Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role

International audience In mammals, neurokinin B (NKB) is a short peptide encoded by the gene tac3. It is involved in the brain control of reproduction by stimulating gonadotropin-releasing hormone (GnRH) neurons, mainly via kisspeptin. We investigated tac3 genes and peptides in a basal teleost, the...

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Published in:Frontiers in Endocrinology
Main Authors: Campo, Aurora, Lafont, Anne-Gaelle, Lefranc, Benjamin, Leprince, Jérôme, Tostivint, Hervé, Kamech, Nédia, Dufour, Sylvie, Rousseau, Karine
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), Différenciation et communication neuronale et neuroendocrine (DC2N), Université de Rouen Normandie (UNIROUEN), Normandie Université (NU)-Normandie Université (NU)-Institut National de la Santé et de la Recherche Médicale (INSERM), Evolution des régulations endocriniennes (ERE), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS), Biologie des organismes marins et écosystèmes (BOME), Muséum national d'Histoire naturelle (MNHN)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), ANR-14-CE02-0020,NEMO,Neuropeptides d'organismes marins(2014)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2018
Subjects:
Online Access:https://hal.sorbonne-universite.fr/hal-01822802
https://hal.sorbonne-universite.fr/hal-01822802/document
https://hal.sorbonne-universite.fr/hal-01822802/file/fendo-09-00304.pdf
https://doi.org/10.3389/fendo.2018.00304
id ftanrparis:oai:HAL:hal-01822802v1
record_format openpolar
institution Open Polar
collection Portail HAL-ANR (Agence Nationale de la Recherche)
op_collection_id ftanrparis
language English
topic teleost
phylogeny
neurokinin B
tachykinin-3
synteny
gnrh-r
pituitary cell culture
luteinizing hormone
[SDV.MHEP.EM]Life Sciences [q-bio]/Human health and pathology/Endocrinology and metabolism
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
spellingShingle teleost
phylogeny
neurokinin B
tachykinin-3
synteny
gnrh-r
pituitary cell culture
luteinizing hormone
[SDV.MHEP.EM]Life Sciences [q-bio]/Human health and pathology/Endocrinology and metabolism
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
Campo, Aurora
Lafont, Anne-Gaelle
Lefranc, Benjamin
Leprince, Jérôme
Tostivint, Hervé
Kamech, Nédia
Dufour, Sylvie
Rousseau, Karine
Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role
topic_facet teleost
phylogeny
neurokinin B
tachykinin-3
synteny
gnrh-r
pituitary cell culture
luteinizing hormone
[SDV.MHEP.EM]Life Sciences [q-bio]/Human health and pathology/Endocrinology and metabolism
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
description International audience In mammals, neurokinin B (NKB) is a short peptide encoded by the gene tac3. It is involved in the brain control of reproduction by stimulating gonadotropin-releasing hormone (GnRH) neurons, mainly via kisspeptin. We investigated tac3 genes and peptides in a basal teleost, the European eel, which shows an atypical blockade of the sexual maturation at a prepubertal stage. Two tac3 paralogous genes (tac3a and tac3b) were identified in the eel genome, each encoding two peptides (NKBa or b and NKB-related peptide NKB-RPa or b). Amino acid sequence of eel NKBa is identical to human NKB, and the three others are novel peptide sequences. The four eel peptides present the characteristic C-terminal tachykinin sequence, as well as a similar alpha helix 3D structure. Tac3 genes were identified in silico in 52 species of vertebrates, and a phylogeny analysis was performed on the predicted TAC3 pre-pro-peptide sequences. A synteny analysis was also done to further assess the evolutionary history of tac3 genes. Duplicated tac3 genes in teleosts likely result from the teleost-specific whole genome duplication (3R). Among teleosts, TAC3b precursor sequences are more divergent than TAC3a, and a loss of tac3b gene would have even occurred in some teleost lineages. NKB-RP peptide, encoded beside NKB by tac3 gene in actinopterygians and basal sarcopterygians, would have been lost in ancestral amniotes. Tissue distribution of eel tac3a and tac3b mRNAs showed major expression of both transcripts in the brain especially in the diencephalon, as analyzed by specific qPCRs. Human NKB has been tested in vitro on primary culture of eel pituitary cells. Human NKB dose-dependently inhibited the expression of lhβ, while having no effect on other glycoprotein hormone subunits (fshβ, tshβ, and gpα) nor on gh. Human NKB also dose-dependently inhibited the expression of GnRH receptor (gnrh-r2). The four eel peptides have been synthesized and also tested in vitro. They all inhibited the expression of both lhβ and of ...
