Succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota: a potential new mechanism for mastitis
Abstract Background A high grain diet causes an ecological imbalance in the gut microbiota and serves as an important endogenous trigger of mastitis in dairy cows, but the underlying mechanisms are unclear. Our previous study revealed that subacute rumen acidosis (SARA)-associated mastitis has disti...
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BMC
2024-11-01
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| Series: | Journal of Nanobiotechnology |
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| Online Access: | https://doi.org/10.1186/s12951-024-02997-1 |
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| author | Min Qiu Cong Ye Xiaotong Zhao Chenyu Zou Ruibo Tang Jiaxin Xie Yiheng Liu Yubo Hu Xiaoyu Hu Naisheng Zhang Yunhe Fu Jun Wang Caijun Zhao |
| author_facet | Min Qiu Cong Ye Xiaotong Zhao Chenyu Zou Ruibo Tang Jiaxin Xie Yiheng Liu Yubo Hu Xiaoyu Hu Naisheng Zhang Yunhe Fu Jun Wang Caijun Zhao |
| author_sort | Min Qiu |
| collection | DOAJ |
| description | Abstract Background A high grain diet causes an ecological imbalance in the gut microbiota and serves as an important endogenous trigger of mastitis in dairy cows, but the underlying mechanisms are unclear. Our previous study revealed that subacute rumen acidosis (SARA)-associated mastitis has distinct metabolic profiles in the rumen, especially a significant increase in succinate, but the role of succinate in the pathogenesis of mastitis remains unclear. Results Succinate treatment exacerbates low-grade endotoxemia-induced mastitis in mice. Specifically, succinate increased the production of gut microbiota-extracellular vehicles (mEVs) containing lipopolysaccharides, which can diffuse across the damaged intestinal barrier into the mammary glands. Administration of mEVs promotes mammary inflammation via activation of the TLR4/NF-κB pathway. Conclusions Our findings suggest that succinate promotes mastitis through the proliferation of enteric pathogens and mEVs production, suggesting a potential strategy for mastitis intervention on the basis of intestinal metabolic regulation and pathogen inhibition. The role of mEVs in interspecific communication has also been elucidated. Graphical Abstract |
| format | Article |
| id | doaj-art-7272af7f2e6349b7a92c70528980960f |
| institution | Kabale University |
| issn | 1477-3155 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Nanobiotechnology |
| spelling | doaj-art-7272af7f2e6349b7a92c70528980960f2024-11-17T12:47:00ZengBMCJournal of Nanobiotechnology1477-31552024-11-0122111810.1186/s12951-024-02997-1Succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota: a potential new mechanism for mastitisMin Qiu0Cong Ye1Xiaotong Zhao2Chenyu Zou3Ruibo Tang4Jiaxin Xie5Yiheng Liu6Yubo Hu7Xiaoyu Hu8Naisheng Zhang9Yunhe Fu10Jun Wang11Caijun Zhao12Department of Gynecology, China-Japan Union Hospital of Jilin UniversityDepartment of Gynecology, China-Japan Union Hospital of Jilin UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityDepartment of Anesthesiology, China-Japan Union Hospital of Jilin UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityCollege of Animal Science and Technology, Jilin Agricultural UniversityDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin UniversityAbstract Background A high grain diet causes an ecological imbalance in the gut microbiota and serves as an important endogenous trigger of mastitis in dairy cows, but the underlying mechanisms are unclear. Our previous study revealed that subacute rumen acidosis (SARA)-associated mastitis has distinct metabolic profiles in the rumen, especially a significant increase in succinate, but the role of succinate in the pathogenesis of mastitis remains unclear. Results Succinate treatment exacerbates low-grade endotoxemia-induced mastitis in mice. Specifically, succinate increased the production of gut microbiota-extracellular vehicles (mEVs) containing lipopolysaccharides, which can diffuse across the damaged intestinal barrier into the mammary glands. Administration of mEVs promotes mammary inflammation via activation of the TLR4/NF-κB pathway. Conclusions Our findings suggest that succinate promotes mastitis through the proliferation of enteric pathogens and mEVs production, suggesting a potential strategy for mastitis intervention on the basis of intestinal metabolic regulation and pathogen inhibition. The role of mEVs in interspecific communication has also been elucidated. Graphical Abstracthttps://doi.org/10.1186/s12951-024-02997-1SuccinateMastitisExtracellular vesiclesTLR4/NF-κB |
| spellingShingle | Min Qiu Cong Ye Xiaotong Zhao Chenyu Zou Ruibo Tang Jiaxin Xie Yiheng Liu Yubo Hu Xiaoyu Hu Naisheng Zhang Yunhe Fu Jun Wang Caijun Zhao Succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota: a potential new mechanism for mastitis Journal of Nanobiotechnology Succinate Mastitis Extracellular vesicles TLR4/NF-κB |
| title | Succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota: a potential new mechanism for mastitis |
| title_full | Succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota: a potential new mechanism for mastitis |
| title_fullStr | Succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota: a potential new mechanism for mastitis |
| title_full_unstemmed | Succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota: a potential new mechanism for mastitis |
| title_short | Succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota: a potential new mechanism for mastitis |
| title_sort | succinate exacerbates mastitis in mice via extracellular vesicles derived from the gut microbiota a potential new mechanism for mastitis |
| topic | Succinate Mastitis Extracellular vesicles TLR4/NF-κB |
| url | https://doi.org/10.1186/s12951-024-02997-1 |
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