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Modulation of ovomucoid-specific oral tolerance in mice fed plant extracts containing lectins

Published online by Cambridge University Press:  09 March 2007

Tanja M. R. Kjær  and
Hanne Frøkiær
Tanja M. R. Kjær
Affiliation:
BioCentrum-DTU, Biochemistry and Nutrition, Technical University of Denmark, Lyngby, Denmark
Hanne Frøkiær*
Affiliation:
BioCentrum-DTU, Biochemistry and Nutrition, Technical University of Denmark, Lyngby, Denmark
*
*Corresponding author: Dr Hanne Frøkiær, fax +45 45886307, email hf@biocentrum.dtu.dk
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Abstract

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We investigated the effect of feeding extracts of four different legumes (red kidney bean (Phaseolus vulgaris), peanut (Arachis hypogaea), soyabean (Glycine max) and pea (Pisum sativum) on the specific immune response against a food protein. Mice were fed ovomucoid and the specific immune response was evaluated. Ovomucoid fed alone resulted in oral tolerance induction measured as both a reduced ovomucoid-specific spleen cell proliferation and antibody response. Feeding kidney-bean extract prevented induction of oral tolerance to ovomucoid measured as spleen cell proliferation in vitro. Pure kidney-bean lectin also prevented oral tolerance induction, suggesting that lectin in the kidney-bean extract caused inhibition of oral tolerance. Parenteral administration (intravenous and intraperitoneal) of pure kidney-bean lectin had no significant influence on oral tolerance induction. Soyabean extract also influenced the immune response against ovomucoid; however, this was not as pronounced as for kidney bean and was only significant (P<0·001) for the antibody response. No effect was observed when pea extract was fed and peanut extract had a non-significant effect on induction of oral tolerance and on the general immune response. Plasma antibodies against kidney-bean lectin, but not against the three other legume lectins, were detected. Our current findings show that other dietary components can influence the specific immune response against food proteins. Various dietary components may thus contribute to the onset of adverse immunological responses.

Keywords

Mucosal immunityOral toleranceLegume lectins
Type
Research Article
Information
British Journal of Nutrition , Volume 88 , Issue 6 , December 2002 , pp. 671 - 680
Copyright
Copyright © The Nutrition Society 2002

