Abstract
Food allergies are abnormal responses to a food triggered by the immune system. The majority of allergenic foods are often subjected to thermal processing before consumption. The Maillard reaction is a non-enzymatic reaction between reducing sugars and compounds with free amino groups such as amino acids and proteins, and takes place during thermal processing and storage of foods. Among many other effects the reaction leads to modification of proteins with various types of glycation structures such as Nε(carboxymethyl)lysine (CML), pentosidine, pyrraline and methylglyoxal-H1, which are collectively called advanced glycation end-products (AGEs). Notably, evidence has accumulated that some glycation structures of AGEs function as immune epitopes. Here we discuss the possible involvement of food allergen AGEs in the pathogenesis of food allergies.
We thank Prof. Thomas Henle (Technische Universität Dresden) and Dr. Stephan Scheurer (Paul-Ehrlich-Institut) for their helpful discussions.
Conflict of interest statement
Authors’ conflict of interest disclosure: The authors stated that there are no conflicts of interest regarding the publication of this article.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
References
1. Rona RJ, Keil T, Summers C, Gislason D, Zuidmeer L, Sodergren E, et al. The prevalence of food allergy: a meta-analysis. J Allergy Clin Immunol 2007;120:638–46.10.1016/j.jaci.2007.05.026Search in Google Scholar PubMed
2. Sicherer SH, Sampson HA. Food allergy. J Allergy Clin Immunol 2010;125:S116–25.10.1016/j.jaci.2009.08.028Search in Google Scholar PubMed
3. Zuidmeer L, Goldhahn K, Rona RJ, Gislason D, Madsen C, Summers C, et al. The prevalence of plant food allergies: a systematic review. J Allergy Clin Immunol 2008;121:1210–8.10.1016/j.jaci.2008.02.019Search in Google Scholar PubMed
4. Henle T. Protein-bound advanced glycation endproducts (AGEs) as bioactive amino acid derivatives in foods. Amino Acids 2005;29:313–22.10.1007/s00726-005-0200-2Search in Google Scholar PubMed
5. Kawakami T, Galli SJ. Regulation of mast-cell and basophil function and survival by IgE. Nat Rev Immunol 2002;2:773–86.10.1038/nri914Search in Google Scholar PubMed
6. Berrens L. The chemical classification of atopic allergens: an attempt at integration. Int Arch Allergy 1971;41;186–98.10.1159/000230517Search in Google Scholar PubMed
7. Berrens L. Neoallergens in heated pecan nut: products of Maillard-type degradation? Allergy 1996;51:277–8.10.1111/j.1398-9995.1996.tb04610.xSearch in Google Scholar PubMed
8. Prausnitz C, Küstner H. Studien über die Ueberempfindlichkeit. Zentralbl Bakteriol 1921;86:160–9.Search in Google Scholar
9. Malanin K, Lundberg M, Johansson SG. Anaphylactic reaction caused by neoallergens in heated pecan nut. Allergy 1995;50:988–91.10.1111/j.1398-9995.1995.tb02513.xSearch in Google Scholar PubMed
10. Simonato B, Pasini G, Giannattasio M, Peruffo AD, De Lazzari F, Curioni A. Food allergy to wheat products: the effect of bread baking and in vitro digestion on wheat allergenic proteins. A study with bread dough, crumb, and crust. J Agric Food Chem 2001;49:5668–73.10.1021/jf0104984Search in Google Scholar PubMed
11. Maleki SJ, Chung SY, Champagne ET, Raufman JP. The effects of roasting on the allergenic properties of peanut proteins. J Allergy Clin Immunol 2000;106:763–8.10.1067/mai.2000.109620Search in Google Scholar PubMed
