The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax

The female sex steroid 17β-oestradiol (E2) is involved in the regulation of numerous physiological functions, including the immune system development and performance. The role of oestrogens during ontogenesis is, however, not well studied. In rodents and fish, thymus maturation appears to be oestrog...

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Autores: Moreira, Catarina, Paiola, Matthieu, Duflot, A., Varó, Inmaculada, Sitjà-Bobadilla, Ariadna, Knigge, Thomas, Pinto, Patrícia I. S., Monsinjon, Tiphaine
Tipo de recurso: artículo
Estado:Versión enviada para evaluación y publicación
Fecha de publicación:2021
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/228489
Acceso en línea:http://hdl.handle.net/10261/228489
Access Level:acceso abierto
Palabra clave:Liver
Oestrogen receptor
T cell
Teleost fish
Thymus
Spleen
id ES_4e0983db099bb51dd0baf13e4b261cfd
oai_identifier_str oai:digital.csic.es:10261/228489
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax
title The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax
spellingShingle The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax
Moreira, Catarina
Liver
Oestrogen receptor
T cell
Teleost fish
Thymus
Spleen
title_short The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax
title_full The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax
title_fullStr The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax
title_full_unstemmed The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax
title_sort The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labrax
dc.creator.none.fl_str_mv Moreira, Catarina
Paiola, Matthieu
Duflot, A.
Varó, Inmaculada
Sitjà-Bobadilla, Ariadna
Knigge, Thomas
Pinto, Patrícia I. S.
Monsinjon, Tiphaine
author Moreira, Catarina
author_facet Moreira, Catarina
Paiola, Matthieu
Duflot, A.
Varó, Inmaculada
Sitjà-Bobadilla, Ariadna
Knigge, Thomas
Pinto, Patrícia I. S.
Monsinjon, Tiphaine
author_role author
author2 Paiola, Matthieu
Duflot, A.
Varó, Inmaculada
Sitjà-Bobadilla, Ariadna
Knigge, Thomas
Pinto, Patrícia I. S.
Monsinjon, Tiphaine
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Fundação para a Ciência e a Tecnologia (Portugal)
Universidade do Algarve
European Commission
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Liver
Oestrogen receptor
T cell
Teleost fish
Thymus
Spleen
topic Liver
Oestrogen receptor
T cell
Teleost fish
Thymus
Spleen
description The female sex steroid 17β-oestradiol (E2) is involved in the regulation of numerous physiological functions, including the immune system development and performance. The role of oestrogens during ontogenesis is, however, not well studied. In rodents and fish, thymus maturation appears to be oestrogen-dependent. Nevertheless, little is known about the function of oestrogen in immune system development. To further the understanding of the role of oestrogens in fish immune system ontogenesis, fingerlings of European sea bass (Dicentrarchus labrax) were exposed for 30 days to 20 ng E2·L−1, at two ages tightly related to thymic maturation, i.e., 60 or 90 days post hatch (dph). The expression of nuclear and membrane oestrogen receptors was measured in the thymus and spleen, and the expression of several T cell-related gene markers was studied in both immune organs, as well as in the liver. Waterborne E2-exposure at 20.2 ± 2.1 (S.E.) ng·L−1 was confirmed by radioimmunoassay, leading to significantly higher E2-contents in the liver of exposed fish. The majority of gene markers presented age-dependent dynamics in at least one of the organs, confirming thymus maturation, but also suggesting a critical ontogenetic window for the implementation of liver resident γδ and αβ T cells. The oestrogen receptors, however, remained unchanged over the age and treatment comparisons with the exception of esr2b, which was modulated by E2 in the younger cohort and increased its expression with age in the thymus of the older cohort, as did the membrane oestrogen receptor gpera. These results confirm that oestrogen-signalling is involved in thymus maturation in European sea bass, as it is in mammals. This suggests that esr2b and gpera play key roles during thymus ontogenesis, particularly during medulla maturation. In contrast, the spleen expressed low or non-detectable levels of oestrogen receptors. The E2-exposure decreased the expression of tcrγ in the liver in the cohort exposed from 93 to 122 dph, but not the expression of any other immune-related gene analysed. These results indicate that the proliferation/migration of these innate-like T cell populations is oestrogen-sensitive. In regard to the apparent prominent role of oestrogen-signalling in the late thymus maturation stage, the thymic differentiation of the corresponding subpopulations of T cells might be regulated by oestrogen. To the best of our knowledge, this is the first study investigating the dynamics of both nuclear and membrane oestrogen receptors in specific immune organs in a teleost fish at very early stages of immune system development as well as to examine thymic function in sea bass after an exposure to E2 during ontogenesis.
publishDate 2021
dc.date.none.fl_str_mv 2021
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Preprint
info:eu-repo/semantics/submittedVersion
format article
status_str submittedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/228489
url http://hdl.handle.net/10261/228489
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/EC/H2020/652831
https://doi.org/10.1016/j.dci.2021.104011

