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. 2023 Feb;13(2):e12222.
doi: 10.1002/clt2.12222.

Soluble IgE-binding factors in the serum of food-allergic patients: Possible pathophysiological role of soluble FcεRI as protective factor

Carolin Steinert  1   2   3 , Sherezade Moñino-Romero  1   2 , Monique Butze  1   2   4 , Jörg Scheffel  1   2 , Sabine Dölle-Bierke  5 , Josefine Dobbertin-Welsch  6 , Kirsten Beyer  6 , Marcus Maurer  1   2 , Sabine Altrichter  1   2   7
Affiliations

Soluble IgE-binding factors in the serum of food-allergic patients: Possible pathophysiological role of soluble FcεRI as protective factor

Carolin Steinert et al. Clin Transl Allergy. 2023 Feb.

Abstract

Background: IgE-mediated food allergy is the result of an aberrant immune response involving the interaction of a food allergen with its specific IgE bound to FcɛRI, the high affinity IgE receptor, on mast cells. Allergen-specific IgE also binds to soluble binding factors, but, their expression and role in food allergy is not well characterized. Here, we assess the prevalence and relevance of soluble IgE binding factors in food allergy and tolerance.

Methods: We measured serum levels of four IgE binding factors, that is, galectin-3, galectin-9, soluble FcɛRI (sFcεRI) and soluble CD23 (sCD23) in 67 adults sensitized to peanut or hazelnut and sFcɛRI in 29 children sensitized to hen's egg. Adults without food allergen sensitization (n = 17) served as healthy controls. We compared serum levels of patients and controls and assessed them, in the former, for links to clinical features including allergy and tolerance.

Results: Serum levels of sFcɛRI and sCD23, but not galectin-3 and galectin-9, significantly differ in food-sensitized patients as compared to healthy controls. A subgroup (28%) of peanut and hazelnut allergic patients had elevated sFcεRI levels, that were associated with higher total and specific IgE levels. Furthermore, sFcεRI levels were significantly higher in tolerant subjects compared to allergics. Among hazelnut allergic patients, those with high sFcεRI levels tolerated the highest protein amounts in the oral food challenge.

Conclusion: sFcɛRI but not sCD23, galectin-3 and galectin-9 might play a role in the pathophysiology of food allergy. Its functional role or use as biomarker should be assessed in further studies.

Keywords: CD23; FcεRI; IgE receptor; food allergy; galectin-3; galectin-9.

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Conflict of interest statement

Carolin Steinert: No conflict of interests. Sherezade Moñino‐Romero: No conflict of interests. Monique Butze: No conflict of interests. Jörg Scheffel: No conflict of interests in relation to this paper. Outside of it JS has conducted studies for, received research funds/was advisor for Allakos, Ascilion, AstraZeneca, CSL Behring, Escient, Novartis, Sanofi, Third Harmonic Bio, ThirdRock, ThermoFisher. Sabine Dölle‐Bierke: No conflict of interests. Josefine Dobbertin‐Welsch: No conflict of interests. Kirsten Beyer: No conflict of interests in relation to this paper. Outside of it, KB received personal fee from Aimmune, Bencard, Danone, DBV, Hipp, Hycor, Jenapharma, Infectopharm, Mylan/Meda, Nestle, Novartis and ThermoFisher. Marcus Maurer: No conflict of interest in relation to this paper. Outside of it, MM is or recently was a speaker and/or advisor for and/or has received research funding from Allakos, Amgen, Aralez, ArgenX, AstraZeneca, Celldex, Centogene, CSL Behring, FAES, Genentech, GIInnovation, GSK, Innate Pharma, Kyowa Kirin, Leo Pharma, Lilly, Menarini, Moxie, Novartis, Pfizer, Roche, Sanofi/Regeneron, Third Harmonic Bio, UCB, and Uriach. Sabine Altrichter: No conflict of interest in relation to this paper. Outside of it, SA has conducted studies for/was advisor for/was speaker for AstraZeneca, Allakos, ALK, CSLBehring, LeoPharma, Moxie, Novartis, Sanofi, Takeda, Thermofisher.

Figures

FIGURE 1
FIGURE 1
Levels of soluble high and low affinity IgE receptors are up and downregulated, respectively, in food allergen‐sensitized subjects. (A) Detection of soluble IgE receptor levels by ELISA in peanut and hazelnut sensitized adults (gray dots) and healthy controls (black dots). Galectin‐3 levels were detected in 55 sensitized patients and 9 healthy controls. Galectin‐9 was measured in 50 sensitized patients and 9 healthy controls. Soluble FcεRI and sCD23 levels were investigated in 63 and 66 sensitized patients, respectively, and 17 healthy controlss. Galectin‐3, Galectin‐9 and sFcεRI levels were measured in ng/ml (left ordinate) and sCD23 levels were measured in U/ml (right ordinate). Undetectable Galectin‐3 and sCD23 levels are depicted as levels <0.01. Mann‐Whitney test was used for group comparison and p‐values <0.05 were considered significant. (B) Detection of sFcεRI levels in 29 hen's egg sensitized children (gray squares).
FIGURE 2
FIGURE 2
Soluble FcεRI serum levels are associated with total IgE levels and peanut allergen sensitization. (A) Correlation between sFcεRI and total IgE in peanut and/or hazelnut sensitized patients. Patient cohort is subdivided in allergic patients (orange, n = 48) and sensitized but tolerant subjects (blue, n = 15). (B) sFcεRI levels and sIgE against peanut positively correlate in peanut allergic patients (n = 36). (C) Correlation between sFcεRI serum levels and wheal size after SPT in peanut allergic patients (n = 30). (A/B/C) Spearman's correlation coefficient was used to measure the strength and direction of association. The dotted line represents the 90% percentile of healthy controls.
FIGURE 3
FIGURE 3
Soluble FcεRI serum levels as predictor of tolerance and allergy. (A) Bar Chart shows individual sFcεRI serum levels of tolerant (blue) and allergic (orange) individuals with median and IQR. Mann‐Whitney test was performed and p‐values < 0.05 were considered significant. (B) Receiver operator characteristics shows the ability of sIgE (gray, AUC = 0.8357) and sFcεRI (black, AUC = 0.6548) to discriminate between sensitization and allergy. (C) Individual sFcεRI serum levels of tolerant (blue) and allergic (orange) individuals according to the allergens (peanut, hazelnut and hen's egg) with median and IQR. Mann‐Whitney test was performed and p‐values < 0.05 were considered significant.
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