A tryptophan metabolite of the skin microbiota attenuates inflammation in patients with atopic dermatitis through the aryl hydrocarbon receptor
Previous studies have revealed significant alterations in the skin microbiota of patients with atopic dermatitis (AD) not only in diversity and composition but also in function, and the tryptophan (Trp) metabolic pathway is attenuated in the skin microbiota of patients with AD. We sought to assess T...
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| Published in: | Journal of allergy and clinical immunology Vol. 143; no. 6; pp. 2108 - 2119.e12 |
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| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Elsevier Inc
01.06.2019
Elsevier Limited |
| Subjects: | |
| ISSN: | 0091-6749, 1097-6825, 1097-6825 |
| Online Access: | Get full text |
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| Abstract | Previous studies have revealed significant alterations in the skin microbiota of patients with atopic dermatitis (AD) not only in diversity and composition but also in function, and the tryptophan (Trp) metabolic pathway is attenuated in the skin microbiota of patients with AD.
We sought to assess Trp metabolites on the skin surfaces of patients with AD and to explore the function of the microbial Trp metabolites in skin inflammation in patients with AD.
A gel-patch method was developed to collect metabolites on the skin surface, which were then assessed by using liquid chromatography–tandem mass spectrometry. A mouse model of calcipotriol (MC903)–induced AD-like dermatitis was used to evaluate the effects of microbial metabolites on AD, and aryl hydrocarbon receptor (AhR)–null mice and keratinocyte cultures were used to investigate the mechanism.
Major microbial metabolites of Trp were detected on the skin surfaces of healthy subjects, and the level of indole-3-aldehyde (IAId), an indole derivative of Trp catabolism, was significantly lower in lesional and nonlesional skin of patients with AD than that of healthy subjects. IAId significantly attenuated skin inflammation in mice with MC903-induced AD-like dermatitis, and this effect was blocked by an AhR antagonist and abolished in AhR-null mice. Furthermore, IAId was found to inhibit the MC903-induced expression of thymic stromal lymphopoietin in keratinocytes in vivo and in vitro, which was mediated by binding of AhR to the thymic stromal lymphopoietin promoter.
IAId, a skin microbiota–derived Trp metabolite, negatively regulated skin inflammation in patients with AD, revealing that skin microbiota play a significant functional role in the pathogenesis of AD.
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| AbstractList | BackgroundPrevious studies have revealed significant alterations in the skin microbiota of patients with atopic dermatitis (AD) not only in diversity and composition but also in function, and the tryptophan (Trp) metabolic pathway is attenuated in the skin microbiota of patients with AD.ObjectiveWe sought to assess Trp metabolites on the skin surfaces of patients with AD and to explore the function of the microbial Trp metabolites in skin inflammation in patients with AD.MethodsA gel-patch method was developed to collect metabolites on the skin surface, which were then assessed by using liquid chromatography–tandem mass spectrometry. A mouse model of calcipotriol (MC903)–induced AD-like dermatitis was used to evaluate the effects of microbial metabolites on AD, and aryl hydrocarbon receptor (AhR)–null mice and keratinocyte cultures were used to investigate the mechanism.ResultsMajor microbial metabolites of Trp were detected on the skin surfaces of healthy subjects, and the level of indole-3-aldehyde (IAId), an indole derivative of Trp catabolism, was significantly lower in lesional and nonlesional skin of patients with AD than that of healthy subjects. IAId significantly attenuated skin inflammation in mice with MC903-induced AD-like dermatitis, and this effect was blocked by an AhR antagonist and abolished in AhR-null mice. Furthermore, IAId was found to inhibit the MC903-induced expression of thymic stromal lymphopoietin in keratinocytes in vivo and in vitro, which was mediated by binding of AhR to the thymic stromal lymphopoietin promoter.ConclusionIAId, a skin microbiota–derived Trp metabolite, negatively regulated skin inflammation in patients with AD, revealing that skin microbiota play a significant functional role in the pathogenesis of AD. Previous studies have revealed significant alterations in the skin microbiota of patients with atopic dermatitis (AD) not only in diversity and composition but also in function, and the tryptophan (Trp) metabolic pathway is attenuated in the skin microbiota of patients with AD.BACKGROUNDPrevious studies have revealed significant alterations in the skin microbiota of patients with atopic dermatitis (AD) not only in diversity and composition but also in function, and the tryptophan (Trp) metabolic pathway is attenuated in the skin microbiota of patients with AD.We sought to assess Trp metabolites on the skin surfaces of