Immunomodulatory Effects of Lactiplantibacillus plantarum Strain RW1 During Salmonella Infection in Murine Intestinal Epithelial Cells and Dextran Sulfate Sodium-Induced Murine Colitis.

IF 4.4 2区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
Guangzhi Zhang, Abdul Raheem, Xiaofeng Xu, Xuezheng Fan, Jianwei Zhang, Tong Qin, Li Jia, Min Yue, Weifang Yang, Liang Wang, Mingyan Wang, Yajie Yin, Qiuchen Li, Ying Jiang, Ye Tian, Hui Jiang, Ting Xin, Jiabo Ding
{"title":"Immunomodulatory Effects of Lactiplantibacillus plantarum Strain RW1 During Salmonella Infection in Murine Intestinal Epithelial Cells and Dextran Sulfate Sodium-Induced Murine Colitis.","authors":"Guangzhi Zhang, Abdul Raheem, Xiaofeng Xu, Xuezheng Fan, Jianwei Zhang, Tong Qin, Li Jia, Min Yue, Weifang Yang, Liang Wang, Mingyan Wang, Yajie Yin, Qiuchen Li, Ying Jiang, Ye Tian, Hui Jiang, Ting Xin, Jiabo Ding","doi":"10.1007/s12602-024-10411-3","DOIUrl":null,"url":null,"abstract":"<p><p>Inflammatory diseases resulting from bacterial infections or inflammatory bowel disease pose significant threats to the health of both animals and humans. Although probiotics have emerged as a crucial preventive and adjunctive therapy for these conditions, the precise mechanisms through which probiotics regulate inflammatory diseases remain incompletely understood. In our previous study, animal-derived Lactiplantibacillus plantarum strain RW1 (L. plantarum RW1) with probiotic potential was isolated and characterized. In this study, the signaling pathway of L. plantarum RW1 inhibiting the inflammatory response of mouse intestinal epithelial cells caused by Salmonella infection was studied. Our results revealed that infection of Salmonella enterica subsp. enterica serovar Typhimurium strain ATCC14028 (S. Typhimurium ATCC14028) and Salmonella enterica subsp. enterica serovar Typhimurium strain SL1344 (S. Typhimurium SL1344) significantly increased NF-κB/p65 and TLR4 mRNA levels while decreasing IκB and TLR2 mRNA levels. Whereas L. plantarum RW1 treatment significantly reversed these changes. Western blotting confirmed these findings. Additionally, we explored the protective effects of L. plantarum RW1 in a murine colitis model induced by dextran sulfate sodium (DSS). Treatment with L. plantarum RW1 significantly increased both intestinal length and body weight compared to DSS-treated mice. 16S rRNA sequencing analysis demonstrated that L. plantarum RW1 restored the dysbiosis caused by DSS. Flow cytometry analyses further revealed that L. plantarum RW1 specifically increased regulatory T-cell proportions in Peyer's patches while reducing macrophage and neutrophil proportions, indicating the modulatory effects of L. plantarum RW1 on immune responses in gut-associated lymphatic tissue in the context of colitis. This study sheds light on the intricate interaction between probiotics and hosts, offering valuable insights into their potential application for treating inflammatory diseases in animals and humans.