Escherichia coli aggravates inflammatory response in mice oral mucositis through regulating Th17/Treg imbalance

IntroductionMicrobial dysbiosis links to mucosal immune dysregulation, but the specific bacterial contributions to oral mucosal inflammation remain unclear. Escherichia coli (E. coli), a pathogen well-characterized in mucosal immunity and immune regulation studies, has been observed to be enriched i...

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Main Authors: Jia Liu, Wenhui Xia, Juehua Cheng, Yanlin Geng, Weiping Li, Yuan Fan
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Cellular and Infection Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2025.1585020/full
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author Jia Liu
Jia Liu
Jia Liu
Wenhui Xia
Wenhui Xia
Wenhui Xia
Wenhui Xia
Juehua Cheng
Juehua Cheng
Juehua Cheng
Yanlin Geng
Yanlin Geng
Yanlin Geng
Weiping Li
Weiping Li
Weiping Li
Yuan Fan
Yuan Fan
Yuan Fan
author_facet Jia Liu
Jia Liu
Jia Liu
Wenhui Xia
Wenhui Xia
Wenhui Xia
Wenhui Xia
Juehua Cheng
Juehua Cheng
Juehua Cheng
Yanlin Geng
Yanlin Geng
Yanlin Geng
Weiping Li
Weiping Li
Weiping Li
Yuan Fan
Yuan Fan
Yuan Fan
author_sort Jia Liu
collection DOAJ
description IntroductionMicrobial dysbiosis links to mucosal immune dysregulation, but the specific bacterial contributions to oral mucosal inflammation remain unclear. Escherichia coli (E. coli), a pathogen well-characterized in mucosal immunity and immune regulation studies, has been observed to be enriched in chronic oral inflammatory lesions and was reported to modulate T helper 17 cells (Th17)/T regulatory cells (Treg) homeostasis. Here, we developed an oral mucositis mouse model via tongue scratch and E. coli topical application to investigate its role in Th17/Treg imbalance.MethodsThe inflammatory infiltration was evaluated by macroscopic photography and HE staining. The expression of inflammatory factors in tongue tissue and peripheral blood of mice were detected by immunohistochemical staining and enzyme-linked immunosorbent assay. The number of Th17 and Treg in mice spleen lymphocytes were evaluated with flow cytometry. Differential gene expression analysis, functional enrichment analysis and immune infiltration analysis were performed using RNA-seq data from oral lichen planus (OLP).ResultsE. coli stimulation aggravated inflammatory responses induced by scratching in lingual mucosa of mice, including increased local and systemic expression of interleukin 6 (IL6), interleukin 17 (IL17), chemokine receptor 6 (CCR6) and chemokine C-C motif ligand 20 (CCL20), increased proportions of Th17 cells and increased Th17/Treg ratio in spleen lymphocytes. Analysis of RNA-seq data from OLP revealed alterations in antimicrobial responses and inflammatory factors associated with upregulation of Th17/Treg balance.ConclusionThis study supports the role of E. coli in promoting oral mucosal inflammation and provides an experimental basis for in vivo study of OLP from the perspective of microorganisms.
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spelling doaj-art-0f79553e7b8b4cf28e36edad902876f32025-08-20T02:29:34ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882025-04-011510.3389/fcimb.2025.15850201585020Escherichia coli aggravates inflammatory response in mice oral mucositis through regulating Th17/Treg imbalanceJia Liu0Jia Liu1Jia Liu2Wenhui Xia3Wenhui Xia4Wenhui Xia5Wenhui Xia6Juehua Cheng7Juehua Cheng8Juehua Cheng9Yanlin Geng10Yanlin Geng11Yanlin Geng12Weiping Li13Weiping Li14Weiping Li15Yuan Fan16Yuan Fan17Yuan Fan18Department of Oral Mucosal Diseases, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, ChinaState Key Laboratory Cultivation Base of Research, Prevention and Treatment for Oral Diseases, Nanjing, ChinaJiangsu Province Engineering Research Center of Stomatological Translational Medicine, Nanjing, ChinaDepartment of Oral Mucosal Diseases, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, ChinaState Key Laboratory Cultivation Base of Research, Prevention and Treatment for Oral Diseases, Nanjing, ChinaJiangsu Province Engineering Research Center of Stomatological Translational Medicine, Nanjing, ChinaHefei Stomatological Hospital, Hefei Stomatology Clinical College of Anhui Medical University, Hefei, ChinaDepartment of Oral Mucosal Diseases, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, ChinaState Key Laboratory Cultivation Base of Research, Prevention and Treatment