Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-29T07:47:34.510Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterisation of immune responses to food allergens in mice

Published online by Cambridge University Press:  07 March 2007

Rebecca J. Dearman  and
Ian Kimber
Rebecca J. Dearman*
Affiliation:
Syngenta Central Toxicology Laboratory, Alderley Park, Macclesfield, Cheshire SK10 4TJ, UK
Ian Kimber
Affiliation:
Syngenta Central Toxicology Laboratory, Alderley Park, Macclesfield, Cheshire SK10 4TJ, UK
*
*Corresponding author: fax +44 1625 590996, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

There is considerable interest in the development and evaluation of approaches for the safety assessment of novel foods, and in particular in methods for characterisation of allergenic potential. One strategy that has found favour is a tiered approach in which the potential of novel proteins to induce allergic sensitisation is assessed based on considerations of stability of the protein in a simulated gastric juice and homology with, or structural similarity to, known allergens. Linked to such an approach may be evaluation of serological identity with proteins known to cause allergic disease. With the aim of supplementing such approaches with a more direct measurement of potential allergenic activity, attempts have been made to characterise the quality of immune responses elicited in BALB/c strain mice. Such evaluations comprise measurement of IgG and IgE antibody production and (to a lesser extent) of induced cytokine expression patterns. Investigations to date suggest that in mice proteins provoke variable immune responses, those with the potential to cause allergic sensitisation stimulating IgE (and IgG) antibody production. In contrast, non-allergenic, but nevertheless immunogenic, proteins are associated with IgG antibody responses in the absence of marked IgE production. Consistent with the selective activation of selective type 2 T lymphocyte responses, exposure of mice to allergenic protein is associated with preferential expression of IL-4, -5, -10 and -13. Collectively these data suggest that characterisation of the nature of immune response induced in mice by proteins may provide a useful adjunct or alternative to current strategies for the assessment of allergenic potential.

Keywords

Allergic sensitisationAnimal modelsFood allergyIgE antibody
Type
Symposium on ‘Reacting to allergy’
Information
Proceedings of the Nutrition Society , Volume 64 , Issue 4 , November 2005 , pp. 426 - 433
Copyright
Copyright © The Nutrition Society 2005

