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IL-33 induces histidine decarboxylase, especially in c-kit+ cells and mast cells, and roles of histamine include negative regulation of IL-33-induced eosinophilia

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Abstract

Objective and methods

IL-33 is present in endothelial, epithelial, and fibroblast-like cells and released upon cell injury. IL-33 reportedly induces mast-cell degranulation and is involved in various diseases, including allergic diseases. So, IL-33-related diseases seem to overlap with histamine-related diseases. In addition to the release from mast cells, histamine is newly formed by the induction of histidine decarboxylase (HDC). Some inflammatory and/or hematopoietic cytokines (IL-1, IL-3, etc.) are known to induce HDC, and the histamine produced by HDC induction is released without storage. We examined the involvement of HDC and histamine in the effects of IL-33.

Results

A single intraperitoneal injection of IL-33 into mice induced HDC directly and/or via other cytokines (including IL-5) within a few hours in various tissues, particularly strongly in hematopoietic organs. The major cells exhibiting HDC-induction were mast cells and c-kit+ cells in the bone marrow. HDC was also induced in non-mast cells in non-hematopoietic organs. HDC, histamine, and histamine H4 receptors (H4Rs) contributed to the suppression of IL-33-induced eosinophilia.

Conclusion

IL-33 directly and indirectly (via IL-5) induces HDC in various cells, particularly potently in c-kit+ cells and mature mast cells, and the newly formed histamine contributes to the negative regulation of IL-33-induced eosinophilia via H4Rs.

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Acknowledgements

We are grateful to Dr. Robert Timms for editing the manuscript. We thank the Biomedical Research Core of Tohoku University Graduate School of Medicine for the use of its equipment. We thank Dr. Takashi Moriguchi and Dr. Jun Takai for providing HDC-GFP mice.

Funding

This work was supported by Grants from the Japan Society for the Promotion of Science [18K17240 and 21K10157 (Bando Kanan)].

Author information

Authors and Affiliations

  1. Division of Orthodontics and Dentofacial Orthopedics, Graduate School of Dentistry, Tohoku University, 4-1 Seiryo-Machi, Aoba-Ku, Sendai, 980-8575, Japan

    Kanan Bando & Itaru Mizoguchi

  2. Division of Dento-Oral Anesthesiology, Graduate School of Dentistry, Tohoku University, 4-1 Seiryo-Machi, Aoba-Ku, Sendai, 980-8575, Japan

    Yukinori Tanaka & Saka Winias

  3. Division of Oral Immunology, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-Machi, Sendai, 980-8575, Japan

    Shunji Sugawara

  4. Division of Oral and Maxillofacial Surgery, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-Machi, Sendai, 980-8575, Japan

    Yasuo Endo

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  1. Kanan Bando
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  2. Yukinori Tanaka
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  4. Shunji Sugawara
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  5. Itaru Mizoguchi
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  6. Yasuo Endo
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Study was designed and conducted by KB, YT, SS, IM, and YE. Data collected by KB. Data analyzed by KB and YE. Technically assisted by YT and SW. Manuscript written by KB and YE and approved by all authors.

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Correspondence to Kanan Bando.

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All animal procedures were approved by the Institutional Animal Care and Use Committee of Tohoku University (approval number: 2018DnA-013). All experiments complied with the Regulations for Animal Experiments and Related Activities at Tohoku University.

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Bando, K., Tanaka, Y., Winias, S. et al. IL-33 induces histidine decarboxylase, especially in c-kit+ cells and mast cells, and roles of histamine include negative regulation of IL-33-induced eosinophilia. Inflamm. Res. 72, 651–667 (2023). https://doi.org/10.1007/s00011-023-01699-y

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