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling The influence of 17β-oestradiol on lymphopoiesis and immune system ontogenesis in juvenile sea bass, Dicentrarchus labraxMoreira, CatarinaPaiola, MatthieuDuflot, A.Varó, InmaculadaSitjà-Bobadilla, AriadnaKnigge, ThomasPinto, Patrícia I. S.Monsinjon, TiphaineLiverOestrogen receptorT cellTeleost fishThymusSpleenThe female sex steroid 17β-oestradiol (E2) is involved in the regulation of numerous physiological functions, including the immune system development and performance. The role of oestrogens during ontogenesis is, however, not well studied. In rodents and fish, thymus maturation appears to be oestrogen-dependent. Nevertheless, little is known about the function of oestrogen in immune system development. To further the understanding of the role of oestrogens in fish immune system ontogenesis, fingerlings of European sea bass (Dicentrarchus labrax) were exposed for 30 days to 20 ng E2·L−1, at two ages tightly related to thymic maturation, i.e., 60 or 90 days post hatch (dph). The expression of nuclear and membrane oestrogen receptors was measured in the thymus and spleen, and the expression of several T cell-related gene markers was studied in both immune organs, as well as in the liver. Waterborne E2-exposure at 20.2 ± 2.1 (S.E.) ng·L−1 was confirmed by radioimmunoassay, leading to significantly higher E2-contents in the liver of exposed fish. The majority of gene markers presented age-dependent dynamics in at least one of the organs, confirming thymus maturation, but also suggesting a critical ontogenetic window for the implementation of liver resident γδ and αβ T cells. The oestrogen receptors, however, remained unchanged over the age and treatment comparisons with the exception of esr2b, which was modulated by E2 in the younger cohort and increased its expression with age in the thymus of the older cohort, as did the membrane oestrogen receptor gpera. These results confirm that oestrogen-signalling is involved in thymus maturation in European sea bass, as it is in mammals. This suggests that esr2b and gpera play key roles during thymus ontogenesis, particularly during medulla maturation. In contrast, the spleen expressed low or non-detectable levels of oestrogen receptors. The E2-exposure decreased the expression of tcrγ in the liver in the cohort exposed from 93 to 122 dph, but not the expression of any other immune-related gene analysed. These results indicate that the proliferation/migration of these innate-like T cell populations is oestrogen-sensitive. In regard to the apparent prominent role of oestrogen-signalling in the late thymus maturation stage, the thymic differentiation of the corresponding subpopulations of T cells might be regulated by oestrogen. To the best of our knowledge, this is the first study investigating the dynamics of both nuclear and membrane oestrogen receptors in specific immune organs in a teleost fish at very early stages of immune system development as well as to examine thymic function in sea bass after an exposure to E2 during ontogenesis.This research was supported by ANR financed project ETaT (ANR-15-CE32-0014), by FCT (project UID/Multi/04326/2019, fellowship SFRH/BPD/84033/2012 and contract with the University of Algarve with reference DL57/2016/CP6321/CT0015 for P.I.S.P.) and by the EU H2020 Research and Innovation Programme AQUAEXCEL2020 (grant agreement 652831; TNA project AE050029) and ASSEMBLE PLUS (contract SR02022018976f).Peer reviewedElsevierFundação para a Ciência e a Tecnologia (Portugal)Universidade do AlgarveEuropean CommissionConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202120212021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Preprintinfo:eu-repo/semantics/submittedVersionhttp://hdl.handle.net/10261/228489reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/EC/H2020/652831https://doi.org/10.1016/j.dci.2021.104011Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2284892026-05-22T06:33:51Z
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