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B-cell-derived IL-10 promotes allergic sensitization in asthma regulated by Bcl-3

Cellular & Molecular Immunology volume 20, pages 1313–1327 (2023)Cite this article

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Abstract

Aeroallergen sensitization, mainly mediated by lung epithelium and dendritic cells (DCs), is integral to allergic asthma pathogenesis and progression. IL-10 has a dual role in immune responses, as it inhibits myeloid cell activation but promotes B-cell responses and epithelial cell proliferation. Here, we report a proinflammatory function of B-cell-derived IL-10 modulated by Bcl-3 in allergic asthma. Specifically, Bcl-3−/− mice showed elevated IL-10 levels and were found to be highly vulnerable to allergic asthma induced by house dust mites (HDMs). IL-10 had a positive correlation with the levels of the DC chemoattractant CCL-20 in HDM-sensitized mice and in patients with asthma and induced a selective increase in CCL-20 production by mouse lung epithelial cells. Blockade of IL-10 or IL-10 receptors during sensitization dampened both HDM-induced sensitization and asthma development. IL-10 levels peaked 4 h post sensitization with HDM and IL-10 was primarily produced by B cells under Bcl-3–Blimp-1–Bcl-6 regulation. Mice lacking B-cell-derived IL-10 displayed decreased lung epithelial CCL-20 production and diminished DC recruitment to the lungs upon HDM sensitization, thereby demonstrating resistance to HDM-induced asthma. Moreover, responses to HDM stimulation in Bcl-3−/− mice lacking B-cell-derived IL-10 were comparable to those in Bcl-3+/+ mice. The results revealed an unexpected role of B-cell-derived IL-10 in promoting allergic sensitization and demonstrated that Bcl-3 prevents HDM-induced asthma by inhibiting B-cell-derived IL-10 production. Thus, targeting the Bcl-3/IL-10 axis to inhibit allergic sensitization is a promising approach for treating allergic asthma.

IL-10 is released rapidly from lung plasma cells under Bcl-3–Blimp-1–Bcl-6 regulation upon house dust mite exposure and amplifies lung epithelial cell (EC)‐derived CCL-20 production and subsequent dendritic cell (DC) recruitment to promote allergic sensitization in asthma.

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Acknowledgements

We thank Dr. Mingfang Lu, Dr. Wei Jiang, Dr. Guohong Hu, Dr. Jin Li, and Dr. Xubo Huang for providing advice as well as some reagents used in this study. We appreciate Dr. Michael Reth and Dr. Axel Roers for gifting Il10fl/fl and Mb1-Cre mice. This investigation was funded by the National Natural Science Foundation of China (grants 81901633 to GQ and 91949102 to XZ), the National Program on Key Research (2021YFA0804703 to XZ), and the Discipline Construction Projects of Guangzhou Medical University (02-445-2301246XM to XZ).

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  1. Guojun Qian

    Present address: Key Laboratory of Anesthesiology (Shanghai Jiao Tong University), Ministry of Education, 200001, Shanghai, China

  2. These authors contributed equally: Guojun Qian, Wenxia Jiang, Donglin Sun, Zhun Sun.

Authors and Affiliations

  1. Affiliated Cancer Hospital/Institute and GMU-GIBH Joint School of Life Sciences of Guangzhou Medical University, The Guangdong-Hong Kong-Macau Joint Laboratory for Cell Fate Regulation and Diseases, State Key Laboratory of Respiratory Disease, 511436, Guangzhou, China

    Guojun Qian, Donglin Sun, Zhun Sun, Anning Chen, Jingyao Wang & Xiaoren Zhang

  2. Shanghai Institute of Nutrition and Health, Chinese Academy of Sciences, 200031, Shanghai, China

    Wenxia Jiang & Xiaoren Zhang

  3. Department of Anesthesiology, Zhongshan Hospital, Fudan University, 200032, Shanghai, China

    Hongwei Fang & Hao Fang

  4. Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine, 200032, Shanghai, China

    Yongzhong Liu

  5. Zhuhai People’s Hospital, Biomedical Translational Research Institute, Jinan University, 510632, Guangzhou, China

    Zhinan Yin

  6. Institute of Immunology, University of Science and Technology of China, 230000, Hefei, China

    Haiming Wei

  7. Department of Anesthesiology, Minhang Hospital, Fudan University, 201100, Shanghai, China

    Hao Fang

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Contributions

XZ, GQ, and HF conceptualized the study. GQ, XZ, and HF designed the experiments. GQ, WJ, DS, ZS conducted the experiments. AC and HWF helped to perform the experiments; JW completed the acquisition and processing of microarray datasets. GQ, WJ, DS and ZS analyzed the data. GQ wrote the manuscript. XZ and HF revised the manuscript. YL, ZY, and HW provided advice and some reagents.

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Correspondence to Guojun Qian, Hao Fang or Xiaoren Zhang.

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Qian, G., Jiang, W., Sun, D. et al. B-cell-derived IL-10 promotes allergic sensitization in asthma regulated by Bcl-3. Cell Mol Immunol 20, 1313–1327 (2023). https://doi.org/10.1038/s41423-023-01079-w

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