Intestinal Macrophages Balance Inflammatory Expression Profiles via Vitamin A and Dectin-1-Mediated Signaling

Tissue resident intestinal macrophages are known to exhibit an anti-inflammatory phenotype and produce little pro-inflammatory cytokines upon TLR ligation, allowing symbiotic co-existence with the intestinal microbiota. However, upon acute events such as epithelial damage and concomitant influx of m...

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Main Authors: Martje N. Erkelens, Gera Goverse, Tanja Konijn, Rosalie Molenaar, Marieke R. Beijer, Jan Van den Bossche, Kyra E. de Goede, Sanne G. S. Verberk, Wouter J. de Jonge, Joke M. M. den Haan, Reina E. Mebius
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-03-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/article/10.3389/fimmu.2020.00551/full
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author Martje N. Erkelens
Gera Goverse
Tanja Konijn
Rosalie Molenaar
Marieke R. Beijer
Jan Van den Bossche
Kyra E. de Goede
Sanne G. S. Verberk
Wouter J. de Jonge
Joke M. M. den Haan
Reina E. Mebius
author_facet Martje N. Erkelens
Gera Goverse
Tanja Konijn
Rosalie Molenaar
Marieke R. Beijer
Jan Van den Bossche
Kyra E. de Goede
Sanne G. S. Verberk
Wouter J. de Jonge
Joke M. M. den Haan
Reina E. Mebius
author_sort Martje N. Erkelens
collection DOAJ
description Tissue resident intestinal macrophages are known to exhibit an anti-inflammatory phenotype and produce little pro-inflammatory cytokines upon TLR ligation, allowing symbiotic co-existence with the intestinal microbiota. However, upon acute events such as epithelial damage and concomitant influx of microbes, these macrophages must be able to quickly mount a pro-inflammatory response while more inflammatory macrophages are recruited from the blood stream simultaneously. Here, we show that dietary intake of vitamin A is required for the maintenance of the anti-inflammatory state of tissue resident intestinal macrophages. Interestingly, these anti-inflammatory macrophages were characterized by high levels of Dectin-1 expression. We show that Dectin-1 expression is enhanced by the vitamin A metabolite retinoic acid and our data suggests that Dectin-1 triggering might provide a switch to induce a rapid production of pro-inflammatory cytokines. In addition, Dectin-1 stimulation resulted in an altered metabolic profile which is linked to a pro-inflammatory response. Together, our data suggests that presence of vitamin A in the small intestine enhances an anti-inflammatory phenotype as well as Dectin-1 expression by macrophages and that this anti-inflammatory phenotype can rapidly convert toward a pro-inflammatory state upon Dectin-1 signaling.
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spelling doaj.art-7c1b2ccba2044b309c010d925ddfa5de2022-12-21T22:52:04ZengFrontiers Media S.A.Frontiers in Immunology1664-32242020-03-011110.3389/fimmu.2020.00551510774Intestinal Macrophages Balance Inflammatory Expression Profiles via Vitamin A and Dectin-1-Mediated SignalingMartje N. Erkelens0Gera Goverse1Tanja Konijn2Rosalie Molenaar3Marieke R. Beijer4Jan Van den Bossche5Kyra E. de Goede6Sanne G. S. Verberk7Wouter J. de Jonge8Joke M. M. den Haan9Reina E. Mebius10Department of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsTytgat Institute for Gastro Intestinal and Liver Research, Amsterdam Gastroenterology Endocrinology and Metabolism Research Institute, Amsterdam UMC, University of Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Molecular Cell Biology and Immunology, Amsterdam Infection and Immunity Institute, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsTissue resident intestinal macrophages are known to exhibit an anti-inflammatory phenotype and produce little pro-inflammatory cytokines upon TLR ligation, allowing symbiotic co-existence with the intestinal microbiota. However, upon acute events such as epithelial damage and concomitant influx of microbes, these macrophages must be able to quickly mount a pro-inflammatory response while more inflammatory macrophages are recruited from the blood stream simultaneously. Here, we show that dietary intake of vitamin A is required for the maintenance of the anti-inflammatory state of tissue resident intestinal macrophages. Interestingly, these anti-inflammatory macrophages were characterized by high levels of Dectin-1 expression. We show that Dectin-1 expression is enhanced by the vitamin A metabolite retinoic acid and our data suggests that Dectin-1 triggering might provide a switch to induce a rapid production of pro-inflammatory cytokines. In addition, Dectin-1 stimulation resulted in an altered metabolic profile which is linked to a pro-inflammatory response. Together, our data suggests that presence of vitamin A in the small intestine enhances an anti-inflammatory phenotype as well as Dectin-1 expression by macrophages and that this anti-inflammatory phenotype can rapidly convert toward a pro-inflammatory state upon Dectin-1 signaling.https://www.frontiersin.org/article/10.3389/fimmu.2020.00551/fullmacrophageretinoic acidDectin-1pro-inflammatoryanti-inflammatoryvitamin A
spellingShingle Martje N. Erkelens
Gera Goverse
Tanja Konijn
Rosalie Molenaar
Marieke R. Beijer
Jan Van den Bossche
Kyra E. de Goede
Sanne G. S. Verberk
Wouter J. de Jonge
Joke M. M. den Haan
Reina E. Mebius
Intestinal Macrophages Balance Inflammatory Expression Profiles via Vitamin A and Dectin-1-Mediated Signaling
Frontiers in Immunology
macrophage
retinoic acid
Dectin-1
pro-inflammatory
anti-inflammatory
vitamin A
title Intestinal Macrophages Balance Inflammatory Expression Profiles via Vitamin A and Dectin-1-Mediated Signaling
title_full Intestinal Macrophages Balance Inflammatory Expression Profiles via Vitamin A and Dectin-1-Mediated Signaling
title_fullStr Intestinal Macrophages Balance Inflammatory Expression Profiles via Vitamin A and Dectin-1-Mediated Signaling
title_full_unstemmed Intestinal Macrophages Balance Inflammatory Expression Profiles via Vitamin A and Dectin-1-Mediated Signaling
title_short Intestinal Macrophages Balance Inflammatory Expression Profiles via Vitamin A and Dectin-1-Mediated Signaling
title_sort intestinal macrophages balance inflammatory expression profiles via vitamin a and dectin 1 mediated signaling
topic macrophage
retinoic acid
Dectin-1
pro-inflammatory
anti-inflammatory
vitamin A
url https://www.frontiersin.org/article/10.3389/fimmu.2020.00551/full
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