Vaccination of Gilthead Seabream After Continuous Xenoestrogen Oral Exposure Enhances the Gut Endobolome and Immune Status via GPER1
In fish culture settings, the exogenous input of steroids is a matter of concern. Recently, we unveiled that in the gilthead seabream (Sparus aurata), the G protein-coupled estrogen receptor agonist G-1 (G1) and the endocrine disruptor 17α-ethinylestradiol (EE2) are potent modulators in polyreactive...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-10-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.742827/full |
| _version_ | 1818583715590176768 |
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| author | Pablo Castejón Isabel Cabas Victoria Gómez Elena Chaves-Pozo Isabel Cerezo-Ortega Miguel Ángel Moriñigo Eduardo Martínez-Manzanares Jorge Galindo-Villegas Alfonsa García-Ayala |
| author_facet | Pablo Castejón Isabel Cabas Victoria Gómez Elena Chaves-Pozo Isabel Cerezo-Ortega Miguel Ángel Moriñigo Eduardo Martínez-Manzanares Jorge Galindo-Villegas Alfonsa García-Ayala |
| author_sort | Pablo Castejón |
| collection | DOAJ |
| description | In fish culture settings, the exogenous input of steroids is a matter of concern. Recently, we unveiled that in the gilthead seabream (Sparus aurata), the G protein-coupled estrogen receptor agonist G-1 (G1) and the endocrine disruptor 17α-ethinylestradiol (EE2) are potent modulators in polyreactive antibody production. However, the integral role of the microbiota upon immunity and antibody processing in response to the effect of EE2 remains largely unexplored. Here, juvenile seabreams continuously exposed for 84 days to oral G1 or EE2 mixed in the fish food were intraperitoneally (i.p.) immune primed on day 42 with the model antigen keyhole limpet hemocyanin (KLH). A critical panel of systemic and mucosal immune markers, serum VTG, and humoral, enzymatic, and bacteriolytic activities were recorded and correlated with gut bacterial metagenomic analysis 1 day post-priming (dpp). Besides, at 15 dpp, animals received a boost to investigate the possible generation of specific anti-KLH antibodies at the systemic and mucosal interphases by the end of the trial. On day 43, EE2 but not G1 induced a significant shift in the serum VTG level of naive fish. Simultaneously, significant changes in some immune enzymatic activities in the serum and gut mucus of the EE2-treated group were recorded. In comparison, the vaccine priming immunization resulted in an attenuated profile of most enzymatic activities in the same group. The gut genes qPCR analysis exhibited a related pattern, only emphasized by a significant shift in the EE2 group’s il1b expression. The gut bacterial microbiome status underwent 16S rRNA dynamic changes in alpha diversity indices, only with the exposure to oral G1, supporting functional alterations on cellular processes, signaling, and lipid metabolism in the microbiota. By the same token, the immunization elevated the relative abundance of Fusobacteria only in the control group, while this phylum was depleted in both the treated groups. Remarkably, the immunization also promoted changes in the bacterial class Betaproteobacteria and the estrogen-associated genus Novosphingobium. Furthermore, systemic and mucosal KLH-specific immunoglobulin (Ig)M and IgT levels in the fully vaccinated fish showed only slight changes 84 days post-estrogenic oral administration. In summary, our results highlight the intrinsic relationship among estrogens, their associated receptors, and immunization in the ubiquitous fish immune regulation and the subtle but significant crosstalk with the gut endobolome. |
| first_indexed | 2024-12-16T08:09:41Z |
| format | Article |
| id | doaj.art-25dea52d3b9841da8722bc6bcce06ac0 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-16T08:09:41Z |
| publishDate | 2021-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-25dea52d3b9841da8722bc6bcce06ac02022-12-21T22:38:22ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-10-011210.3389/fimmu.2021.742827742827Vaccination of Gilthead Seabream After Continuous Xenoestrogen Oral Exposure Enhances the Gut Endobolome and Immune Status via GPER1Pablo Castejón0Isabel Cabas1Victoria Gómez2Elena Chaves-Pozo3Isabel Cerezo-Ortega4Miguel Ángel Moriñigo5Eduardo Martínez-Manzanares6Jorge Galindo-Villegas7Alfonsa García-Ayala8Department of Cell Biology and Histology, Regional Campus of International Excellence “Campus Mare Nostrum”, University of Murcia, Instituto Murciano de Investigacion Biosanitaria (IMIB), Centro de Investigacion Biomedica en Red Enfermedades Raras (CIBERER), Murcia, SpainDepartment of Cell Biology and Histology, Regional Campus of International Excellence “Campus Mare Nostrum”, University of Murcia, Instituto Murciano de Investigacion Biosanitaria (IMIB), Centro de Investigacion Biomedica en Red Enfermedades Raras (CIBERER), Murcia, SpainDepartment of Cell Biology and Histology, Regional Campus of International Excellence “Campus Mare Nostrum”, University of Murcia, Instituto Murciano de Investigacion