Trypsin resistance of the major peanut allergen Ara h 6 and allergenicity of the digestion products are abolished after selective disruption of disulfide bonds

Molecular Nutrition and Food Research

Volumn 56, Issue 4, 2012, Pages 548-557

  Hazebrouck, Stéphane ^a   Guillon, Blanche ^a   Drumare, Marie Françoise ^a   Paty, Evelyne ^b   Wal, Jean Michel ^a   Bernard, Hervé ^a  

^a Bâtiment 136 CEA de Saclay   (France)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

2S albumin; Allergenicity; Disulfide bridges; Peanut; Trypsin resistance

Indexed keywords

ALLERGEN; ARA H 6 ALLERGEN, ARACHIS HYPOGAEA; IMMUNOGLOBULIN E; NAPIN; PLANT ANTIGEN; TRYPSIN;

AMINO ACID SEQUENCE; ARTICLE; CHILD; CIRCULAR DICHROISM; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION REGULATION; HUMAN; IMMUNOLOGY; INFANT; MALE; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; PATHOPHYSIOLOGY; PEANUT ALLERGY; PRESCHOOL CHILD; PROTEIN DEGRADATION; SITE DIRECTED MUTAGENESIS;

2S ALBUMINS, PLANT; ALLERGENS; AMINO ACID SEQUENCE; ANTIGENS, PLANT; CHILD; CHILD, PRESCHOOL; CIRCULAR DICHROISM; CLONING, MOLECULAR; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULIN E; INFANT; MALE; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEANUT HYPERSENSITIVITY; PROTEOLYSIS; TRYPSIN;

ARA; ARACHIS HYPOGAEA;

EID: 84859738551     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201100614     Document Type: Article

References (39)

