Environmental noise stress disturbs commensal microbiota homeostasis and induces oxi-inflammmation and AD-like neuropathology through epithelial barrier disruption in the EOAD mouse model

Abstract Background Both genetic factors and environmental hazards, including environmental noise stress, have been associated with gut microbiome that exacerbates Alzheimer’s disease (AD) pathology. However, the role and mechanism of environmental risk factors in early-onset AD (EOAD) pathogenesis...

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Main Authors: Huimin Chi, Wa Cao, Ming Zhang, Donghong Su, Honglian Yang, Zhe Li, Chao Li, Xiaojun She, Kun Wang, Xiujie Gao, Kefeng Ma, Pengfang Zheng, Xiaofang Li, Bo Cui
Format: Article
Language:English
Published: BMC 2021-01-01
Series:Journal of Neuroinflammation
Subjects:
Online Access:https://doi.org/10.1186/s12974-020-02053-3
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author Huimin Chi
Wa Cao
Ming Zhang
Donghong Su
Honglian Yang
Zhe Li
Chao Li
Xiaojun She
Kun Wang
Xiujie Gao
Kefeng Ma
Pengfang Zheng
Xiaofang Li
Bo Cui
author_facet Huimin Chi
Wa Cao
Ming Zhang
Donghong Su
Honglian Yang
Zhe Li
Chao Li
Xiaojun She
Kun Wang
Xiujie Gao
Kefeng Ma
Pengfang Zheng
Xiaofang Li
Bo Cui
author_sort Huimin Chi
collection DOAJ
description Abstract Background Both genetic factors and environmental hazards, including environmental noise stress, have been associated with gut microbiome that exacerbates Alzheimer’s disease (AD) pathology. However, the role and mechanism of environmental risk factors in early-onset AD (EOAD) pathogenesis remain unclear. Methods The molecular pathways underlying EOAD pathophysiology following environmental noise exposure were evaluated using C57BL/6 wild-type (WT) and APP/PS1 Tg mouse models. The composition differences in intestinal microbiota were analyzed by 16S rRNA sequencing and Tax4Fun to predict the metagenome content from sequencing results. An assessment of the flora dysbiosis-triggered dyshomeostasis of oxi-inflamm-barrier and the effects of the CNS end of the gut–brain axis was conducted to explore the underlying pathological mechanisms. Results Both WT and APP/PS1 mice showed a statistically significant relationship between environmental noise and the taxonomic composition of the corresponding gut microbiome. Bacterial-encoded functional categories in noise-exposed WT and APP/PS1 mice included phospholipid and galactose metabolism, oxidative stress, and cell senescence. These alterations corresponded with imbalanced intestinal oxidation and anti-oxidation systems and low-grade systemic inflammation following noise exposure. Mechanistically, axis-series experiments demonstrated that following noise exposure, intestinal and hippocampal tight junction protein levels reduced, whereas serum levels of inflammatory mediator were elevated. Regarding APP/PS1 overexpression, noise-induced abnormalities in the gut–brain axis may contribute to aggravation of neuropathology in the presymptomatic stage of EOAD mice model. Conclusion Our results demonstrate that noise exposure has deleterious effects on the homeostasis of oxi-inflamm-barrier in the microbiome–gut–brain axis. Therefore, at least in a genetic context, chronic noise may aggravate the progression of EOAD.
