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A Rapid Shift from Chronic Hyperoxia to Normoxia Induces Systemic Anaphylaxis via Transient Receptor Potential Ankyrin 1 Channels on Mast Cells

Kenshiro Matsuda, Peter D. Arkwright, Yasuo Mori, Masa-aki Oikawa, Ryo Muko, Akane Tanaka and Hiroshi Matsuda
J Immunol December 1, 2020, 205 (11) 2959-2967; DOI: https://doi.org/10.4049/jimmunol.2000149
Kenshiro Matsuda
*Laboratory of Comparative Animal Medicine, Division of Animal Life Science, Institute of Agriculture, Tokyo University of Agriculture and Technology, Tokyo 183-8509, Japan;
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Peter D. Arkwright
†Lydia Becker Institute of Immunity and Inflammation, University of Manchester, Manchester M13 9WL, United Kingdom;
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Yasuo Mori
‡Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Kyoto 615-8510, Japan;
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Masa-aki Oikawa
§Diagnostic and Research Laboratory, Equine Veterinary Medical Center, Doha, Qatar; and
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Ryo Muko
¶Cooperative Major in Advanced Health Science, Graduate School of Bio-Applications and System Engineering, Tokyo University of Agriculture and Technology, Tokyo 183-8509, Japan
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Akane Tanaka
*Laboratory of Comparative Animal Medicine, Division of Animal Life Science, Institute of Agriculture, Tokyo University of Agriculture and Technology, Tokyo 183-8509, Japan;
¶Cooperative Major in Advanced Health Science, Graduate School of Bio-Applications and System Engineering, Tokyo University of Agriculture and Technology, Tokyo 183-8509, Japan
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Hiroshi Matsuda
*Laboratory of Comparative Animal Medicine, Division of Animal Life Science, Institute of Agriculture, Tokyo University of Agriculture and Technology, Tokyo 183-8509, Japan;
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Key Points

  • Rapid reductions in oxygen tension triggered the degranulation of mast cells.

  • Oxygen-induced activation of mast cells was mediated via TRPA1 channels.

  • Rapid reductions in oxygen tension induced anaphylactic shock.

Abstract

Extensive activation of mast cells is the major switch that triggers systemic anaphylaxis, resulting in the subsequent release of anaphylactic mediators into circulation. We previously demonstrated that rapid changes in oxygen tension lead to mast cell degranulation, and the released tryptase triggers retinal angiogenesis in a murine oxygen-induced retinopathy model. However, whether a rapid shift from hyperoxia to normoxia (relative hypoxic stress) is a risk factor for systemic anaphylaxis remains unknown. In this study, we demonstrated that the relative hypoxia stress induces systemic mast cell activation via transient receptor potential ankyrin 1 (TRPA1) channels, which immediately leads to hypothermia and increased vascular permeability in adult mice. Although mast cell–deficient or TRPA1-deficient mice did not exhibit anaphylactic symptoms following a rapid sift to normoxia, preinjection with bone marrow–derived cultured mast cells (BMCMCs) derived from wild-type TRPA1-expressing mice restored anaphylactic responses. In addition, we found that the rapid reductions in oxygen tension in a culture atmosphere triggered the degranulation of BMCMCs derived from wild-type TRPA1-expressing mice but not that of BMCMCs derived from TRPA1-deficient mice. In human LAD2 mast cells, the relative hypoxic stress led to the degranulation, which was suppressed by the addition of a TRPA1 inhibitor. Gradual reductions from hyperoxia to normoxia led to no anaphylactic symptoms. Our results demonstrated that TRPA1-triggered mast cell degranulation is a novel pathway that induces anaphylactic shock without Ag–Ab reactions. These findings introduce a potential role for oxygen in inducing mast cell–dependent anaphylaxis and highlight the need to reconsider chronic pure oxygen therapy for anoxic diseases.

This article is featured in Top Reads, p.2939

Footnotes

  • This work was supported by Ministry of Education, Culture, Sports, Science and Technology/Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research: Start-up Grant 17H06669 (to K.M.), Early-Career Scientists Grant 19K15977 (to K.M.), S Grant 16H06383 (to H.M.), A Grant 19H00969 (to A.T.), and Fostering Joint International Research B Grant 18KK0191 (to A.T.).

  • The online version of this article contains supplemental material.

  • Abbreviations used in this article:

    BMCMC
    bone marrow–derived cultured mast cell
    NP
    4-hydroxy-3-nitrophenylacetyl
    TRPA1
    transient receptor potential ankyrin 1
    WT
    wild-type.

  • Received February 7, 2020.
  • Accepted September 28, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 205 (11)
The Journal of Immunology
Vol. 205, Issue 11
1 Dec 2020
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A Rapid Shift from Chronic Hyperoxia to Normoxia Induces Systemic Anaphylaxis via Transient Receptor Potential Ankyrin 1 Channels on Mast Cells
Kenshiro Matsuda, Peter D. Arkwright, Yasuo Mori, Masa-aki Oikawa, Ryo Muko, Akane Tanaka, Hiroshi Matsuda
The Journal of Immunology December 1, 2020, 205 (11) 2959-2967; DOI: 10.4049/jimmunol.2000149

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A Rapid Shift from Chronic Hyperoxia to Normoxia Induces Systemic Anaphylaxis via Transient Receptor Potential Ankyrin 1 Channels on Mast Cells
Kenshiro Matsuda, Peter D. Arkwright, Yasuo Mori, Masa-aki Oikawa, Ryo Muko, Akane Tanaka, Hiroshi Matsuda
The Journal of Immunology December 1, 2020, 205 (11) 2959-2967; DOI: 10.4049/jimmunol.2000149
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