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Epithelial Heat Shock Proteins Mediate the Protective Effects of Limosilactobacillus reuteri in Dextran Sulfate Sodium-Induced Colitis

Liu, Hao-Yu and Gu, Fang and Zhu, Cuipeng and Yuan, Long and Zhu, Chuyang and Zhu, Miaonan and Yao, Jiacheng and Hu, Ping and Zhang, Yunzeng and Dicksved, Johan and Bao, Wenbin and Cai, Demin (2022). Epithelial Heat Shock Proteins Mediate the Protective Effects of Limosilactobacillus reuteri in Dextran Sulfate Sodium-Induced Colitis. Frontiers in Immunology. 13 , 865982
[Research article]

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Abstract

Defects in gut barrier function are implicated in gastrointestinal (GI) disorders like inflammatory bowel disease (IBD), as well as in systemic inflammation. With the increasing incidence of IBD worldwide, more attention should be paid to dietary interventions and therapeutics with the potential to boost the natural defense mechanisms of gut epithelial cells. The current study aimed to investigate the protective effects of Limosilactobacillus reuteri ATCC PTA 4659 in a colitis mouse model and delineate the mechanisms behind it. Wild-type mice were allocated to the control group; or given 3% dextran sulfate sodium (DSS) in drinking water for 7 days to induce colitis; or administered L. reuteri for 7 days as pretreatment; or for 14 days starting 7 days before subjecting to the DSS. Peroral treatment with L. reuteri improved colitis severity clinically and morphologically and reduced the colonic levels of Tumor necrosis factor-alpha (TNF-alpha) (Tnf), Interleukin 1-beta (Il1 beta), and nterferon-gamma (Ifng), the crucial pro-inflammatory cytokines in colitis onset. It also prevented the CD11b(+)Ly6G(+) neutrophil recruitment and the skewed immune responses in mesenteric lymph nodes (MLNs) of CD11b(+)CD11c(+) dendritic cell (DC) expansion and Foxp3(+)CD4(+) T-cell reduction. Using 16S rRNA gene amplicon sequencing and RT-qPCR, we demonstrated a colitis-driven bacterial translocation to MLNs and gut microbiota dysbiosis that were in part counterbalanced by L. reuteri treatment. Moreover, the expression of barrier-preserving tight junction (TJ) proteins and cytoprotective heat shock protein (HSP) 70 and HSP25 was reduced by colitis but boosted by L. reuteri treatment. A shift in expression pattern was also observed with HSP70 in response to the pretreatment and with HSP25 in response to L. reuteri-DSS. In addition, the changes of HSPs were found to be correlated to bacterial load and epithelial cell proliferation. In conclusion, our results demonstrate that the human-derived L. reuteri strain 4659 confers protection in experimental colitis in young mice, while intestinal HSPs may mediate the probiotic effects by providing a supportive protein-protein network for the epithelium in health and colitis.

Authors/Creators:Liu, Hao-Yu and Gu, Fang and Zhu, Cuipeng and Yuan, Long and Zhu, Chuyang and Zhu, Miaonan and Yao, Jiacheng and Hu, Ping and Zhang, Yunzeng and Dicksved, Johan and Bao, Wenbin and Cai, Demin
Title:Epithelial Heat Shock Proteins Mediate the Protective Effects of Limosilactobacillus reuteri in Dextran Sulfate Sodium-Induced Colitis
Series Name/Journal:Frontiers in Immunology
Year of publishing :2022
Volume:13
Article number:865982
Number of Pages:15
Publisher:FRONTIERS MEDIA SA
ISSN:1664-3224
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Immunology (Immunology in the medical area to be 30110)
Keywords:inflammatory bowel disease, barrier function, heat shock proteins, probiotics, gut microbiota
URN:NBN:urn:nbn:se:slu:epsilon-p-116591
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-116591
Additional ID:
Type of IDID
DOI10.3389/fimmu.2022.865982
Web of Science (WoS)000772603300001
ID Code:27566
Faculty:VH - Faculty of Veterinary Medicine and Animal Science
Department:(VH) > Dept. of Animal Nutrition and Management
Deposited By: SLUpub Connector
Deposited On:19 Apr 2022 07:59
Metadata Last Modified:19 Apr 2022 08:01

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