for Oral Diseases, Nanjing, ChinaJiangsu Province Engineering Research Center of Stomatological Translational Medicine, Nanjing, ChinaDepartment of Oral Mucosal Diseases, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, ChinaState Key Laboratory Cultivation Base of Research, Prevention and Treatment for Oral Diseases, Nanjing, ChinaJiangsu Province Engineering Research Center of Stomatological Translational Medicine, Nanjing, ChinaDepartment of Oral Mucosal Diseases, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, ChinaState Key Laboratory Cultivation Base of Research, Prevention and Treatment for Oral Diseases, Nanjing, ChinaJiangsu Province Engineering Research Center of Stomatological Translational Medicine, Nanjing, ChinaDepartment of Oral Mucosal Diseases, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, ChinaState Key Laboratory Cultivation Base of Research, Prevention and Treatment for Oral Diseases, Nanjing, ChinaJiangsu Province Engineering Research Center of Stomatological Translational Medicine, Nanjing, ChinaIntroductionMicrobial dysbiosis links to mucosal immune dysregulation, but the specific bacterial contributions to oral mucosal inflammation remain unclear. Escherichia coli (E. coli), a pathogen well-characterized in mucosal immunity and immune regulation studies, has been observed to be enriched in chronic oral inflammatory lesions and was reported to modulate T helper 17 cells (Th17)/T regulatory cells (Treg) homeostasis. Here, we developed an oral mucositis mouse model via tongue scratch and E. coli topical application to investigate its role in Th17/Treg imbalance.MethodsThe inflammatory infiltration was evaluated by macroscopic photography and HE staining. The expression of inflammatory factors in tongue tissue and peripheral blood of mice were detected by immunohistochemical staining and enzyme-linked immunosorbent assay. The number of Th17 and Treg in mice spleen lymphocytes were evaluated with flow cytometry. Differential gene expression analysis, functional enrichment analysis and immune infiltration analysis were performed using RNA-seq data from oral lichen planus (OLP).ResultsE. coli stimulation aggravated inflammatory responses induced by scratching in lingual mucosa of mice, including increased local and systemic expression of interleukin 6 (IL6), interleukin 17 (IL17), chemokine receptor 6 (CCR6) and chemokine C-C motif ligand 20 (CCL20), increased proportions of Th17 cells and increased Th17/Treg ratio in spleen lymphocytes. Analysis of RNA-seq data from OLP revealed alterations in antimicrobial responses and inflammatory factors associated with upregulation of Th17/Treg balance.ConclusionThis study supports the role of E. coli in promoting oral mucosal inflammation and provides an experimental basis for in vivo study of OLP from the perspective of microorganisms.https://www.frontiersin.org/articles/10.3389/fcimb.2025.1585020/fulloral mucosal immune inflammationEscherichia colimice modelTh17/Treg responsemucosal immunity
spellingShingle Jia Liu
Jia Liu
Jia Liu
Wenhui Xia
Wenhui Xia
Wenhui Xia
Wenhui Xia
Juehua Cheng
Juehua Cheng
Juehua Cheng
Yanlin Geng
Yanlin Geng
Yanlin Geng
Weiping Li
Weiping Li
Weiping Li
Yuan Fan
Yuan Fan
Yuan Fan
Escherichia coli aggravates inflammatory response in mice oral mucositis through regulating Th17/Treg imbalance
Frontiers in Cellular and Infection Microbiology
oral mucosal immune inflammation
Escherichia coli
mice model
Th17/Treg response
mucosal immunity
title Escherichia coli aggravates inflammatory response in mice oral mucositis through regulating Th17/Treg imbalance
title_full Escherichia coli aggravates inflammatory response in mice oral mucositis through regulating Th17/Treg imbalance
title_fullStr Escherichia coli aggravates inflammatory response in mice oral mucositis through regulating Th17/Treg imbalance
title_full_unstemmed Escherichia coli aggravates inflammatory response in mice oral mucositis through regulating Th17/Treg imbalance
title_short Escherichia coli aggravates inflammatory response in mice oral mucositis through regulating Th17/Treg imbalance
title_sort escherichia coli aggravates inflammatory response in mice oral mucositis through regulating th17 treg imbalance
topic oral mucosal immune inflammation
Escherichia coli
mice model
Th17/Treg response
mucosal immunity
url https://www.frontiersin.org/articles/10.3389/fcimb.2025.1585020/full
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