patients with AD and to explore the function of the microbial Trp metabolites in skin inflammation in patients with AD.OBJECTIVEWe sought to assess Trp metabolites on the skin surfaces of patients with AD and to explore the function of the microbial Trp metabolites in skin inflammation in patients with AD.A gel-patch method was developed to collect metabolites on the skin surface, which were then assessed by using liquid chromatography-tandem mass spectrometry. A mouse model of calcipotriol (MC903)-induced AD-like dermatitis was used to evaluate the effects of microbial metabolites on AD, and aryl hydrocarbon receptor (AhR)-null mice and keratinocyte cultures were used to investigate the mechanism.METHODSA gel-patch method was developed to collect metabolites on the skin surface, which were then assessed by using liquid chromatography-tandem mass spectrometry. A mouse model of calcipotriol (MC903)-induced AD-like dermatitis was used to evaluate the effects of microbial metabolites on AD, and aryl hydrocarbon receptor (AhR)-null mice and keratinocyte cultures were used to investigate the mechanism.Major microbial metabolites of Trp were detected on the skin surfaces of healthy subjects, and the level of indole-3-aldehyde (IAId), an indole derivative of Trp catabolism, was significantly lower in lesional and nonlesional skin of patients with AD than that of healthy subjects. IAId significantly attenuated skin inflammation in mice with MC903-induced AD-like dermatitis, and this effect was blocked by an AhR antagonist and abolished in AhR-null mice. Furthermore, IAId was found to inhibit the MC903-induced expression of thymic stromal lymphopoietin in keratinocytes in vivo and in vitro, which was mediated by binding of AhR to the thymic stromal lymphopoietin promoter.RESULTSMajor microbial metabolites of Trp were detected on the skin surfaces of healthy subjects, and the level of indole-3-aldehyde (IAId), an indole derivative of Trp catabolism, was significantly lower in lesional and nonlesional skin of patients with AD than that of healthy subjects. IAId significantly attenuated skin inflammation in mice with MC903-induced AD-like dermatitis, and this effect was blocked by an AhR antagonist and abolished in AhR-null mice. Furthermore, IAId was found to inhibit the MC903-induced expression of thymic stromal lymphopoietin in keratinocytes in vivo and in vitro, which was mediated by binding of AhR to the thymic stromal lymphopoietin promoter.IAId, a skin microbiota-derived Trp metabolite, negatively regulated skin inflammation in patients with AD, revealing that skin microbiota play a significant functional role in the pathogenesis of AD.CONCLUSIONIAId, a skin microbiota-derived Trp metabolite, negatively regulated skin inflammation in patients with AD, revealing that skin microbiota play a significant functional role in the pathogenesis of AD. Previous studies have revealed significant alterations in the skin microbiota of patients with atopic dermatitis (AD) not only in diversity and composition but also in function, and the tryptophan (Trp) metabolic pathway is attenuated in the skin microbiota of patients with AD. We sought to assess Trp metabolites on the skin surfaces of patients with AD and to explore the function of the microbial Trp metabolites in skin inflammation in patients with AD. A gel-patch method was developed to collect metabolites on the skin surface, which were then assessed by using liquid chromatography-tandem mass spectrometry. A mouse model of calcipotriol (MC903)-induced AD-like dermatitis was used to evaluate the effects of microbial metabolites on AD, and aryl hydrocarbon receptor (AhR)-null mice and keratinocyte cultures were used to investigate the mechanism. Major microbial metabolites of Trp were detected on the skin surfaces of healthy subjects, and the level of indole-3-aldehyde (IAId), an indole derivative of Trp catabolism, was significantly lower in lesional and nonlesional skin of patients with AD than that of healthy subjects. IAId significantly attenuated skin inflammation in mice with MC903-induced AD-like dermatitis, and this effect was blocked by an AhR antagonist and abolished in AhR-null mice. Furthermore, IAId was found to inhibit the MC903-induced expression of thymic stromal lymphopoietin in keratinocytes in vivo and in vitro, which was mediated by binding of AhR to the thymic stromal lymphopoietin promoter. IAId, a skin microbiota-derived Trp metabolite, negatively regulated skin inflammation in patients with AD, revealing that skin microbiota play a significant functional role in the pathogenesis of AD. Previous studies have revealed significant alterations in the skin microbiota of patients with atopic dermatitis (AD) not only in diversity and composition but also in function, and the tryptophan (Trp) metabolic pathway is attenuated in the skin microbiota of patients with AD. We sought to assess Trp metabolites on the skin surfaces of patients with AD and to explore the function of the microbial Trp metabolites in skin inflammation in patients with AD. A gel-patch method was developed to collect