Membrane vesicles derived from Streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the NLRP3/Caspase-1/GSDMD pathway
Streptococcus suis serotype 2 (S. suis 2) is a zoonotic pathogen that clinically causes severe swine and human infections (such as meningitis, endocarditis, and septicemia). In order to cause widespread diseases in different organs, S. suis 2 must colonize the host, break the blood barrier, and caus...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-04-01
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| Series: | Journal of Integrative Agriculture |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2095311923003222 |
| _version_ | 1797220552441593856 |
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| author | Keda Shi Yan Li Minsheng Xu Kunli Zhang Hongchao Gou Chunling Li Shaolun Zhai |
| author_facet | Keda Shi Yan Li Minsheng Xu Kunli Zhang Hongchao Gou Chunling Li Shaolun Zhai |
| author_sort | Keda Shi |
| collection | DOAJ |
| description | Streptococcus suis serotype 2 (S. suis 2) is a zoonotic pathogen that clinically causes severe swine and human infections (such as meningitis, endocarditis, and septicemia). In order to cause widespread diseases in different organs, S. suis 2 must colonize the host, break the blood barrier, and cause exaggerated inflammation. In the last few years, most studies have focused on a single virulence factor and its influences on the host. Membrane vesicles (MVs) can be actively secreted into the extracellular environment contributing to bacteria-host interactions. Gram-negative bacteria-derived outer membrane vesicles (OMVs) were recently shown to activate host Caspase-11-mediated non-canonical inflammasome pathway via deliverance of OMV-bound lipopolysaccharide (LPS), causing host cell pyroptosis. However, little is known about the effect of the MVs from S. suis 2 (Gram-positive bacteria without LPS) on cell pyroptosis. Thus, we investigated the molecular mechanism by which S. suis 2 MVs participate in endothelial cell pyroptosis. In this study, we used proteomics, electron scanning microscopy, fluorescence microscope, Western blotting, and bioassays, to investigate the MVs secreted by S. suis 2. First, we demonstrated that S. suis 2 secreted MVs with an average diameter of 72.04 nm, and 200 proteins in MVs were identified. Then, we showed that MVs were transported to cells via mainly dynamin-dependent endocytosis. The S. suis 2 MVs activated NLRP3/Caspase-1/GSDMD canonical inflammasome signaling pathway, resulting in cell pyroptosis, but it did not activate the Caspase-4/-5 pathway. More importantly, endothelial cells produce large amounts of reactive oxygen species (ROS) and lost their mitochondrial membrane potential under induction by S. suis 2 MVs. The results in this study suggest for the first time that MVs from S. suis 2 were internalized by endothelial cells via mainly dynamin-dependent endocytosis and might promote NLRP3/Caspase-1/GSDMD pathway by mitochondrial damage, which produced mtDNA and ROS under induction, leading to the pyroptosis of endothelial cells. |
| first_indexed | 2024-04-24T12:51:21Z |
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| id | doaj.art-a7dcec0aa66548ca9f29a8c2e4600902 |
| institution | Directory Open Access Journal |
| issn | 2095-3119 |
| language | English |
| last_indexed | 2024-04-24T12:51:21Z |
| publishDate | 2024-04-01 |
| publisher | Elsevier |
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| series | Journal of Integrative Agriculture |
| spelling | doaj.art-a7dcec0aa66548ca9f29a8c2e46009022024-04-06T04:39:49ZengElsevierJournal of Integrative Agriculture2095-31192024-04-0123413381353Membrane vesicles derived from Streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the NLRP3/Caspase-1/GSDMD pathwayKeda Shi0Yan Li1Minsheng Xu2Kunli Zhang3Hongchao Gou4Chunling Li5Shaolun Zhai6Institute of Animal Health, Guangdong Academy of Agricultural Sciences/Key Laboratory of Livestock Disease Prevention of Guangdong Province/Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China; Maoming Branch, Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, China; College of Animal Science & Technology, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, ChinaInstitute of Animal Health, Guangdong Academy of Agricultural Sciences/Key Laboratory of Livestock Disease Prevention of Guangdong Province/Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China; Maoming Branch, Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, ChinaInstitute of Animal Health, Guangdong Academy of Agricultural Sciences/Key Laboratory of Livestock Disease Prevention of Guangdong Province/Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China; Maoming Branch, Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, China; College of Animal Science & Technology, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, ChinaInstitute of Animal