12. Chung SY, Champagne ET. Association of end-product adducts with increased IgE binding of roasted peanuts. J Agric Food Chem 2001;49:3911–6.10.1021/jf001186oSearch in Google Scholar PubMed
13. Chung SY, Butts CL, Maleki SJ, Champagne ET. Linking peanut allergenicity to the processes of maturation, curing, and roasting. J Agric Food Chem 2003;51:4273–7.10.1021/jf021212dSearch in Google Scholar PubMed
14. Gruber P, Becker WM, Hofmann T. Influence of the Maillard reaction on the allergenicity of rAra h 2, a recombinant major allergen from peanut (Arachis hypogaea), its major epitopes, and peanut agglutinin. J Agric Food Chem 2005;53:2289–96.10.1021/jf048398wSearch in Google Scholar PubMed
15. Vissers YM, Iwan M, Adel-Patient K, Stahl Skov P, Rigby NM, Johnson PE, et al. Effect of roasting on the allergenicity of major peanut allergens Ara h 1 and Ara h 2/6: the necessity of degranulation assays. Clin Exp Allergy 2011;41:1631–42.10.1111/j.1365-2222.2011.03830.xSearch in Google Scholar PubMed
16. Nakamura A, Watanabe K, Ojima T, Ahn DH, Saeki H. Effect of Maillard reaction on allergenicity of scallop tropomyosin. J Agric Food Chem 2005;53:7559–64.10.1021/jf0502045Search in Google Scholar PubMed
17. Nakamura A, Sasaki F, Watanabe K, Ojima T, Ahn DH, Saeki H. Changes in allergenicity and digestibility of squid tropomyosin during the Maillard reaction with ribose. J Agric Food Chem 2006;54:9529–34.10.1021/jf061070dSearch in Google Scholar PubMed
18. Jimenez-Saiz R, Belloque J, Molina E, Lopez-Fandino R. Human immunoglobulin E (IgE) binding to heated and glycated ovalbumin and ovomucoid before and after in vitro digestion. J Agric Food Chem 2011;59:10044–51.10.1021/jf2014638Search in Google Scholar PubMed
19. Taheri-Kafrani A, Gaudin JC, Rabesona H, Nioi C, Agarwal D, Drouet M, et al. Effects of heating and glycation of beta-lactoglobulin on its recognition by IgE of sera from cow milk allergy patients. J Agric Food Chem 2009;57: 4974–82.10.1021/jf804038tSearch in Google Scholar PubMed
20. Iwan M, Vissers YM, Fiedorowicz E, Kostyra H, Kostyra E, Savelkoul HF, et al. Impact of Maillard reaction on immunoreactivity and allergenicity of the hazelnut allergen Cor a 11. J Agric Food Chem 2011;59:7163–71.10.1021/jf2007375Search in Google Scholar PubMed
21. Cucu T, De Meulenaer B, Bridts C, Devreese B, Ebo D. Impact of thermal processing and the Maillard reaction on the basophil activation of hazelnut allergic patients. Food Chem Toxicol 2012;50:1722–8.10.1016/j.fct.2012.02.069Search in Google Scholar PubMed
22. Gruber P, Vieths S, Wangorsch A, Nerkamp J, Hofmann T. Maillard reaction and enzymatic browning affect the allergenicity of Pru av 1, the major allergen from cherry (Prunus avium). J Agric Food Chem 2004;52:4002–7.10.1021/jf035458+Search in Google Scholar
23. Sancho AI, Rigby NM, Zuidmeer L, Asero R, Mistrello G, Amato S, et al. The effect of thermal processing on the IgE reactivity of the non-specific lipid transfer protein from apple, Mal d 3. Allergy 2005;60:1262–8.10.1111/j.1398-9995.2005.00876.xSearch in Google Scholar
24. Blanc F, Vissers YM, Adel-Patient K, Rigby NM, Mackie AR, Gunning AP, et al. Boiling peanut Ara h 1 results in the formation of aggregates with reduced allergenicity. Mol Nutr Food Res 2011;55:1887–94.10.1002/mnfr.201100251Search in Google Scholar
