Fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosion
BackgroundDysbiosis of gut microbiota (GM) is intricately linked with cognitive impairment and the incidence of traumatic brain injury (TBI) in both animal models and human subjects. However, there is limited understanding of the impact and mechanisms of fecal microbiota transplantation (FMT) on bra...
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Frontiers Media S.A.
2024-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1485936/full |
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| author | Xinwen Dong Yaguang Su Zheng Luo Cuiying Li Jie Gao Xiaofeng Han Sanqiao Yao Weidong Wu Linqiang Tian Yichun Bai Guizhi Wang Wenjie Ren |
| author_facet | Xinwen Dong Yaguang Su Zheng Luo Cuiying Li Jie Gao Xiaofeng Han Sanqiao Yao Weidong Wu Linqiang Tian Yichun Bai Guizhi Wang Wenjie Ren |
| author_sort | Xinwen Dong |
| collection | DOAJ |
| description | BackgroundDysbiosis of gut microbiota (GM) is intricately linked with cognitive impairment and the incidence of traumatic brain injury (TBI) in both animal models and human subjects. However, there is limited understanding of the impact and mechanisms of fecal microbiota transplantation (FMT) on brain and gut barrier function in the treatment of TBI induced by gas explosion (GE).MethodsWe have employed FMT technology to establish models of gut microbiota dysbiosis in male rats, and subsequently conducted non-targeted metabolomics and microbiota diversity analysis to explore the bacteria with potential functional roles.ResultsHematoxylin–eosin and transmission electron microscopy revealed that GE induced significant pathological damage and inflammation responses, as well as varying degrees of mitochondrial impairment in neuronal cells in the brains of rats, which was associated with cognitive decline. Furthermore, GE markedly elevated the levels of regulatory T cell (Tregs)-related factors interleukin-10, programmed death 1, and fork head box protein P3 in the brains of rats. Similar changes in these indicators were also observed in the colon; however, these alterations were reversed upon transfer of normal flora into the GE-exposed rats. Combined microbiome and metabolome analysis indicated up-regulation of Clostridium_T and Allobaculum, along with activation of fatty acid biosynthesis after FMT. Correlation network analysis indirectly suggested a causal relationship between FMT and alleviation of GE-induced TBI. FMT improved intestinal structure and up-regulated expression of tight junction proteins Claudin-1, Occludin, and ZO-1, potentially contributing to its protective effects on both brain and gut.ConclusionTransplantation of gut microbiota from healthy rats significantly enhanced cognitive function in male rats with traumatic brain injury caused by a gas explosion, through the modulation of gut microbiome composition and the improvement of both gut and brain barrier integrity via the gut-brain axis. These findings may offer a scientific foundation for potential clinical interventions targeting gas explosion-induced TBI using FMT. |
| format | Article |
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| institution | OA Journals |
| issn | 1664-302X |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-ced8ce1c2da3462481b5e9150a6f1e7e2025-08-20T01:47:25ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-11-011510.3389/fmicb.2024.14859361485936Fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosionXinwen Dong0Yaguang Su1Zheng Luo2Cuiying Li3Jie Gao4Xiaofeng Han5Sanqiao Yao6Weidong Wu7Linqiang Tian8Yichun Bai9Guizhi Wang10Wenjie Ren11Department of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaDepartment of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaDepartment of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaDepartment of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaDepartment of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaDepartment of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaDepartment of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaDepartment of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaInstitute of Trauma and Orthopedics, Xinxiang Medical University, Xinxiang, ChinaDepartment of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, ChinaDepartment of Pathology, The Fifth Affiliated Hospital of Zhengzhou University, Zhengzhou, ChinaInstitute of Health Central Plains, Xinxiang Medical University, Xinxiang, ChinaBackgroundDysbiosis of gut microbiota (GM) is intricately linked with cognitive impairment and the incidence of traumatic brain injury (TBI) in both animal models and human subjects. However, there is limited understanding of the impact and mechanisms of fecal microbiota transplantation (FMT) on brain and gut barrier function in the treatment of TBI induced by gas explosion (GE).MethodsWe have employed FMT technology to establish models of gut microbiota dysbiosis in male rats, and subsequently conducted non-targeted metabolomics and microbiota diversity analysis to explore the bacteria with potential functional roles.ResultsHematoxylin–eosin and transmission electron microscopy revealed that GE induced significant pathological damage and inflammation responses, as well as varying degrees of mitochondrial impairment in neuronal cells in the brains of rats, which was associated with cognitive decline. Furthermore, GE markedly elevated the levels of regulatory T cell (Tregs)-related factors interleukin-10, programmed death 1, and fork head box protein P3 in the brains of rats. Similar changes in these indicators were also observed in the colon; however, these alterations were reversed upon transfer of normal flora into the GE-exposed rats. Combined microbiome and metabolome analysis indicated up-regulation of Clostridium_T and Allobaculum, along with activation of fatty acid biosynthesis after FMT. Correlation network analysis indirectly suggested a causal relationship between FMT and alleviation of GE-induced TBI. FMT improved intestinal structure and up-regulated expression of tight junction proteins Claudin-1, Occludin, and ZO-1, potentially contributing to its protective effects on both brain and gut.ConclusionTransplantation of gut microbiota from healthy rats significantly enhanced cognitive function in male rats with traumatic brain injury caused by a gas explosion, through the modulation of gut microbiome composition and the improvement of both gut and brain barrier integrity via the gut-brain axis. These findings may offer a scientific foundation for potential clinical interventions targeting gas explosion-induced TBI using FMT.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1485936/fullgas explosioncognitive impairmentmicrobiota-gut-brain axisfecal microbiota transplantationgut barrier function16S rRNA gene sequencing |
| spellingShingle | Xinwen Dong Yaguang Su Zheng Luo Cuiying Li Jie Gao Xiaofeng Han Sanqiao Yao Weidong Wu Linqiang Tian Yichun Bai Guizhi Wang Wenjie Ren Fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosion Frontiers in Microbiology gas explosion cognitive impairment microbiota-gut-brain axis fecal microbiota transplantation gut barrier function 16S rRNA gene sequencing |
| title | Fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosion |
| title_full | Fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosion |
| title_fullStr | Fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosion |
| title_full_unstemmed | Fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosion |
| title_short | Fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosion |
| title_sort | fecal microbiota transplantation alleviates cognitive impairment by improving gut microbiome composition and barrier function in male rats of traumatic brain injury following gas explosion |
| topic | gas explosion cognitive impairment microbiota-gut-brain axis fecal microbiota transplantation gut barrier function 16S rRNA gene sequencing |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1485936/full |
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