Trichinella spiralis excretory/secretory antigens ameliorate porcine epidemic diarrhea virus-induced mucosal damage in porcine intestinal oganoids by alleviating inflammation and promoting tight junction.

IF 3.7 2区 医学 Q1 PARASITOLOGY
Yinju Liu, Jinlong Tan, Nianzhang Zhang, Zigang Qu, Wenhui Li, Yaodong Wu, Hong Yin, Guangliang Liu, Baoquan Fu
{"title":"Trichinella spiralis excretory/secretory antigens ameliorate porcine epidemic diarrhea virus-induced mucosal damage in porcine intestinal oganoids by alleviating inflammation and promoting tight junction.","authors":"Yinju Liu, Jinlong Tan, Nianzhang Zhang, Zigang Qu, Wenhui Li, Yaodong Wu, Hong Yin, Guangliang Liu, Baoquan Fu","doi":"10.1016/j.ijpara.2024.12.002","DOIUrl":null,"url":null,"abstract":"<p><p>Trichinella spiralis and porcine epidemic diarrhea virus (PEDV) are two infectious swine pathogens. Parasite excretory/secretory antigens play critical roles in various disease processes. To explore the coexistence mechanism of two pathogens infecting the same host, the intestinal organoid was utilized to reproduce these biological processes. In this study, we investigated the effects of T. spiralis excretory/secretory antigens (TsES) on PEDV-induced inflammatory regulation, lesion recovery, and mucosal barrier repair in porcine intestinal organoids. The results showed that PEDV effectively infected the porcine intestinal organoids. Next, TsES inhibited pro-inflammatory cytokines and increased the anti-inflammatory cytokines produced by PEDV-infected porcine intestinal organoids. Further, four-dimensional (4D) label-free quantitative proteomics and western blotting confirmed that TsES regulate the inflammation caused by PEDV infection through the nuclear factor kappa-B (NF-κB) pathway. In addition, TsES promoted cell proliferation, inhibited apoptosis, and reduced PEDV-induced lesions in intestinal organoids. The elevated secretory immunoglobulin A (sIgA) levels caused by PEDV infection were downregulated by TsES treatment in intestinal organoids. TsES treatment reversed the mucosal barrier damage caused by PEDV infection in intestinal organoids. Finally, PEDV replication increased after TsES treatment in organoids. We highlight the potential of TsES to ameliorate PEDV-induced inflammation, mucosal lesions, and barrier damage in porcine intestinal organoids. TsES also contribute to PEDV replication. This study presents a novel research model for research on host-virus-parasite interactions, while also providing a theoretical foundation to consider parasite derivatives as a potential adjunctive therapy for intestinal inflammation.</p>","PeriodicalId":13725,"journal":{"name":"International journal for parasitology","volume":" ","pages":""},"PeriodicalIF":3.7000,"publicationDate":"2024-12-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"International journal for parasitology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1016/j.ijpara.2024.12.002","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PARASITOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Trichinella spiralis and porcine epidemic diarrhea virus (PEDV) are two infectious swine pathogens. Parasite excretory/secretory antigens play critical roles in various disease processes. To explore the coexistence mechanism of two pathogens infecting the same host, the intestinal organoid was utilized to reproduce these biological processes. In this study, we investigated the effects of T. spiralis excretory/secretory antigens (TsES) on PEDV-induced inflammatory regulation, lesion recovery, and mucosal barrier repair in porcine intestinal organoids. The results showed that PEDV effectively infected the porcine intestinal organoids. Next, TsES inhibited pro-inflammatory cytokines and increased the anti-inflammatory cytokines produced by PEDV-infected porcine intestinal organoids. Further, four-dimensional (4D) label-free quantitative proteomics and western blotting confirmed that TsES regulate the inflammation caused by PEDV infection through the nuclear factor kappa-B (NF-κB) pathway. In addition, TsES promoted cell proliferation, inhibited apoptosis, and reduced PEDV-induced lesions in intestinal organoids. The elevated secretory immunoglobulin A (sIgA) levels caused by PEDV infection were downregulated by TsES treatment in intestinal organoids. TsES treatment reversed the mucosal barrier damage caused by PEDV infection in intestinal organoids. Finally, PEDV replication increased after TsES treatment in organoids. We highlight the potential of TsES to ameliorate PEDV-induced inflammation, mucosal lesions, and barrier damage in porcine intestinal organoids. TsES also contribute to PEDV replication. This study presents a novel research model for research on host-virus-parasite interactions, while also providing a theoretical foundation to consider parasite derivatives as a potential adjunctive therapy for intestinal inflammation.

求助全文
约1分钟内获得全文 求助全文
来源期刊
CiteScore
8.40
自引率
2.50%
发文量
76
审稿时长
23 days
期刊介绍: International Journal for Parasitology offers authors the option to sponsor nonsubscriber access to their articles on Elsevier electronic publishing platforms. For more information please view our Sponsored Articles page. The International Journal for Parasitology publishes the results of original research in all aspects of basic and applied parasitology, including all the fields covered by its Specialist Editors, and ranging from parasites and host-parasite relationships of intrinsic biological interest to those of social and economic importance in human and veterinary medicine and agriculture.
×
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