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

Cell Rep Med. 2023 Dec 19;4(12):101340. doi: 10.1016/j.xcrm.2023.101340.

Authors

Xiaochun Liu¹, Beilei Xu¹, Xiaoqiang Xu², Zhifeng Wang³, Yang Luo¹, Yingxia Gao¹, Shiqi Ling¹, Ao Wang¹, Yuan Zhou¹, Xiaokai Wang⁴, Sean Xiao Leng⁵, Wei Li⁶, Xu Yao⁷

Affiliations

¹ Department of Allergy and Rheumatology, Jiangsu Key Laboratory of Molecular Biology for Skin Diseases and STIs, Hospital for Skin Diseases, Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing 210042, China.
² Department of Dermatology, Huashan Hospital, Fudan University, Shanghai Institute of Dermatology, Shanghai 200040, China.
³ 01Life Institute, Shenzhen 518000, China.
⁴ Department of Biomedical Engineering, City University of Hong Kong, Hong Kong 999077, China.
⁵ Division of Geriatric Medicine and Gerontology, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA; Johns Hopkins Center on Aging and Immune Remodeling, Baltimore, MD, USA. Electronic address: sleng1@jhu.edu.
⁶ Department of Dermatology, Huashan Hospital, Fudan University, Shanghai Institute of Dermatology, Shanghai 200040, China. Electronic address: liweiderma@fudan.edu.cn.
⁷ Department of Allergy and Rheumatology, Jiangsu Key Laboratory of Molecular Biology for Skin Diseases and STIs, Hospital for Skin Diseases, Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing 210042, China. Electronic address: dryao_xu@126.com.

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.

Keywords: allergen-specific immunotherapy; atopic dermatitis; gut; microbiota; oral cavity.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Allergens
Animals
Dermatitis, Atopic* / therapy
Desensitization, Immunologic
Humans
Intestines
Mice

Substances

Allergens

Supplementary concepts

Brevundimonas vesicularis