1. Burks, A. W., Peanut allergy. Lancet 2008, 371, 1538-1546.
2. Bock, S. A., Muñoz-Furlong, A., Sampson, H. A., Further fatalities caused by anaphylactic reactions to food, 2001-2006. J. Allergy Clin. Immunol. 2007, 119, 1016-1018.
3. Pumphrey, R. S., Gowland, M. H., Further fatal allergic reactions to food in the United Kingdom, 1999-2006. J. Allergy Clin. Immunol. 2007, 119, 1018-1019.
4. Rona, R. J., Keil, T., Summers, C., Gislason, D. et al., The prevalence of food allergy: a meta-analysis. J. Allergy Clin. Immunol. 2007, 120, 638-646.
5. Sicherer, S. H., Munoz-Furlong, A., Godbold, J. H., Sampson, H. A., US prevalence of self-reported peanut, tree nut, and sesame allergy: 11-year follow-up. J. Allergy Clin. Immunol. 2010, 125, 1322-1326.
6. Hofmann, A. M., Scurlock, A. M., Jones, S. M., Palmer, K. P. et al., Safety of a peanut oral immunotherapy protocol in children with peanut allergy. J. Allergy Clin. Immunol. 2009, 124, 286-291.
7. Jones, S. M., Pons, L., Roberts, J. L., Scurlock, A. M. et al., Clinical efficacy and immune regulation with peanut oral immunotherapy. J. Allergy Clin. Immunol. 2009, 124, 292-300.
8. Thyagarajan, A., Varshney, P., Jones, S. M., Sicherer, S. et al., Peanut oral immunotherapy is not ready for clinical use. J. Allergy Clin. Immunol. 2010, 126, 31-32.
9. Varshney, P., Steele, P. H., Vickery, B. P., Bird, J. A. et al., Adverse reactions during peanut oral immunotherapy home dosing. J. Allergy Clin. Immunol. 2009, 124, 1351-1352.
10. Ferreira, F., Ebner, C., Kramer, B., Casari, G. et al., Modulation of IgE reactivity of allergens by site-directed mutagenesis: potential use of hypoallergenic variants for immunotherapy. FASEB J 1998, 12, 231-242.
11. King, N., Helm, R., Stanley, J. S., Vieths, S. et al., Allergenic characteristics of a modified peanut allergen. Mol. Nutr. Food Res. 2005, 49, 963-971.
12. Burks, A. W., Williams, L. W., Connaughton, C., Cockrell, G. et al., Identification and characterization of a second major peanut allergen, Ara h II, with use of the sera of patients with atopic dermatitis and positive peanut challenge. J. Allergy Clin. Immunol. 1992, 90, 962-969.
13. Chatel, J. M., Bernard, H., Orson, F. M., Isolation and characterization of two complete Ara h 2 isoforms cDNA. Int. Arch Allergy Immunol. 2003, 131, 14-18.
14. Suhr, M., Wicklein, D., Lepp, U., Becker, W. M., Isolation and characterization of natural Ara h 6: evidence for a further peanut allergen with putative clinical relevance based on resistance to pepsin digestion and heat. Mol. Nutr. Food Res. 2004, 48, 390-399.
15. Koppelman, S. J., de Jong, G. A., Laaper-Ertmann, M., Peeters, K. A. et al., Purification and immunoglobulin E-binding properties of peanut allergen Ara h 6: evidence for cross-reactivity with Ara h 2. Clin. Exp. Allergy. 2005, 35, 490-497.
16. Bernard, H., Mondoulet, L., Drumare, M. F., Paty, E. et al., Identification of a new natural Ara h 6 isoform and of its proteolytic product as major allergens in peanut. J. Agric. Food Chem. 2007, 55, 9663-9669.
17. Flinterman, A. E., van, H. E., den Hartog Jager, C. F., Koppelman, S. et al., Children with peanut allergy recognize predominantly Ara h2 and Ara h6, which remains stable over time. Clin. Exp. Allergy. 2007, 37, 1221-1228.
18. Moreno, F. J., Clemente, A., 2S albumin storage proteins: what makes them food allergens? Open. Biochem. J. 2008, 2, 16-28.
19. Shewry, P. R., Napier, J. A., Tatham, A. S., Seed storage proteins: structures and biosynthesis. Plant Cell. 1995, 7, 945-956.
20. Marsh, J., Rigby, N., Wellner, K., Reese, G. et al., Purification and characterisation of a panel of peanut allergens suitable for use in allergy diagnosis. Mol. Nutr. Food Res. 2008, 52 Suppl 2, S272-285.
21. Lehmann, K., Schweimer, K., Reese, G., Randow, S. et al., Structure and stability of 2S albumin-type peanut allergens: implications for the severity of peanut allergic reactions. Biochem. J. 2006, 395, 463-472.
22. Koppelman, S. J., Hefle, S. L., Taylor, S. L., de Jong, G. A., Digestion of peanut allergens Ara h 1, Ara h 2, Ara h 3, and Ara h 6: a comparative in vitro study and partial characterization of digestion-resistant peptides. Mol. Nutr. Food Res. 2010, 54, 1711-1721.
23. Sen, M., Kopper, R., Pons, L., Abraham, E. C. et al., Protein structure plays a critical role in peanut allergen stability and may determine immunodominant IgE-binding epitopes. J. Immunol. 2002, 169, 882-887.
24. Blanc, F., del-Patient, K., Drumare, M. F., Paty, E. et al., Capacity of purified peanut allergens to induce degranulation in a functional in vitro assay: Ara h 2 and Ara h 6 are the most efficient elicitors. Clin. Exp. Allergy. 2009, 39, 1277-1285.
25. Palmer, G. W., Dibbern, D. A., Jr., Burks, A. W., Bannon, G. A. et al., Comparative potency of Ara h 1 and Ara h 2 in immunochemical and functional assays of allergenicity. Clin. Immunol. 2005, 115, 302-312.
26. Albrecht, M., Kuhne, Y., Ballmer-Weber, B. K., Becker, W. M. et al., Relevance of IgE binding to short peptides for the allergenic activity of food allergens. J. Allergy Clin. Immunol. 2009, 124, 328-336, 336.
27. Porterfield, H. S., Murray, K. S., Schlichting, D. G., Chen, X. et al., Effector activity of peanut allergens: a critical role for Ara h 2, Ara h 6, and their variants. Clin. Exp. Allergy. 2009, 39, 1099-1108.
28. Pomes, A., Relevant B cell epitopes in allergic disease. Int. Arch Allergy Immunol. 2010, 152, 1-11.
29. Shreffler, W. G., Lencer, D. A., Bardina, L., Sampson, H. A., IgE and IgG4 epitope mapping by microarray immunoassay reveals the diversity of immune response to the peanut allergen, Ara h 2. J. Allergy Clin. Immunol. 2005, 116, 893-899.
30. Stanley, J. S., King, N., Burks, A. W., Huang, S. K. et al., Identification and mutational analysis of the immunodominant IgE binding epitopes of the major peanut allergen Ara h 2. Arch Biochem. Biophys. 1997, 342, 244-253.
31. Reese, G., Ballmer-Weber, B. K., Wangorsch, A., Randow, S., Vieths, S., Allergenicity and antigenicity of wild-type and mutant, monomeric, and dimeric carrot major allergen Dau c 1: destruction of conformation, not oligomerization, is the roadmap to save allergen vaccines. J. Allergy Clin. Immunol. 2007, 119, 944-951.
32. Clement, G., Boquet, D., Mondoulet, L., Lamourette, P. et al., Expression in Escherichia coli and disulfide bridge mapping of PSC33, an allergenic 2S albumin from peanut. Protein Expr. Purif. 2005, 44, 110-120.
33. Caruelle, D., Grassi, J., Courty, J., Groux-Muscatelli, B. et al., Development and testing of radio and enzyme immunoassays for acidic fibroblast growth factor (aFGF). Anal. Biochem. 1988, 173, 328-339.
34. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S. et al., in: Walker, J. M. (Ed.), The Proteomics Protocols Handbook. Humana Press, Totowa, NJ 2005.
35. Bernard, H., Drumare, M. F., Guillon, B., Paty, E. et al., Immunochemical characterisation of structure and allergenicity of peanut 2S albumins using different formats of immunoassays. Anal. Bioanal. Chem. 2009, 395, 139-146.
36. Takai, T., Yokota, T., Yasue, M., Nishiyama, C. et al., Engineering of the major house dust mite allergen Der f 2 for allergen-specific immunotherapy. Nat. Biotechnol. 1997, 15, 754-758.
37. Toda, M., Reese, G., Gadermaier, G., Schulten, V. et al., Protein unfolding strongly modulates the allergenicity and immunogenicity of Pru p 3, the major peach allergen. J. Allergy Clin. Immunol. 2011.
38. Orlandi, A., Grasso, F., Corinti, S., Marinaro, M. et al., The recombinant major allergen of Parietaria judaica and its hypoallergenic variant: in vivo evaluation in a murine model of allergic sensitization. Clin. Exp. Allergy 2004, 34, 470-477.
39. Mueller, G. A., Gosavi, R. A., Pomés, A., Wünschmann, S. et al., Ara h 2: crystal structure and IgE binding distinguish two subpopulations of peanut allergic patients by epitope diversity. Allergy 2011, 66, 878-885.