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...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-09-01
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| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1005992/full |
| _version_ | 1798031871434555392 |
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| author | Huiqing Long Huiqing Long Li Yan Juncai Pu Juncai Pu Yiyun Liu Yiyun Liu Xiaogang Zhong Xiaogang Zhong Haiyang Wang Haiyang Wang Lu Yang Lu Yang Fangzhi Lou Fangzhi Lou Shihong Luo Shihong Luo Yingying Zhang Yingying Zhang Yang Liu Yang Liu Peng Xie Peng Xie Ping Ji Ping Ji Xin Jin Xin Jin |
| author_facet | Huiqing Long Huiqing Long Li Yan Juncai Pu Juncai Pu Yiyun Liu Yiyun Liu Xiaogang Zhong Xiaogang Zhong Haiyang Wang Haiyang Wang Lu Yang Lu Yang Fangzhi Lou Fangzhi Lou Shihong Luo Shihong Luo Yingying Zhang Yingying Zhang Yang Liu Yang Liu Peng Xie Peng Xie Ping Ji Ping Ji Xin Jin Xin Jin |
| author_sort | Huiqing Long |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T20:04:44Z |
| format | Article |
| id | doaj.art-668f2c514c65405a9a0cc7dd111666c5 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-11T20:04:44Z |
| publishDate | 2022-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-668f2c514c65405a9a0cc7dd111666c52022-12-22T04:05:22ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-09-011310.3389/fimmu.2022.10059921005992Multi-omics analysis reveals the effects of microbiota on oral homeostasisHuiqing Long0Huiqing Long1Li Yan2Juncai Pu3Juncai Pu4Yiyun Liu5Yiyun Liu6Xiaogang Zhong7Xiaogang Zhong8Haiyang Wang9Haiyang Wang10Lu Yang11Lu Yang12Fangzhi Lou13Fangzhi Lou14Shihong Luo15Shihong Luo16Yingying Zhang17Yingying Zhang18Yang Liu19Yang Liu20Peng Xie21Peng Xie22Ping Ji23Ping Ji24Xin Jin25Xin Jin26Key Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Oral Diseases and Biomedical Sciences, Chongqing, ChinaSchool of Public Health and Management, Chongqing Medical University, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaNHC Key Laboratory of Diagnosis and Treatment on Brain Functional Diseases, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaNHC Key Laboratory of Diagnosis and Treatment on Brain Functional Diseases, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaNHC Key Laboratory of Diagnosis and Treatment on Brain Functional Diseases, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaNHC Key Laboratory of Diagnosis and Treatment on Brain Functional Diseases, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Oral Diseases and Biomedical Sciences, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Oral Diseases and Biomedical Sciences, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Oral Diseases and Biomedical Sciences, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Oral Diseases and Biomedical Sciences, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Oral Diseases and Biomedical Sciences, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaNHC Key Laboratory of Diagnosis and Treatment on Brain Functional Diseases, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Oral Diseases and Biomedical Sciences, Chongqing, ChinaKey Laboratory of Psychoseomadsy, Stomatological Hospital of Chongqing Medical University, Chongqing, ChinaChongqing Key Laboratory of Oral Diseases and Biomedical Sciences, Chongqing, ChinaThe 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.https://www.frontiersin.org/articles/10.3389/fimmu.2022.1005992/fullmicrobiotatonguehomeostasisimmunitytranscriptomeproteome |
| spellingShingle | Huiqing Long Huiqing Long Li Yan Juncai Pu Juncai Pu Yiyun Liu Yiyun Liu Xiaogang Zhong Xiaogang Zhong Haiyang Wang Haiyang Wang Lu Yang Lu Yang Fangzhi Lou Fangzhi Lou Shihong Luo Shihong Luo Yingying Zhang Yingying Zhang Yang Liu Yang Liu Peng Xie Peng Xie Ping Ji Ping Ji Xin Jin Xin Jin Multi-omics analysis reveals the effects of microbiota on oral homeostasis Frontiers in Immunology microbiota tongue homeostasis immunity transcriptome proteome |
| 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 | microbiota tongue homeostasis immunity transcriptome proteome |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1005992/full |
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