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Exophilin-5 regulates allergic airway inflammation by controlling IL-33–mediated Th2 responses
Katsuhide Okunishi, … , Susumu Nakae, Tetsuro Izumi
Katsuhide Okunishi, … , Susumu Nakae, Tetsuro Izumi
Published April 2, 2020
Citation Information: J Clin Invest. 2020;130(7):3919-3935. https://doi.org/10.1172/JCI127839.
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Research Article Immunology

Exophilin-5 regulates allergic airway inflammation by controlling IL-33–mediated Th2 responses

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Abstract

A common variant in the RAB27A gene in adults was recently found to be associated with the fractional exhaled nitric oxide level, a marker of eosinophilic airway inflammation. The small GTPase Rab27 is known to regulate intracellular vesicle traffic, although its role in allergic responses is unclear. We demonstrated that exophilin-5, a Rab27-binding protein, was predominantly expressed in both of the major IL-33 producers, lung epithelial cells, and the specialized IL-5 and IL-13 producers in the CD44hiCD62LloCXCR3lo pathogenic Th2 cell population in mice. Exophilin-5 deficiency increased stimulant-dependent damage and IL-33 secretion by lung epithelial cells. Moreover, it enhanced IL-5 and IL-13 production in response to TCR and IL-33 stimulation from a specific subset of pathogenic Th2 cells that expresses a high level of IL-33 receptor, which exacerbated allergic airway inflammation in a mouse model of asthma. Mechanistically, exophilin-5 regulates extracellular superoxide release, intracellular ROS production, and phosphoinositide 3-kinase activity by controlling intracellular trafficking of Nox2-containing vesicles, which seems to prevent the overactivation of pathogenic Th2 cells mediated by IL-33. This is the first report to our knowledge to establish the significance of the Rab27-related protein exophilin-5 in the development of allergic airway inflammation, and provides insights into the pathophysiology of asthma.

Authors

Katsuhide Okunishi, Hao Wang, Maho Suzukawa, Ray Ishizaki, Eri Kobayashi, Miho Kihara, Takaya Abe, Jun-ichi Miyazaki, Masafumi Horie, Akira Saito, Hirohisa Saito, Susumu Nakae, Tetsuro Izumi

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Figure 7

Exophilin-5 deficiency increases the specific IL-5/IL-13 producers, IL-33R–expressing cells, in pathogenic Th2 cells.

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Exophilin-5 deficiency increases the specific IL-5/IL-13 producers, IL-3...
(A) Percentages of pathogenic Th2 cells (Tpath2) in total CD4+ T cells before culture in each mouse. (B) Percentages of cells positive for cell surface IL-33R in pathogenic Th2 cells from each group. CD4+ T cells obtained from the indicated BM-chimeric mice were cultured with and without plate-bound anti-CD3ε Ab (CD3) for 2.5 hours. Then, cells were harvested and stained against cell surface molecules as described in Methods. Zero hours and 2.5 hours indicate before culture and after 2.5 hours of culture, respectively. A representative dot plot after 2.5 hours of culture is shown in B. (C) Cytokine profiles of IL-33R– versus IL-33R+ cells in pathogenic Th2 cells. Each fraction was sorted from splenic CD4+ Th cells of OVA-sensitized Exph5-KO mice, and were cultured at 1.5 × 104 cells/well (one-tenth of the cell number used in the other experiments) on anti-CD3ε Ab–coated wells for 2 days. Next, levels of typical Th2 and Th1 cytokines in the supernatants were determined by ELISA. Data in A–C were obtained from 3 to 5 independent experiments. (D) Expression of Exph5 mRNA in IL-33Rlo versus IL-33Rint/+ fractions. Each fraction was sorted from splenic CD4+ T cells of WT mice, and the levels of Il1rl1 mRNA and Exph5 mRNA in the 2 fractions were determined. Data were obtained from 5 independent experiments. (E) Pearson’s correlation between IL1RL1 and EXPH5 mRNA expression in human Th2-enriched CD4+CCR4+ T cells. Human CD4+CCR4+ T cells, which contain memory-type Th2 cells, were isolated from human peripheral blood, and the mRNA levels relative to ACTB (β-actin) were determined as described in Methods (n = 12 subjects). *P < 0.05; **P < 0.01 by paired (B) or unpaired (C and D) t test.

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