References

Aalberse, RC (2000) Structural biology of allergens. Journal of Allergy and Clinical Immunology 106, 228–238 CrossRefGoogle ScholarPubMed
Atherton, KT, Dearman, RJ & Kimber, I (2002) Protein allergenicity in mice: a potential approach for hazard identification. Annals of the New York Academy of Sciences 964, 163–172 Google Scholar
Atkinson, HAC, Johnson, IT, Gee, JM, Grigoriadou, F & Miller, K (1996) Brown Norway model of food allergy: effect of plant components on the development of oral sensitization. Food and Chemical Toxicology 34, 27–32 CrossRefGoogle ScholarPubMed
Atkinson, HAC & Miller, K (1994) Assessment of the Brown Norway rat as a suitable model for the investigation of food allergy. Toxicology 91, 281–288 CrossRefGoogle ScholarPubMed
Astwood, JD, Leach, JN & Fuchs, RL (1996) Stability of food allergens to digestion in vitro. Nature Biotechnology 14, 1269–1273 CrossRefGoogle ScholarPubMed
Bae, SJ, Tanaka, Y, Hakugawa, J & Katayama, I (1999) Interleukin-5 involvement in ovalbumin-induced eosinophil infiltration in mouse food allergy model. Journal of Dermatological Science 21, 1–7 Google Scholar
Betts, CJ, Flanagan, BF, Caddick, HT, Dearman, RJ & Kimber, I (2004) Intradermal exposure of BALB/c strain mice to peanut protein elicits a type 2 cytokine response. Food and Chemical Toxicology 42, 1589–1599 CrossRefGoogle ScholarPubMed
Bock, SA, Stoneham, MD & Sampson, HA (2001) Fatalities due to anaphylactic reactions to foods. Journal of Allergy and Clinical Immunology 107, 191–193 CrossRefGoogle ScholarPubMed
Bredehorst, R & David, K (2001) What establishes a protein as an allergen. Journal of Chromatography Biomedical Science Applications 756, 33–40 CrossRefGoogle ScholarPubMed
Bufe, A (1998) The biological function of allergens: relevance for induction of allergic disease. International Archives of Allergy and Immunology 117, 215–219 CrossRefGoogle Scholar
Burks, AW, Cockrell, G, Connaughton, C, Guin, J, Allen, W & Helm, RM (1994) Identification of peanut agglutinin and soybean trypsin inhibitor as minor legume allergens. International Archives of Allergy and Immunology 105, 143–149 CrossRefGoogle ScholarPubMed
Bush, RR & Hefle, SL (1996) Food allergens. Critical Reviews in Food Science and Nutrition 36, S119–S163 CrossRefGoogle ScholarPubMed
Dearman, RJ, Basketter, DA & Kimber, I (1999) Anti-protein antibody isotype distribution: influence of adjuvant. Immunology Letters 69, 102. Abstr.Google Scholar
Dearman, RJ, Caddick, H, Stone, S, Basketter, DA & Kimber, I (2001) Characterization of antibody responses induced in rodents by exposure to food proteins: influence of route of exposure. Toxicology 167, 217–231 CrossRefGoogle ScholarPubMed
Dearman, RJ & Kimber, I (2001) Determination of protein allergenicity: studies in mice. Toxicology Letters 120, 181–186 Google Scholar
Dearman, RJ, Skinner, RA, Herouet, C, Labay, K, Debruyne, E & Kimber, I (2003a) Induction of IgE antibody responses by protein allergens: inter-laboratory comparisons. Food and Chemical Toxicology 41, 1509–1516 Google Scholar
Dearman, RJ, Stone, S, Caddick, HT, Basketter, DA & Kimber, I (2003b) Evaluation of protein allergenic potential in mice: dose-response analyses. Clinical and Experimental Allergy 33, 1586–1594 CrossRefGoogle ScholarPubMed
Ermel, RW, Kock, M, Griffey, SM, Reinhart, GA & Frick, OL (1997) The atopic dog: a model for food allergy. Laboratory Animal Science 47, 40–49 Google Scholar
Finkelman, FD, Katona, IM, Mosmann TR, Coffman (1988a) IFN-gamma regulates the isotypes of Ig secreted during in vivo humoral responses. Journal of Immunology 140, 1022–1027 CrossRefGoogle Scholar
Finkelman, FD, Katona, IM, Urban, JF, Jr, Holmes, J, Ohara, J, Tunge, AS, Sample, JV Paul, WE (1988b) IL-4 is required to generate and sustain in vivo IgE responses. Journal of Immunology 141, 2335–2341 CrossRefGoogle ScholarPubMed
