Listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responses

Abstract Bacterial extracellular vesicles (BEVs) are actively secreted nanostructures that play a unique role in the pathogenesis of bacterial infections. In this study, we established an intestinal epithelial cell (IEC)/macrophage coculture system and found that Listeria monocytogenes (LM) membrane...

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Main Authors: Yao Lei, Kehan Chen, Mingyuan Tang, Qiuyang Zhang, Jie Yu, Yunwen Zhang, Tian Tang, Chuan Wang
Format: Article
Language:English
Published: Wiley-VCH 2025-05-01
Series:Interdisciplinary Medicine
Subjects:
Online Access:https://doi.org/10.1002/INMD.20240066
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author Yao Lei
Kehan Chen
Mingyuan Tang
Qiuyang Zhang
Jie Yu
Yunwen Zhang
Tian Tang
Chuan Wang
author_facet Yao Lei
Kehan Chen
Mingyuan Tang
Qiuyang Zhang
Jie Yu
Yunwen Zhang
Tian Tang
Chuan Wang
author_sort Yao Lei
collection DOAJ
description Abstract Bacterial extracellular vesicles (BEVs) are actively secreted nanostructures that play a unique role in the pathogenesis of bacterial infections. In this study, we established an intestinal epithelial cell (IEC)/macrophage coculture system and found that Listeria monocytogenes (LM) membrane vesicles (MVs) acted on macrophages and caused intestinal barrier disruption. Further studies revealed that LM MVs not only induced the M1‐type polarization in macrophages through the MAPK signaling pathway but also activated AIM2 and NLRP3 inflammasomes in macrophages to induce pyroptosis. The inflammatory factors IFN‐α and TNF‐α released by macrophages can bind to IFNAR and TNFR in IECs and activate the JAK‐STAT3 signaling pathway, disrupting the intestinal barrier. Our study illustrates the role and mechanism of LM MVs in disrupting the intestinal barrier by regulating the inflammatory response of macrophages, which helps understand the function of LM MVs, explains the mechanism of LM‐intestinal infection, and may provide new targets for the treatment of intestinal invasive infections with LM.
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institution Kabale University
issn 2832-6245
language English
publishDate 2025-05-01
publisher Wiley-VCH
record_format Article
series Interdisciplinary Medicine
spelling doaj-art-2129a1943ef44f148887fcd18958d3362025-08-20T03:26:39ZengWiley-VCHInterdisciplinary Medicine2832-62452025-05-0133n/an/a10.1002/INMD.20240066Listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responsesYao Lei0Kehan Chen1Mingyuan Tang2Qiuyang Zhang3Jie Yu4Yunwen Zhang5Tian Tang6Chuan Wang7West China School of Public Health and West China Fourth Hospital Sichuan University Chengdu ChinaWest China School of Public Health and West China Fourth Hospital Sichuan University Chengdu ChinaWest China School of Public Health and West China Fourth Hospital Sichuan University Chengdu ChinaWest China School of Public Health and West China Fourth Hospital Sichuan University Chengdu ChinaWest China School of Public Health and West China Fourth Hospital Sichuan University Chengdu ChinaWest China School of Public Health and West China Fourth Hospital Sichuan University Chengdu ChinaWest China School of Public Health and West China Fourth Hospital Sichuan University Chengdu ChinaWest China School of Public Health and West China Fourth Hospital Sichuan University Chengdu ChinaAbstract Bacterial extracellular vesicles (BEVs) are actively secreted nanostructures that play a unique role in the pathogenesis of bacterial infections. In this study, we established an intestinal epithelial cell (IEC)/macrophage coculture system and found that Listeria monocytogenes (LM) membrane vesicles (MVs) acted on macrophages and caused intestinal barrier disruption. Further studies revealed that LM MVs not only induced the M1‐type polarization in macrophages through the MAPK signaling pathway but also activated AIM2 and NLRP3 inflammasomes in macrophages to induce pyroptosis. The inflammatory factors IFN‐α and TNF‐α released by macrophages can bind to IFNAR and TNFR in IECs and activate the JAK‐STAT3 signaling pathway, disrupting the intestinal barrier. Our study illustrates the role and mechanism of LM MVs in disrupting the intestinal barrier by regulating the inflammatory response of macrophages, which helps understand the function of LM MVs, explains the mechanism of LM‐intestinal infection, and may provide new targets for the treatment of intestinal invasive infections with LM.https://doi.org/10.1002/INMD.20240066inflammatory responseintestinal epithelial cellsListeria monocytogenesmacrophagesmembrane vesicles
spellingShingle Yao Lei
Kehan Chen
Mingyuan Tang
Qiuyang Zhang
Jie Yu
Yunwen Zhang
Tian Tang
Chuan Wang
Listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responses
Interdisciplinary Medicine
inflammatory response
intestinal epithelial cells
Listeria monocytogenes
macrophages
membrane vesicles
title Listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responses
title_full Listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responses
title_fullStr Listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responses
title_full_unstemmed Listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responses
title_short Listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responses
title_sort listeria monocytogenes membrane vesicles disrupting intestinal epithelial barrier function via modulating macrophage inflammatory responses
topic inflammatory response
intestinal epithelial cells
Listeria monocytogenes
macrophages
membrane vesicles
url https://doi.org/10.1002/INMD.20240066
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