Differences in allergenic potential of food extracts following oral exposure in mice reflect differences in digestibility: Potential approaches to safety assessment

Toxicological Sciences

Volumn 102, Issue 1, 2008, Pages 100-109

  Bowman, Christal C ^a   Selgrade, Maryjane K ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Allergenicity; Biotechnology; Food allergy

Indexed keywords

CHOLERA TOXIN; EGG WHITE; FOOD ANTIGEN; IMMUNOGLOBULIN E; PEPSIN A;

ALLERGENICITY; ALLERGY TEST; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; BRAZIL NUT; CONTROLLED STUDY; DIGESTION; EGG ALLERGY; FEMALE; FOOD ALLERGY; FOOD INTAKE; FOOD SAFETY; IMMUNOLOGICAL TOLERANCE; MOUSE; NONHUMAN; NUT ALLERGY; PEANUT; RAT; RISK ASSESSMENT; SPINACH;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, ORAL; ANIMALS; CHOLERA TOXIN; DIETARY PROTEINS; DIGESTION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; EGG HYPERSENSITIVITY; FEMALE; FOOD HYPERSENSITIVITY; FOOD, GENETICALLY MODIFIED; IMMUNE TOLERANCE; IMMUNOGLOBULIN E; INJECTIONS, SUBCUTANEOUS; MICE; MICE, INBRED C3H; NUT HYPERSENSITIVITY; PEANUT HYPERSENSITIVITY; PEPSIN A; PROTEIN DENATURATION; RISK ASSESSMENT; TIME FACTORS;

ANIMALIA; ARACHIS HYPOGAEA; BERTHOLLETIA EXCELSA; MUS; SPINACIA OLERACEA;

EID: 39149113114     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfm288     Document Type: Article

References (41)

