Bifidobacterium spp. and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responses
Severe acute pancreatitis (SAP) is a critical illness characterized by a severe systemic inflammatory response resulting in persistent multiple organ failure and sepsis. The intestinal microbiome is increasingly appreciated to play a crucial role in modulation of AP disease outcome, but limited info...
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2022-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2022.2127456 |
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| author | Han Li Jinyan Xie Xiuliu Guo Guilian Yang Bin Cai Jingtianyi Liu Mengjia Yue Yixin Tang Gan Wang Shuxian Chen Jialin Guo Xuchen Qi Donghai Wang Huijun Zheng Wei Liu Hong Yu Chunfeng Wang Shu Jeffrey Zhu Feng Guo |
| author_facet | Han Li Jinyan Xie Xiuliu Guo Guilian Yang Bin Cai Jingtianyi Liu Mengjia Yue Yixin Tang Gan Wang Shuxian Chen Jialin Guo Xuchen Qi Donghai Wang Huijun Zheng Wei Liu Hong Yu Chunfeng Wang Shu Jeffrey Zhu Feng Guo |
| author_sort | Han Li |
| collection | DOAJ |
| description | Severe acute pancreatitis (SAP) is a critical illness characterized by a severe systemic inflammatory response resulting in persistent multiple organ failure and sepsis. The intestinal microbiome is increasingly appreciated to play a crucial role in modulation of AP disease outcome, but limited information is available about the identity and mechanism of action for specific commensal bacteria involved in AP-associated inflammation. Here we show that Bifidobacteria, particularly B. animalis, can protect against AP by regulating pancreatic and systemic inflammation in germ-free (GF) and oral antibiotic-treated (Abx) mouse models. Colonization by B. animalis and administration of its metabolite lactate protected Abx and GF mice from AP by reducing serum amylase concentration, ameliorating pancreatic lesions and improving survival rate after retrograde injection of sodium taurocholate. B. animalis relieved macrophage-associated local and systemic inflammation of AP in a TLR4/MyD88- and NLRP3/Caspase1-dependent manner through its metabolite lactate. Supporting our findings from the mouse study, clinical AP patients exhibited a decreased fecal abundance of Bifidobacteria that was inversely correlated with the severity of systemic inflammatory responses. These results may shed light on the heterogeneity of clinical outcomes and drive the development of more efficacious therapeutic interventions for AP, and potentially for other inflammatory disorders. |
| format | Article |
| id | doaj-art-bb45aceff66b4bfcb99b92d5f3859f77 |
| institution | DOAJ |
| issn | 1949-0976 1949-0984 |
| language | English |
| publishDate | 2022-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj-art-bb45aceff66b4bfcb99b92d5f3859f772025-08-20T03:12:50ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2022.2127456Bifidobacterium spp. and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responsesHan Li0Jinyan Xie1Xiuliu Guo2Guilian Yang3Bin Cai4Jingtianyi Liu5Mengjia Yue6Yixin Tang7Gan Wang8Shuxian Chen9Jialin Guo10Xuchen Qi11Donghai Wang12Huijun Zheng13Wei Liu14Hong Yu15Chunfeng Wang16Shu Jeffrey Zhu17Feng Guo18Key Laboratory of Animal Virology of Ministry of Agriculture, Center for Veterinary Sciences, Zhejiang University, Hangzhou, ChinaKey Laboratory of Animal Virology of Ministry of Agriculture, Center for Veterinary Sciences, Zhejiang University, Hangzhou, ChinaDepartment of Critical Care Medicine, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaCollege of Veterinary Medicine, Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaDepartment of Quality Management, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaKey Laboratory of Animal Virology of Ministry of Agriculture, Center for Veterinary Sciences, Zhejiang University, Hangzhou, ChinaKey Laboratory of Animal Virology of Ministry of Agriculture, Center for Veterinary Sciences, Zhejiang University, Hangzhou, ChinaKey Laboratory of Animal Virology of Ministry of Agriculture, Center for Veterinary Sciences, Zhejiang University, Hangzhou, ChinaKey Laboratory of Animal Virology of Ministry of Agriculture, Center for Veterinary Sciences, Zhejiang University, Hangzhou, ChinaKey Laboratory of Animal Virology of Ministry of Agriculture, Center for Veterinary Sciences, Zhejiang University, Hangzhou, ChinaInstitute of Land and Food Systems, University of British Columbia, Vancouver, BC, CanadaCentral Laboratory of Medicine, Shaoxing People’s Hospital, Shaoxing, ChinaDepartment of Critical Care Medicine, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Critical Care Medicine, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, ChinaDepartment of General Surgery, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaCollege of Veterinary Medicine, Jilin Provincial Engineering Research Center of Animal Probiotics, Jilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Virology of Ministry of Agriculture, Center for Veterinary Sciences, Zhejiang University, Hangzhou, ChinaDepartment of Critical Care Medicine, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaSevere acute pancreatitis (SAP) is a critical illness characterized by a severe systemic inflammatory response resulting in persistent multiple organ failure and sepsis. The intestinal microbiome is increasingly appreciated to play a crucial role in modulation of AP disease outcome, but limited information is available about the identity and mechanism of action for specific commensal bacteria involved in AP-associated inflammation. Here we show that Bifidobacteria, particularly B. animalis, can protect against AP by regulating pancreatic and systemic inflammation in germ-free (GF) and oral antibiotic-treated (Abx) mouse models. Colonization by B. animalis and administration of its metabolite lactate protected Abx and GF mice from AP by reducing serum amylase concentration, ameliorating pancreatic lesions and improving survival rate after retrograde injection of sodium taurocholate. B. animalis relieved macrophage-associated local and systemic inflammation of AP in a TLR4/MyD88- and NLRP3/Caspase1-dependent manner through its metabolite lactate. Supporting our findings from the mouse study, clinical AP patients exhibited a decreased fecal abundance of Bifidobacteria that was inversely correlated with the severity of systemic inflammatory responses. These results may shed light on the heterogeneity of clinical outcomes and drive the development of more efficacious therapeutic interventions for AP, and potentially for other inflammatory disorders.https://www.tandfonline.com/doi/10.1080/19490976.2022.2127456Bifidobacteriummicrobial metabolitelactatemacrophagespancreatic and systemic inflammationimmunomodulation |
| spellingShingle | Han Li Jinyan Xie Xiuliu Guo Guilian Yang Bin Cai Jingtianyi Liu Mengjia Yue Yixin Tang Gan Wang Shuxian Chen Jialin Guo Xuchen Qi Donghai Wang Huijun Zheng Wei Liu Hong Yu Chunfeng Wang Shu Jeffrey Zhu Feng Guo Bifidobacterium spp. and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responses Gut Microbes Bifidobacterium microbial metabolite lactate macrophages pancreatic and systemic inflammation immunomodulation |
| title | Bifidobacterium spp. and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responses |
| title_full | Bifidobacterium spp. and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responses |
| title_fullStr | Bifidobacterium spp. and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responses |
| title_full_unstemmed | Bifidobacterium spp. and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responses |
| title_short | Bifidobacterium spp. and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responses |
| title_sort | bifidobacterium spp and their metabolite lactate protect against acute pancreatitis via inhibition of pancreatic and systemic inflammatory responses |
| topic | Bifidobacterium microbial metabolite lactate macrophages pancreatic and systemic inflammation immunomodulation |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2022.2127456 |
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