Glycation of a food allergen by the Maillard reaction enhances its T-cell immunogenicity: role of macrophage scavenger receptor class A type I and II.

Abstract

BACKGROUND:

The Maillard reaction occurs between reducing sugars and proteins during thermal processing of foods. It produces chemically glycated proteins termed advanced glycation end products (AGEs). The glycation structures of AGEs are suggested to function as pathogenesis-related immune epitopes in food allergy.

OBJECTIVE:

This study aimed at defining the T-cell immunogenicity of food AGEs by using ovalbumin (OVA) as a model allergen.

METHODS:

AGE-OVA was prepared by means of thermal processing of OVA in the presence of glucose. Activation of OVA-specific CD4(+) T cells by AGE-OVA was evaluated in cocultures with bone marrow-derived murine myeloid dendritic cells (mDCs) as antigen-presenting cells. The uptake mechanisms of mDCs for AGE-OVA were investigated by using inhibitors of putative cell-surface receptors for AGEs, as well as mDCs deficient for these receptors.

RESULTS:

Compared with the controls (native OVA and OVA thermally processed without glucose), AGE-OVA enhanced the activation of OVA-specific CD4(+) T cells on coculture with mDCs, indicating that the glycation of OVA enhanced the T-cell immunogenicity of the allergen. The mDC uptake of AGE-OVA was significantly higher than that of the controls. We identified scavenger receptor class A type I and II (SR-AI/II) as a mediator of the AGE-OVA uptake, whereas the receptor for AGEs and galectin-3 were not responsible. Importantly, the activation of OVA-specific CD4(+) T cells by AGE-OVA was attenuated on coculture with SR-AI/II-deficient mDCs.

CONCLUSION:

SR-AI/II targets AGE-OVA to the MHC class II loading pathway in mDCs, leading to an enhanced CD4(+) T-cell activation. The Maillard reaction might thus play an important role in the T-cell immunogenicity of food allergens.

• Authors: Anne Ilchmann, Sven Burgdorf, Stephan Scheurer, Zoe Waibler, Ryoji Nagai, Anne Wellner, Yasuhiko Yamamoto, Hiroshi Yamamoto, Thomas Henle, Christian Kurts, Ulrich Kalinke, Stefan Vieths, Masako Toda
• Journal: The Journal of allergy and clinical immunology (J Allergy Clin Immunol) Vol. 125 Issue 1 Pg. 175-83.e1-11 (Jan 2010) ISSN: 1097-6825 [Electronic] United States
• PMID: 19864011 (Publication Type: Journal Article, Research Support, Non-U.S. Gov't)
• Copyright: Copyright 2010 American Academy of Allergy, Asthma & Immunology. Published by Mosby, Inc. All rights reserved.

Chemical References

• Allergens
• Glycation End Products, Advanced
• Scavenger Receptors, Class A
• Ovalbumin

Topics

• Allergens (immunology, metabolism)
• Animals
• Antigen Presentation
• Bone Marrow Cells
• CD4-Positive T-Lymphocytes (immunology)
• CD8-Positive T-Lymphocytes (immunology)
• Coculture Techniques
• Dendritic Cells (cytology, immunology)
• Food Hypersensitivity (immunology, physiopathology)
• Glycation End Products, Advanced (immunology, metabolism)
• Lymphocyte Activation
• Maillard Reaction
• Mice
• Mice, Inbred BALB C
• Mice, Inbred C57BL
• Ovalbumin (immunology, metabolism)
• Scavenger Receptors, Class A (metabolism)
• T-Lymphocytes (cytology, immunology)