Health, Guangdong Academy of Agricultural Sciences/Key Laboratory of Livestock Disease Prevention of Guangdong Province/Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China; Maoming Branch, Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, ChinaInstitute of Animal Health, Guangdong Academy of Agricultural Sciences/Key Laboratory of Livestock Disease Prevention of Guangdong Province/Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China; Maoming Branch, Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, ChinaInstitute of Animal Health, Guangdong Academy of Agricultural Sciences/Key Laboratory of Livestock Disease Prevention of Guangdong Province/Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China; Maoming Branch, Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, China; Correspondence Chunling Li, Shaolun ZhaiInstitute of Animal Health, Guangdong Academy of Agricultural Sciences/Key Laboratory of Livestock Disease Prevention of Guangdong Province/Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, China; Maoming Branch, Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, China; Correspondence Chunling Li, Shaolun ZhaiStreptococcus suis serotype 2 (S. suis 2) is a zoonotic pathogen that clinically causes severe swine and human infections (such as meningitis, endocarditis, and septicemia). In order to cause widespread diseases in different organs, S. suis 2 must colonize the host, break the blood barrier, and cause exaggerated inflammation. In the last few years, most studies have focused on a single virulence factor and its influences on the host. Membrane vesicles (MVs) can be actively secreted into the extracellular environment contributing to bacteria-host interactions. Gram-negative bacteria-derived outer membrane vesicles (OMVs) were recently shown to activate host Caspase-11-mediated non-canonical inflammasome pathway via deliverance of OMV-bound lipopolysaccharide (LPS), causing host cell pyroptosis. However, little is known about the effect of the MVs from S. suis 2 (Gram-positive bacteria without LPS) on cell pyroptosis. Thus, we investigated the molecular mechanism by which S. suis 2 MVs participate in endothelial cell pyroptosis. In this study, we used proteomics, electron scanning microscopy, fluorescence microscope, Western blotting, and bioassays, to investigate the MVs secreted by S. suis 2. First, we demonstrated that S. suis 2 secreted MVs with an average diameter of 72.04 nm, and 200 proteins in MVs were identified. Then, we showed that MVs were transported to cells via mainly dynamin-dependent endocytosis. The S. suis 2 MVs activated NLRP3/Caspase-1/GSDMD canonical inflammasome signaling pathway, resulting in cell pyroptosis, but it did not activate the Caspase-4/-5 pathway. More importantly, endothelial cells produce large amounts of reactive oxygen species (ROS) and lost their mitochondrial membrane potential under induction by S. suis 2 MVs. The results in this study suggest for the first time that MVs from S. suis 2 were internalized by endothelial cells via mainly dynamin-dependent endocytosis and might promote NLRP3/Caspase-1/GSDMD pathway by mitochondrial damage, which produced mtDNA and ROS under induction, leading to the pyroptosis of endothelial cells.http://www.sciencedirect.com/science/article/pii/S2095311923003222Streptococcus suis serotype 2membrane vesiclesendocytosispyroptosisNLRP3 inflammasomesmitochondrial damage |
| spellingShingle | Keda Shi Yan Li Minsheng Xu Kunli Zhang Hongchao Gou Chunling Li Shaolun Zhai Membrane vesicles derived from Streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the NLRP3/Caspase-1/GSDMD pathway Journal of Integrative Agriculture Streptococcus suis serotype 2 membrane vesicles endocytosis pyroptosis NLRP3 inflammasomes mitochondrial damage |
| title | Membrane vesicles derived from Streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the NLRP3/Caspase-1/GSDMD pathway |
| title_full | Membrane vesicles derived from Streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the NLRP3/Caspase-1/GSDMD pathway |
| title_fullStr | Membrane vesicles derived from Streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the NLRP3/Caspase-1/GSDMD pathway |
| title_full_unstemmed | Membrane vesicles derived from Streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the NLRP3/Caspase-1/GSDMD pathway |
| title_short | Membrane vesicles derived from Streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the NLRP3/Caspase-1/GSDMD pathway |
| title_sort | membrane vesicles derived from streptococcus suis serotype 2 induce cell pyroptosis in endothelial cells via the nlrp3 caspase 1 gsdmd pathway |
| topic | Streptococcus suis serotype 2 membrane vesicles endocytosis pyroptosis NLRP3 inflammasomes mitochondrial damage |
| url | http://www.sciencedirect.com/science/article/pii/S2095311923003222 |
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