The Journal of Allergy and Clinical Immunology
Volume 125, Issue 1 , Pages 175-183.e11 , January 2010

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

  • Anne Ilchmann, BSc

      Affiliations

    • Junior Research Group 1 “Experimental Allergology,”, Paul-Ehrlich-Institut, Langen, Germany
    • ,
  • Sven Burgdorf, PhD

      Affiliations

    • Institute for Molecular Medicine and Experimental Immunology, Rheinische Friedrich-Wilhelms-Universität, Bonn, Germany
    • ,
  • Stephan Scheurer, PhD

      Affiliations

    • Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany
    • ,
  • Zoe Waibler, PhD

      Affiliations

    • Junior Research Group 2 “Novel vaccination strategies and early immune responses,” Paul-Ehrlich-Institut, Langen, Germany
    • ,
  • Ryoji Nagai, PhD

      Affiliations

    • Department of Food and Nutrition, Laboratory of Biochemistry & Nutritional Science, Japan Women's University, Tokyo, Japan
    • ,
  • Anne Wellner, BSc

      Affiliations

    • Institute of Food Chemistry, Technische Universität Dresden, Dresden, Germany
    • ,
  • Yasuhiko Yamamoto, MD, PhD

      Affiliations

    • Department of Biochemistry and Molecular Vascular Biology, Kanazawa University Graduate School of Medical Science, Kanazawa, Japan
    • ,
  • Hiroshi Yamamoto, MD, PhD

      Affiliations

    • Department of Biochemistry and Molecular Vascular Biology, Kanazawa University Graduate School of Medical Science, Kanazawa, Japan
    • ,
  • Thomas Henle, PhD

      Affiliations

    • Institute of Food Chemistry, Technische Universität Dresden, Dresden, Germany
    • ,
  • Christian Kurts, MD

      Affiliations

    • Institute for Molecular Medicine and Experimental Immunology, Rheinische Friedrich-Wilhelms-Universität, Bonn, Germany
    • ,
  • Ulrich Kalinke, PhD

      Affiliations

    • TWINCORE, Centre for Experimental and Clinical Infection Research, Hannover, Germany
    • ,
  • Stefan Vieths, PhD

      Affiliations

    • Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany
    • ,
  • Masako Toda, PhD

      Affiliations

    • Junior Research Group 1 “Experimental Allergology,”, Paul-Ehrlich-Institut, Langen, Germany
    • Corresponding Author InformationReprint requests: Masako Toda, PhD, Junior Research Group 1 “Experimental Allergology,” Paul-Ehrlich-Institut, Paul Ehrlich St 59, Langen 63225, Germany.

Received 14 March 2009 ,Revised 6 July 2009 ,Accepted 11 August 2009.