References

Banwell, JG, Howard, R, Kabir, I, Adrian, TE, Diamond, RH & Abramowsky, C (1993) Small intestinal growth caused by feeding red kidney bean phytohemagglutinin lectin to rats. Gastroenterology 104, 1669–1677.CrossRefGoogle ScholarPubMed
Benjamin, CF, Figueiredo, RC, Henriques, MG & Barja-Fidalgo, C (1997) Inflammatory and anti-inflammatory effects of soybean agglutinin. Brazilian Journal of Medical and Biological Research 30, 873–881.CrossRefGoogle ScholarPubMed
Bernhisel-Broadbent, J, Dintzis, HM, Dintzis, RZ & Sampson, HA (1994) Allergenicity and antigenicity of chinken egg ovomucoid (Gal d III) compared with ovalbumin (Gal d I) in children with egg allergy and in mice. Journal of Allergy and Clinical Immunology 93, 1047–1059.CrossRefGoogle Scholar
Chilson, OP, Boylston, AW & Crumpton, MJ (1984) Phaseolus vulgaris phytohaemagglutinin (PHA) binds to the human T lymphocyte antigen receptor. EMBO Journal 3, 3239–3245.CrossRefGoogle Scholar
de Aizpurua, HJ & Russell-Jones, GJ (1988) Oral vaccination. Identification of classes of proteins that provoke an immune response upon oral feeding. Journal of Experimental Medicine 167, 440–451.CrossRefGoogle ScholarPubMed
Ebbehoj, K, Dahl, AM, Frokiaer, H, Norgaard, A, Poulsen, LK & Barkholt, V (1995) Purification of egg-white allergens. Allergy 50, 133–141.CrossRefGoogle ScholarPubMed
European Treaty Series (1986) European convention for the protection of vertebrate animals used for experimental and other scientific purposes. Strasbourg: ETS no. 123, 18.III.Google Scholar
Frøkiær, H, Hørlyck, L, Barkholt, V, Sørensen, H & Sørensen, S (1994) Monoclonal antibodies against soybean and pea proteinase inhibitors: characterization and applications for immunoassays in food processing and plant breeding. Food and Agricultural Immunology 6, 63–72.Google Scholar
Frøkiær, H, Jørgensen, TMR, Rosendal, A, Tonsgaard, MC & Barkholt, V (1997) Antinutritional and allergenic proteins. In Antinutrients and Phytochemicals in Food, pp. 44–60 [Shahidi, F, editor]. Washington, DC: American Chemical Society.CrossRefGoogle Scholar
Furrie, E, Turner, MW & Strobel, S (1995) Partial characterization of a circulating tolerogenic moiety which, after a feed of ovalbumin, suppresses delayed-type hypersensitivity in recipient mice. Immunology 86, 480–486.Google ScholarPubMed
Gollapudi, VS & Kind, LS (1975) Enhancement of reaginic antibody formation in the mouse by concanavalin A. International Archives of Allergy and Applied Immunology 48, 94–100.CrossRefGoogle ScholarPubMed
Goncalves, RB & Costa, CP (1995) Isolation of the lectin and an L4 isolectin from Phaseolus vulgaris by affinity chromatography on insoluble ovomucoid. Brazilian Journal of Medicinal and Biological Research 28, 191–194.Google Scholar
Haas, H, Falcone, FH, Schramm, G, Haisch, K, Gibbs, BF, Klaucke, J, Poppelmann, M, Becker, WM, Gabius, HJ & Schlaak, M (1999) Dietary lectins can induce in vitro release of IL-4 and IL-13 from human basophils. European Journal of Immunology 29, 918–927.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Hirahara, K, Hisatsune, T, Nishijima, K, Kato, H, Shiho, O & Kaminogawa, S (1995) CD4 + T cells anergized by high dose feeding establish oral tolerance to antibody responses when transferred in SCID and nude mice. Journal of Immunology 154, 6238–6245.CrossRefGoogle ScholarPubMed
Inada, S, Yoshino, S, Haque, MA, Ogata, Y & Kohashi, O (1997) Clonal anergy is a potent mechanism of oral tolerance in the suppression of acute antigen-induced arthritis in rats by oral administration of the inducing antigen. Cellular Immunology 175, 67–75.CrossRefGoogle ScholarPubMed
Jørgensen, TMR, Mikkelsen, T, Tonsgaard, MC, Rossen, M, Sørensen, S & Frøkiær, H (1998) The influence of plant lectins on immune response against another dietary protein. In Plant Proteins from European Crops. Food and Non-Food Applications, pp. 198–202 [Gueguenand, J and Popineau, Y, editors]. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Knuutila, S & Kovanen, PE (1987) Relative proportions of mitotic T and B cells in PHA-stimulated lymphocyte cultures. Cancer Genetic Cytogenetics 29, 151–154.CrossRefGoogle Scholar
Koninkx, JF, Hendriks, HG, Van Rossum, JM, van den Ingh, TS & Mouwen, JM (1992) Interaction of legume lectins with the cellular metabolism of differentiated Caco-2 cells. Gastroenterology 102, 1516–1523.CrossRefGoogle ScholarPubMed
