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Multi-omics analysis reveals the effects of microbiota on oral homeostasis

The oral epithelium’s normal morphological structure and function play an important role in maintaining oral homeostasis, among which microbiota and chronic stress are key contributing factors. However, the effects of microbiota and chronic stress on the morphological structures and molecular functi...

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Autores principales: Long, Huiqing, Yan, Li, Pu, Juncai, Liu, Yiyun, Zhong, Xiaogang, Wang, Haiyang, Yang, Lu, Lou, Fangzhi, Luo, Shihong, Zhang, Yingying, Liu, Yang, Xie, Peng, Ji, Ping, Jin, Xin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9533175/
https://www.ncbi.nlm.nih.gov/pubmed/36211346
http://dx.doi.org/10.3389/fimmu.2022.1005992
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author Long, Huiqing
Yan, Li
Pu, Juncai
Liu, Yiyun
Zhong, Xiaogang
Wang, Haiyang
Yang, Lu
Lou, Fangzhi
Luo, Shihong
Zhang, Yingying
Liu, Yang
Xie, Peng
Ji, Ping
Jin, Xin
author_facet Long, Huiqing
Yan, Li
Pu, Juncai
Liu, Yiyun
Zhong, Xiaogang
Wang, Haiyang
Yang, Lu
Lou, Fangzhi
Luo, Shihong
Zhang, Yingying
Liu, Yang
Xie, Peng
Ji, Ping
Jin, Xin
author_sort Long, Huiqing
collection PubMed
description The oral epithelium’s normal morphological structure and function play an important role in maintaining oral homeostasis, among which microbiota and chronic stress are key contributing factors. However, the effects of microbiota and chronic stress on the morphological structures and molecular function of oral homeostasis remain unclear. In this study, morphological staining was used to compare the tongue structure of specific pathogen-free and germ-free mice, and an integrated multi-omics analysis based on transcriptomics, proteomics, and metabolomics was performed to investigate the regulatory mechanisms of microbiota and chronic stress on oral homeostasis. We found that the morphological structure of the tongue in germ-free mice was disordered compared with in specific pathogen-free mice, especially in the epithelium. Multi-omics analysis indicated that differentially expressed molecules of the tongue between germ-free and specific pathogen-free mice were significantly enriched in the mitochondrial metabolic process and immune response. Interestingly, microbiota also significantly influenced the permeability of the oral epithelial barrier, represented by the differential expression of keratinization, and cell adhesion molecules. It was worth noting that the above changes in the tongue between specific pathogen-free and germ-free mice were more significant after chronic stress. Collectively, this is the first study to reveal that the microbiota might maintain oral homeostasis by reshaping the structure of the oral epithelial barrier and changing the function of molecular biology, a process that may be driven by the immune response and mitochondrial metabolic process of oral tissue. Furthermore, chronic stress can enhance the regulatory effects of microbiota on oral homeostasis.
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spelling pubmed-95331752022-10-06 Multi-omics analysis reveals the effects of microbiota on oral homeostasis Long, Huiqing Yan, Li Pu, Juncai Liu, Yiyun Zhong, Xiaogang Wang, Haiyang Yang, Lu Lou, Fangzhi Luo, Shihong Zhang, Yingying Liu, Yang Xie, Peng Ji, Ping Jin, Xin Front Immunol Immunology The oral epithelium’s normal morphological structure and function play an important role in maintaining oral homeostasis, among which microbiota and chronic stress are key contributing factors. However, the effects of microbiota and chronic stress on the morphological structures and molecular function of oral homeostasis remain unclear. In this study, morphological staining was used to compare the tongue structure of specific pathogen-free and germ-free mice, and an integrated multi-omics analysis based on transcriptomics, proteomics, and metabolomics was performed to investigate the regulatory mechanisms of microbiota and chronic stress on oral homeostasis. We found that the morphological structure of the tongue in germ-free mice was disordered compared with in specific pathogen-free mice, especially in the epithelium. Multi-omics analysis indicated that differentially expressed molecules of the tongue between germ-free and specific pathogen-free mice were significantly enriched in the mitochondrial metabolic process and immune response. Interestingly, microbiota also significantly influenced the permeability of the oral epithelial barrier, represented by the differential expression of keratinization, and cell adhesion molecules. It was worth noting that the above changes in the tongue between specific pathogen-free and germ-free mice were more significant after chronic stress. Collectively, this is the first study to reveal that the microbiota might maintain oral homeostasis by reshaping the structure of the oral epithelial barrier and changing the function of molecular biology, a process that may be driven by the immune response and mitochondrial metabolic process of oral tissue. Furthermore, chronic stress can enhance the regulatory effects of microbiota on oral homeostasis. Frontiers Media S.A. 2022-09-20 /pmc/articles/PMC9533175/ /pubmed/36211346 http://dx.doi.org/10.3389/fimmu.2022.1005992 Text en Copyright © 2022 Long, Yan, Pu, Liu, Zhong, Wang, Yang, Lou, Luo, Zhang, Liu, Xie, Ji and Jin https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Long, Huiqing
Yan, Li
Pu, Juncai
Liu, Yiyun
Zhong, Xiaogang
Wang, Haiyang
Yang, Lu
Lou, Fangzhi
Luo, Shihong
Zhang, Yingying
Liu, Yang
Xie, Peng
Ji, Ping
Jin, Xin
Multi-omics analysis reveals the effects of microbiota on oral homeostasis
title Multi-omics analysis reveals the effects of microbiota on oral homeostasis
title_full Multi-omics analysis reveals the effects of microbiota on oral homeostasis
title_fullStr Multi-omics analysis reveals the effects of microbiota on oral homeostasis
title_full_unstemmed Multi-omics analysis reveals the effects of microbiota on oral homeostasis
title_short Multi-omics analysis reveals the effects of microbiota on oral homeostasis
title_sort multi-omics analysis reveals the effects of microbiota on oral homeostasis
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9533175/
https://www.ncbi.nlm.nih.gov/pubmed/36211346
http://dx.doi.org/10.3389/fimmu.2022.1005992
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