Enhancement of liver mitochondrial complex I and energy metabolism induced by enteritis: The key role of gut microbiota derived endotoxins
Inflammation is an energy-intensive process and the liver is a key organ in energy regulation. Since the intestine and liver exchange nutrients and metabolites, enteritis can affect the liver. To investigate the correlation between enteritis and liver metabolism, we developed an intestinal inflammat...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.981917/full |
| _version_ | 1798006289692884992 |
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| author | Lele Fu Lele Fu Haokun Liu Wen Chen Wen Chen Jamie Marie Hooft Margareth Øverland Wanjie Cai Wanjie Cai Dong Han Dong Han Dong Han Xiaoming Zhu Xiaoming Zhu Yunxia Yang Junyan Jin Shouqi Xie Shouqi Xie Shouqi Xie Shouqi Xie |
| author_facet | Lele Fu Lele Fu Haokun Liu Wen Chen Wen Chen Jamie Marie Hooft Margareth Øverland Wanjie Cai Wanjie Cai Dong Han Dong Han Dong Han Xiaoming Zhu Xiaoming Zhu Yunxia Yang Junyan Jin Shouqi Xie Shouqi Xie Shouqi Xie Shouqi Xie |
| author_sort | Lele Fu |
| collection | DOAJ |
| description | Inflammation is an energy-intensive process and the liver is a key organ in energy regulation. Since the intestine and liver exchange nutrients and metabolites, enteritis can affect the liver. To investigate the correlation between enteritis and liver metabolism, we developed an intestinal inflammation model with concentration-dependent 2,4,6-trinitrobenzene sulfonic acid (TNBS) in gibel carp (Carassius gibelio). The results showed the dysregulation of intestinal tight junction, increased permeability of the gut barrier, and apoptosis of epithelial cells during the development of enteritis. The liver metabolome was analyzed by LC-MS and the live respiration was determined using Oxygraph-2k. The results showed that glycolysis, the TCA cycle and pyrimidine metabolism were affected by intestinal inflammation. In particular, the activity of hepatic mitochondrial respiratory chain complex I was significantly increased. Structure and abundance changes of gut microbiota were analyzed by 16S rRNA sequencing analysis. Pathogenic bacteria in the intestine, as well as plasma LPS, increased significantly. Using a liver cell line, we verified that the dysfunctional metabolism of the liver is related to the dislocation of LPS. All results imply the existence of a connection between enteritis and liver metabolism in gibel carp, and the gut microbiome plays a critical role in this process. |
| first_indexed | 2024-04-11T12:52:23Z |
| format | Article |
| id | doaj.art-f58ce6b9d4ad4bfebeb2e6fa50d1eb9c |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-11T12:52:23Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-f58ce6b9d4ad4bfebeb2e6fa50d1eb9c2022-12-22T04:23:10ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-08-011310.3389/fimmu.2022.981917981917Enhancement of liver mitochondrial complex I and energy metabolism induced by enteritis: The key role of gut microbiota derived endotoxinsLele Fu0Lele Fu1Haokun Liu2Wen Chen3Wen Chen4Jamie Marie Hooft5Margareth Øverland6Wanjie Cai7Wanjie Cai8Dong Han9Dong Han10Dong Han11Xiaoming Zhu12Xiaoming Zhu13Yunxia Yang14Junyan Jin15Shouqi Xie16Shouqi Xie17Shouqi Xie18Shouqi Xie19State Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaState Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaDepartment of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Ås, NorwayDepartment of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Ås, NorwayState Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaHubei Engineering Research Center for Aquatic Animal Nutrition and Feed, Wuhan, ChinaState Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaHubei Engineering Research Center for Aquatic Animal Nutrition and Feed, Wuhan, ChinaState Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaState Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaState Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaHubei Engineering Research Center for Aquatic Animal Nutrition and Feed, Wuhan, ChinaThe Innovative Academy of Seed Design, Chinese Academy of Sciences, Wuhan, ChinaInflammation is an energy-intensive process and the liver is a key organ in energy regulation. Since the intestine and liver exchange nutrients and metabolites, enteritis can affect the liver. To investigate the correlation between enteritis and liver metabolism, we developed an intestinal inflammation model with concentration-dependent 2,4,6-trinitrobenzene sulfonic acid (TNBS) in gibel carp (Carassius gibelio). The results showed the dysregulation of intestinal tight junction, increased permeability of the gut barrier, and apoptosis of epithelial cells during the development of enteritis. The liver metabolome was analyzed by LC-MS and the live respiration was determined using Oxygraph-2k. The results showed that glycolysis, the TCA cycle and pyrimidine metabolism were affected by intestinal inflammation. In particular, the activity of hepatic mitochondrial respiratory chain complex I was significantly increased. Structure and abundance changes of gut microbiota were analyzed by 16S rRNA sequencing analysis. Pathogenic bacteria in the intestine, as well as plasma LPS, increased significantly. Using a liver cell line, we verified that the dysfunctional metabolism of the liver is related to the dislocation of LPS. All results imply the existence of a connection between enteritis and liver metabolism in gibel carp, and the gut microbiome plays a critical role in this process.https://www.frontiersin.org/articles/10.3389/fimmu.2022.981917/fullintestinal inflammationintestinal permeabilityendotoxinmetabolismmitochondrial complex I |
| spellingShingle | Lele Fu Lele Fu Haokun Liu Wen Chen Wen Chen Jamie Marie Hooft Margareth Øverland Wanjie Cai Wanjie Cai Dong Han Dong Han Dong Han Xiaoming Zhu Xiaoming Zhu Yunxia Yang Junyan Jin Shouqi Xie Shouqi Xie Shouqi Xie Shouqi Xie Enhancement of liver mitochondrial complex I and energy metabolism induced by enteritis: The key role of gut microbiota derived endotoxins Frontiers in Immunology intestinal inflammation intestinal permeability endotoxin metabolism mitochondrial complex I |
| title | Enhancement of liver mitochondrial complex I and energy metabolism induced by enteritis: The key role of gut microbiota derived endotoxins |
| title_full | Enhancement of liver mitochondrial complex I and energy metabolism induced by enteritis: The key role of gut microbiota derived endotoxins |
| title_fullStr | Enhancement of liver mitochondrial complex I and energy metabolism induced by enteritis: The key role of gut microbiota derived endotoxins |
| title_full_unstemmed | Enhancement of liver mitochondrial complex I and energy metabolism induced by enteritis: The key role of gut microbiota derived endotoxins |
| title_short | Enhancement of liver mitochondrial complex I and energy metabolism induced by enteritis: The key role of gut microbiota derived endotoxins |
| title_sort | enhancement of liver mitochondrial complex i and energy metabolism induced by enteritis the key role of gut microbiota derived endotoxins |
| topic | intestinal inflammation intestinal permeability endotoxin metabolism mitochondrial complex I |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.981917/full |
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