25. Vissers YM, Blanc F, Skov PS, Johnson PE, Rigby NM, Przybylski-Nicaise L, et al. Effect of heating and glycation on the allergenicity of 2S albumins (Ara h 2/6) from peanut. PLoS One 2011;6:e23998.10.1371/journal.pone.0023998Search in Google Scholar
26. Schmidt AM, Vianna M, Gerlach M, Brett J, Ryan J, Kao J, et al. Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J Biol Chem 1992;267:14987–97.10.1016/S0021-9258(18)42137-0Search in Google Scholar
27. Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, et al. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 1992;267:14998–5004.10.1016/S0021-9258(18)42138-2Search in Google Scholar
28. Vlassara H, Li YM, Imani F, Wojciechowicz D, Yang Z, Liu FT, et al. Identification of galectin-3 as a high-affinity binding protein for advanced glycation end products (AGE): a new member of the AGE-receptor complex. Mol Med 1995;1:634–46.10.1007/BF03401604Search in Google Scholar
29. Suzuki H, Kurihara Y, Takeya M, Kamada N, Kataoka M, Jishage K, et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 1997;386:292–6.10.1038/386292a0Search in Google Scholar PubMed
30. Ohgami N, Nagai R, Miyazaki A, Ikemoto M, Arai H, Horiuchi S, et al. Scavenger receptor class B type I-mediated reverse cholesterol transport is inhibited by advanced glycation end products. J Biol Chem 2001;276:13348–55.10.1074/jbc.M011613200Search in Google Scholar PubMed
31. Ohgami N, Nagai R, Ikemoto M, Arai H, Kuniyasu A, Horiuchi S, et al. CD36, a member of the class b scavenger receptor family, as a receptor for advanced glycation end products. J Biol Chem 2001;276:3195–202.10.1074/jbc.M006545200Search in Google Scholar PubMed
32. Burgdorf S, Kurts C. Endocytosis mechanisms and the cell biology of antigen presentation. Curr Opin Immunol 2008;20:89–95.10.1016/j.coi.2007.12.002Search in Google Scholar PubMed
33. Li P, Gregg JL, Wang N, Zhou D, O’Donnell P, Blum JS, et al. Compartmentalization of class II antigen presentation: contribution of cytoplasmic and endosomal processing. Immunol Rev 2005;207:206–17.10.1111/j.0105-2896.2005.00297.xSearch in Google Scholar PubMed
34. Barth H, Schnober EK, Neumann-Haefelin C, Thumann C, Zeisel MB, Diepolder HM, et al. Scavenger receptor class B is required for hepatitis C virus uptake and cross-presentation by human dendritic cells. J Virol 2008;82:3466–79.10.1128/JVI.02478-07Search in Google Scholar PubMed PubMed Central
35. Fioravanti J, Medina-Echeverz J, Berraondo P. Scavenger receptor class B, type I: a promising immunotherapy target. Immunotherapy 2011;3:395–406.10.2217/imt.10.104Search in Google Scholar PubMed
36. Tagliani E, Guermonprez P, Sepúlveda J, López-Bravo M, Ardavín C, Amigorena S, et al. Selection of an antibody library identifies a pathway to induce immunity by targeting CD36 on steady-state CD8 alpha+ dendritic cells. J Immunol 2008;180:3201–9.10.4049/jimmunol.180.5.3201Search in Google Scholar PubMed
37. Ilchmann A, Burgdorf S, Scheurer S, Waibler Z, Nagai R, Wellner A, et al. 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. J Allergy Clin Immunol 2010;125:175–83.10.1016/j.jaci.2009.08.013Search in Google Scholar PubMed
38. Hilmenyuk T, Bellinghausen I, Heydenreich B, Ilchman A, Toda M, Grabbe S, et al. Effects of glycation of the model food allergen ovalbumin on antigen uptake and presentation by human dendritic cells. Immunology 2010;129:437–45.10.1111/j.1365-2567.2009.03199.xSearch in Google Scholar PubMed PubMed Central
