Multiple Thyrotropin β-Subunit and Thyrotropin Receptor-Related Genes Arose during Vertebrate Evolution

International audience Thyroid-stimulating hormone (TSH) is composed of a specific b subunit and an a subunit that is shared with the two pituitary gonadotropins. The three b subunits derive from a common ancestral gene through two genome duplications (1R and 2R) that took place before the radiation...

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Published in:PLoS ONE
Main Authors: Maugars, Gersende, Dufour, Sylvie, Cohen-Tannoudji, Joëlle, Quérat, Bruno
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), Unité de Biologie Fonctionnelle et Adaptative (BFA (UMR_8251 / U1133)), Université Paris Diderot - Paris 7 (UPD7)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2014
Subjects:
Online Access:https://hal.sorbonne-universite.fr/hal-01366759
https://hal.sorbonne-universite.fr/hal-01366759/document
https://hal.sorbonne-universite.fr/hal-01366759/file/journal.pone.0111361.PDF
https://doi.org/10.1371/journal.pone.0111361
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spelling ftsorbonneuniv:oai:HAL:hal-01366759v1 2024-05-19T07:39:55+00:00 Multiple Thyrotropin β-Subunit and Thyrotropin Receptor-Related Genes Arose during Vertebrate Evolution Maugars, Gersende Dufour, Sylvie Cohen-Tannoudji, Joëlle Quérat, Bruno 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) Unité de Biologie Fonctionnelle et Adaptative (BFA (UMR_8251 / U1133)) Université Paris Diderot - Paris 7 (UPD7)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS) 2014 https://hal.sorbonne-universite.fr/hal-01366759 https://hal.sorbonne-universite.fr/hal-01366759/document https://hal.sorbonne-universite.fr/hal-01366759/file/journal.pone.0111361.PDF https://doi.org/10.1371/journal.pone.0111361 en eng HAL CCSD Public Library of Science info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0111361 hal-01366759 https://hal.sorbonne-universite.fr/hal-01366759 https://hal.sorbonne-universite.fr/hal-01366759/document https://hal.sorbonne-universite.fr/hal-01366759/file/journal.pone.0111361.PDF doi:10.1371/journal.pone.0111361 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1932-6203 EISSN: 1932-6203 PLoS ONE https://hal.sorbonne-universite.fr/hal-01366759 PLoS ONE, 2014, 9 (11), pp.e111361. ⟨10.1371/journal.pone.0111361⟩ [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology info:eu-repo/semantics/article Journal articles 2014 ftsorbonneuniv https://doi.org/10.1371/journal.pone.0111361 2024-04-25T04:14:12Z International audience Thyroid-stimulating hormone (TSH) is composed of a specific b subunit and an a subunit that is shared with the two pituitary gonadotropins. The three b subunits derive from a common ancestral gene through two genome duplications (1R and 2R) that took place before the radiation of vertebrates. Analysis of genomic data from phylogenetically relevant species allowed us to identify an additional Tshb subunit-related gene that was generated through 2R. This gene, named Tshb2, present in cartilaginous fish, little skate and elephant shark, and in early lobe-finned fish, coelacanth and lungfish, was lost in ray-finned fish and tetrapods. The absence of a second type of TSH receptor (Tshr) gene in these species suggests that both TSHs act through the same receptor. A novel Tshb sister gene, named Tshb3, was generated through the third genomic duplication (3R) that occurred early in the teleost lineage. Tshb3 is present in most teleost groups but was lostin tedraodontiforms. The 3R also generated a second Tshr, named Tshrb. Interestingly, the new Tshrb was translocated from its original chromosomic position after the emergence of eels and was then maintained in its new position. Tshrb was lost in tetraodontiforms and in ostariophysians including zebrafish although the latter species have two TSHs, suggesting that TSHRb may be dispensable. The tissue distribution of duplicated Tshbs and Tshrs was studied in the European eel. The endocrine thyrotropic function in the eel would be essentially mediated by the classical Tshb and Tshra, which are mainly expressed in the pituitary and thyroid, respectively. Tshb3 and Tshrb showed a similar distribution pattern in the brain, pituitary, ovary and adipose tissue, suggesting a possible paracrine/autocrine mode of action in these non-thyroidal tissues. Further studies will be needed to determine the binding specificity of the two receptors and how these two TSH systems are interrelated. Article in Journal/Newspaper European eel HAL Sorbonne Université PLoS ONE 9 11 e111361
