Sensitization and elicitation of an allergic reaction to wheat gliadins in mice

Journal of Agricultural and Food Chemistry

Volumn 57, Issue 4, 2009, Pages 1219-1225

  Bodinier, M ^a   Leroy, M ^a   Ah Leung, S ^b   Blanc, F ^b   Tranquet, O ^a   Denery Papini, S ^a   Wal, J M ^b   Adel Patient, K ^b,c  

^a INRA   (France)

^b Bâtiment 136 CEA de Saclay   (France)

^c CEA SACLAY   (France)

Author keywords

Allergy; Balb cJ; Gliadins; IgE; Mouse model; Wheat

Indexed keywords

CYTOKINE; GLIADIN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G;

ADULT; ANIMAL; ANTIBODY SPECIFICITY; ARTICLE; BAGG ALBINO MOUSE; BLOOD; C3H MOUSE; CHEMISTRY; CHILD; DISEASE MODEL; EOSINOPHIL; FEMALE; HUMAN; HYPERSENSITIVITY; IMMUNIZATION; IMMUNOLOGY; MOUSE; SECRETION; TH2 CELL; WHEAT;

ADULT; ANIMALS; ANTIBODY SPECIFICITY; CHILD; CYTOKINES; DISEASE MODELS, ANIMAL; EOSINOPHILS; FEMALE; GLIADIN; HUMANS; HYPERSENSITIVITY; IMMUNIZATION; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; TH2 CELLS; TRITICUM;

MUS; TRITICUM AESTIVUM;

EID: 64549158436     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf802898u     Document Type: Article

References (46)