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)
Différenciation et communication neuronale et neuroendocrine (DC2N)
Université de Rouen Normandie (UNIROUEN)
Normandie Université (NU)-Normandie Université (NU)-Institut National de la Santé et de la Recherche Médicale (INSERM)
Evolution des régulations endocriniennes (ERE)
Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS)
Biologie des organismes marins et écosystèmes (BOME)
Muséum national d'Histoire naturelle (MNHN)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)
ANR-14-CE02-0020,NEMO,Neuropeptides d'organismes marins(2014)
format Article in Journal/Newspaper
author Campo, Aurora
Lafont, Anne-Gaelle
Lefranc, Benjamin
Leprince, Jérôme
Tostivint, Hervé
Kamech, Nédia
Dufour, Sylvie
Rousseau, Karine
author_facet Campo, Aurora
Lafont, Anne-Gaelle
Lefranc, Benjamin
Leprince, Jérôme
Tostivint, Hervé
Kamech, Nédia
Dufour, Sylvie
Rousseau, Karine
author_sort Campo, Aurora
title Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role
title_short Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role
title_full Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role
title_fullStr Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role
title_full_unstemmed Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role
title_sort tachykinin-3 genes and peptides characterized in a basal teleost, the european eel: evolutionary perspective and pituitary role
publisher HAL CCSD
publishDate 2018
url https://hal.sorbonne-universite.fr/hal-01822802
https://hal.sorbonne-universite.fr/hal-01822802/document
https://hal.sorbonne-universite.fr/hal-01822802/file/fendo-09-00304.pdf
https://doi.org/10.3389/fendo.2018.00304
genre European eel
genre_facet European eel
op_source ISSN: 1664-2392
Frontiers in Endocrinology
https://hal.sorbonne-universite.fr/hal-01822802
Frontiers in Endocrinology, 2018, 9, pp.304. ⟨10.3389/fendo.2018.00304⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.3389/fendo.2018.00304
hal-01822802
https://hal.sorbonne-universite.fr/hal-01822802
https://hal.sorbonne-universite.fr/hal-01822802/document
https://hal.sorbonne-universite.fr/hal-01822802/file/fendo-09-00304.pdf
doi:10.3389/fendo.2018.00304
op_rights http://creativecommons.org/licenses/by/
info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.3389/fendo.2018.00304
container_title Frontiers in Endocrinology
container_volume 9
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spelling ftanrparis:oai:HAL:hal-01822802v1 2024-09-09T19:39:29+00:00 Tachykinin-3 Genes and Peptides Characterized in a Basal Teleost, the European Eel: Evolutionary Perspective and Pituitary Role Campo, Aurora Lafont, Anne-Gaelle Lefranc, Benjamin Leprince, Jérôme Tostivint, Hervé Kamech, Nédia Dufour, Sylvie Rousseau, Karine 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) Différenciation et communication neuronale et neuroendocrine (DC2N) Université de Rouen Normandie (UNIROUEN) Normandie Université (NU)-Normandie Université (NU)-Institut National de la Santé et de la Recherche Médicale (INSERM) Evolution des régulations endocriniennes (ERE) Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS) Biologie des organismes marins et écosystèmes (BOME) Muséum national d'Histoire naturelle (MNHN)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS) ANR-14-CE02-0020,NEMO,Neuropeptides d'organismes marins(2014) 2018 https://hal.sorbonne-universite.fr/hal-01822802 https://hal.sorbonne-universite.fr/hal-01822802/document https://hal.sorbonne-universite.fr/hal-01822802/file/fendo-09-00304.pdf https://doi.org/10.3389/fendo.2018.00304 en eng HAL CCSD Frontiers info:eu-repo/semantics/altIdentifier/doi/10.3389/fendo.2018.00304 hal-01822802 https://hal.sorbonne-universite.fr/hal-01822802 https://hal.sorbonne-universite.fr/hal-01822802/document https://hal.sorbonne-universite.fr/hal-01822802/file/fendo-09-00304.pdf doi:10.3389/fendo.2018.00304 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1664-2392 Frontiers in Endocrinology https://hal.sorbonne-universite.fr/hal-01822802 Frontiers in Endocrinology, 2018, 9, pp.304. ⟨10.3389/fendo.2018.00304⟩ teleost phylogeny neurokinin B tachykinin-3 synteny gnrh-r pituitary cell culture luteinizing hormone [SDV.MHEP.EM]Life Sciences [q-bio]/Human health and pathology/Endocrinology and metabolism [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry Molecular Biology/Genomics [q-bio.GN] info:eu-repo/semantics/article Journal articles 2018 ftanrparis https://doi.org/10.3389/fendo.2018.00304 2024-07-12T11:26:50Z International audience In mammals, neurokinin B (NKB) is a short peptide encoded by the gene tac3. It is involved in the brain control of reproduction by stimulating gonadotropin-releasing hormone (GnRH) neurons, mainly via kisspeptin. We investigated tac3 genes and peptides in a basal teleost, the European eel, which shows an atypical blockade of the sexual maturation at a prepubertal stage. Two tac3 paralogous genes (tac3a and tac3b) were identified in the eel genome, each encoding two peptides (NKBa or b and NKB-related peptide NKB-RPa or b). Amino acid sequence of eel NKBa is identical to human NKB, and the three others are novel peptide sequences. The four eel peptides present the characteristic C-terminal tachykinin sequence, as well as a similar alpha helix 3D structure. Tac3 genes were identified in silico in 52 species of vertebrates, and a phylogeny analysis was performed on the predicted TAC3 pre-pro-peptide sequences. A synteny analysis was also done to further assess the evolutionary history of tac3 genes. Duplicated tac3 genes in teleosts likely result from the teleost-specific whole genome duplication (3R). Among teleosts, TAC3b precursor sequences are more divergent than TAC3a, and a loss of tac3b gene would have even occurred in some teleost lineages. NKB-RP peptide, encoded beside NKB by tac3 gene in actinopterygians and basal sarcopterygians, would have been lost in ancestral amniotes. Tissue distribution of eel tac3a and tac3b mRNAs showed major expression of both transcripts in the brain especially in the diencephalon, as analyzed by specific qPCRs. Human NKB has been tested in vitro on primary culture of eel pituitary cells. Human NKB dose-dependently inhibited the expression of lhβ, while having no effect on other glycoprotein hormone subunits (fshβ, tshβ, and gpα) nor on gh. Human NKB also dose-dependently inhibited the expression of GnRH receptor (gnrh-r2). The four eel peptides have been synthesized and also tested in vitro. They all inhibited the expression of both lhβ and of ... Article in Journal/Newspaper European eel Portail HAL-ANR (Agence Nationale de la Recherche) Frontiers in Endocrinology 9