org/10.1371/journal.pone.0135184
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 ISSN: 1932-6203
EISSN: 1932-6203
PLoS ONE
https://hal.sorbonne-universite.fr/hal-01236229
PLoS ONE, 2015, 10 (8), pp.e0135184. ⟨10.1371/journal.pone.0135184⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0135184
hal-01236229
https://hal.sorbonne-universite.fr/hal-01236229
https://hal.sorbonne-universite.fr/hal-01236229/document
https://hal.sorbonne-universite.fr/hal-01236229/file/journal.pone.0135184.pdf
doi:10.1371/journal.pone.0135184
op_rights http://creativecommons.org/licenses/by/
info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1371/journal.pone.0135184
container_title PLOS ONE
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