New insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the Gfra1/Gdnf and Kit/Kitlg regulatory pathways in rainbow trout testis

Electronic supplementary material : the online version of this article (https://doi.org/10.1007/s10695-018-0547-4) contains supplementary material, which is available to authorized users. International audience The present study aimed to investigate whether the Gfra1/Gdnf and/or Kit/Kitlg regulatory...

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Published in:Fish Physiology and Biochemistry
Main Authors: Maouche, Ahmed, Curran, Edouard, Goupil, Anne-Sophie, Sambroni, Elisabeth, Bellaïche, Johanna, Le Gac, Florence, Lareyre, Jean-Jacques
Other Authors: Laboratoire de Physiologie et Génomique des Poissons (LPGP), Institut National de la Recherche Agronomique (INRA)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ), Région Bretagne and the INRA PHASE department, Martin Pšenicka, ANR-11-INBS-0003,CRB-Anim,Réseau de Centres de Ressources Biologiques pour les animaux domestiques(2011), European Project: 652831,H2020,H2020-INFRAIA-2014-2015,AQUAEXCEL2020(2015)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2018
Subjects:
Kit
Online Access:https://hal-univ-rennes1.archives-ouvertes.fr/hal-02019264
https://doi.org/10.1007/s10695-018-0547-4
id ftccsdartic:oai:HAL:hal-02019264v1
record_format openpolar
institution Open Polar
collection Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
op_collection_id ftccsdartic
language English
topic Stem cell factor
Kit ligand
Kit
Spermatogenesis
Oncorhynchus mykiss
Germ stem cell
Gfra1
Gdnf
[SDV]Life Sciences [q-bio]
spellingShingle Stem cell factor
Kit ligand
Kit
Spermatogenesis
Oncorhynchus mykiss
Germ stem cell
Gfra1
Gdnf
[SDV]Life Sciences [q-bio]
Maouche, Ahmed
Curran, Edouard
Goupil, Anne-Sophie
Sambroni, Elisabeth
Bellaïche, Johanna
Le Gac, Florence
Lareyre, Jean-Jacques
New insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the Gfra1/Gdnf and Kit/Kitlg regulatory pathways in rainbow trout testis
topic_facet Stem cell factor
Kit ligand
Kit
Spermatogenesis
Oncorhynchus mykiss
Germ stem cell
Gfra1
Gdnf
[SDV]Life Sciences [q-bio]
description Electronic supplementary material : the online version of this article (https://doi.org/10.1007/s10695-018-0547-4) contains supplementary material, which is available to authorized users. International audience The present study aimed to investigate whether the Gfra1/Gdnf and/or Kit/Kitlg regulatory pathways could be involved in the regulation of spermatogonial cell proliferation and/or differentiation in fish. Homologs of the mammalian gfra1, gdnf, kitr, and kitlg genes were identified in gnathostomes and reliable orthologous relationships were established using phylogenetic reconstructions and analyses of syntenic chromosomal fragments. Gene duplications and losses occurred specifically in teleost fish and members of the Salmoninae family including rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Some duplicated genes exhibited distinct spatiotemporal expression profiles and were differently regulated by hormones in rainbow trout. Undifferentiated type A spermatogonia expressed higher levels of kitrb and kitra2 making them possible target cells for the gonadal kitlgb and somatic kitlga before the onset of spermatogenesis. Interestingly, gdnfa and gdnfb ohnologous genes were poorly expressed before the onset of spermatogenesis. The expression level of gdnfb was correlated with that of the vasa gene suggesting that the late increased abundance of gdnfb during spermatogenesis onset was due to the increased number of spermatogonial cells. gfra1a2 was expressed in undifferentiated typeA spermatogoniawhereas gfra1a1 was mainly detected in somatic cells. These observations indicate that the germinal gdnfb ligand could exert autocrine and paracrine functions on spermatogonia and on testicular somatic cells, respectively. Fsh and androgens inhibited gfra1a2 and gdnfb whereas gfra1a1 was stimulated by Fsh, androgens, and 17α, 20β progesterone. Finally, our data provide evidences that the molecular identity of the male germ stem cells changes during ontogenesis prior to spermatogenesis onset.
