A role for early oral exposure to house dust mite allergens through breast milk in IgE-mediated food allergy susceptibility

Akila Rekima, Chrystelle Bonnart, Patricia Macchiaverni, Jessica Metcalfe, Meri K. Tulic, Nicolas Halloin, Samah Rekima, Jon Genuneit, Samantha Zanelli, Samara Medeiros, Debra J. Palmer, Susan Prescott, Valerie Verhasselt

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Background: Successful prevention of food allergy requires the identification of the factors adversely affecting the capacity to develop oral tolerance to food antigen in early life. Objectives: This study sought to determine whether oral exposure to Dermatophagoides pteronyssinus through breast milk affects gut mucosal immunity with long-term effects on IgE-mediated food allergy susceptibility. Methods: Gut immunity was explored in 2-week-old mice breast-fed by mothers exposed to D pteronyssinus, protease-inactivated D pteronyssinus, or to PBS during lactation. We further analyzed oral tolerance to a bystander food allergen, ovalbumin (OVA). In a proof-of-concept study, Der p 1 and OVA levels were determined in 100 human breast milk samples and the association with prevalence of IgE-mediated egg allergy at 1 year was assessed. Results: Increased permeability, IL-33 levels, type 2 innate lymphoid cell activation, and TH2 cell differentiation were found in gut mucosa of mice nursed by mothers exposed to D pteronyssinus compared with PBS. This pro-TH2 gut mucosal environment inhibited the induction of antigen-specific FoxP3 regulatory T cells and the prevention of food allergy by OVA exposure through breast milk. In contrast, protease-inactivated D pteronyssinus had no effect on offspring gut mucosal immunity. Based on the presence of Der p 1 and/or OVA in human breast milk, we identified groups of lactating mothers, which mirror the ones found in mice to be responsible for different egg allergy risk. Conclusions: This study highlights an unpredicted potential risk factor for the development of food allergy, that is, D pteronyssinus allergens in breast milk, which disrupt gut immune homeostasis and prevents oral tolerance induction to bystander food antigen through their protease activity.

Original languageEnglish
Pages (from-to)1416-1429.e11
JournalJournal of Allergy and Clinical Immunology
Volume145
Issue number5
DOIs
Publication statusPublished - May 2020

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