institution Open Polar
collection HAL Sorbonne Université
op_collection_id ftsorbonneuniv
language English
topic [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology
spellingShingle [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology
Maugars, Gersende
Dufour, Sylvie
Cohen-Tannoudji, Joëlle
Quérat, Bruno
Multiple Thyrotropin β-Subunit and Thyrotropin Receptor-Related Genes Arose during Vertebrate Evolution
topic_facet [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology
description International audience Thyroid-stimulating hormone (TSH) is composed of a specific b subunit and an a subunit that is shared with the two pituitary gonadotropins. The three b subunits derive from a common ancestral gene through two genome duplications (1R and 2R) that took place before the radiation of vertebrates. Analysis of genomic data from phylogenetically relevant species allowed us to identify an additional Tshb subunit-related gene that was generated through 2R. This gene, named Tshb2, present in cartilaginous fish, little skate and elephant shark, and in early lobe-finned fish, coelacanth and lungfish, was lost in ray-finned fish and tetrapods. The absence of a second type of TSH receptor (Tshr) gene in these species suggests that both TSHs act through the same receptor. A novel Tshb sister gene, named Tshb3, was generated through the third genomic duplication (3R) that occurred early in the teleost lineage. Tshb3 is present in most teleost groups but was lostin tedraodontiforms. The 3R also generated a second Tshr, named Tshrb. Interestingly, the new Tshrb was translocated from its original chromosomic position after the emergence of eels and was then maintained in its new position. Tshrb was lost in tetraodontiforms and in ostariophysians including zebrafish although the latter species have two TSHs, suggesting that TSHRb may be dispensable. The tissue distribution of duplicated Tshbs and Tshrs was studied in the European eel. The endocrine thyrotropic function in the eel would be essentially mediated by the classical Tshb and Tshra, which are mainly expressed in the pituitary and thyroid, respectively. Tshb3 and Tshrb showed a similar distribution pattern in the brain, pituitary, ovary and adipose tissue, suggesting a possible paracrine/autocrine mode of action in these non-thyroidal tissues. Further studies will be needed to determine the binding specificity of the two receptors and how these two TSH systems are interrelated.
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)
Unité de Biologie Fonctionnelle et Adaptative (BFA (UMR_8251 / U1133))
Université Paris Diderot - Paris 7 (UPD7)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
format Article in Journal/Newspaper
author Maugars, Gersende
Dufour, Sylvie
Cohen-Tannoudji, Joëlle
Quérat, Bruno
author_facet Maugars, Gersende
Dufour, Sylvie
Cohen-Tannoudji, Joëlle
Quérat, Bruno
author_sort Maugars, Gersende
title Multiple Thyrotropin β-Subunit and Thyrotropin Receptor-Related Genes Arose during Vertebrate Evolution
title_short Multiple Thyrotropin β-Subunit and Thyrotropin Receptor-Related Genes Arose during Vertebrate Evolution
title_full Multiple Thyrotropin β-Subunit and Thyrotropin Receptor-Related Genes Arose during Vertebrate Evolution
title_fullStr Multiple Thyrotropin β-Subunit and Thyrotropin Receptor-Related Genes Arose during Vertebrate Evolution
title_full_unstemmed Multiple Thyrotropin β-Subunit and Thyrotropin Receptor-Related Genes Arose during Vertebrate Evolution
title_sort multiple thyrotropin β-subunit and thyrotropin receptor-related genes arose during vertebrate evolution
publisher HAL CCSD
publishDate 2014
url https://hal.sorbonne-universite.fr/hal-01366759
https://hal.sorbonne-universite.fr/hal-01366759/document
https://hal.sorbonne-universite.fr/hal-01366759/file/journal.pone.0111361.PDF
https://doi.org/10.1371/journal.pone.0111361
genre European eel
genre_facet European eel
op_source ISSN: 1932-6203
EISSN: 1932-6203
PLoS ONE
https://hal.sorbonne-universite.fr/hal-01366759
PLoS ONE, 2014, 9 (11), pp.e111361. ⟨10.1371/journal.pone.0111361⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0111361
hal-01366759
https://hal.sorbonne-universite.fr/hal-01366759
https://hal.sorbonne-universite.fr/hal-01366759/document
https://hal.sorbonne-universite.fr/hal-01366759/file/journal.pone.0111361.PDF
doi:10.1371/journal.pone.0111361
op_rights http://creativecommons.org/licenses/by/
info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1371/journal.pone.0111361
container_title PLoS ONE
container_volume 9
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