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Article

Glutenin from the Ancient Wheat Progenitor Is Intrinsically Allergenic as It Can Clinically Sensitize Mice for Systemic Anaphylaxis by Activating Th2 Immune Pathway

by
Rick Jorgensen
1,
Tamil Selvan Arul Arasan
1,
Maya Blanka Srkalovic
1,
Chris Van Antwerp
1,
Perry K. W. Ng
2 and
Venu Gangur
1,*
1
Food Allergy and Immunology Laboratory, Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI 48823, USA
2
Cereal Science Laboratory, Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI 48823, USA
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2024, 25(13), 7324; https://doi.org/10.3390/ijms25137324
Submission received: 14 May 2024 / Revised: 24 June 2024 / Accepted: 27 June 2024 / Published: 3 July 2024
(This article belongs to the Special Issue Molecular Mechanisms and Treatment of Allergic Reactions)

Abstract

Wheat allergy is a major type of food allergy with the potential for life-threatening anaphylactic reactions. Common wheat, Triticum aestivum (hexaploid, AABBDD genome), was developed using tetraploid wheat (AABB genome) and the ancient diploid wheat progenitor (DD genome)-Aegilops tauschii. The potential allergenicity of gluten from ancient diploid wheat is unknown. In this study, using a novel adjuvant-free gluten allergy mouse model, we tested the hypothesis that the glutenin extract from this ancient wheat progenitor will be intrinsically allergenic in this model. The ancient wheat was grown, and wheat berries were used to extract the glutenin for testing. A plant protein-free colony of Balb/c mice was established and used in this study. The intrinsic allergic sensitization potential of the glutenin was determined by measuring IgE response upon transdermal exposure without the use of an adjuvant. Clinical sensitization for eliciting systemic anaphylaxis (SA) was determined by quantifying the hypothermic shock response (HSR) and the mucosal mast cell response (MMCR) upon intraperitoneal injection. Glutenin extract elicited a robust and specific IgE response. Life-threatening SA associated and a significant MMCR were induced by the glutenin challenge. Furthermore, proteomic analysis of the spleen tissue revealed evidence of in vivo Th2 pathway activation. In addition, using a recently published fold-change analysis method, several immune markers positively and negatively associated with SA were identified. These results demonstrate for the first time that the glutenin from the ancient wheat progenitor is intrinsically allergenic, as it has the capacity to elicit clinical sensitization for anaphylaxis via activation of the Th2 pathway in vivo in mice.
Keywords: gluten allergy; ancient wheat; glutenin; life-threatening anaphylaxis; sensitization; Th2 pathway gluten allergy; ancient wheat; glutenin; life-threatening anaphylaxis; sensitization; Th2 pathway

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MDPI and ACS Style

Jorgensen, R.; Arul Arasan, T.S.; Srkalovic, M.B.; Van Antwerp, C.; Ng, P.K.W.; Gangur, V. Glutenin from the Ancient Wheat Progenitor Is Intrinsically Allergenic as It Can Clinically Sensitize Mice for Systemic Anaphylaxis by Activating Th2 Immune Pathway. Int. J. Mol. Sci. 2024, 25, 7324. https://doi.org/10.3390/ijms25137324

AMA Style

Jorgensen R, Arul Arasan TS, Srkalovic MB, Van Antwerp C, Ng PKW, Gangur V. Glutenin from the Ancient Wheat Progenitor Is Intrinsically Allergenic as It Can Clinically Sensitize Mice for Systemic Anaphylaxis by Activating Th2 Immune Pathway. International Journal of Molecular Sciences. 2024; 25(13):7324. https://doi.org/10.3390/ijms25137324

Chicago/Turabian Style

Jorgensen, Rick, Tamil Selvan Arul Arasan, Maya Blanka Srkalovic, Chris Van Antwerp, Perry K. W. Ng, and Venu Gangur. 2024. "Glutenin from the Ancient Wheat Progenitor Is Intrinsically Allergenic as It Can Clinically Sensitize Mice for Systemic Anaphylaxis by Activating Th2 Immune Pathway" International Journal of Molecular Sciences 25, no. 13: 7324. https://doi.org/10.3390/ijms25137324

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