Cargando…

Desulfovibrio fairfieldensis-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages

Sulfate-reducing bacteria Desulfovibrio fairfieldensis 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 me...

Descripción completa

Detalles Bibliográficos
Autores principales: Nie, Yawen, Xie, Xiao-Qian, Zhou, Lingxi, Guan, Qijie, Ren, Yilin, Mao, Yong, Shi, Jin-Song, Xu, Zheng-Hong, Geng, Yan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9818291/
https://www.ncbi.nlm.nih.gov/pubmed/36611884
http://dx.doi.org/10.3390/cells12010089
_version_ 1784864948991557632
author Nie, Yawen
Xie, Xiao-Qian
Zhou, Lingxi
Guan, Qijie
Ren, Yilin
Mao, Yong
Shi, Jin-Song
Xu, Zheng-Hong
Geng, Yan
author_facet Nie, Yawen
Xie, Xiao-Qian
Zhou, Lingxi
Guan, Qijie
Ren, Yilin
Mao, Yong
Shi, Jin-Song
Xu, Zheng-Hong
Geng, Yan
author_sort Nie, Yawen
collection PubMed
description Sulfate-reducing bacteria Desulfovibrio fairfieldensis 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 D. fairfieldensis 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 D. fairfieldensis 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 D. fairfieldensis OMVs can damage the intestinal epithelial barrier and activate intrinsic inflammation.
format Online
Article
Text
id pubmed-9818291
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-98182912023-01-07 Desulfovibrio fairfieldensis-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages Nie, Yawen Xie, Xiao-Qian Zhou, Lingxi Guan, Qijie Ren, Yilin Mao, Yong Shi, Jin-Song Xu, Zheng-Hong Geng, Yan Cells Article Sulfate-reducing bacteria Desulfovibrio fairfieldensis 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 D. fairfieldensis 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 D. fairfieldensis 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 D. fairfieldensis OMVs can damage the intestinal epithelial barrier and activate intrinsic inflammation. MDPI 2022-12-25 /pmc/articles/PMC9818291/ /pubmed/36611884 http://dx.doi.org/10.3390/cells12010089 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Nie, Yawen
Xie, Xiao-Qian
Zhou, Lingxi
Guan, Qijie
Ren, Yilin
Mao, Yong
Shi, Jin-Song
Xu, Zheng-Hong
Geng, Yan
Desulfovibrio fairfieldensis-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages
title Desulfovibrio fairfieldensis-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages
title_full Desulfovibrio fairfieldensis-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages
title_fullStr Desulfovibrio fairfieldensis-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages
title_full_unstemmed Desulfovibrio fairfieldensis-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages
title_short Desulfovibrio fairfieldensis-Derived Outer Membrane Vesicles Damage Epithelial Barrier and Induce Inflammation and Pyroptosis in Macrophages
title_sort desulfovibrio fairfieldensis-derived outer membrane vesicles damage epithelial barrier and induce inflammation and pyroptosis in macrophages
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9818291/
https://www.ncbi.nlm.nih.gov/pubmed/36611884
http://dx.doi.org/10.3390/cells12010089
work_keys_str_mv AT nieyawen desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages
AT xiexiaoqian desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages
AT zhoulingxi desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages
AT guanqijie desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages
AT renyilin desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages
AT maoyong desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages
AT shijinsong desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages
AT xuzhenghong desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages
AT gengyan desulfovibriofairfieldensisderivedoutermembranevesiclesdamageepithelialbarrierandinduceinflammationandpyroptosisinmacrophages