References 

  1. Henle T. Protein-bound advanced glycation endproducts (AGEs) as bioactive amino acid derivatives in foods. Amino Acids. 2005;29:313–322
  2. Malanin K, Lundberg M, Johansson SG. Anaphylactic reaction caused by neoallergens in heated pecan nut. Allergy. 1995;50:988–991
  3. Berrens L. Neoallergens in heated pecan nut: products of Maillard-type degradation?. Allergy. 1996;51:277–278
  4. Scheurer S, Lauer I, Foetisch K, San Miguel Moncin M, Retzek M, Hartz C, et al. Strong allergenicity of Pru av 3, the lipid transfer protein from cherry, is related to high stability against thermal processing and digestion. J Allergy Clin Immunol. 2004;114:900–907
  5. 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;53:2289–2296
  6. Chung SY, Champagne ET. Association of end-products with increased IgE binding of roasted peanuts. J Agric Food Chem. 2001;49:3911–3916
  7. Chung SY, Butts CL, Maleki SJ, Champagne ET. Linking peanut allergenicity to the processes of maturation, curing, and roasting. J Agric Food Chem. 2003;51:4273–4277
  8. 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;25:2157–2163
  9. 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;53:1452–1458
  10. Geijtenbeek TB, van Vliet SJ, Engering A, ‘t Hart BA, van Kooyk Y. Self- and nonself-recognition by C-type lectins on dendritic cells. Annu Rev Immunol. 2004;22:33–54
  11. Burgdorf S, Kurts C. Endocytosis mechanisms and the cell biology of antigen presentation. Curr Opin Immunol. 2008;20:89–95
  12. 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;267:14987–14997
  13. 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;267:14998–15004
  14. 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;1:634–646
  15. 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;386:292–296
  16. Araki N, Higashi T, Mori T, Shibayama R, Kawabe Y, Kodama T, et al. Macrophage scavenger receptor mediates the endocytic uptake and degradation of advanced glycation end products of the Maillard reaction. Eur J Biochem. 1999;230:408–415
  17. 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;276:13348–13355
  18. 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;276:3195–3202
  19. 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;386:292–296
  20. Myint KM, Yamamoto Y, Doi T, Kato I, Harashima A, Yonekura H, et al. RAGE control of diabetic nephropathy in a mouse model: effects of RAGE gene disruption and administration of low-molecular weight heparin. Diabetes. 2006;55:2510–2522
  21. Turner SJ, Jameson SC, Carbone FR. Functional mapping of the orientation for TCR recognition of an H2-Kb-restricted ovalbumin peptide suggests that the beta-chain subunit can dominate the determination of peptide side chain specificity. J Immunol. 1997;159:2312–2317
  22. Gasic-Milenkovic J, Dukic-Stefanovic S, Deuther-Conrad W, Gärtner U, Münch G. Beta-amyloid peptide potentiates inflammatory responses induced by lipopolysaccharide, interferon-gamma and advanced glycation endproducts” in a murine microglia cell line. Eur J Neurosci. 2003;17:813–821
  23. Henle T, Walter H, Krause I, Klostermeyer H. Efficient determination of individual Maillard compounds in heat-treated milk products by amino acid analysis. Int Dairy J. 1991;1:125–135
  24. Förster A, Kühne Y, Henle T. Studies on absorption and elimination of dietary maillard reaction products. Ann N Y Acad Sci. 2005;1043:474–481
  25. Huntington JA, Stein PE. Structure and properties of ovalbumin. J Chromatogr B. 2001;756:189–198
  26. Burgdorf S, Kautz A, Böhnert V, Knolle PA, Kurts C. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science. 2007;316:612–616
  27. Cherayil BJ, Weiner SJ, Pillai S. The Mac-2 antigen is a galecose-specific lectin that binds IgE. J Exp Med. 1989;170:1959–1972
  28. Wada Y. Primary sequence and glycation at lysine-548 of bovine serum albumin. J Mass Spectrom. 1996;31:263–266
  29. Abraham R, Singh N, Mukhopadhyay A, Basu SK, Bal V, Rath S. Modulation of immunogenicity and antigenicity of proteins by maleylation to target scavenger receptors on macrophages. J Immunol. 1995;154:1–8
  30. Abraham R, Choudhury A, Basu SK, Bal V, Rath S. Disruption of T cell tolerance by directing a self antigen to macrophage-specific scavenger receptors. J Immunol. 1997;158:4029–4035
  31. Nicoletti A, Caligiuri G, Tornberg I, Kodama T, Stemme S, Hansson GK. The macrophage scavenger receptor type A directs modified proteins to antigen presentation. Eur J Immunol. 1999;29:512–521
  32. Plüddemann A, Neyen C, Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods. 2007;43:207–217
  33. Platt N, Gordon S. Is the class A macrophage scavenger receptor (SR-A) multifunctional? The mouse's tale. J Clin Invest. 2001;108:649–654
  34. Hughes DA, Fraser IP, Gordon S. Murine macrophage scavenger receptor: in vivo expression and function as receptor for macrophage adhesion in lymphoid and non-lymphoid organs. Eur J Immunol. 1995;25:466–473
  35. Engering A, Geijtenbeek TB, van Vliet SJ, Wijers M, van Liempt E, Demaurex N, et al. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol. 2002;168:2118–2126
  36. Manfredi AA, Capobianco A, Esposito A, De Cobelli F, Canu T, Monno A, et al. Maturing dendritic cells depend on RAGE for in vivo homing to lymph nodes. J Immunol. 2008;180:2270–2275
  37. Dumitriu IE, Baruah P, Bianchi ME, Manfredi AA, Rovere-Querini P. Requirement of HMGB1 and RAGE for the maturation of human plasmacytoid dendritic cells. Eur J Immunol. 2005;35:2184–2190
  38. Hudson BI, Bucciarelli LG, Wendt T, Sakaguchi T, Lalla E, Qu W, et al. Blockade of receptor for advanced glycation endproducts: a new target for therapeutic intervention in diabetic complications and inflammatory disorders. Arch Biochem Biophys. 2003;419:80–88
  39. Akdis M, Blaser K, Akdis CA. T regulatory cells in allergy: novel concepts in the pathogenesis, prevention, and treatment of allergic diseases. J Allergy Clin Immunol. 2005;116:961–968
  40. Akdis M, Verhagen J, Taylor A, Karamloo F, Karagiannidis C, Crameri R, et al. Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells. J Exp Med. 2004;199:1567–1575

 Supported in part by Paul-Ehrlich-Institut and Deutsche Forschungsgemeinschaft (DFG Vi 165/6)

 Disclosure of potential conflict of interest: S. Burgdorf has received research support from the German Research Foundation. S. Vieths is an Associate of the Institute for Product Quality, Berlin; has received honoraria from Phadia, Uppsala, Sweden, and the Food Allergy Resource and Research Program, United States; is a consultant for MARS Chocolate UK Ltd; has received research support from the European Union (EuroPrevall), the German Research Foundation, the Research Fund of the German Food Industry, Monsanto Company, Pioneer Hi-Bred International, the Food Allergy Research & Resource Program, and the European Directorate for the Quality of Medicines and Health Care (EDQM); is an Executive Committee Member of the European Academy of Allergy and Clinical Immunology; is Chairman of the Allergen Standardization Subcommittee and Secretary of the Allergen Nomenclatures Subcommittee of the International Union of Immunological Societies (IUIS); is a Registered Expert with the European Agency for the Evaluation of Medicinal Products (EMEA) and the European Pharmacopoeia Commission; is Chairman of Technical Committee 275 of the European Committee for Standardization (CEN); and is a Member of the Food Allergy Working Group for the German Society for Allergy and Clinical Immunology. The rest of the authors have declared that they have no conflict of interest.

PII: S0091-6749(09)01250-0

doi: 10.1016/j.jaci.2009.08.013

The Journal of Allergy and Clinical Immunology
Volume 125, Issue 1 , Pages 175-183.e11 , January 2010

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