1. Hischenhuber, C.; Crevel, R.; Jarry, B.; Maki, M.; Moneret-Vautrin, D. A.; Romano, A.; Troncone, R.; Ward, R. Review article: Safe amounts of gluten for patients with wheat allergy or coeliac disease. Aliment. Pharmacol. Ther. 2006, 23 (5), 559-75.
2. Moneret-Vautrin, D. A.; Kanny, G. Update on threshold doses of food allergens: Implications for patients and the food industry. Curr. Opin. Allergy Clin. Immunol. 2004, 4 (3), 215-9.
3. Moneret-Vautrin, D. A.; Morisset, M. Adult food allergy. Curr. Allergy Asthma Rep. 2005, 5 (1), 80-5.
4. Scibilia, J.; Pastorello, E. A.; Zisa, G.; Ottolenghi, A.; Bindslev-Jensen, C.; Pravettoni, V.; Scovena, E.; Robino, A.; Ortolani, C. Wheat allergy: A double-blind, placebo-controlled study in adults. J. Allergy Clin. Immunol. 2006, 117 (2), 433-9.
5. Venter, C.; Pereira, B.; Grundy, J.; Clayton, C. B.; Arshad, S. H.; Dean, T. Prevalence of sensitization reported and objectively assessed food hypersensitivity amongst six-year-old children: A population-based study. Pediatr. Allergy Immunol. 2006, 17 (5), 356-63.
6. Roehr, C. C.; Edenharter, G.; Reimann, S.; Ehlers, I.; Worm, M.; Zuberbier, T.; Niggemann, B. Food allergy and non-allergic food hypersensitivity in children and adolescents. Clin. Exp. Allergy 2004, 34 (10), 1534-41.
7. Battais, F.; Courcoux, P.; Popineau, Y.; Kanny, G.; Moneret-Vautrin, A.; Denery-Papini, S. Food allergy to wheat: Differences in immunoglobulin E-binding proteins as a function of age or symptoms. J. Cereal Sci. 2005, 42 (1), 109-17.
8. Battais, F.; Pineau, F.; Popineau, Y.; Aparicio, C.; Kanny, G; Guerin, L.; Moneret-Vautrin, D. A.; Denery-Papini, S. Food allergy to wheat: Identification of immunogloglin E and immunoglobulin G-binding proteins with sequential extracts and purified proteins from wheat flour. Clin. Exp. Allergy 2003, 33 (7), 962-70.
9. Mittag, D.; Niggemann, B.; Sander, I.; Reese, I.; Fiedler, E. M.; Worm, M.; Vieths, S.; Reese, G Immunoglobulin E-reactivity of wheat-allergic subjects (baker's asthma, food allergy, wheatdependent, exercise-induced anaphylaxis) to wheat protein fractions with different solubility and digestibility. Mol. Nutr. Food Res. 2004, 48 (5), 380-9.
10. Wieser, H.; Seilmeirer, W.; Belitz, H. D. Quantitative determination of gliadin subgroups from different wheat cultivars. J. Cereal Sci. 1994, 19, 149-55.
11. Lehto, M.; Palosuo, K; Varjonen, E.; Majuri, M. L.; Andersson, U.; Reunala, T.; Alenius, H. Humoral and cellular responses to gliadin in wheat-dependent, exercise-induced anaphylaxis. Clin. Exp. Allergy 2003, 33 (1), 90-5.
12. Matsuo, H.; Morita, E.; Tatham, A. S.; Morimoto, K; Horikawa, T.; Osuna, H.; Ikezawa, Z.; Kaneko, S.; Kohno, K; Dekio, S. Identification of the IgE-binding epitope in ω5 gliadin, a major allergen in wheat-dependent exercise-induced anaphylaxis. J. Biol. Chem. 2004, 279 (13), 12135-40.
13. Lauriere, M.; Pecquet, C.; Boulenc, E.; Bouchez-Mahiout, I.; Snegaroff, J.; Choudat, D.; Raison-Peyron, N.; Vigan, M.; Branlard, G Genetic differences in ω-gliadins involved in two different immediate food hypersensitivities to wheat. Allergy 2007, 62 (8), 890-6.
14. Mosmann, T. R.; Cherwinski, H.; Bond, M. W.; Giedlin, M. A.; Coffman, R. L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 1986, 136 (7), 2348-57.
15. Schmidt-Weber, C. B.; Akdis, M.; Akdis, C. A. TH17 cells in the big picture of immunology. J. Allergy Clin. Immunol. 2007, 120 (2), 247-54.
16. Dearman, R. J.; Kimber, I. Determination of protein allergenicity: Studies in mice. Toxicol. Lett. 2001, 120 (1-3), 181-6.
17. Adel-Patient, K; Nahori, M. A.; Proust, B.; Lapa e Silva, J. R.; Créminon, C.; Wal, J.-M.; Vargaftig, B. B. Elicitation of the allergic reaction in β-lactoglobulin-sensitized Balb/c mice: Biochemical and clinical manifestations differ according to the structure of the allergen used for challenge. Clin. Exp. Allergy 2003, 33 (3), 376-85.
18. Adel-Patient, K; Bernard, H.; Ah-Leung, S.; Créminon, C.; Wal, J.-M. Peanut- and cow's milk-specific IgE, Th2 cells and local anaphylactic reaction are induced in Balb/c mice orally sensitized with cholera toxin. Allergy 2005, 60 (5), 658-64.
19. Mine, Y.; Yang, M. Epitope characterization of ovalbumin in BALB/c mice using different entry routes. Biochim. Biophys. Acta 2007, 1774 (2), 200-12.
20. Adel-Patient, K; Creminon, C.; Boquet, D.; Wal, J. M.; Chatel, J. M. Genetic immunisation with bovine β-lactoglobulin cDNA induces a preventive and persistent inhibition of specific anti-BLG IgE response in mice. Int. Arch. Allergy Immunol. 2001, 126 (1), 59-67.
21. Li, X. M.; Schofield, B. H.; Huang, C. K; Kleiner, G I.; Sampson, H. A. A murine model of IgE-mediated cow's milk hypersensitivity. J. Allergy Clin. Immunol. 1999, 103 (2, Part 1), 206-14.
22. Li, X. M.; Serebrisky, D.; Lee, S. Y.; Huang, C. K; Bardina, L.; Schofield, B. H; Stanley, J. S.; Burks, A. W.; Bannon, G A.; Sampson, H. A. A murine model of peanut anaphylaxis: T- and B-cell responses to a major peanut allergen mimic human responses. J. Allergy Clin. Immunol. 2000, 106 (1, Part 1), 150-8.
