SaaS sRNA promotes Salmonella intestinal invasion via modulating MAPK inflammatory pathway
ABSTRACTSalmonella Enteritidis is a foodborne enteric pathogen that infects humans and animals, utilizing complex survival strategies. Bacterial small RNA (sRNA) plays an important role in these strategies. However, the virulence regulatory network of S. Enteritidis remains largely incomplete and kn...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2023-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2023.2211184 |
| _version_ | 1827303797681029120 |
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| author | Linlin Cai Yunting Xie Liangting Shao Haijing Hu Xinglian Xu Huhu Wang Guanghong Zhou |
| author_facet | Linlin Cai Yunting Xie Liangting Shao Haijing Hu Xinglian Xu Huhu Wang Guanghong Zhou |
| author_sort | Linlin Cai |
| collection | DOAJ |
| description | ABSTRACTSalmonella Enteritidis is a foodborne enteric pathogen that infects humans and animals, utilizing complex survival strategies. Bacterial small RNA (sRNA) plays an important role in these strategies. However, the virulence regulatory network of S. Enteritidis remains largely incomplete and knowledge of gut virulence mechanisms of sRNAs is limited. Here, we characterized the function of a previously identified Salmonella adhesive-associated sRNA (SaaS) in the intestinal pathogenesis of S. Enteritidis. We found that SaaS promoted bacterial colonization in both cecum and colon of a BALB/c mouse model; it was preferentially expressed in colon. Moreover, our results showed that SaaS enhanced damage to mucosal barrier by affecting expressions of antimicrobial products, decreasing the number of goblet cells, suppressing mucin gene expression, and eventually reducing thickness of mucus layer; it further breached below physical barrier by strengthening invasion into epithelial cells in Caco-2 cell model as well as decreasing tight junction expressions. High throughput 16S rRNA gene sequencing revealed that SaaS also altered gut homeostasis by depleting beneficial gut microbiota while increasing harmful ones. Furthermore, by employing ELISA and western blot analysis, we demonstrated that SaaS regulated intestinal inflammation through sequential activation P38-JNK-ERK MAPK signaling pathway, which enabled immune escape at primary infection stage but strengthened pathogenesis at later stage, respectively. These findings suggest that SaaS plays an essential role in the virulence of S. Enteritidis and reveals its biological role in intestinal pathogenesis. |
| first_indexed | 2024-03-11T14:19:10Z |
| format | Article |
| id | doaj.art-516816305b64483699c80eee059b0d8f |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-04-24T17:07:09Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-516816305b64483699c80eee059b0d8f2024-03-28T22:38:20ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2211184SaaS sRNA promotes Salmonella intestinal invasion via modulating MAPK inflammatory pathwayLinlin Cai0Yunting Xie1Liangting Shao2Haijing Hu3Xinglian Xu4Huhu Wang5Guanghong Zhou6Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University, Nanjing, P.R. ChinaJiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University, Nanjing, P.R. ChinaJiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University, Nanjing, P.R. ChinaJiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University, Nanjing, P.R. ChinaJiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University, Nanjing, P.R. ChinaJiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University, Nanjing, P.R. ChinaJiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University, Nanjing, P.R. ChinaABSTRACTSalmonella Enteritidis is a foodborne enteric pathogen that infects humans and animals, utilizing complex survival strategies. Bacterial small RNA (sRNA) plays an important role in these strategies. However, the virulence regulatory network of S. Enteritidis remains largely incomplete and knowledge of gut virulence mechanisms of sRNAs is limited. Here, we characterized the function of a previously identified Salmonella adhesive-associated sRNA (SaaS) in the intestinal pathogenesis of S. Enteritidis. We found that SaaS promoted bacterial colonization in both cecum and colon of a BALB/c mouse model; it was preferentially expressed in colon. Moreover, our results showed that SaaS enhanced damage to mucosal barrier by affecting expressions of antimicrobial products, decreasing the number of goblet cells, suppressing mucin gene expression, and eventually reducing thickness of mucus layer; it further breached below physical barrier by strengthening invasion into epithelial cells in Caco-2 cell model as well as decreasing tight junction expressions. High throughput 16S rRNA gene sequencing revealed that SaaS also altered gut homeostasis by depleting beneficial gut microbiota while increasing harmful ones. Furthermore, by employing ELISA and western blot analysis, we demonstrated that SaaS regulated intestinal inflammation through sequential activation P38-JNK-ERK MAPK signaling pathway, which enabled immune escape at primary infection stage but strengthened pathogenesis at later stage, respectively. These findings suggest that SaaS plays an essential role in the virulence of S. Enteritidis and reveals its biological role in intestinal pathogenesis.https://www.tandfonline.com/doi/10.1080/19490976.2023.2211184Salmonella EnteritidissRNAvirulenceintestinal barriergut microbiotaMAPK pathway |
| spellingShingle | Linlin Cai Yunting Xie Liangting Shao Haijing Hu Xinglian Xu Huhu Wang Guanghong Zhou SaaS sRNA promotes Salmonella intestinal invasion via modulating MAPK inflammatory pathway Gut Microbes Salmonella Enteritidis sRNA virulence intestinal barrier gut microbiota MAPK pathway |
| title | SaaS sRNA promotes Salmonella intestinal invasion via modulating MAPK inflammatory pathway |
| title_full | SaaS sRNA promotes Salmonella intestinal invasion via modulating MAPK inflammatory pathway |
| title_fullStr | SaaS sRNA promotes Salmonella intestinal invasion via modulating MAPK inflammatory pathway |
| title_full_unstemmed | SaaS sRNA promotes Salmonella intestinal invasion via modulating MAPK inflammatory pathway |
| title_short | SaaS sRNA promotes Salmonella intestinal invasion via modulating MAPK inflammatory pathway |
| title_sort | saas srna promotes salmonella intestinal invasion via modulating mapk inflammatory pathway |
| topic | Salmonella Enteritidis sRNA virulence intestinal barrier gut microbiota MAPK pathway |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2023.2211184 |
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