1. Adel-Patient, K., Bernard, H., Ah-Leung, S., Creminoh, C., and Wal, J. M. (2005). 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 60, 658-664.
2. Akiyama, H., Teshima, R., Sakushima, J. I., Okunuki, H., Goda, Y., Sawada, J. I., and Toyoda, M. (2001). Examination of oral sensitization with ovalbumin in Brown Norway rats and three strains of mice. Immunol. Lett. 78, 1-5.
3. AAAAI (2005). The Allergy Report, Volume 3. The American Academy of Allergy, Asthma & Immunology.
4. Astwood, J. D., Leach, J. N., and Fuchs, R. L. (1996). Stability of food allergens to digestion in vitro. Nat. Biotechnol. 14, 1269-1273.
5. Bannon, G., Fu, T. J., Kimber, I., and Hinton, D. M. 9W3). Protein digestibility and relevance to allergenicity. Environ. Health Perspect. 111, 1122-1124.
6. Betts, C. J., Flanagan, B. F., Caddick, H. T., Dearrman, R. J., and Kimber, I. (2004). Intradermal exposure of BALB/c strain mice to peanut protein elicits a type 2 cytokine response. Food Chem. Toxicol. 42, 1589-1599.
7. Bowman, C. C., and Selgrade, M. S. (200). Digestibility and oral tolerance in a mouse model for food allergy. The Toxicologist 96(Suppl.), 1131 (Abstract).
8. Bucchini, L., and Goldman, L. R. (2002). Starlink com: A risk analysis. Environ. Health Perspect. 110, 5-13.
9. Christensen, H. R., Kjaer, T. M., and Frokiaer, H. (2003). Low-dose oral tolerance due to antigen in the diet suppresses differentially the cholera toxin-adjuvantized IgE, IgA and IgG response. Int. Arch. Allergy Immunol. 132, 248-257.
10. Dearman, R. J., Caddick, H., Stone, S., Basketter, D. A., and Kimber, I. (2001). Characterization of antibody responses induced in rodents by exposure to food proteins: Influence of route of exposure. Toxicology 167, 217-231.
11. Dearman, R. J., Caddick, H., Stone, S., Kenna, J. G., Basketter, D. A., and Kimber, I. (2002). Immunogenic properties of rapidly digested food proteins following gavage exposure of mice: A comparison of ovalbumin with a potato acid phosphatase preparation. Food Chem. Toxicol. 40, 625-633.
12. Dearman, R. J., and Kimber, I. (2001). Determination of protein allergenicity: Studies in mice. Toxicol. Lett. 120, 181-186.
13. Dearman, R. J., Skinner, R. A., Herouet, C., Labay, K., Debruyne, E., and Kimber, I. (2003). Induction of IgE antibody responses by protein allergens: Inter-laboratory comparisons. Food Chem. Toxicol. 41 1509-1516.
14. Dioun, A. F., Harris, S. K., and Hibberd, P. L. (2003). Is maternal age at delivery related to childhood food allergy? Pediatr. Allergy Immunol. 14, 307-311.
15. FAO/WHO (2003). Codex alimentarius guideline for conduct of food safety assessment of foods derived from recombinant-DNA plants; Appendix IV: Annex on assessment of possible allergenicity. In Joint FAO/WHO Food Standard Programme (C. A. Commission, Ed.), pp. 47-60. Codex Alimentarius Commission, Rome, Italy.
16. Fischer, R., McGhee, J. R., Vu, H. L., Atkinson, T. P., Jackson, R. J., Tome, D., and Boyaka, P. N. (2005). Oral and nasal sensitization promote distinct immune responses and lung reactivity in a mouse model of peanut allergy. Am. J. Pathol. 167, 1621-1630.
17. Fu, T. J. (2002). Digestion stability as a criterion for protein allergenicity assessment. Ann. N. Y. Acad. Sci. 964, 99-110.
18. Fu, T. J., Abbott, U. R., And Hatzos, C. (2002). Digestibility of food allergens and nonallergenic proteins in simulated gastric fluid and simulated intestinal fluid a comparative study. J. Agric. Food Chem. 50, 7154-7100.
19. Gaudry, P. A., Fernandes, J., Reish, R., Roux, K. H., Sathe, S. K., Teuber,.S. S., Reese, G., and Lehrer, S. B. (2004). Murine IgE and IgG antibody responses to allergen ic and non-allergenic foods: Potential model for allergenicity assessment of foods in man. J. Allergy Clin. Immunol. 113(Suppl.), 234 (Abstract).
20. Herman, R. A., Storer, N. P., and Gao, Y. (2006). Digestion Assays in allergenicity assessment of transgenic proteins. Environ. Health Perspect. 114, 1154-1157.
21. Hilton, J, Dearman, R. J., Sattar, N., Basketter, D. A., and Kimber, L. (1997). Characteristics of antibody responses induced in mice by protein allergens. Food Chem. Toxicol. 35, 1209-1218.
22. Kimber, I., Betts, C. J, and Dearman, R. J. (2003). Assessment of the allergenic potential of proteins. Toxicol. Lett. 140-141, 297-302.
