Eosinophil‐derived IL‐4 is necessary to establish the inflammatory structure in innate inflammation

Abstract Pathogen‐induced inflammation comprises pro‐ and anti‐inflammatory processes, which ensure pathogen removal and containment of the proinflammatory activities. Here, we aimed to identify the development of inflammatory microenvironments and their maintenance throughout the course of a toll‐l...

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Main Authors: Anja Kolbinger, Tim J Schäufele, Hanna Steigerwald, Joschua Friedel, Sandra Pierre, Gerd Geisslinger, Klaus Scholich
Format: Article
Language:English
Published: Springer Nature 2022-12-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202216796
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author Anja Kolbinger
Tim J Schäufele
Hanna Steigerwald
Joschua Friedel
Sandra Pierre
Gerd Geisslinger
Klaus Scholich
author_facet Anja Kolbinger
Tim J Schäufele
Hanna Steigerwald
Joschua Friedel
Sandra Pierre
Gerd Geisslinger
Klaus Scholich
author_sort Anja Kolbinger
collection DOAJ
description Abstract Pathogen‐induced inflammation comprises pro‐ and anti‐inflammatory processes, which ensure pathogen removal and containment of the proinflammatory activities. Here, we aimed to identify the development of inflammatory microenvironments and their maintenance throughout the course of a toll‐like receptor 2‐mediated paw inflammation. Within 24 h after pathogen‐injection, the immune cells were organized in three zones, which comprised a pathogen‐containing “core‐region”, a bordering proinflammatory (PI)‐region and an outer anti‐inflammatory (AI)‐region. Eosinophils were present in all three inflammatory regions and adapted their cytokine profile according to their localization. Eosinophil depletion reduced IL‐4 levels and increased edema formation as well as mechanical and thermal hypersensitivities during resolution of inflammation. Also, in the absence of eosinophils PI‐ and AI‐regions could not be determined anymore, neutrophil numbers increased, and efferocytosis as well as M2‐macrophage polarization were reduced. IL‐4 administration restored in eosinophil‐depleted mice PI‐ and AI‐regions, normalized neutrophil numbers, efferocytosis, M2‐macrophage polarization as well as resolution of zymosan‐induced hypersensitivity. In conclusion, IL‐4‐expressing eosinophils support the resolution of inflammation by enabling the development of an anti‐inflammatory framework, which encloses proinflammatory regions.
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spelling doaj-art-498a7c3b871e4cb6bba74af3f2022d422025-08-24T11:43:48ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842022-12-0115211710.15252/emmm.202216796Eosinophil‐derived IL‐4 is necessary to establish the inflammatory structure in innate inflammationAnja Kolbinger0Tim J Schäufele1Hanna Steigerwald2Joschua Friedel3Sandra Pierre4Gerd Geisslinger5Klaus Scholich6Institute of Clinical Pharmacology, Goethe‐University FrankfurtInstitute of Clinical Pharmacology, Goethe‐University FrankfurtInstitute of Clinical Pharmacology, Goethe‐University FrankfurtInstitute of Clinical Pharmacology, Goethe‐University FrankfurtInstitute of Clinical Pharmacology, Goethe‐University FrankfurtInstitute of Clinical Pharmacology, Goethe‐University FrankfurtInstitute of Clinical Pharmacology, Goethe‐University FrankfurtAbstract Pathogen‐induced inflammation comprises pro‐ and anti‐inflammatory processes, which ensure pathogen removal and containment of the proinflammatory activities. Here, we aimed to identify the development of inflammatory microenvironments and their maintenance throughout the course of a toll‐like receptor 2‐mediated paw inflammation. Within 24 h after pathogen‐injection, the immune cells were organized in three zones, which comprised a pathogen‐containing “core‐region”, a bordering proinflammatory (PI)‐region and an outer anti‐inflammatory (AI)‐region. Eosinophils were present in all three inflammatory regions and adapted their cytokine profile according to their localization. Eosinophil depletion reduced IL‐4 levels and increased edema formation as well as mechanical and thermal hypersensitivities during resolution of inflammation. Also, in the absence of eosinophils PI‐ and AI‐regions could not be determined anymore, neutrophil numbers increased, and efferocytosis as well as M2‐macrophage polarization were reduced. IL‐4 administration restored in eosinophil‐depleted mice PI‐ and AI‐regions, normalized neutrophil numbers, efferocytosis, M2‐macrophage polarization as well as resolution of zymosan‐induced hypersensitivity. In conclusion, IL‐4‐expressing eosinophils support the resolution of inflammation by enabling the development of an anti‐inflammatory framework, which encloses proinflammatory regions.https://doi.org/10.15252/emmm.202216796eosinophilinnate inflammationinterleukin‐4macrophagesmicroenvironments
spellingShingle Anja Kolbinger
Tim J Schäufele
Hanna Steigerwald
Joschua Friedel
Sandra Pierre
Gerd Geisslinger
Klaus Scholich
Eosinophil‐derived IL‐4 is necessary to establish the inflammatory structure in innate inflammation
EMBO Molecular Medicine
eosinophil
innate inflammation
interleukin‐4
macrophages
microenvironments
title Eosinophil‐derived IL‐4 is necessary to establish the inflammatory structure in innate inflammation
title_full Eosinophil‐derived IL‐4 is necessary to establish the inflammatory structure in innate inflammation
title_fullStr Eosinophil‐derived IL‐4 is necessary to establish the inflammatory structure in innate inflammation
title_full_unstemmed Eosinophil‐derived IL‐4 is necessary to establish the inflammatory structure in innate inflammation
title_short Eosinophil‐derived IL‐4 is necessary to establish the inflammatory structure in innate inflammation
title_sort eosinophil derived il 4 is necessary to establish the inflammatory structure in innate inflammation
topic eosinophil
innate inflammation
interleukin‐4
macrophages
microenvironments
url https://doi.org/10.15252/emmm.202216796
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