metabolites on the skin surface, which were then assessed by using liquid chromatography–tandem mass spectrometry. A mouse model of calcipotriol (MC903)–induced AD-like dermatitis was used to evaluate the effects of microbial metabolites on AD, and aryl hydrocarbon receptor (AhR)–null mice and keratinocyte cultures were used to investigate the mechanism. Major microbial metabolites of Trp were detected on the skin surfaces of healthy subjects, and the level of indole-3-aldehyde (IAId), an indole derivative of Trp catabolism, was significantly lower in lesional and nonlesional skin of patients with AD than that of healthy subjects. IAId significantly attenuated skin inflammation in mice with MC903-induced AD-like dermatitis, and this effect was blocked by an AhR antagonist and abolished in AhR-null mice. Furthermore, IAId was found to inhibit the MC903-induced expression of thymic stromal lymphopoietin in keratinocytes in vivo and in vitro, which was mediated by binding of AhR to the thymic stromal lymphopoietin promoter. IAId, a skin microbiota–derived Trp metabolite, negatively regulated skin inflammation in patients with AD, revealing that skin microbiota play a significant functional role in the pathogenesis of AD. [Display omitted] |
| Author | Sun, Jinlv Zhu, Zhenlai Sun, Licheng Gao, Jixin Li, Wei Yao, Xu Zhou, Yufeng Wang, Gang Luo, Yang Yu, Jinlei |
| Author_xml | – sequence: 1 givenname: Jinlei surname: Yu fullname: Yu, Jinlei organization: Department of Dermatology, Xijing Hospital, Fourth Military Medical University, Xi'an, China – sequence: 2 givenname: Yang surname: Luo fullname: Luo, Yang organization: Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing, China – sequence: 3 givenname: Zhenlai surname: Zhu fullname: Zhu, Zhenlai organization: Department of Dermatology, Xijing Hospital, Fourth Military Medical University, Xi'an, China – sequence: 4 givenname: Yufeng surname: Zhou fullname: Zhou, Yufeng organization: Children's Hospital and Institute of Biomedical Sciences, Shanghai, China – sequence: 5 givenname: Licheng surname: Sun fullname: Sun, Licheng organization: Children's Hospital and Institute of Biomedical Sciences, Shanghai, China – sequence: 6 givenname: Jixin surname: Gao fullname: Gao, Jixin organization: Department of Dermatology, Xijing Hospital, Fourth Military Medical University, Xi'an, China – sequence: 7 givenname: Jinlv surname: Sun fullname: Sun, Jinlv organization: Department of Allergy, Peking Union Hospital, Peking Union Medical College, Beijing, China – sequence: 8 givenname: Gang surname: Wang fullname: Wang, Gang organization: Department of Dermatology, Xijing Hospital, Fourth Military Medical University, Xi'an, China – sequence: 9 givenname: Xu surname: Yao fullname: Yao, Xu email: dryao_xu@126.com organization: Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing, China – sequence: 10 givenname: Wei surname: Li fullname: Li, Wei email: liweiderma@163.com organization: Department of Dermatology, Xijing Hospital, Fourth Military Medical University, Xi'an, China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30578876$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2018 American Academy of Allergy, Asthma & Immunology Copyright © 2018 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. 2018. American Academy of Allergy, Asthma & Immunology |
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| ISSN | 0091-6749 1097-6825 |
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| Issue | 6 |
| Keywords | microbiota DMSO skin FACS aryl hydrocarbon receptor CHS LC-MS/MS Trp Atopic dermatitis tryptophan KYN AD TSLP AhRE IAA AhR siRNA 5-HTP IMQ metabolites SCFA IAId thymic stromal lymphopoietin indole-3-aldehyde CYP1A1 OXA |
| Language | English |
| License | Copyright © 2018 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. |
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| PublicationDate | June 2019 2019-06-00 20190601 |
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| PublicationTitle | Journal of allergy and clinical immunology |
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| SubjectTerms | Animals aryl hydrocarbon receptor Atopic dermatitis Calcitriol - analogs & derivatives Calcitriol - immunology Cells, Cultured Cytokines - metabolism Dermatitis Dermatitis, Atopic - drug therapy Disease Models, Animal Eczema Homeostasis Humans Hydrocarbons indole-3-aldehyde Indoles Indoles - therapeutic use Inflammation Keratinocytes Keratinocytes - physiology Ligands Liquid chromatography Mass spectroscopy Metabolic pathways Metabolism Metabolites Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Knockout Microbiota Microbiota - immunology Receptors, Aryl Hydrocarbon - genetics Receptors, Aryl Hydrocarbon - metabolism Skin Skin - metabolism Skin - microbiology Skin diseases Thymic stromal lymphopoietin Thymus Tryptophan Tryptophan - metabolism Up-Regulation |
| Title | A tryptophan metabolite of the skin microbiota attenuates inflammation in patients with atopic dermatitis through the aryl hydrocarbon receptor |
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