Fogg, MI & Spergel, JM (2003) Management of food allergies. Expert Opinion in Pharmacotherapeutics 4, 1025–1037 Google Scholar
Food and, Agriculture Organization/World & Health Organization (2001) Report of a Joint FAO/WHO Expert Consultation on Allergenicity of Foods Derived from Biotechnology. Rome: FAO/WHO.Google Scholar
Fu, TJ, Abbott, U & Hatzos, C (2002) Digestibility of food allergens and non-allergenic proteins in simulated gastric and intestinal fluids – a comparative study. Journal of Agriculture and Food Chemistry 50, 7154–7160 CrossRefGoogle Scholar
Hefle, SL, Nordlee, JA & Taylor, SL (1996) Allergenic foods. Critical Reviews in Food Science and Nutrition 36, S69–S89 CrossRefGoogle ScholarPubMed
Helm, RM (2003) Food biotechnology: is this good or bad? Implications to allergic diseases. Annals of Allergy Asthma and Immunology 90, 90–98 CrossRefGoogle ScholarPubMed
Helm, RM, Furuta, GT, Stanley, JS, Ye, J, Cockrell, G, Connaughton, C, Simpson, P, Bannon, GA & Burks, AW (2002) A neonatal swine model for peanut allergy. Journal of Allergy and Clinical Immunology 109, 136–142 Google Scholar
Hollingworth, RM, Bjeldanes, LF, Bolger, M, Kimber, I, Meade, BJ, Taylor, SL & Wallace, KB (2003) Toxicological Sciences 71, 2–8 Google Scholar
Hourihane, JOB (1998) Prevalence and severity of food allergy – need for control. Allergy 53, 84 Google Scholar
Huby, RDJ, Dearman, RJ & Kimber, I (2000) Why are some proteins allergens. Toxicological Sciences 55, 84–88 CrossRefGoogle ScholarPubMed
Jeannet-Peter, N, Piletta-Zanin, PA & Hauser, C (1999) Facial dermatitis, contact urticaria, rhinoconjunctivitis, and asthma induced by potato. American Journal of Contact Dermatitis 10, 40–42 Google Scholar
Kanny, G, De Hauteclocque, C, Moneret-Vautrin, DA (1996) Sesame seed and sesame seed oil contain masked allergens of growing importance. Allergy 51, 952 CrossRefGoogle ScholarPubMed
Kimber, I & Dearman, RJ (1997) Cell and molecular biology of chemical allergy. Clinical Reviews in Allergy and Immunology 15, 145–168 Google Scholar
Kimber, I & Dearman, RJ (2002) Factors affecting the development of food allergy. Proceedings of the Nutrition Society 61, 435–439 CrossRefGoogle ScholarPubMed
Knippels, LM & Penninks, AH (2003) Assessment of the allergic potential of food protein extracts and proteins on oral application using the Brown Norway rat model. Environmental Health Perspectives 111, 233–238 CrossRefGoogle ScholarPubMed
Knippels, LMJ, Penninks, AH, Spanhaak, S & Houben, GF (1998) Oral sensitization to food proteins: a Brown Norway rat model. Clinical and Experimental Allergy 28, 368–375 Google Scholar
Knippels, LMJ, van der, Kleij, HPM, Koppelman, SJ, Houben, GF, Penninks, AH Felius, AA (2000) Comparison of antibody responses to hen's egg and cow's milk proteins in orally sensitized rats and food-allergic patients. Allergy 55, 251–258 CrossRefGoogle ScholarPubMed
Lack, G, Chapman, M, Kalsheker, N, King, V, Robinson, C & Venables, K (2002) Report on the potential allergenicity of genetically modified organisms and their products. Clinical and Experimental Allergy 32, 1131–1143 Google ScholarPubMed
Lack, G, Fox, D, Northstone, K, Golding, J & Avon Longitudinal, Study of, Parents and, Children Study Team (2003) Factors associated with the development of peanut allergy in childhood. New England Journal of Medicine 348, 977–985 CrossRefGoogle ScholarPubMed
Li, X-M, Schofield, BH, Huang, C-K, Kleiner, GI & Sampson, HA (1999) A murine model of IgE-mediated cows milk hypersensitivity. Journal of Allergy and Clinical Immunology 103, 206–214 Google Scholar
Li, X-M, Serebrisky, D, Lee, S-Y, Huang, C-K, Bardina, L, Schofield, BH, Stanley, JH, Burks, AW, Bannon, GA & Sampson, HA (2000) A murine model of peanut anaphylaxis: T- and B-cell responses to a major peanut allergen mimic human responses. Journal of Allergy and Clinical Immunology 106, 150–158 CrossRefGoogle Scholar