Kovanen, PE & Knuutila, S (1989) Mitotic cells in different lymphocyte subsets in unfractionated cultures stimulated by phytohaemagglutinin or pokeweed mitogen. Hereditas 110, 69–74.CrossRefGoogle ScholarPubMed
Kruisbeek, AM (1993) Isolation of mouse mononuclear cells. In Current Protocols in Immunology, pp. 3.1.2–3.1.5 [Coligan, JE, Kruisbeek, AM, Magulies, DH, Shevachand, EM and Strober, W, editors]. New York: Greene Publishing and Wiley-InterscienceGoogle Scholar
Kruisbeek, AM & Shevach, EM (1991) Proliferative assays for T cell function. In Current Protocols in Immunology, pp. 3.12.1–3.12.14 [Coligan, JE, Kruisbeek, AM, Magulies, DH, Shevachand, EM and Strober, W, editors]. New York: Greene Publishing and Wiley-Interscience.Google Scholar
Lavelle, EC, Grant, G, Pusztai, A, Pfüller, U & O'Hagan, DT (2000) Mucosal immunogenicity of plant lectins in mice. Immunology 99, 30–37.CrossRefGoogle ScholarPubMed
Lavelle, EC, Grant, G, Pusztai, A, Pfuller, U & O'Hagan, DT (2001) The identification of plant lectins with mucosal adjuvant activity. Immunology 102, 77–86.CrossRefGoogle ScholarPubMed
Leivestad, T, Halvorsen, R, Gaudernack, G & Thorsby, E (1988) Requirements for phytohaemagglutinin activation of resting pure CD4+ and CD8+ T cells. Scandinavian Journal of Immunology 27, 565–572.CrossRefGoogle ScholarPubMed
Liener, IE (1997) Plant lectins: properties, nutritional significance, and function. In Antinutrients and Phytochemicals in Food, pp. 31–43 [Shahidi, F, editor]. Washington, DC: American Chemical Society.CrossRefGoogle Scholar
Martinez, JA, Esparza, ML & Larralde, J (1995) Immunological changes in growing mice fed on diets containing casein or peas (Pisum sativum var. Belinda) as the source of protein. British Journal of Nutrition 73, 87–97.CrossRefGoogle ScholarPubMed
Matsuda, T & Nakamura, R (1993) Molecular structure and immunological properties of food allergens. Trends in Food Science and Technology 4, 289–293.CrossRefGoogle Scholar
Miller, K (1983) The stimulation of human B and T lymphocytes by various lectins. Immunobiology 165, 132–146.CrossRefGoogle Scholar
Montgomery, DC (1991) Design and Analysis of Experiments, 3rd ed., New York: John Wiley & Sons.Google Scholar
Okumura, S, McIntosh, K & Drachman, DB (1994) Oral administration of acetylcholine receptor: effects on experimental myasthenia gravis. Annals of Neurology 36, 704–713.CrossRefGoogle ScholarPubMed
Pusztai, A (1993) Dietary lectins are metabolic signals for the gut and modulate immune and hormone functions. European Journal of Clinical Nutrition 47, 691–699.Google ScholarPubMed
Pusztai, A, Ewen, SW, Grant, G, Peumans, WJ, Van Damme, EJ, Rubio, L & Bardocz, S (1990) Relationship between survival and binding of plant lectins during small intestinal passage and their effectiveness as growth factors. Digestion 46, Suppl. 2, 308–316CrossRefGoogle ScholarPubMed
Pusztai, A, Greer, F & Grant, G (1989) Specific uptake of dietary lectins into the systemic circulation of rats. Biochemical Society Transactions 17, 481–482.CrossRefGoogle Scholar
Restum-Miguel, N & Prouvost-Danon, A (1985) Effects of multiple oral dosing on IgE synthesis in mice: oral sensitization by albumin extracts from seeds of Jack fruit (Artocarpus integrifolia) containing lectins. Immunology 54, 497–504.Google ScholarPubMed
Ryan, JJ (1997) Interleukin-4 and its receptor: essential mediators of the allergic response. Journal of Allergy and Clinical Immunology 99, 1–5.Google ScholarPubMed
Snapper, CM & Paul, WE (1987) Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 236, 944–947.CrossRefGoogle Scholar
Strobel, S (1991) Mechanisms of gastrointestinal immunoregulation and food induced injury to the gut. European Journal of Clinical Nutrition 45, 1–9.Google ScholarPubMed
Strobel, S & Mowat, AM (1998) Immune responses to dietary antigens: oral tolerance. Immunology Today 19, 173–181.CrossRefGoogle ScholarPubMed
Stokes, CR, Newby, TJ & Bourne, FJ (1983) The influence of oral immunization on local and systemic immune responses to heterologous antigens. Clinical and Experimental Immunology, 52,, 399–406.Google ScholarPubMed
Watzl, B, Neudecker, C, Hänsch, GM, Rechkemmer, G & Pool-Zobel, BL (2001) Dietary wheat germ agglutinin modulates ovalbumin-induced immune responses in Brown Norway rats. British Journal of Nutrition 85, 483–490.CrossRefGoogle ScholarPubMed