Fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut–brain axis

IntroductionRecent studies have highlighted the vital role of gut microbiota in traumatic brain injury (TBI). Fecal microbiota transplantation (FMT) is an effective means of regulating the microbiota–gut–brain axis, while the beneficial effect and potential mechanisms of FMT against TBI remain uncle...

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Main Authors: Xuezhen Hu, Hangqi Jin, Shushu Yuan, Tao Ye, Zhibo Chen, Yu Kong, Jiaming Liu, Kaihong Xu, Jing Sun
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1254610/full
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author Xuezhen Hu
Hangqi Jin
Shushu Yuan
Tao Ye
Zhibo Chen
Yu Kong
Jiaming Liu
Kaihong Xu
Jing Sun
author_facet Xuezhen Hu
Hangqi Jin
Shushu Yuan
Tao Ye
Zhibo Chen
Yu Kong
Jiaming Liu
Kaihong Xu
Jing Sun
author_sort Xuezhen Hu
collection DOAJ
description IntroductionRecent studies have highlighted the vital role of gut microbiota in traumatic brain injury (TBI). Fecal microbiota transplantation (FMT) is an effective means of regulating the microbiota–gut–brain axis, while the beneficial effect and potential mechanisms of FMT against TBI remain unclear. Here, we elucidated the anti-neuroinflammatory effect and possible mechanism of FMT against TBI in mice via regulating the microbiota–gut–brain axis.MethodsThe TBI mouse model was established by heavy object falling impact and then treated with FMT. The neurological deficits, neuropathological change, synaptic damage, microglia activation, and neuroinflammatory cytokine production were assessed, and the intestinal pathological change and gut microbiota composition were also evaluated. Moreover, the population of Treg cells in the spleen was measured.ResultsOur results showed that FMT treatment significantly alleviated neurological deficits and neuropathological changes and improved synaptic damage by increasing the levels of the synaptic plasticity-related protein such as postsynaptic density protein 95 (PSD-95) and synapsin I in the TBI mice model. Moreover, FMT could inhibit the activation of microglia and reduce the production of the inflammatory cytokine TNF-α, alleviating the inflammatory response of TBI mice. Meanwhile, FMT treatment could attenuate intestinal histopathologic changes and gut microbiota dysbiosis and increase the Treg cell population in TBI mice.ConclusionThese findings elucidated that FMT treatment effectively suppressed the TBI-induced neuroinflammation via regulating the gut microbiota–gut–brain axis, and its mechanism was involved in the regulation of peripheral immune cells, which implied a novel strategy against TBI.
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spelling doaj.art-8514d4aafe1b4dc7b2a1bc2aa126a0f82023-09-07T21:15:50ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-09-011310.3389/fcimb.2023.12546101254610Fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut–brain axisXuezhen Hu0Hangqi Jin1Shushu Yuan2Tao Ye3Zhibo Chen4Yu Kong5Jiaming Liu6Kaihong Xu7Jing Sun8Department of Emergency Medicine, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, ChinaDepartment of Preventive Medicine, School of Public Health and Management, Wenzhou Medical University, Wenzhou, ChinaDepartment of Preventive Medicine, School of Public Health and Management, Wenzhou Medical University, Wenzhou, ChinaDepartment of Geriatrics, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, ChinaDepartment of Geriatrics, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, ChinaDepartment of Preventive Medicine, School of Public Health and Management, Wenzhou Medical University, Wenzhou, ChinaDepartment of Preventive Medicine, School of Public Health and Management, Wenzhou Medical University, Wenzhou, ChinaDepartment of Hematology, Ningbo First Hospital, Ningbo, ChinaDepartment of Geriatrics, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, ChinaIntroductionRecent studies have highlighted the vital role of gut microbiota in traumatic brain injury (TBI). Fecal microbiota transplantation (FMT) is an effective means of regulating the microbiota–gut–brain axis, while the beneficial effect and potential mechanisms of FMT against TBI remain unclear. Here, we elucidated the anti-neuroinflammatory effect and possible mechanism of FMT against TBI in mice via regulating the microbiota–gut–brain axis.MethodsThe TBI mouse model was established by heavy object falling impact and then treated with FMT. The neurological deficits, neuropathological change, synaptic damage, microglia activation, and neuroinflammatory cytokine production were assessed, and the intestinal pathological change and gut microbiota composition were also evaluated. Moreover, the population of Treg cells in the spleen was measured.ResultsOur results showed that FMT treatment significantly alleviated neurological deficits and neuropathological changes and improved synaptic damage by increasing the levels of the synaptic plasticity-related protein such as postsynaptic density protein 95 (PSD-95) and synapsin I in the TBI mice model. Moreover, FMT could inhibit the activation of microglia and reduce the production of the inflammatory cytokine TNF-α, alleviating the inflammatory response of TBI mice. Meanwhile, FMT treatment could attenuate intestinal histopathologic changes and gut microbiota dysbiosis and increase the Treg cell population in TBI mice.ConclusionThese findings elucidated that FMT treatment effectively suppressed the TBI-induced neuroinflammation via regulating the gut microbiota–gut–brain axis, and its mechanism was involved in the regulation of peripheral immune cells, which implied a novel strategy against TBI.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1254610/fulltraumatic brain injuryfecal microbiota transplantneuroinflammationgut microbiotagut–brain axisTreg cell
spellingShingle Xuezhen Hu
Hangqi Jin
Shushu Yuan
Tao Ye
Zhibo Chen
Yu Kong
Jiaming Liu
Kaihong Xu
Jing Sun
Fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut–brain axis
Frontiers in Cellular and Infection Microbiology
traumatic brain injury
fecal microbiota transplant
neuroinflammation
gut microbiota
gut–brain axis
Treg cell
title Fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut–brain axis
title_full Fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut–brain axis
title_fullStr Fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut–brain axis
title_full_unstemmed Fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut–brain axis
title_short Fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut–brain axis
title_sort fecal microbiota transplantation inhibited neuroinflammation of traumatic brain injury in mice via regulating the gut brain axis
topic traumatic brain injury
fecal microbiota transplant
neuroinflammation
gut microbiota
gut–brain axis
Treg cell
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1254610/full
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