Mould allergen Alt a 1 spiked with the micronutrient retinoic acid reduces Th2 response and ameliorates Alternaria allergy in BALB/c mice

Allergy. 2024 Aug;79(8):2144-2156. doi: 10.1111/all.16181. Epub 2024 May 31.

Abstract

Background: We investigated the biological function of the mould allergen Alt a 1 as a carrier of micronutrients, such as the vitamin A metabolite retinoic acid (RA) and the influence of RA binding on its allergenicity in vitro and in vivo.

Methods: Alt a 1-RA complex formation was analyzed in silico and in vitro. PBMCs from Alternaria-allergic donors were stimulated with Alt a 1 complexed with RA (holo-Alt a 1) or empty apo-Alt a 1 and analyzed for cytokine production and CD marker expression. Serum IgE-binding and crosslinking assays to apo- and holo-protein were correlated to B-cell epitope analysis. Female BALB/c mice already sensitized to Alt a 1 were intranasally treated with apo-Alt a 1, holo-Alt a 1 or RA alone before measuring anaphylactic response, serum antibody levels, splenic cytokines and CD marker expression.

Results: In silico docking calculations and in vitro assays showed that the extent of RA binding depended on the higher quaternary state of Alt a 1. Holo-Alt a 1 loaded with RA reduced IL-13 released from PBMCs and CD3+CD4+CRTh2 cells. Complexing Alt a 1 to RA masked its IgE B-cell epitopes and reduced its IgE-binding capacity. In a therapeutic mouse model of Alternaria allergy nasal application of holo-Alt a 1, but not of apo-Alt a 1, significantly impeded the anaphylactic response, impaired splenic antigen-presenting cells and induced IL-10 production.

Conclusion: Holo-Alt a 1 binding to RA was able to alleviate Th2 immunity in vitro, modulate an ongoing Th2 response and prevent anaphylactic symptoms in vivo, presenting a novel option for improving allergen-specific immunotherapy in Alternaria allergy.

Keywords: Alternaria alternata; fungal allergy; immunomodulation; retinoic acid; vitamin A.

MeSH terms

  • Allergens* / immunology
  • Alternaria* / immunology
  • Animals
  • Antigens, Fungal* / immunology
  • Cytokines* / metabolism
  • Disease Models, Animal*
  • Female
  • Fungal Proteins / immunology
  • Humans
  • Hypersensitivity / immunology
  • Immunoglobulin E* / immunology
  • Mice
  • Mice, Inbred BALB C*
  • Th2 Cells* / immunology
  • Th2 Cells* / metabolism
  • Tretinoin* / pharmacology

Substances

  • Allergens
  • Tretinoin
  • Immunoglobulin E
  • Cytokines
  • Antigens, Fungal
  • ALTA1 protein, Alternaria alternata
  • Fungal Proteins