<i>Desulfovibrio fairfieldensis</i>-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages
Sulfate-reducing bacteria <i>Desulfovibrio fairfieldensis</i> is an opportunistic pathogen that widely exists in the human intestine and can cause severe infectious diseases. However, the mechanisms contributing to its pathogenesis remain of great interest. In this study, we aim to inves...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-12-01
|
| Series: | Cells |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2073-4409/12/1/89 |
| _version_ | 1797626110727421952 |
|---|---|
| author | Yawen Nie Xiao-Qian Xie Lingxi Zhou Qijie Guan Yilin Ren Yong Mao Jin-Song Shi Zheng-Hong Xu Yan Geng |
| author_facet | Yawen Nie Xiao-Qian Xie Lingxi Zhou Qijie Guan Yilin Ren Yong Mao Jin-Song Shi Zheng-Hong Xu Yan Geng |
| author_sort | Yawen Nie |
| collection | DOAJ |
| description | Sulfate-reducing bacteria <i>Desulfovibrio fairfieldensis</i> is an opportunistic pathogen that widely exists in the human intestine and can cause severe infectious diseases. However, the mechanisms contributing to its pathogenesis remain of great interest. In this study, we aim to investigate the outer membrane vesicles (OMVs) secreted by <i>D. fairfieldensis</i> and their pathogenic effect. The OMVs separated by ultracentrifugation were spherical and displayed a characteristic bilayer lipid structure observed by transmission electron microscopy, with an average hydrodynamic diameter of 75 nm measurement using the particle size analyzer. We identified 1496 and 916 proteins from <i>D. fairfieldensis</i> and its OMVs using label-free non-target quantitative proteomics, respectively. The 560 co-expressed proteins could participate in bacterial life activities by function prediction. The translocation protein TolB, which participates in OMVs biogenesis and transporting toxins was highly expressed in OMVs. The OMVs inhibited the expression of tight junction proteins OCCLUDIN and ZO-1 in human colonic epithelial cells (Caco-2). The OMVs decreased the cell viability of monocyte macrophages (THP-1-Mφ) and activated various inflammatory factors secretion, including interferon-γ (IFN-γ), tumor necrosis factor (TNF-α), and many interleukins. Further, we found the OMVs induced the expression of cleaved-gasdermin D, caspase-1, and c-IL-1β and caused pyroptosis in THP-1-Mφ cells. Taken together, these data reveal that the <i>D. fairfieldensis</i> OMVs can damage the intestinal epithelial barrier and activate intrinsic inflammation. |
| first_indexed | 2024-03-11T10:05:50Z |
| format | Article |
| id | doaj.art-5da19e84a2324415a188e1cc17d1141a |
| institution | Directory Open Access Journal |
| issn | 2073-4409 |
| language | English |
| last_indexed | 2024-03-11T10:05:50Z |
| publishDate | 2022-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Cells |
| spelling | doaj.art-5da19e84a2324415a188e1cc17d1141a2023-11-16T15:05:57ZengMDPI AGCells2073-44092022-12-011218910.3390/cells12010089<i>Desulfovibrio fairfieldensis</i>-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in MacrophagesYawen Nie0Xiao-Qian Xie1Lingxi Zhou2Qijie Guan3Yilin Ren4Yong Mao5Jin-Song Shi6Zheng-Hong Xu7Yan Geng8School of Life Sciences and Health Engineering, Jiangnan University, Wuxi 214122, ChinaSchool of Life Sciences and Health Engineering, Jiangnan University, Wuxi 214122, ChinaThe Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi 214122, ChinaNational Engineering Laboratory for Cereal Fermentation Technology, Jiangnan University, Wuxi 214122, ChinaDepartment of Gastroenterology, Affiliated Hospital of Jiangnan University, Wuxi 214122, ChinaDepartment of Oncology, Affiliated Hospital of Jiangnan University, Wuxi214122, ChinaSchool of Life Sciences and Health Engineering, Jiangnan University, Wuxi 214122, ChinaThe Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi 214122, ChinaSchool of Life Sciences and Health Engineering, Jiangnan University, Wuxi 214122, ChinaSulfate-reducing bacteria <i>Desulfovibrio fairfieldensis</i> is an opportunistic pathogen that widely exists in the human intestine and can cause severe infectious diseases. However, the mechanisms contributing to its pathogenesis remain of great interest. In this study, we aim to investigate the outer membrane vesicles (OMVs) secreted by <i>D. fairfieldensis</i> and their pathogenic effect. The OMVs separated by ultracentrifugation were spherical and displayed a characteristic bilayer lipid structure observed by transmission electron microscopy, with an average hydrodynamic diameter of 75 nm measurement using the particle size analyzer. We identified 1496 and 916 proteins from <i>D. fairfieldensis</i> and its OMVs using label-free non-target quantitative proteomics, respectively. The 560 co-expressed proteins could participate in bacterial life activities by function prediction. The translocation protein TolB, which participates in OMVs biogenesis and transporting toxins was highly expressed in OMVs. The OMVs inhibited the expression of tight junction proteins OCCLUDIN and ZO-1 in human colonic epithelial cells (Caco-2). The OMVs decreased the cell viability of monocyte macrophages (THP-1-Mφ) and activated various inflammatory factors secretion, including interferon-γ (IFN-γ), tumor necrosis factor (TNF-α), and many interleukins. Further, we found the OMVs induced the expression of cleaved-gasdermin D, caspase-1, and c-IL-1β and caused pyroptosis in THP-1-Mφ cells. Taken together, these data reveal that the <i>D. fairfieldensis</i> OMVs can damage the intestinal epithelial barrier and activate intrinsic inflammation.https://www.mdpi.com/2073-4409/12/1/89<i>Desulfovibrio fairfieldensis</i>outer membrane vesiclesintestinal inflammationpyroptosis |
| spellingShingle | Yawen Nie Xiao-Qian Xie Lingxi Zhou Qijie Guan Yilin Ren Yong Mao Jin-Song Shi Zheng-Hong Xu Yan Geng <i>Desulfovibrio fairfieldensis</i>-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages Cells <i>Desulfovibrio fairfieldensis</i> outer membrane vesicles intestinal inflammation pyroptosis |
| title | <i>Desulfovibrio fairfieldensis</i>-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages |
| title_full | <i>Desulfovibrio fairfieldensis</i>-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages |
| title_fullStr | <i>Desulfovibrio fairfieldensis</i>-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages |
| title_full_unstemmed | <i>Desulfovibrio fairfieldensis</i>-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages |
| title_short | <i>Desulfovibrio fairfieldensis</i>-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages |
| title_sort | i desulfovibrio fairfieldensis i derived outer membrane vesicles damage epithelial barrier and induce inflammation and pyroptosis in macrophages |
| topic | <i>Desulfovibrio fairfieldensis</i> outer membrane vesicles intestinal inflammation pyroptosis |
| url | https://www.mdpi.com/2073-4409/12/1/89 |
| work_keys_str_mv | AT yawennie idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages AT xiaoqianxie idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages AT lingxizhou idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages AT qijieguan idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages AT yilinren idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages AT yongmao idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages AT jinsongshi idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages AT zhenghongxu idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages AT yangeng idesulfovibriofairfieldensisiderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages |