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Increased estrogen to androgen ratio enhances immunoglobulin levels and impairs B cell function in male mice

Sex steroids, such as estrogens and androgens, are important regulators of the humoral immune response. Studies in female mice have demonstrated that alteration of circulating estrogen concentration regulates antibody-mediated immunity. As males have normally little endogenous estrogen, we hypothesi...

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Autores principales: Aguilar-Pimentel, Juan Antonio, Cho, Yi-Li, Gerlini, Raffaele, Calzada-Wack, Julia, Wimmer, Maria, Mayer-Kuckuk, Philipp, Adler, Thure, Schmidt-Weber, Carsten B., Busch, Dirk H., Fuchs, Helmut, Gailus-Durner, Valérie, Ollert, Markus, Hrabě de Angelis, Martin, Ohlsson, Claes, Poutanen, Matti, Teperino, Raffaele, Strauss, Leena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7591566/
https://www.ncbi.nlm.nih.gov/pubmed/33110090
http://dx.doi.org/10.1038/s41598-020-75059-9
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author Aguilar-Pimentel, Juan Antonio
Cho, Yi-Li
Gerlini, Raffaele
Calzada-Wack, Julia
Wimmer, Maria
Mayer-Kuckuk, Philipp
Adler, Thure
Schmidt-Weber, Carsten B.
Busch, Dirk H.
Fuchs, Helmut
Gailus-Durner, Valérie
Ollert, Markus
Hrabě de Angelis, Martin
Ohlsson, Claes
Poutanen, Matti
Teperino, Raffaele
Strauss, Leena
author_facet Aguilar-Pimentel, Juan Antonio
Cho, Yi-Li
Gerlini, Raffaele
Calzada-Wack, Julia
Wimmer, Maria
Mayer-Kuckuk, Philipp
Adler, Thure
Schmidt-Weber, Carsten B.
Busch, Dirk H.
Fuchs, Helmut
Gailus-Durner, Valérie
Ollert, Markus
Hrabě de Angelis, Martin
Ohlsson, Claes
Poutanen, Matti
Teperino, Raffaele
Strauss, Leena
author_sort Aguilar-Pimentel, Juan Antonio
collection PubMed
description Sex steroids, such as estrogens and androgens, are important regulators of the humoral immune response. Studies in female mice have demonstrated that alteration of circulating estrogen concentration regulates antibody-mediated immunity. As males have normally little endogenous estrogen, we hypothesized that in males high estrogens and low androgens affect the immune system and enhance the allergic inflammatory response. Here, we studied transgenic male mice expressing human aromatase (AROM+). These animals have a high circulating estrogen to androgen ratio (E/A), causing female traits such as gynecomastia. We found that AROM+ male mice had significantly higher plasma immunoglobulin levels, particularly IgE. Flow cytometry analyses of splenocytes revealed changes in mature/immature B cell ratio together with a transcriptional upregulation of the Igh locus. Furthermore, higher proliferation rate and increased IgE synthesis after IgE class-switching was found. Subsequently, we utilized an ovalbumin airway challenge model to test the allergic response in AROM+ male mice. In line with above observations, an increase in IgE levels was measured, albeit no impact on immune cell infiltration into the lungs was detected. Together, our findings suggest that high circulating E/A in males significantly alters B cell function without any significant enhancement in allergic inflammation.
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spelling pubmed-75915662020-10-28 Increased estrogen to androgen ratio enhances immunoglobulin levels and impairs B cell function in male mice Aguilar-Pimentel, Juan Antonio Cho, Yi-Li Gerlini, Raffaele Calzada-Wack, Julia Wimmer, Maria Mayer-Kuckuk, Philipp Adler, Thure Schmidt-Weber, Carsten B. Busch, Dirk H. Fuchs, Helmut Gailus-Durner, Valérie Ollert, Markus Hrabě de Angelis, Martin Ohlsson, Claes Poutanen, Matti Teperino, Raffaele Strauss, Leena Sci Rep Article Sex steroids, such as estrogens and androgens, are important regulators of the humoral immune response. Studies in female mice have demonstrated that alteration of circulating estrogen concentration regulates antibody-mediated immunity. As males have normally little endogenous estrogen, we hypothesized that in males high estrogens and low androgens affect the immune system and enhance the allergic inflammatory response. Here, we studied transgenic male mice expressing human aromatase (AROM+). These animals have a high circulating estrogen to androgen ratio (E/A), causing female traits such as gynecomastia. We found that AROM+ male mice had significantly higher plasma immunoglobulin levels, particularly IgE. Flow cytometry analyses of splenocytes revealed changes in mature/immature B cell ratio together with a transcriptional upregulation of the Igh locus. Furthermore, higher proliferation rate and increased IgE synthesis after IgE class-switching was found. Subsequently, we utilized an ovalbumin airway challenge model to test the allergic response in AROM+ male mice. In line with above observations, an increase in IgE levels was measured, albeit no impact on immune cell infiltration into the lungs was detected. Together, our findings suggest that high circulating E/A in males significantly alters B cell function without any significant enhancement in allergic inflammation. Nature Publishing Group UK 2020-10-27 /pmc/articles/PMC7591566/ /pubmed/33110090 http://dx.doi.org/10.1038/s41598-020-75059-9 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Aguilar-Pimentel, Juan Antonio
Cho, Yi-Li
Gerlini, Raffaele
Calzada-Wack, Julia
Wimmer, Maria
Mayer-Kuckuk, Philipp
Adler, Thure
Schmidt-Weber, Carsten B.
Busch, Dirk H.
Fuchs, Helmut
Gailus-Durner, Valérie
Ollert, Markus
Hrabě de Angelis, Martin
Ohlsson, Claes
Poutanen, Matti
Teperino, Raffaele
Strauss, Leena
Increased estrogen to androgen ratio enhances immunoglobulin levels and impairs B cell function in male mice
title Increased estrogen to androgen ratio enhances immunoglobulin levels and impairs B cell function in male mice
title_full Increased estrogen to androgen ratio enhances immunoglobulin levels and impairs B cell function in male mice
title_fullStr Increased estrogen to androgen ratio enhances immunoglobulin levels and impairs B cell function in male mice
title_full_unstemmed Increased estrogen to androgen ratio enhances immunoglobulin levels and impairs B cell function in male mice
title_short Increased estrogen to androgen ratio enhances immunoglobulin levels and impairs B cell function in male mice
title_sort increased estrogen to androgen ratio enhances immunoglobulin levels and impairs b cell function in male mice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7591566/
https://www.ncbi.nlm.nih.gov/pubmed/33110090
http://dx.doi.org/10.1038/s41598-020-75059-9
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