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spelling doaj.art-13fdc8c70c7f45b384e2d8a94979aeb32022-12-21T19:51:19ZengBMCJournal of Neuroinflammation1742-20942021-01-0118111610.1186/s12974-020-02053-3Environmental noise stress disturbs commensal microbiota homeostasis and induces oxi-inflammmation and AD-like neuropathology through epithelial barrier disruption in the EOAD mouse modelHuimin Chi0Wa Cao1Ming Zhang2Donghong Su3Honglian Yang4Zhe Li5Chao Li6Xiaojun She7Kun Wang8Xiujie Gao9Kefeng Ma10Pengfang Zheng11Xiaofang Li12Bo Cui13Institute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesShenzhen Prevention and Treatment Center for Occupational DiseasesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesInstitute of Environmental and Operational Medicine, Chinese Academy of Military Medical sciencesAbstract Background Both genetic factors and environmental hazards, including environmental noise stress, have been associated with gut microbiome that exacerbates Alzheimer’s disease (AD) pathology. However, the role and mechanism of environmental risk factors in early-onset AD (EOAD) pathogenesis remain unclear. Methods The molecular pathways underlying EOAD pathophysiology following environmental noise exposure were evaluated using C57BL/6 wild-type (WT) and APP/PS1 Tg mouse models. The composition differences in intestinal microbiota were analyzed by 16S rRNA sequencing and Tax4Fun to predict the metagenome content from sequencing results. An assessment of the flora dysbiosis-triggered dyshomeostasis of oxi-inflamm-barrier and the effects of the CNS end of the gut–brain axis was conducted to explore the underlying pathological mechanisms. Results Both WT and APP/PS1 mice showed a statistically significant relationship between environmental noise and the taxonomic composition of the corresponding gut microbiome. Bacterial-encoded functional categories in noise-exposed WT and APP/PS1 mice included phospholipid and galactose metabolism, oxidative stress, and cell senescence. These alterations corresponded with imbalanced intestinal oxidation and anti-oxidation systems and low-grade systemic inflammation following noise exposure. Mechanistically, axis-series experiments demonstrated that following noise exposure, intestinal and hippocampal tight junction protein levels reduced, whereas serum levels of inflammatory mediator were elevated. Regarding APP/PS1 overexpression, noise-induced abnormalities in the gut–brain axis may contribute to aggravation of neuropathology in the presymptomatic stage of EOAD mice model. Conclusion Our results demonstrate that noise exposure has deleterious effects on the homeostasis of oxi-inflamm-barrier in the microbiome–gut–brain axis. Therefore, at least in a genetic context, chronic noise may aggravate the progression of EOAD.https://doi.org/10.1186/s12974-020-02053-3Environmental noiseMicrobiome–gut–brain axisOxidative stressInflammationEarly-onset Alzheimer’s disease (EOAD)APP/PS1 mouse
spellingShingle Huimin Chi
Wa Cao
Ming Zhang
Donghong Su
Honglian Yang
Zhe Li
Chao Li
Xiaojun She
Kun Wang
Xiujie Gao
Kefeng Ma
Pengfang Zheng
Xiaofang Li
Bo Cui
Environmental noise stress disturbs commensal microbiota homeostasis and induces oxi-inflammmation and AD-like neuropathology through epithelial barrier disruption in the EOAD mouse model
Journal of Neuroinflammation
Environmental noise
Microbiome–gut–brain axis
Oxidative stress
Inflammation
Early-onset Alzheimer’s disease (EOAD)
APP/PS1 mouse
title Environmental noise stress disturbs commensal microbiota homeostasis and induces oxi-inflammmation and AD-like neuropathology through epithelial barrier disruption in the EOAD mouse model
title_full Environmental noise stress disturbs commensal microbiota homeostasis and induces oxi-inflammmation and AD-like neuropathology through epithelial barrier disruption in the EOAD mouse model
title_fullStr Environmental noise stress disturbs commensal microbiota homeostasis and induces oxi-inflammmation and AD-like neuropathology through epithelial barrier disruption in the EOAD mouse model
title_full_unstemmed Environmental noise stress disturbs commensal microbiota homeostasis and induces oxi-inflammmation and AD-like neuropathology through epithelial barrier disruption in the EOAD mouse model
title_short Environmental noise stress disturbs commensal microbiota homeostasis and induces oxi-inflammmation and AD-like neuropathology through epithelial barrier disruption in the EOAD mouse model
title_sort environmental noise stress disturbs commensal microbiota homeostasis and induces oxi inflammmation and ad like neuropathology through epithelial barrier disruption in the eoad mouse model
topic Environmental noise
Microbiome–gut–brain axis
Oxidative stress
Inflammation
Early-onset Alzheimer’s disease (EOAD)
APP/PS1 mouse
url https://doi.org/10.1186/s12974-020-02053-3
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