Spi-B alleviates food allergy by securing mucosal barrier and immune tolerance in the intestine

Food allergy is a type I allergic reaction induced by mast cells and is mainly activated by allergen-specific immunoglobulin (Ig)E. Spi-B is an E26-transformation-specific (Ets) family transcription factor essential for the differentiation and functional maturation of several immune cell subsets, in...

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Main Authors: Narumi Ishihara, Yutaka Nakamura, Kyosuke Yakabe, Seiga Komiyama, Yumiko Fujimura, Tsuneyasu Kaisho, Shunsuke Kimura, Koji Hase
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Allergy
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/falgy.2022.996657/full
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author Narumi Ishihara
Yutaka Nakamura
Yutaka Nakamura
Kyosuke Yakabe
Seiga Komiyama
Yumiko Fujimura
Tsuneyasu Kaisho
Tsuneyasu Kaisho
Shunsuke Kimura
Shunsuke Kimura
Koji Hase
Koji Hase
Koji Hase
author_facet Narumi Ishihara
Yutaka Nakamura
Yutaka Nakamura
Kyosuke Yakabe
Seiga Komiyama
Yumiko Fujimura
Tsuneyasu Kaisho
Tsuneyasu Kaisho
Shunsuke Kimura
Shunsuke Kimura
Koji Hase
Koji Hase
Koji Hase
author_sort Narumi Ishihara
collection DOAJ
description Food allergy is a type I allergic reaction induced by mast cells and is mainly activated by allergen-specific immunoglobulin (Ig)E. Spi-B is an E26-transformation-specific (Ets) family transcription factor essential for the differentiation and functional maturation of several immune cell subsets, including mast cells. However, the possible involvement of Spi-B in food allergy remains unclear. In this study, we found that Spi-B-deficient mice were highly susceptible to food allergy to ovalbumin (OVA), as indicated by the exacerbation of diarrhea and elevation of serum IgE levels. These pathological changes were associated with enhanced mast cell infiltration into the intestinal lamina propria. Activation of mast cells in the intestinal mucosa was observed in Spib−/− mice, even under physiological conditions. Accordingly, Spi-B deficiency increased the translocation of fluorescently labeled dextran from the lumen to the serum, suggesting increased intestinal permeability in Spib−/− mice. Moreover, Spib−/− mice showed defects in oral tolerance induction to OVA. These data illustrate that Spi-B suppresses the development of food allergies by controlling the activation of intestinal mast cells and by inducing immune tolerance to food allergens.
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spelling doaj.art-53b2f1b39ea94fc8a85cc97a3437b6fd2022-12-22T04:07:48ZengFrontiers Media S.A.Frontiers in Allergy2673-61012022-10-01310.3389/falgy.2022.996657996657Spi-B alleviates food allergy by securing mucosal barrier and immune tolerance in the intestineNarumi Ishihara0Yutaka Nakamura1Yutaka Nakamura2Kyosuke Yakabe3Seiga Komiyama4Yumiko Fujimura5Tsuneyasu Kaisho6Tsuneyasu Kaisho7Shunsuke Kimura8Shunsuke Kimura9Koji Hase10Koji Hase11Koji Hase12Division of Biochemistry, Faculty of Pharmacy, School of Pharmaceutical Sciences, Keio University, Tokyo, JapanDivision of Biochemistry, Faculty of Pharmacy, School of Pharmaceutical Sciences, Keio University, Tokyo, JapanDepartment of Microbiology and Immunology, School of Pharmaceutical Sciences, Wakayama Medical University, Wakayama, JapanDivision of Biochemistry, Faculty of Pharmacy, School of Pharmaceutical Sciences, Keio University, Tokyo, JapanDivision of Biochemistry, Faculty of Pharmacy, School of Pharmaceutical Sciences, Keio University, Tokyo, JapanDivision of Biochemistry, Faculty of Pharmacy, School of Pharmaceutical Sciences, Keio University, Tokyo, JapanDepartment of Immunology, Institute of Advanced Medicine, Wakayama Medical University, Wakayama, JapanLaboratory for Inflammatory Regulation, RIKEN Center for Integrative Medical Science (IMS-RCAI), Yokohama, JapanDivision of Biochemistry, Faculty of Pharmacy, School of Pharmaceutical Sciences, Keio University, Tokyo, JapanPrecursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Agency, Saitama, JapanDivision of Biochemistry, Faculty of Pharmacy, School of Pharmaceutical Sciences, Keio University, Tokyo, JapanInstitute of Fermentation Sciences (IFeS), Faculty of Food and Agricultural Sciences, Fukushima University, Fukushima, JapanInternational Research and Development Center for Mucosal Vaccines, The Institute of Medical Science, The University of Tokyo (IMSUT), Tokyo, JapanFood allergy is a type I allergic reaction induced by mast cells and is mainly activated by allergen-specific immunoglobulin (Ig)E. Spi-B is an E26-transformation-specific (Ets) family transcription factor essential for the differentiation and functional maturation of several immune cell subsets, including mast cells. However, the possible involvement of Spi-B in food allergy remains unclear. In this study, we found that Spi-B-deficient mice were highly susceptible to food allergy to ovalbumin (OVA), as indicated by the exacerbation of diarrhea and elevation of serum IgE levels. These pathological changes were associated with enhanced mast cell infiltration into the intestinal lamina propria. Activation of mast cells in the intestinal mucosa was observed in Spib−/− mice, even under physiological conditions. Accordingly, Spi-B deficiency increased the translocation of fluorescently labeled dextran from the lumen to the serum, suggesting increased intestinal permeability in Spib−/− mice. Moreover, Spib−/− mice showed defects in oral tolerance induction to OVA. These data illustrate that Spi-B suppresses the development of food allergies by controlling the activation of intestinal mast cells and by inducing immune tolerance to food allergens.https://www.frontiersin.org/articles/10.3389/falgy.2022.996657/fullSpi-Bfood allergyepithelial barrierIgEoral tolerance
spellingShingle Narumi Ishihara
Yutaka Nakamura
Yutaka Nakamura
Kyosuke Yakabe
Seiga Komiyama
Yumiko Fujimura
Tsuneyasu Kaisho
Tsuneyasu Kaisho
Shunsuke Kimura
Shunsuke Kimura
Koji Hase
Koji Hase
Koji Hase
Spi-B alleviates food allergy by securing mucosal barrier and immune tolerance in the intestine
Frontiers in Allergy
Spi-B
food allergy
epithelial barrier
IgE
oral tolerance
title Spi-B alleviates food allergy by securing mucosal barrier and immune tolerance in the intestine
title_full Spi-B alleviates food allergy by securing mucosal barrier and immune tolerance in the intestine
title_fullStr Spi-B alleviates food allergy by securing mucosal barrier and immune tolerance in the intestine
title_full_unstemmed Spi-B alleviates food allergy by securing mucosal barrier and immune tolerance in the intestine
title_short Spi-B alleviates food allergy by securing mucosal barrier and immune tolerance in the intestine
title_sort spi b alleviates food allergy by securing mucosal barrier and immune tolerance in the intestine
topic Spi-B
food allergy
epithelial barrier
IgE
oral tolerance
url https://www.frontiersin.org/articles/10.3389/falgy.2022.996657/full
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