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IL-33 released during challenge phase regulates allergic asthma in an age-dependent way

Cellular & Molecular Immunology volume 22, pages 191–207 (2025)Cite this article

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Abstract

Epithelial-derived cytokines, especially type 2 alarmins (TSLP, IL-25, and IL-33), have emerged as critical mediators of type 2 inflammation. IL-33 attracts more interest for its strong association with allergic asthma, especially in childhood asthma. However, the age-dependent role of IL-33 to the development of allergic asthma remains elusive. Here, using OVA-induced allergic asthma model in neonatal and adult mice, we report that IL-33 is the most important alarmin in neonatal lung both at steady state or inflammation. The deficiency of IL-33/ST2 abrogated the development of allergic asthma only in neonates, whereas in adults the effect was limited. Interestingly, the deficiency of IL-33/ST2 equally dampened the ILC2 responses in both neonatal and adult models. However, the effect of IL-33/ST2 deficiency on Th2 responses is age-dependent, which is only blocked in neonates. Furthermore, IL-33/ST2 signaling is dispensable for OVA sensitization. Following OVA challenge in adults, the deficiency of IL-33/ST2 results in compensational more TSLP, which in turn recruits and activates lung DCs and boosts Th2 responses. The enriched γδ T17 cells in IL-33/ST2 deficient neonatal lung suppress the expression of type 2 alarmins, CCL20 and GM-CSF via IL-17A, thus might confer the inhibition of allergic asthma. Finally, on the basis of IL-33 deficiency, the additive protective effects of TSLP blocking is much more pronounced than IL-25 blocking in adults. Our studies demonstrate that the role of IL-33 for ILC2 and Th2 responses varies among ages in OVA models and indicate that the factor of age should be considered for intervention of asthma.

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Acknowledgements

Thanks for the technical support by the Huazhong University of Science and Technology Analytical & Testing center, Medical sub-center. Thanks for the support of animal experiments and FACS experiments by Innovation and Research Center, Tongji Medical College, HUST. Thanks for the technical support by the Laboratory Animal Center, Huazhong University of Science and Technology. This work was supported in part by grants from the National Natural Science Foundation of China (grant 31970865) to J.H., and by the Postdoctoral Fellowship Program of CPSF under Grant Number GZC20241497 to M.W.

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  1. These authors contributed equally: Hangyu Liu, Min Wu.

Authors and Affiliations

  1. Department of Immunology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China

    Hangyu Liu, Qiangqiang Wang, Ketai Shi, Yawen Lin, Junyi Zhou, Ju Huang, Fang Zheng & Junyan Han

  2. Department of Pathogen Biology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China

    Hangyu Liu, Han Jiang, Shen Qu, Yuwei Zhang & Yafei Huang

  3. Department of Gynecologic Oncology, Women’s Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China

    Min Wu

  4. Department of Clinical Laboratory, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China

    Liuchuang Gao

  5. Key Clinical Laboratory of Henan Province, Zhengzhou, 450052, China

    Liuchuang Gao

  6. State Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Huazhong University of Science and Technology, Wuhan, China

    Yafei Huang

  7. Key Laboratory of Vascular Aging, Ministry of Education, Tongji Hospital of Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China

    Junyan Han

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Contributions

H.L., M.W., Y.H. and J.H. conceived the idea, designed the experiments, and composed the paper. H.L. and M.W. conducted all the experiments; Q.W., L.G. and H.J. assisted in animal experiments; Y.L., J.Z. and J.H. assisted in flow cytometry analysis; S.Q. and Y.Z. assisted in cell culture and in vitro experiments; H.L., M.W., F.Z., Y.H. and J.H. contributed to the interpretation of the results. Y.H. and J.H. supervised the project.

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Correspondence to Yafei Huang or Junyan Han.

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Liu, H., Wu, M., Wang, Q. et al. IL-33 released during challenge phase regulates allergic asthma in an age-dependent way. Cell Mol Immunol 22, 191–207 (2025). https://doi.org/10.1038/s41423-024-01205-2

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