Biosanitaria (IMIB), Centro de Investigacion Biomedica en Red Enfermedades Raras (CIBERER), Murcia, SpainAquaculture Department, Oceanographic Center of Murcia, Spanish Institute of Oceanography (IEO-CSIC), Murcia, SpainDepartment of Microbiology, Faculty of Sciences, University of Malaga, Málaga, SpainDepartment of Microbiology, Faculty of Sciences, University of Malaga, Málaga, SpainDepartment of Microbiology, Faculty of Sciences, University of Malaga, Málaga, SpainFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayDepartment of Cell Biology and Histology, Regional Campus of International Excellence “Campus Mare Nostrum”, University of Murcia, Instituto Murciano de Investigacion Biosanitaria (IMIB), Centro de Investigacion Biomedica en Red Enfermedades Raras (CIBERER), Murcia, SpainIn fish culture settings, the exogenous input of steroids is a matter of concern. Recently, we unveiled that in the gilthead seabream (Sparus aurata), the G protein-coupled estrogen receptor agonist G-1 (G1) and the endocrine disruptor 17α-ethinylestradiol (EE2) are potent modulators in polyreactive antibody production. However, the integral role of the microbiota upon immunity and antibody processing in response to the effect of EE2 remains largely unexplored. Here, juvenile seabreams continuously exposed for 84 days to oral G1 or EE2 mixed in the fish food were intraperitoneally (i.p.) immune primed on day 42 with the model antigen keyhole limpet hemocyanin (KLH). A critical panel of systemic and mucosal immune markers, serum VTG, and humoral, enzymatic, and bacteriolytic activities were recorded and correlated with gut bacterial metagenomic analysis 1 day post-priming (dpp). Besides, at 15 dpp, animals received a boost to investigate the possible generation of specific anti-KLH antibodies at the systemic and mucosal interphases by the end of the trial. On day 43, EE2 but not G1 induced a significant shift in the serum VTG level of naive fish. Simultaneously, significant changes in some immune enzymatic activities in the serum and gut mucus of the EE2-treated group were recorded. In comparison, the vaccine priming immunization resulted in an attenuated profile of most enzymatic activities in the same group. The gut genes qPCR analysis exhibited a related pattern, only emphasized by a significant shift in the EE2 group’s il1b expression. The gut bacterial microbiome status underwent 16S rRNA dynamic changes in alpha diversity indices, only with the exposure to oral G1, supporting functional alterations on cellular processes, signaling, and lipid metabolism in the microbiota. By the same token, the immunization elevated the relative abundance of Fusobacteria only in the control group, while this phylum was depleted in both the treated groups. Remarkably, the immunization also promoted changes in the bacterial class Betaproteobacteria and the estrogen-associated genus Novosphingobium. Furthermore, systemic and mucosal KLH-specific immunoglobulin (Ig)M and IgT levels in the fully vaccinated fish showed only slight changes 84 days post-estrogenic oral administration. In summary, our results highlight the intrinsic relationship among estrogens, their associated receptors, and immunization in the ubiquitous fish immune regulation and the subtle but significant crosstalk with the gut endobolome.https://www.frontiersin.org/articles/10.3389/fimmu.2021.742827/full16S rRNAendocrine disruptors (EDCs)endobolomeestrogensfishG protein-coupled receptor 1 |
| spellingShingle | Pablo Castejón Isabel Cabas Victoria Gómez Elena Chaves-Pozo Isabel Cerezo-Ortega Miguel Ángel Moriñigo Eduardo Martínez-Manzanares Jorge Galindo-Villegas Alfonsa García-Ayala Vaccination of Gilthead Seabream After Continuous Xenoestrogen Oral Exposure Enhances the Gut Endobolome and Immune Status via GPER1 Frontiers in Immunology 16S rRNA endocrine disruptors (EDCs) endobolome estrogens fish G protein-coupled receptor 1 |
| title | Vaccination of Gilthead Seabream After Continuous Xenoestrogen Oral Exposure Enhances the Gut Endobolome and Immune Status via GPER1 |
| title_full | Vaccination of Gilthead Seabream After Continuous Xenoestrogen Oral Exposure Enhances the Gut Endobolome and Immune Status via GPER1 |
| title_fullStr | Vaccination of Gilthead Seabream After Continuous Xenoestrogen Oral Exposure Enhances the Gut Endobolome and Immune Status via GPER1 |
| title_full_unstemmed | Vaccination of Gilthead Seabream After Continuous Xenoestrogen Oral Exposure Enhances the Gut Endobolome and Immune Status via GPER1 |
| title_short | Vaccination of Gilthead Seabream After Continuous Xenoestrogen Oral Exposure Enhances the Gut Endobolome and Immune Status via GPER1 |
| title_sort | vaccination of gilthead seabream after continuous xenoestrogen oral exposure enhances the gut endobolome and immune status via gper1 |
| topic | 16S rRNA endocrine disruptors (EDCs) endobolome estrogens fish G protein-coupled receptor 1 |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.742827/full |
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