Lucas, JS, Grimshaw, KE, Collins, K, Warner, JO & Hourihane, JO (2004) Kiwi fruit is a significant allergen and is associated with differing patterns of reactivity in children and adults. Clinical and Experimental Allergy 34, 1115–1121 CrossRefGoogle ScholarPubMed
Metcalfe, DD, Astwood, JD, Townsend, R, Sampson, HA, Taylor, SL & Fuchs, RL (1996) Assessment of the allergenic potential of foods derived from genetically engineered crop plants. Critical Reviews in Food Science and Nutrition 36, S165–S186 CrossRefGoogle ScholarPubMed
Morafo, V, Srivastava, K, Huang, C-K, Kleiner, G, Lee, S-Y, Sampson, HA, Li, X-M (2003) Genetic susceptibility to food allergy is linked to differential Th1-Th2 responses in C3H-HeJ and BALB/c mice. Journal of Allergy and Clinical Immunology 111, 1122–1128 CrossRefGoogle Scholar
Mosmann, TR, Cherwinski, H, Bond, MW, Giedlin, MA & Coffman, RL (1986) Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of Immunology 136, 2348–2357 CrossRefGoogle ScholarPubMed
Mosmann, TR & Coffman, RL (1989) Heterogeneity of cytokine secretion patterns and functions of helper T cells. Advances in Immunology 46, 111–145 Google Scholar
Mosmann, TR, Li, L & Sad, S (1997) Functions of CD8 T-cell subsets secreting different cytokine patterns. Seminars in Immunology 9, 87–92 Google Scholar
Mosmann, TR & Sad, S (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunology Today 17, 138–146 CrossRefGoogle ScholarPubMed
Pumphrey, RS (2000) Lessons for management of anaphylaxis from a study of fatal reactions. Clinical and Experimental Allergy 30, 1144–1150 CrossRefGoogle ScholarPubMed
Sampson, HA (1988) IgE-mediated food intolerance. Journal of Allergy and Clinical Immunology 81, 495–504 CrossRefGoogle ScholarPubMed
Sampson, HA (2004) Update on food allergy. Journal of Allergy and Clinical Immunology 113, 805–819 CrossRefGoogle ScholarPubMed
Selgrade, MK, Kimber, I, Goldman, L & Germolec, DR (2003) Assessment of allergenic potential of genetically modified foods: an agenda for future research. Environmental Health Perspectives 111, 1140–1141 Google Scholar
Sloane, D & Sheffer, A (2001) Oral allergy syndrome. Allergy and Asthma Proceedings 22, 321–325 Google ScholarPubMed
Spergel, JM, Beausoleil, JL & Pawlowski, NA (2000) Resolution of childhood peanut allergy. Annals of Allergy Asthma and Immunology 85, 473–476 CrossRefGoogle ScholarPubMed
Taylor, SL & Hefle, SL (2001) Will genetically modified foods be allergenic. Journal of Allergy and Clinical Immunology 107, 765–771 CrossRefGoogle ScholarPubMed
Teuber, SS, Del, Val, G, Morigasaki, S, Jung, HR, Eisele, PH, Frick, OL Buchanan, BB (2002) The atopic dog as a model of peanut and tree nut food allergy. Journal of Allergy and Clinical Immunology 110, 921–927 CrossRefGoogle Scholar
Thomas, K, Aalbers, M, Bannon, GA, Bartels, M, Dearman, RJ, Esdaile, DJ et al. (2004) A multi-laboratory evaluation of a common in vitro pepsin digestion assay protocol used in assessing the safety of novel proteins. Regulatory Toxicology and Pharmacology 39, 87–98 CrossRefGoogle ScholarPubMed
Turcanu, V, Maleki, SJ & Lack, G (2003) Characterization of lymphocyte responses to peanuts in normal children, peanut-allergic children, and allergic children who acquired tolerance to peanuts. Journal of Clinical Investigation 111, 1065–1072 CrossRefGoogle ScholarPubMed
van Wijk, F, Hartgring, S, Koppelman, SJ, Pieters, R & Knippels, LM (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. Clinical and Experimental Allergy 34, 1422–1428 CrossRefGoogle Scholar
Young, E, Stoneham, MD, Petruckevitch, A, Barton, J & Rona, R (1994) A population study of food intolerance. Lancet 343, 1127–1130 Google Scholar