Escherichia coli adhesion protein FimH exacerbates colitis via CD11b+CD103- dendritic cell activation

IntroductionImmune stimulators are used to improve vaccine efficiency; however, they are accompanied by various side effects. In previous studies, we reported that the Escherichia coli adhesion protein, FimH, induces immune activity; however, we did not examine any side effects in colon inflammation...

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Main Authors: Wei Zhang, Eun-Koung An, So-Jung Kim, Hae-Bin Park, Peter C. W. Lee, Jun-O Jin
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2023.1284770/full
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author Wei Zhang
Eun-Koung An
So-Jung Kim
Hae-Bin Park
Peter C. W. Lee
Jun-O Jin
author_facet Wei Zhang
Eun-Koung An
So-Jung Kim
Hae-Bin Park
Peter C. W. Lee
Jun-O Jin
author_sort Wei Zhang
collection DOAJ
description IntroductionImmune stimulators are used to improve vaccine efficiency; however, they are accompanied by various side effects. In previous studies, we reported that the Escherichia coli adhesion protein, FimH, induces immune activity; however, we did not examine any side effects in colon inflammation.MethodsFimH was administered orally or intraperitoneally (i.p.) to mice with dextran sulfate sodium (DSS)-induced colitis, and changes in symptoms were observed. Immune cells infiltrated into the colon after the induction of colon inflammation were analyzed using a flow cytometer. Changes in Th1 and Th17 cells that induce colitis were analyzed. Further, mesenteric lymph node (mLN) dendritic cells (DCs) activated by FimH were identified and isolated to examine their ability to induce T-cell immunity.ResultsFimH oral and i.p. administration in C57BL/6 mice did not induce inflammation in the colon; however, DSS-induced colitis was exacerbated by oral and i.p. FimH administration. FimH treatment increased immune cell infiltration in the colon compared to that in DSS colitis. Th1 and Th17 cells, which are directly related to colitis, were increased in the colon by FimH; however, FimH did not directly affect the differentiation of these T cells. FimH upregulated the CD11b+CD103- DC activity in the mLNs, which produced the signature cytokines required for Th1 and Th17. In addition, isolated CD11b+CD103- DCs, after stimulation with FimH, directly induced Th1 and Th17 differentiation in a co-culture of CD4 T cells.ConclusionThis study demonstrated the side effects of FimH and indicated that the use of FimH can aggravate the disease in patients with colitis.
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spelling doaj.art-fd381f088a5b403d9ad641dba08b49742023-11-23T15:41:11ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-11-011410.3389/fimmu.2023.12847701284770Escherichia coli adhesion protein FimH exacerbates colitis via CD11b+CD103- dendritic cell activationWei Zhang0Eun-Koung An1So-Jung Kim2Hae-Bin Park3Peter C. W. Lee4Jun-O Jin5Shanghai Public Health Clinical Center, Shanghai Medical College, Fudan University, Shanghai, ChinaDepartment of Microbiology, ASAN Medical Center, University of Ulsan College of Medicine, Seoul, Republic of KoreaDepartment of Microbiology, ASAN Medical Center, University of Ulsan College of Medicine, Seoul, Republic of KoreaDepartment of Microbiology, ASAN Medical Center, University of Ulsan College of Medicine, Seoul, Republic of KoreaDepartment of Biochemistry and Molecular Biology, ASAN Medical Center, University of Ulsan College of Medicine, Seoul, Republic of KoreaDepartment of Microbiology, ASAN Medical Center, University of Ulsan College of Medicine, Seoul, Republic of KoreaIntroductionImmune stimulators are used to improve vaccine efficiency; however, they are accompanied by various side effects. In previous studies, we reported that the Escherichia coli adhesion protein, FimH, induces immune activity; however, we did not examine any side effects in colon inflammation.MethodsFimH was administered orally or intraperitoneally (i.p.) to mice with dextran sulfate sodium (DSS)-induced colitis, and changes in symptoms were observed. Immune cells infiltrated into the colon after the induction of colon inflammation were analyzed using a flow cytometer. Changes in Th1 and Th17 cells that induce colitis were analyzed. Further, mesenteric lymph node (mLN) dendritic cells (DCs) activated by FimH were identified and isolated to examine their ability to induce T-cell immunity.ResultsFimH oral and i.p. administration in C57BL/6 mice did not induce inflammation in the colon; however, DSS-induced colitis was exacerbated by oral and i.p. FimH administration. FimH treatment increased immune cell infiltration in the colon compared to that in DSS colitis. Th1 and Th17 cells, which are directly related to colitis, were increased in the colon by FimH; however, FimH did not directly affect the differentiation of these T cells. FimH upregulated the CD11b+CD103- DC activity in the mLNs, which produced the signature cytokines required for Th1 and Th17. In addition, isolated CD11b+CD103- DCs, after stimulation with FimH, directly induced Th1 and Th17 differentiation in a co-culture of CD4 T cells.ConclusionThis study demonstrated the side effects of FimH and indicated that the use of FimH can aggravate the disease in patients with colitis.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1284770/fullcolitisdendritic cellFimHTh1Th17
spellingShingle Wei Zhang
Eun-Koung An
So-Jung Kim
Hae-Bin Park
Peter C. W. Lee
Jun-O Jin
Escherichia coli adhesion protein FimH exacerbates colitis via CD11b+CD103- dendritic cell activation
Frontiers in Immunology
colitis
dendritic cell
FimH
Th1
Th17
title Escherichia coli adhesion protein FimH exacerbates colitis via CD11b+CD103- dendritic cell activation
title_full Escherichia coli adhesion protein FimH exacerbates colitis via CD11b+CD103- dendritic cell activation
title_fullStr Escherichia coli adhesion protein FimH exacerbates colitis via CD11b+CD103- dendritic cell activation
title_full_unstemmed Escherichia coli adhesion protein FimH exacerbates colitis via CD11b+CD103- dendritic cell activation
title_short Escherichia coli adhesion protein FimH exacerbates colitis via CD11b+CD103- dendritic cell activation
title_sort escherichia coli adhesion protein fimh exacerbates colitis via cd11b cd103 dendritic cell activation
topic colitis
dendritic cell
FimH
Th1
Th17
url https://www.frontiersin.org/articles/10.3389/fimmu.2023.1284770/full
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