author2 Laboratoire de Physiologie et Génomique des Poissons (LPGP)
Institut National de la Recherche Agronomique (INRA)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique )
Région Bretagne and the INRA PHASE department
Martin Pšenicka
ANR-11-INBS-0003,CRB-Anim,Réseau de Centres de Ressources Biologiques pour les animaux domestiques(2011)
European Project: 652831,H2020,H2020-INFRAIA-2014-2015,AQUAEXCEL2020(2015)
format Article in Journal/Newspaper
author Maouche, Ahmed
Curran, Edouard
Goupil, Anne-Sophie
Sambroni, Elisabeth
Bellaïche, Johanna
Le Gac, Florence
Lareyre, Jean-Jacques
author_facet Maouche, Ahmed
Curran, Edouard
Goupil, Anne-Sophie
Sambroni, Elisabeth
Bellaïche, Johanna
Le Gac, Florence
Lareyre, Jean-Jacques
author_sort Maouche, Ahmed
title New insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the Gfra1/Gdnf and Kit/Kitlg regulatory pathways in rainbow trout testis
title_short New insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the Gfra1/Gdnf and Kit/Kitlg regulatory pathways in rainbow trout testis
title_full New insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the Gfra1/Gdnf and Kit/Kitlg regulatory pathways in rainbow trout testis
title_fullStr New insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the Gfra1/Gdnf and Kit/Kitlg regulatory pathways in rainbow trout testis
title_full_unstemmed New insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the Gfra1/Gdnf and Kit/Kitlg regulatory pathways in rainbow trout testis
title_sort new insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the gfra1/gdnf and kit/kitlg regulatory pathways in rainbow trout testis
publisher HAL CCSD
publishDate 2018
url https://hal-univ-rennes1.archives-ouvertes.fr/hal-02019264
https://doi.org/10.1007/s10695-018-0547-4
long_lat ENVELOPE(25.177,25.177,67.587,67.587)
geographic Vasa
geographic_facet Vasa
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source ISSN: 0920-1742
EISSN: 1573-5168
Fish Physiology and Biochemistry
https://hal-univ-rennes1.archives-ouvertes.fr/hal-02019264
Fish Physiology and Biochemistry, Springer Verlag, 2018, 44 (6), pp.1599-1616. ⟨10.1007/s10695-018-0547-4⟩
https://link.springer.com/journal/10695
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1007/s10695-018-0547-4
info:eu-repo/semantics/altIdentifier/pmid/30121735
info:eu-repo/grantAgreement//652831/EU/AQUAculture infrastructures for EXCELlence in European fish research towards 2020/AQUAEXCEL2020
hal-02019264
https://hal-univ-rennes1.archives-ouvertes.fr/hal-02019264
doi:10.1007/s10695-018-0547-4
PRODINRA: 442753
PUBMED: 30121735
WOS: 000453883600016
op_doi https://doi.org/10.1007/s10695-018-0547-4
container_title Fish Physiology and Biochemistry
container_volume 44
container_issue 6
container_start_page 1599
op_container_end_page 1616
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spelling ftccsdartic:oai:HAL:hal-02019264v1 2023-05-15T15:32:55+02:00 New insights into the evolution, hormonal regulation, and spatiotemporal expression profiles of genes involved in the Gfra1/Gdnf and Kit/Kitlg regulatory pathways in rainbow trout testis Maouche, Ahmed Curran, Edouard Goupil, Anne-Sophie Sambroni, Elisabeth Bellaïche, Johanna Le Gac, Florence Lareyre, Jean-Jacques Laboratoire de Physiologie et Génomique des Poissons (LPGP) Institut National de la Recherche Agronomique (INRA)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ) Région Bretagne and the INRA PHASE department Martin Pšenicka ANR-11-INBS-0003,CRB-Anim,Réseau de Centres de Ressources Biologiques pour les animaux domestiques(2011) European Project: 652831,H2020,H2020-INFRAIA-2014-2015,AQUAEXCEL2020(2015) 2018 https://hal-univ-rennes1.archives-ouvertes.fr/hal-02019264 https://doi.org/10.1007/s10695-018-0547-4 en eng HAL CCSD Springer Verlag info:eu-repo/semantics/altIdentifier/doi/10.1007/s10695-018-0547-4 info:eu-repo/semantics/altIdentifier/pmid/30121735 info:eu-repo/grantAgreement//652831/EU/AQUAculture infrastructures for EXCELlence in European fish research towards 2020/AQUAEXCEL2020 hal-02019264 https://hal-univ-rennes1.archives-ouvertes.fr/hal-02019264 doi:10.1007/s10695-018-0547-4 PRODINRA: 442753 PUBMED: 30121735 WOS: 000453883600016 ISSN: 0920-1742 EISSN: 1573-5168 Fish Physiology and Biochemistry https://hal-univ-rennes1.archives-ouvertes.fr/hal-02019264 Fish Physiology and Biochemistry, Springer Verlag, 2018, 44 (6), pp.1599-1616. ⟨10.1007/s10695-018-0547-4⟩ https://link.springer.com/journal/10695 Stem cell factor Kit ligand Kit Spermatogenesis Oncorhynchus mykiss Germ stem cell Gfra1 Gdnf [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2018 ftccsdartic https://doi.org/10.1007/s10695-018-0547-4 2021-12-12T02:50:55Z Electronic supplementary material : the online version of this article (https://doi.org/10.1007/s10695-018-0547-4) contains supplementary material, which is available to authorized users. International audience The present study aimed to investigate whether the Gfra1/Gdnf and/or Kit/Kitlg regulatory pathways could be involved in the regulation of spermatogonial cell proliferation and/or differentiation in fish. Homologs of the mammalian gfra1, gdnf, kitr, and kitlg genes were identified in gnathostomes and reliable orthologous relationships were established using phylogenetic reconstructions and analyses of syntenic chromosomal fragments. Gene duplications and losses occurred specifically in teleost fish and members of the Salmoninae family including rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Some duplicated genes exhibited distinct spatiotemporal expression profiles and were differently regulated by hormones in rainbow trout. Undifferentiated type A spermatogonia expressed higher levels of kitrb and kitra2 making them possible target cells for the gonadal kitlgb and somatic kitlga before the onset of spermatogenesis. Interestingly, gdnfa and gdnfb ohnologous genes were poorly expressed before the onset of spermatogenesis. The expression level of gdnfb was correlated with that of the vasa gene suggesting that the late increased abundance of gdnfb during spermatogenesis onset was due to the increased number of spermatogonial cells. gfra1a2 was expressed in undifferentiated typeA spermatogoniawhereas gfra1a1 was mainly detected in somatic cells. These observations indicate that the germinal gdnfb ligand could exert autocrine and paracrine functions on spermatogonia and on testicular somatic cells, respectively. Fsh and androgens inhibited gfra1a2 and gdnfb whereas gfra1a1 was stimulated by Fsh, androgens, and 17α, 20β progesterone. Finally, our data provide evidences that the molecular identity of the male germ stem cells changes during ontogenesis prior to spermatogenesis onset. Article in Journal/Newspaper Atlantic salmon Salmo salar Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Vasa ENVELOPE(25.177,25.177,67.587,67.587) Fish Physiology and Biochemistry 44 6 1599 1616