23. Knippels, L. M., Houben, G. F., Spanhaak,.S., and Penninks, A. H. (1999). An oral sensitization model in Brown Norway rats to screen for potential allergenicity of food proteins. Methods 19, 78-82.
24. Knippels, L. M., Penninks, A. H., Spanhaak S., and Houben, G. F. (1998). Oral sensitization to food proteins: A Brown Norway rat model. Clin. Exp. Allergy 28, 368-375.
25. Kroghsbo, S., Christensen, H. R., and Frokiaer, H. (2003). Experimental parameters differentially affect the humoral response of the cholera-toxin-based murine model of food allergy. Int. Arch. Allergy Immunol. 131, 256-263.
26. Li, X. M., Schofield, B. H., Huang, C. K., Kleiner, G. I., and Sampson, H. A. (1999). A murine model of IgE-mediated cow's milk hypersensitivity. J. Allergy Clin. Immunol. 103, 206-214.
27. 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., and Sampson, H. A. (2000). A routine model of peanut anaphylaxis: T- and B-cell responses to a major peanut allergen mimic human responses. J Allergy Clin. Immunol. 106, 150-158.
28. Marinaro, M., Staats, H. F., Hiroi, T., Jackson, R. I., Coste, M., Boyaka, P. N., Okahashi, N., Yamamoto, M., Kiyono, H., Bluethmann, H., et al. (1995). Mucosal adjuvant effect of cholera toxin in mice results from induction of T helper 2 (TH2) cells and IL-4. J. Immunol. 155, 4621-4629.
29. Morafo, V., Srivastava, K., Huang, C. K., Kleiner, G., Lee, S. Y., Sampson, H. A., and Li, A. M. (200). Genetic susceptibility to food allergy is linked to differential TH2-TH1 responses in C3H/HeJ and BALB/ c mice. J. Allergy Clin. Immunol. 111, 1122-1128.
30. Moreno, F. J., Mellon, F. A., Wickham, M. S., Bottrill, A. R., and Mills, E. N. (2005). Stability of the major allergen Brazil nut ZS albumin (Ber e 1) to physiologically relevant in vitro gastrointestinal digestion. FEBS. J. 272, 341-352.
31. Navuluri, L., Parvataneni, S., Hassan, H., Birmingham, N. P., Kelly, C., and Gangur, V. (2006). Allergic and anaphylactic response to sesame seeds in mice: Identification of Ses i 3 and basic subunit of 11s globulins as allergens. Int. Arch. Allergy Immunol. 140, 270-276.
32. NIAID (2006). Report of the NIH Expert Panel on Food Allergy Research National Institute of Allergy and Infectious Diseases, National Institutes of Health.
33. Reese, G., Schicktanz, S., Randow, S., Lehrer, S. B., and Vieths, S. (2004). An animal model for shrimp allergy: The influence of genetic background and adjuvant on die allergen-specific IgE response. J. Allergy Clin. Immunol. 113(Suppl.), 233 (Abstract).
34. Reese, G., Viebranz, J., Leong-Kee, S. M., Plante, M., Lauer, I., Randow, S., Moncin, M. S., Ayuso, R., Lehrer, S. B., and Vieths, S. (2005). Reduced allergenic potency of VR9-R1, a mutant of the major shrimp allergen Pen a 1 (tropomyosin). J. Immunol. 175, 8354-8364.
35. Saklayen, M. G., Pesce, A. J., Pollak, V. E., and Michael, J. G. (1984). Kinetics of oral tolerance: Study of variables affecting tolerance induced by oral administration of antigen. Int. Arch. Allergy Appl. Immunol. 73, 5-9.
36. Sicherer, S. H., Munoz-Furlong, A., and Sampson, H. A. (2003). Prevalence of peanut and tree nut allergy in the United States determined by means of a random digit dial telephone survey: A 5-year follow-up study. J. Allergy Clin. Immunol. 112, 1203-1207.
37. Snider, D. P., Marshall, J. S., Perdue, M. H., and Liang, H. (1994). Production of IgE antibody and allergic sensitization of intestinal and peripheral tissues after oral immunization with Protein Ag and cholera toxin. J. Immunol. 153, 647-657.
38. Takagi, K., Teshima, R., Okunuki, H., and Sawada, J. (2003). Comparative study of in vitro digestibility of food proteins and effect of preheating on the digestion. Biol. Pharm. Bull. 26, 969-973.
39. Thomas, K., Herouet, C., Bannon, G., Ladics, 0., MacIntosh, S., Privalle, L., and Woolhiser, M. (2005). Evaluation of mouse models for assessing the allergenic potential of proteins. The Toxicologist 84(Suppl.), 1307 (Abstract).
40. van Wijk, F., Hartgring, S., Koppelman, S. J., Pieters, R., and Knippels, L. M. (2004). Mixed antibody and T cell responses to peanut and the peanut allergens Ara h 1, Ara h 2, Ara h 3 and Ara h 6 in an oral sensitization model. Clin. Exp. Allergy 34, 1422-1428.
41. van Wijk, F., Nierkens, S., Hassing, I., Feijen, M., Koppelman, S. I., de Jong, G. A., Pieters, R., and Knippels, L. M. (2005). The effect of the food matrix on in vivo immune responses to purified peanut allergens. Toxicol. Sci. 86, 333-341.