Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis
Gut microbial disturbance affects allergic diseases including asthma, atopic dermatitis (AD) via the aberrant immune response. Some Bifidobacterial species and strains have been reported to improve AD via modulating immune-microbe interactions in patients. However, the effective metabolites and mech...
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2022-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2022.2044723 |
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| author | Zhifeng Fang Tong Pan Lingzhi Li Hongchao Wang Jinlin Zhu Hao Zhang Jianxin Zhao Wei Chen Wenwei Lu |
| author_facet | Zhifeng Fang Tong Pan Lingzhi Li Hongchao Wang Jinlin Zhu Hao Zhang Jianxin Zhao Wei Chen Wenwei Lu |
| author_sort | Zhifeng Fang |
| collection | DOAJ |
| description | Gut microbial disturbance affects allergic diseases including asthma, atopic dermatitis (AD) via the aberrant immune response. Some Bifidobacterial species and strains have been reported to improve AD via modulating immune-microbe interactions in patients. However, the effective metabolites and mechanism of alleviating AD in bifidobacteria remain to be elucidated. This study aimed to explore the microbial metabolite and mechanism of Bifidobacterium longum to improve AD. Based on shotgun metagenomic sequencing and UHPLC Q-Exactive-MS targeted metabolic experiments in vitro and in vivo, we focused on tryptophan metabolism and indole derivatives, which are endogenous ligands for aryl hydrocarbon receptor (AHR). Indole-3-carbaldehyde (I3C), a tryptophan metabolite of B. longum CCFM1029 activated AHR-mediated immune signaling pathway to improve AD symptoms in animal and clinical experiments. B. longum CCFM1029 upregulated tryptophan metabolism and increased I3C to suppress aberrant T helper 2 type immune responses, but these benefits were eliminated by AHR antagonist CH223191. Furthermore, B. longum CCFM1029 reshaped gut microbial composition in AD patients, increased fecal and serum I3C, and maintained the abundance of Lachnospiraceae related to tryptophan metabolism of gut microbiota. The results suggested that based on the interactions of the gut-skin axis, B. longum CCFM1029 upregulated tryptophan metabolism and produced I3C to activate AHR-mediated immune response, alleviating AD symptoms. Indole derivates, microbial metabolites of tryptophan, may be the potential metabolites of bifidobacteria to alleviate AD via the AHR signaling pathway. |
| format | Article |
| id | doaj-art-9e439da1afaf4e5f97b3e5ec00cfa8b7 |
| institution | DOAJ |
| issn | 1949-0976 1949-0984 |
| language | English |
| publishDate | 2022-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj-art-9e439da1afaf4e5f97b3e5ec00cfa8b72025-08-20T03:21:40ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2022.2044723Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axisZhifeng Fang0Tong Pan1Lingzhi Li2Hongchao Wang3Jinlin Zhu4Hao Zhang5Jianxin Zhao6Wei Chen7Wenwei Lu8State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaState Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaState Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaState Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaState Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaState Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaState Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaState Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaState Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaGut microbial disturbance affects allergic diseases including asthma, atopic dermatitis (AD) via the aberrant immune response. Some Bifidobacterial species and strains have been reported to improve AD via modulating immune-microbe interactions in patients. However, the effective metabolites and mechanism of alleviating AD in bifidobacteria remain to be elucidated. This study aimed to explore the microbial metabolite and mechanism of Bifidobacterium longum to improve AD. Based on shotgun metagenomic sequencing and UHPLC Q-Exactive-MS targeted metabolic experiments in vitro and in vivo, we focused on tryptophan metabolism and indole derivatives, which are endogenous ligands for aryl hydrocarbon receptor (AHR). Indole-3-carbaldehyde (I3C), a tryptophan metabolite of B. longum CCFM1029 activated AHR-mediated immune signaling pathway to improve AD symptoms in animal and clinical experiments. B. longum CCFM1029 upregulated tryptophan metabolism and increased I3C to suppress aberrant T helper 2 type immune responses, but these benefits were eliminated by AHR antagonist CH223191. Furthermore, B. longum CCFM1029 reshaped gut microbial composition in AD patients, increased fecal and serum I3C, and maintained the abundance of Lachnospiraceae related to tryptophan metabolism of gut microbiota. The results suggested that based on the interactions of the gut-skin axis, B. longum CCFM1029 upregulated tryptophan metabolism and produced I3C to activate AHR-mediated immune response, alleviating AD symptoms. Indole derivates, microbial metabolites of tryptophan, may be the potential metabolites of bifidobacteria to alleviate AD via the AHR signaling pathway.https://www.tandfonline.com/doi/10.1080/19490976.2022.2044723Bifidobacterium longumtryptophan metabolismgut-skin axisaryl hydrocarbon receptorsindole-3-carbaldehydeatopic dermatitis |
| spellingShingle | Zhifeng Fang Tong Pan Lingzhi Li Hongchao Wang Jinlin Zhu Hao Zhang Jianxin Zhao Wei Chen Wenwei Lu Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis Gut Microbes Bifidobacterium longum tryptophan metabolism gut-skin axis aryl hydrocarbon receptors indole-3-carbaldehyde atopic dermatitis |
| title | Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis |
| title_full | Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis |
| title_fullStr | Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis |
| title_full_unstemmed | Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis |
| title_short | Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis |
| title_sort | bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut skin axis |
| topic | Bifidobacterium longum tryptophan metabolism gut-skin axis aryl hydrocarbon receptors indole-3-carbaldehyde atopic dermatitis |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2022.2044723 |
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