Attenuation of allergen-specific immunotherapy for atopic dermatitis by ectopic colonization of Brevundimonas vesicularis in the intestine

Xiaochun Liu; Beilei Xu; Xiaoqiang Xu; Zhifeng Wang; Yang Luo; Yingxia Gao; Shiqi Ling; Ao Wang; Yuan Zhou; Xiaokai Wang; Sean Xiao Leng; Wei Li; Xu Yao

doi:10.1016/j.xcrm.2023.101340

Attenuation of allergen-specific immunotherapy for atopic dermatitis by ectopic colonization of Brevundimonas vesicularis in the intestine

Xiaochun Liu, Beilei Xu, Xiaoqiang Xu, Zhifeng Wang, Yang Luo, Yingxia Gao, Shiqi Ling, Ao Wang, Yuan Zhou, Xiaokai Wang, Sean Xiao Leng^*, Wei Li^*, Xu Yao^*

^*Corresponding author for this work

Department of Biomedical Engineering

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

6 Citations (Scopus)

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Abstract

Allergen-specific immunotherapy (AIT) has shown beneficial effects against atopic dermatitis (AD); however, the mechanisms and parameters underlying the efficacy of AIT remain unclear. Here, we report that the community structure and function of the oral and gut microbiota are changed in patients with AD undergoing AIT. Transplantation of fecal microbiota from patients who respond well to AIT improves AD-like dermatitis in mice. The abundance of Brevundimonas vesicularis in the gut of AD patients has been found to be positively correlated with disease severity and is decreased following AIT. Furthermore, we find that B. vesicularis from the oral cavity might ectopically colonize the gut of AD patients. In AD model mice, meanwhile, B. vesicularis promotes the skewing of the Treg/Th17 balance toward Th17 polarization and attenuates the efficacy of ovalbumin-specific immunotherapy. Our findings provide potential strategies for the optimization of AIT for AD via the modulation of the gut microbiota. © 2023 The Author(s)

Original language	English
Article number	101340
Number of pages	21
Journal	Cell Reports Medicine
Volume	4
Issue number	12
Online published	19 Dec 2023
DOIs	https://doi.org/10.1016/j.xcrm.2023.101340
Publication status	Published - 19 Dec 2023

Funding

This work was supported by the National Natural Science Foundation of China (82073446, 82103735, 81972939, 81803144, and 82273542), the National Key R&D Program of China (2022YFC3601800), the Key Project of Social Development in Jiangsu Province (BE2020632), the CAMS Innovation Fund for Medical Sciences (2021-I2M-1-059), Nanjing Incubation Program for National Clinical Research Center (2019060001), and the Key Project of the Innovation Program of Shanghai Municipal Education Commission (2021-01-07-00-07-E00078).

Research Keywords

allergen-specific immunotherapy
atopic dermatitis
gut
microbiota
oral cavity

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title = "Attenuation of allergen-specific immunotherapy for atopic dermatitis by ectopic colonization of Brevundimonas vesicularis in the intestine",

abstract = "Allergen-specific immunotherapy (AIT) has shown beneficial effects against atopic dermatitis (AD); however, the mechanisms and parameters underlying the efficacy of AIT remain unclear. Here, we report that the community structure and function of the oral and gut microbiota are changed in patients with AD undergoing AIT. Transplantation of fecal microbiota from patients who respond well to AIT improves AD-like dermatitis in mice. The abundance of Brevundimonas vesicularis in the gut of AD patients has been found to be positively correlated with disease severity and is decreased following AIT. Furthermore, we find that B. vesicularis from the oral cavity might ectopically colonize the gut of AD patients. In AD model mice, meanwhile, B. vesicularis promotes the skewing of the Treg/Th17 balance toward Th17 polarization and attenuates the efficacy of ovalbumin-specific immunotherapy. Our findings provide potential strategies for the optimization of AIT for AD via the modulation of the gut microbiota. {\textcopyright} 2023 The Author(s)",

keywords = "allergen-specific immunotherapy, atopic dermatitis, gut, microbiota, oral cavity",

author = "Xiaochun Liu and Beilei Xu and Xiaoqiang Xu and Zhifeng Wang and Yang Luo and Yingxia Gao and Shiqi Ling and Ao Wang and Yuan Zhou and Xiaokai Wang and Leng, {Sean Xiao} and Wei Li and Xu Yao",

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language = "English",

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T1 - Attenuation of allergen-specific immunotherapy for atopic dermatitis by ectopic colonization of Brevundimonas vesicularis in the intestine

AU - Liu, Xiaochun

AU - Xu, Beilei

AU - Xu, Xiaoqiang

AU - Wang, Zhifeng

AU - Luo, Yang

AU - Gao, Yingxia

AU - Ling, Shiqi

AU - Wang, Ao

AU - Zhou, Yuan

AU - Wang, Xiaokai

AU - Leng, Sean Xiao

AU - Li, Wei

AU - Yao, Xu

PY - 2023/12/19

Y1 - 2023/12/19

N2 - Allergen-specific immunotherapy (AIT) has shown beneficial effects against atopic dermatitis (AD); however, the mechanisms and parameters underlying the efficacy of AIT remain unclear. Here, we report that the community structure and function of the oral and gut microbiota are changed in patients with AD undergoing AIT. Transplantation of fecal microbiota from patients who respond well to AIT improves AD-like dermatitis in mice. The abundance of Brevundimonas vesicularis in the gut of AD patients has been found to be positively correlated with disease severity and is decreased following AIT. Furthermore, we find that B. vesicularis from the oral cavity might ectopically colonize the gut of AD patients. In AD model mice, meanwhile, B. vesicularis promotes the skewing of the Treg/Th17 balance toward Th17 polarization and attenuates the efficacy of ovalbumin-specific immunotherapy. Our findings provide potential strategies for the optimization of AIT for AD via the modulation of the gut microbiota. © 2023 The Author(s)

AB - Allergen-specific immunotherapy (AIT) has shown beneficial effects against atopic dermatitis (AD); however, the mechanisms and parameters underlying the efficacy of AIT remain unclear. Here, we report that the community structure and function of the oral and gut microbiota are changed in patients with AD undergoing AIT. Transplantation of fecal microbiota from patients who respond well to AIT improves AD-like dermatitis in mice. The abundance of Brevundimonas vesicularis in the gut of AD patients has been found to be positively correlated with disease severity and is decreased following AIT. Furthermore, we find that B. vesicularis from the oral cavity might ectopically colonize the gut of AD patients. In AD model mice, meanwhile, B. vesicularis promotes the skewing of the Treg/Th17 balance toward Th17 polarization and attenuates the efficacy of ovalbumin-specific immunotherapy. Our findings provide potential strategies for the optimization of AIT for AD via the modulation of the gut microbiota. © 2023 The Author(s)

KW - allergen-specific immunotherapy

KW - atopic dermatitis

KW - gut

KW - microbiota

KW - oral cavity

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DO - 10.1016/j.xcrm.2023.101340

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ER -

Attenuation of allergen-specific immunotherapy for atopic dermatitis by ectopic colonization of Brevundimonas vesicularis in the intestine

Abstract

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Research Keywords

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