</p>","PeriodicalId":20506,"journal":{"name":"Probiotics and Antimicrobial Proteins","volume":" ","pages":""},"PeriodicalIF":4.4000,"publicationDate":"2024-12-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Probiotics and Antimicrobial Proteins","FirstCategoryId":"5","ListUrlMain":"https://doi.org/10.1007/s12602-024-10411-3","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Inflammatory diseases resulting from bacterial infections or inflammatory bowel disease pose significant threats to the health of both animals and humans. Although probiotics have emerged as a crucial preventive and adjunctive therapy for these conditions, the precise mechanisms through which probiotics regulate inflammatory diseases remain incompletely understood. In our previous study, animal-derived Lactiplantibacillus plantarum strain RW1 (L. plantarum RW1) with probiotic potential was isolated and characterized. In this study, the signaling pathway of L. plantarum RW1 inhibiting the inflammatory response of mouse intestinal epithelial cells caused by Salmonella infection was studied. Our results revealed that infection of Salmonella enterica subsp. enterica serovar Typhimurium strain ATCC14028 (S. Typhimurium ATCC14028) and Salmonella enterica subsp. enterica serovar Typhimurium strain SL1344 (S. Typhimurium SL1344) significantly increased NF-κB/p65 and TLR4 mRNA levels while decreasing IκB and TLR2 mRNA levels. Whereas L. plantarum RW1 treatment significantly reversed these changes. Western blotting confirmed these findings. Additionally, we explored the protective effects of L. plantarum RW1 in a murine colitis model induced by dextran sulfate sodium (DSS). Treatment with L. plantarum RW1 significantly increased both intestinal length and body weight compared to DSS-treated mice. 16S rRNA sequencing analysis demonstrated that L. plantarum RW1 restored the dysbiosis caused by DSS. Flow cytometry analyses further revealed that L. plantarum RW1 specifically increased regulatory T-cell proportions in Peyer's patches while reducing macrophage and neutrophil proportions, indicating the modulatory effects of L. plantarum RW1 on immune responses in gut-associated lymphatic tissue in the context of colitis. This study sheds light on the intricate interaction between probiotics and hosts, offering valuable insights into their potential application for treating inflammatory diseases in animals and humans.

植物乳杆菌RW1菌株对沙门氏菌感染小鼠肠上皮细胞和葡聚糖硫酸钠诱导小鼠结肠炎的免疫调节作用。
由细菌感染或炎症性肠病引起的炎症性疾病对动物和人类的健康构成重大威胁。虽然益生菌已成为这些疾病的重要预防和辅助治疗方法,但益生菌调节炎症性疾病的确切机制仍不完全清楚。我们在前期的研究中分离并鉴定了具有益生菌潜力的动物源性植物乳杆菌RW1 (L. plantarum RW1)。本研究研究了植物乳杆菌RW1抑制沙门氏菌感染小鼠肠上皮细胞炎症反应的信号通路。本研究结果显示,肠道沙门氏菌亚群感染。鼠伤寒沙门氏菌ATCC14028 (S. Typhimurium ATCC14028)和肠沙门氏菌亚种。鼠伤寒沙门氏菌SL1344 (S. Typhimurium SL1344)显著升高NF-κB/p65和TLR4 mRNA水平,降低i -κB和TLR2 mRNA水平。而植物乳杆菌RW1处理显著逆转了这些变化。Western blotting证实了这些发现。此外,我们还探讨了植物乳杆菌RW1对葡聚糖硫酸钠(DSS)诱导的小鼠结肠炎模型的保护作用。与dss处理的小鼠相比,植物乳杆菌RW1处理显著增加了肠道长度和体重。16S rRNA测序分析表明,L. plantarum RW1能够恢复DSS引起的生态失调。流式细胞术分析进一步发现,L. plantarum RW1特异性地增加了Peyer’s patches中调节性t细胞的比例,同时降低了巨噬细胞和中性粒细胞的比例,表明L. plantarum RW1对结肠炎背景下肠道相关淋巴组织的免疫反应具有调节作用。这项研究揭示了益生菌与宿主之间复杂的相互作用,为它们在治疗动物和人类炎症性疾病方面的潜在应用提供了有价值的见解。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Probiotics and Antimicrobial Proteins
Probiotics and Antimicrobial Proteins BIOTECHNOLOGY & APPLIED MICROBIOLOGYMICROB-MICROBIOLOGY
CiteScore
11.30
自引率
6.10%
发文量
140
期刊介绍: Probiotics and Antimicrobial Proteins publishes reviews, original articles, letters and short notes and technical/methodological communications aimed at advancing fundamental knowledge and exploration of the applications of probiotics, natural antimicrobial proteins and their derivatives in biomedical, agricultural, veterinary, food, and cosmetic products. The Journal welcomes fundamental research articles and reports on applications of these microorganisms and substances, and encourages structural studies and studies that correlate the structure and functional properties of antimicrobial proteins.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信