39. Ge J, Jia Q, Liang C, Luo Y, Huang D, Sun A, et al. Advanced glycosylation end products might promote atherosclerosis through inducing the immune maturation of dendritic cells. Arterioscler Thromb Vasc Biol 2005;25:2157–63.10.1161/01.ATV.0000181744.58265.63Search in Google Scholar PubMed
40. Price CL, Sharp PS, North ME, Rainbow SJ, Knight SC. Advanced glycation end products modulate the maturation and function of peripheral blood dendritic cells. Diabetes 2004;53:1452–8.10.2337/diabetes.53.6.1452Search in Google Scholar PubMed
41. Kokkola R, Andersson A, Mullins G, Ostberg T, Treutiger CJ, Arnold B, et al. RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol 2005;61:1–9.10.1111/j.0300-9475.2005.01534.xSearch in Google Scholar PubMed
42. Nogueira-Machado JA, Volpe CM, Veloso CA, Chaves MM. HMGB1, TLR and RAGE: a functional tripod that leads to diabetic inflammation. Expert Opin Ther Targets 2011; 15:1023–35.10.1517/14728222.2011.575360Search in Google Scholar PubMed
43. Buttari B, Profumo E, Capozzi A, Facchiano F, Saso L, Sorice M, et al. Advanced glycation end products of human {beta}2glycoproteinI modulate the maturation and function of DCs. Blood 2011;117:6152–61.10.1182/blood-2010-12-325514Search in Google Scholar PubMed
44. Janabi M, Yamashita S, Hirano K, Sakai N, Hiraoka H, Matsumoto K, et al. Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterioscler Thromb Vasc Biol 2000;20:1953–60.10.1161/01.ATV.20.8.1953Search in Google Scholar PubMed
45. El Khoury JB, Moore KJ, Means TK, Leung J, Terada K, Toft M, et al. CD36 mediates the innate host response to beta-amyloid. J Exp Med 2003;197:1657–66.10.1084/jem.20021546Search in Google Scholar PubMed PubMed Central
46. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 2010;11:155–61.10.1038/ni.1836Search in Google Scholar PubMed PubMed Central
47. Baranova IN, Vishnyakova TG, Bocharov AV, Leelahavanichkul A, Kurlander R, Chen Z, et al. Class B scavenger receptor types I and II and CD36 mediate bacterial recognition and proinflammatory signaling induced by Escherichia coli, lipopolysaccharide, and cytosolic chaperonin 60. J Immunol 2012;188:1371–80.10.4049/jimmunol.1100350Search in Google Scholar PubMed PubMed Central
48. Ohnishi K, Komohara Y, Fujiwara Y, Takemura K, Lei X, Nakagawa T, et al. Suppression of TLR4-mediated inflammatory response by macrophage class A scavenger receptor (CD204). Biochem Biophys Res Commun 2011;411:516–22.10.1016/j.bbrc.2011.06.161Search in Google Scholar PubMed
49. Guo L, Song Z, Li M, Wu Q, Wang D, Feng H, et al. Scavenger receptor BI protects against septic death through its role in modulating inflammatory response. J Biol Chem 2009;284:19826–34.10.1074/jbc.M109.020933Search in Google Scholar PubMed PubMed Central
50. Cai L, Wang Z, Meyer JM, Ji A, van der Westhuyzen DR. Macrophage SR-BI regulates LPS-induced pro-inflammatory signaling in mice and isolated macrophages. J Lipid Res 2012;53:1472–81.10.1194/jlr.M023234Search in Google Scholar PubMed PubMed Central
51. Yu H, Ha T, Liu L, Wang X, Gao M, Kelley J, et al. Scavenger receptor A (SR-A) is required for LPS-induced TLR4 mediated NF-κB activation in macrophages. Biochim Biophys Acta 2012;1823:1192–8.10.1016/j.bbamcr.2012.05.004Search in Google Scholar PubMed PubMed Central
52. Wellner A, Nusspickel L, Henle T. Glycation compounds in peanuts. Eur Food Res Technol 2012;234:423–9.10.1007/s00217-011-1649-8Search in Google Scholar
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