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S-Layer From Lactobacillus brevis Modulates Antigen-Presenting Cell Functions via the Mincle-Syk-Card9 Axis
C-type lectin receptors (CLRs) are pattern recognition receptors that are crucial in the innate immune response. The gastrointestinal tract contributes significantly to the maintenance of immune homeostasis; it is the shelter for billions of microorganisms including many genera of Lactobacillus sp....
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2021
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7957004/ https://www.ncbi.nlm.nih.gov/pubmed/33732234 http://dx.doi.org/10.3389/fimmu.2021.602067 |
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author | Prado Acosta, Mariano Goyette-Desjardins, Guillaume Scheffel, Jörg Dudeck, Anne Ruland, Jürgen Lepenies, Bernd |
author_facet | Prado Acosta, Mariano Goyette-Desjardins, Guillaume Scheffel, Jörg Dudeck, Anne Ruland, Jürgen Lepenies, Bernd |
author_sort | Prado Acosta, Mariano |
collection | PubMed |
description | C-type lectin receptors (CLRs) are pattern recognition receptors that are crucial in the innate immune response. The gastrointestinal tract contributes significantly to the maintenance of immune homeostasis; it is the shelter for billions of microorganisms including many genera of Lactobacillus sp. Previously, it was shown that host-CLR interactions with gut microbiota play a crucial role in this context. The Macrophage-inducible C-type lectin (Mincle) is a Syk-coupled CLR that contributes to sensing of mucosa-associated commensals. In this study, we identified Mincle as a receptor for the Surface (S)-layer of the probiotic bacteria Lactobacillus brevis modulating GM-CSF bone marrow-derived cells (BMDCs) functions. We found that the S-layer/Mincle interaction led to a balanced cytokine response in BMDCs by triggering the release of both pro- and anti-inflammatory cytokines. In contrast, BMDCs derived from Mincle(−/−), CARD9(−/−) or conditional Syk(−/−) mice failed to maintain this balance, thus leading to an increased production of the pro-inflammatory cytokines TNF and IL-6, whereas the levels of the anti-inflammatory cytokines IL-10 and TGF-β were markedly decreased. Importantly, this was accompanied by an altered CD4(+) T cell priming capacity of Mincle(−/−) BMDCs resulting in an increased CD4(+) T cell IFN-γ production upon stimulation with L. brevis S-layer. Our results contribute to the understanding of how commensal bacteria regulate antigen-presenting cell (APC) functions and highlight the importance of the Mincle/Syk/Card9 axis in APCs as a key factor in host-microbiota interactions. |
format | Online Article Text |
id | pubmed-7957004 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-79570042021-03-16 S-Layer From Lactobacillus brevis Modulates Antigen-Presenting Cell Functions via the Mincle-Syk-Card9 Axis Prado Acosta, Mariano Goyette-Desjardins, Guillaume Scheffel, Jörg Dudeck, Anne Ruland, Jürgen Lepenies, Bernd Front Immunol Immunology C-type lectin receptors (CLRs) are pattern recognition receptors that are crucial in the innate immune response. The gastrointestinal tract contributes significantly to the maintenance of immune homeostasis; it is the shelter for billions of microorganisms including many genera of Lactobacillus sp. Previously, it was shown that host-CLR interactions with gut microbiota play a crucial role in this context. The Macrophage-inducible C-type lectin (Mincle) is a Syk-coupled CLR that contributes to sensing of mucosa-associated commensals. In this study, we identified Mincle as a receptor for the Surface (S)-layer of the probiotic bacteria Lactobacillus brevis modulating GM-CSF bone marrow-derived cells (BMDCs) functions. We found that the S-layer/Mincle interaction led to a balanced cytokine response in BMDCs by triggering the release of both pro- and anti-inflammatory cytokines. In contrast, BMDCs derived from Mincle(−/−), CARD9(−/−) or conditional Syk(−/−) mice failed to maintain this balance, thus leading to an increased production of the pro-inflammatory cytokines TNF and IL-6, whereas the levels of the anti-inflammatory cytokines IL-10 and TGF-β were markedly decreased. Importantly, this was accompanied by an altered CD4(+) T cell priming capacity of Mincle(−/−) BMDCs resulting in an increased CD4(+) T cell IFN-γ production upon stimulation with L. brevis S-layer. Our results contribute to the understanding of how commensal bacteria regulate antigen-presenting cell (APC) functions and highlight the importance of the Mincle/Syk/Card9 axis in APCs as a key factor in host-microbiota interactions. Frontiers Media S.A. 2021-03-01 /pmc/articles/PMC7957004/ /pubmed/33732234 http://dx.doi.org/10.3389/fimmu.2021.602067 Text en Copyright © 2021 Prado Acosta, Goyette-Desjardins, Scheffel, Dudeck, Ruland and Lepenies. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Immunology Prado Acosta, Mariano Goyette-Desjardins, Guillaume Scheffel, Jörg Dudeck, Anne Ruland, Jürgen Lepenies, Bernd S-Layer From Lactobacillus brevis Modulates Antigen-Presenting Cell Functions via the Mincle-Syk-Card9 Axis |
title | S-Layer From Lactobacillus brevis Modulates Antigen-Presenting Cell Functions via the Mincle-Syk-Card9 Axis |
title_full | S-Layer From Lactobacillus brevis Modulates Antigen-Presenting Cell Functions via the Mincle-Syk-Card9 Axis |
title_fullStr | S-Layer From Lactobacillus brevis Modulates Antigen-Presenting Cell Functions via the Mincle-Syk-Card9 Axis |
title_full_unstemmed | S-Layer From Lactobacillus brevis Modulates Antigen-Presenting Cell Functions via the Mincle-Syk-Card9 Axis |
title_short | S-Layer From Lactobacillus brevis Modulates Antigen-Presenting Cell Functions via the Mincle-Syk-Card9 Axis |
title_sort | s-layer from lactobacillus brevis modulates antigen-presenting cell functions via the mincle-syk-card9 axis |
topic | Immunology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7957004/ https://www.ncbi.nlm.nih.gov/pubmed/33732234 http://dx.doi.org/10.3389/fimmu.2021.602067 |
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