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Allergen-induced NLRP3/caspase1/IL-18 signaling initiate eosinophilic esophagitis and respective inhibitors protect disease pathogenesis

Chandra Sekhar Yadavalli, Sathisha Upparahalli Venkateshaiah, Sandeep Kumar, Hemanth Kumar Kandikattu, Lokanatha Oruganti, Chandrasekhar Kathera, Anil Mishra

2023Communications Biology19 citationsDOIOpen Access PDF

Abstract

Abstract The current report describes a stepwise mechanistic pathway of NLRP3/caspase1/IL-18-regulated immune responses operational in eosinophilic esophagitis (EoE). We show that esophageal epithelial cells and macrophage-derived NLRP3 regulated IL-18 initiate the disease and induced IL-5 facilitates eosinophil growth and survival. We also found that A. fumigatus -exposed IL-18 −/− mice or IL-18-neutralized mice are protected from EoE induction. Most importantly, we present that intravascular rIL-18 delivery to ΔdblGATA mice and CD2-IL-5 mice show the development of EoE characteristics feature like degranulated and intraepithelial eosinophils, basal cell hyperplasia, remodeling and fibrosis. Similarly, we show an induced NLRP3-caspase1-regulated IL-18 pathway is also operational in human EoE. Lastly, we present the evidence that inhibitors of NLRP3 and caspase-1 (MCC950, BHB, and VX-765) protect A. fumigatus - and corn-extract-induced EoE pathogenesis. In conclusion, the current study provides a new understanding by implicating NLRP3/caspase1-regulated IL-18 pathway in EoE pathogenesis. The study has the clinical significance and novel therapeutic strategy, which depletes only IL-18-responsive pathogenic eosinophils, not naïve IL-5-generated eosinophils critical for maintaining innate immunity.

Topics & Concepts

Eosinophilic esophagitisPathogenesisEosinophilImmunologyInnate immune systemInflammasomeImmune systemMedicineInflammationThymic stromal lymphopoietinCancer researchDiseasePathologyAsthmaEosinophilic EsophagitisIL-33, ST2, and ILC PathwaysEosinophilic Disorders and Syndromes
Allergen-induced NLRP3/caspase1/IL-18 signaling initiate eosinophilic esophagitis and respective inhibitors protect disease pathogenesis | Litcius