23. Morafo, V.; Srivastava, K.; Huang, C.-K.; Kleiner, G.; Lee, S.-Y.; Sampson, H. A.; Li, X.-M. Genetic susceptibility to food allergy is linked to differential TH2-TH1 responses in C3H/HeJ and BALB/c mice. J. Allergy Clin. Immunol. 2003, 111 (5), 1122-8.
24. Kim, H.; Lee, S. Y.; Ji, G. E. Timing of bifidobacterium administration influences the development of allergy to ovalbumin in mice. Biotechnol. Lett. 2005, 27 (18), 1361-7.
25. Bashir, M. E.; Louie, S.; Shi, H. N; Nagler-Anderson, C. Toll-like receptor 4 signaling by intestinal microbes influences susceptibility to food allergy. J. Immunol. 2004, 172 (11), 6978-87.
26. Kiyono, H.; McGhee, J. R.; Wannemuehler, M. J.; Michalek, S. M. Lack of oral tolerance in C3H/HeJ mice. J. Exp. Med. 1982, 155 (2), 605-10.
27. Feng, B. S.; Chen, X.; He, S. H.; Zheng, P. Y.; Foster, J.; Xing, Z.; Bienenstock, J.; Yang, P. C. Disruption of T-cell immunoglobulin and mucin domain molecule (TIM) -1/TIM4 interaction as a therapeutic strategy in a dendritic cell-induced peanut allergy model. J. Allergy Clin. Immunol. 2008, 122 (1), 55-61.
28. Kozai, H.; Yano, H; Matsuda, T.; Kato, Y. Wheat-dependent exercise-induced anaphylaxis in mice is caused by gliadin and glutenin treatments. Immunol. Lett. 2006, 102 (1), 83-90.
29. Osborne, T. The Proteins of the Wheat Kernel; Carnegie Institute: Washington DC, 1907; p 84.
30. Nicolas, Y.; Martinant, J. P.; Denery-Papini, S.; Popineau, Y. Analysis of wheat storage proteins by exhaustive sequentile extraction followed by RP-HPLC and nitrogen determination. J. Sci. Food Agric. 1998, 77, 96-102.
31. Clements, R. L. A continuous acetic acid system for polyacrylamide gel electrophoresis of gliadins and other prolamines. Electrophoresis 1988, 9 (2), 90-3.
32. Morisset, M.; Moneret-Vautrin, D. A.; Kanny, G.; Guenard, L.; Beaudouin, E.; Flabbee, J.; Hatahet, R. Thresholds of clinical reactivity to milk, egg, peanut and sesame in immunoglobulin E-dependent allergies: Evaluation by double-blind or single-blind placebo-controlled oral challenges. Clin. Exp. Allergv 2003, 33 (8), 1046-51.
33. Battais, F.; Mothes, T.; Moneret-Vautrin, D. A.; Pineau, F.; Kanny, G.; Popineau, Y.; Bodinier, M.; Denery-Papini, S. Identification of IgE-binding epitopes on gliadins for patients with food allergy to wheat. Allergv 2005, 60 (6), 815-21.
34. Bodinier, M.; Brossard, C.; Triballeau, S.; Morisset, M.; Guerin-Marchand, C.; Pineau, F.; de Coppet, P.; Moneret-Vautrin, D. A.; Blank, U.; Denery-Papini, S. Evaluation of an in vitro mast cell degranulation test in the context of food allergy to wheat. Int. Arch. Allergv Immunol. 2008, 146 (4), 307-20.
35. Adel-Patient, K.; Creminon, C.; Bernard, H.; Clément, G; Négroni, L.; Frobert, Y.; Grassi, J.; Wal, J. M.; Chatel, J. M. Evaluation of a high IgE-responder mouse model of allergy to bovine β-lactoglobulin (BLG) : Development of sandwich immunoassays for total and allergen-specific IgE, IgG1 and IgG2a in BLG-sensitized mice. J. Immunol. Methods 2000, 235 (1-2), 21-32.
36. Bergstedt-Lindqvist, S.; Moon, H. B.; Persson, U.; Moller, G; Heusser, C.; Severinson, E. Interleukin 4 instructs uncommitted B lymphocytes to switch to IgG1 and IgE. Eur. J. Immunol. 1988, 18 (7), 1073-7.
37. Foster, P. S.; Hogan, S. P.; Ramsay, A. J.; Matthaei, K. I.; Young, I. G. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J. Exp. Med. 1996, 183 (1), 195-201.
38. Helm, R. M. Food allergy animal models: An overview. Ann. N. Y. Acad. Sci. 2002, 964, 139-50.
39. Daser, A.; Koetz, K; Batjer, N; Jung, M.; Ruschendorf, F.; Goltz, M.; Ellerbrok, H.; Renz, H.; Walter, J.; Paulsen, M. Genetics of atopy in a mouse model: Polymorphism of the IL-5 receptor a chain. Immunogenetics 2000 51 (8-9), 632-8.
40. Berin, M. C.; Zheng, Y.; Domaradzki, M.; Li, X. M.; Sampson, H. A. Role of TLR4 in allergic sensitization to food proteins in mice. Allergv 2006, 61 (1), 64-71.
41. Yano, H.; Kato, Y.; Matsuda, T. Acute exercise induces gastrointestinal leakage of allergen in lysozyme-sensitized mice. Eur. J. Appl Physiol. 2002,87 (4-5), 358-64.
42. Hsieh, C. S.; Macatonia, S. E.; O'Garra, A.; Murphy, K M. T cell genetic background determines default T helper phenotype development in vitro. J. Exp. Med. 1995, 181 (2), 713-21.
43. Matsuoka, H; Maki, N; Yoshida, S.; Arai, M.; Wang, J.; Oikawa, Y.; Ikeda, T.; Hirota, N; Nakagawa, H.; Ishii, A. A mouse model of the atopic eczema/dermatitis syndrome by repeated application of a crude extract of house-dust mite Dermatophagoides farinae. Allergv 2003, 58 (2), 139-45.
44. Dearman, R. J.; Caddick, H.; Stone, S.; Basketter, D. A.; Kimber, I. Characterization of antibody responses induced in rodents by exposure to food proteins: Influence of route of exposure. Toxicology 2001, 167 (3), 217-31.
45. Pecquet, S.; Pfeifer, A.; Gauldie, S.; Fritsche, R. Immunoglobulin E suppression and cytokine modulation in mice orally tolerized to β-lactoglobulin. Immunology 1999, 96 (2), 278-85.
46. Grun, J. L.; Maurer, P. H. Different T helper cell subsets elicited in mice utilizing two different adjuvant vehicles: The role of endogenous interleukin 1 in proliferative responses. Cell. Immunol. 1989, 121 (1), 134-45.