Oral administration of bovine whey proteins to mice elicits opposing immunoregulatory responses and is adjuvant dependent

Clinical and Experimental Immunology

Volumn 136, Issue 1, 2004, Pages 40-48

  Afuwape, A O ^a,b   Turner, M W ^a   Strobel, S ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Adjuvant; Cytokine; Oral tolerance; Ovalbumin; Sensitization; Whey protein

Indexed keywords

BETA LACTOGLOBULIN; BOVINE SERUM ALBUMIN; FREUND ADJUVANT; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; OVALBUMIN; VEGETABLE PROTEIN;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BODY WEIGHT; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DELAYED HYPERSENSITIVITY; FEMALE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOREGULATION; MILK; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; TREATMENT OUTCOME; WHEY;

ADMINISTRATION, ORAL; ALUM COMPOUNDS; ANIMALS; CATTLE; CELLS, CULTURED; CYTOKINES; FEMALE; FREUND'S ADJUVANT; HYPERSENSITIVITY, DELAYED; IMMUNE TOLERANCE; IMMUNIZATION; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; LACTOGLOBULINS; LYMPH NODES; MICE; MICE, INBRED BALB C; MILK PROTEINS; OVALBUMIN;

EID: 1842611831     PISSN: 00099104     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2004.02400.x     Document Type: Article

References (48)

1. Strobel S, Mowat AM. Immune responses to dietary antigens: oral tolerance. Immunol Today 1998; 19:173-81.
2. Weiner HL, Friedman A, Miller A et al. Oral tolerance, immunologic mechanisms and treatment of animal and human organ-specific autoimmune diseases by oral administration of autoantigens. Annu Rev Immunol 1994; 12:809-37.
3. Mowat AM, Viney JL. The anatomical basis of intestinal immunity. Immunol Rev 1997; 156:145-66.
4. Peng HJ, Turner MW, Strobel S. The kinetics of oral hyposensitization to a protein antigen are determined by immune status and the timing, dose and frequency of antigen administration. Immunology 1989; 67:425-30.
5. Friedman A, Weiner HL. Induction of anergy or active suppression following oral tolerance is determined by antigen dosage. Proc Natl Acad Sci USA 1994; 91:6688-92.
6. Whitacre CC, Gienapp IE, Orosz CG, Bitar DM. Oral tolerance in experimental autoimmune encephalomyelitis. III. Evidence for clonal anergy. J Immunol 1991; 147:2155-63.
7. Chen Y, Inobe J, Marks R, Gonnella P, Kuchroo VK, Weiner HL. Peripheral deletion of antigen-reactive T cells in oral tolerance. Nature 1995; 376:177-80.
8. Garside P, Steel M, Liew FY, Mowat AM. CD4+ but not CD8+ T cells are required for the induction of oral tolerance. Int Immunol 1995; 7:501-4.
9. Ngan J, Kind LS. Suppressor T cells for IgE and IgG in Peyer's patches of mice made tolerant by the oral administration of ovalbumin. J Immunol 1978; 120:861-5.
10. Strobel S. Epidemiology of food sensitivity in childhood-with special reference to cow's milk allergy in infancy. In: M Burr, ed. Epidemiology of Atopic Diseases, 31st Edn. London: Karger, 1993:119.
11. Host A, Halken S. Epidemiology and prevention of cow's milk allergy. Allergy 1998; 53:111-31.
12. Gortler I, Urbanek R, Forster J. Characterization of antigens and allergens in hypo-allergenic infant formulae. Eur J Pediatr 1995; 154:289-94.
13. Kim SM, Enomoto A, Hachimura S, Yamauchi K, Kaminogawa S. Serum antibody response elicited by a casein diet is directed to only limited determinants of alpha s1-casein. Int Arch Allergy Immunol 1993; 101:260-5.
14. Enomoto A, Konishi M, Hachimura S, Kaminogawa S. Milk whey protein fed as a constituent of the diet induced both oral tolerance and a systemic humoral response, while heat-denatured whey protein induced only oral tolerance. Clin Immunol Immunopathol 1993; 66:136-42.
15. Hachimura S, Fujikawa Y, Enomoto A, Kim SM, Ametani A, Kaminogawa S. Differential inhibition of T and B cell responses to individual antigenic determinants in orally tolerized mice. International Immunol 1994; 6:1791-7.
16. Dahlman-Hoglund A, Dahlgren U, Ahlstedt S, Hanson LA, Telemo E. Bystander suppression of the immune response to human serum albumin in rats fed ovalbumin. Immunology 1995; 86:128-33.
17. Melamed D, Friedman A. In vivo tolerization of Th1 lymphocytes following a single feeding with ovalbumin: anergy in the absence of suppression. Eur J Immunol 1994; 24:1974-81.
18. Khoury SJ, Hancock WW, Weiner HL. Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of transforming growth factor beta, interleukin 4, and prostaglandin E expression in the brain. J Exp Med 1992; 176:1355-64.
19. Melamed D, Friedman A. Direct evidence for anergy in T lymphocytes tolerized by oral administration of ovalbumin. Eur J Immunol 1993; 23:935-42.
20. Miller A, Lider O, Weiner HL. Antigen-driven bystander suppression after oral administration of antigens. J Exp Med 1991; 174:791-8.
21. Miller A, Lider O, Roberts AB, Sporn MB, Weiner HL. Suppressor T cells generated by oral tolerization to myelin basic protein suppress both in vitro and in vivo immune responses by the release of transforming growth factor beta after antigen-specific triggering. Proc Natl Acad Sci USA 1992; 89:421-5.
22. Weiner HL. Oral tolerance, an active immunologic process mediated by multiple mechanisms. J Clin Invest, 2000; 106:935-7.
23. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 1994; 265:1237-40.
24. Chen Y, Inobe J, Weiner HL. Inductive events in oral tolerance in the TCR transgenic adoptive transfer model. Cell Immunol 1997; 178:62-8.
25. Furrie E, Turner MW, Strobel S. Failure of SCID mice to generate an oral tolerogen after a feed of ovalbumin: a role for a functioning gut-associated lymphoid system. Immunology 1994; 83:562-7.
26. Mowat AM, Strobel S, Drummond HE, Ferguson A. Immunological responses to fed protein antigens in mice. I. Reversal of oral tolerance to ovalbumin by cyclophosphamide. Immunology 1982; 45:105-13.
27. Strobel S, Ferguson A. Modulation of intestinal and systemic immune responses to a fed protein antigen, in mice. Gut 1986; 27:829-37.
28. Hirahara K, Hisatsune T, Nishijima K, Kato H, Shiho O, Kaminogawa S. CD4+ T cells anergized by high dose feeding establish oral tolerance to antibody responses when transferred in SCID and nude mice. J Immunol 1995; 154:6238-45.
29. Fritsche R, Pahud JJ, Pecquet S, Pfeifer A. Induction of systemic immunologic tolerance to beta-lactoglobulin by oral administration of a whey protein hydrolysate. J Allergy Clin Immunol 1997; 100:266-73.
30. Pecquet S, Pfeifer A, Gauldie S, Fritsche R. Immunoglobulin E suppression and cytokine modulation in mice orally tolerized to beta-lactoglobulin. Immunology 1999; 96:278-85.
31. McMenamin C, Holt PG. The natural immune response to inhaled soluble protein antigens involves major histocompatibility complex (MHC) class I-restricted CD8+ T cell-mediated but MHC class II-restricted CD4+ T cell-dependent immune deviation resulting in selective suppression of immunoglobulin E production. J Exp Med 1993; 178:889-99.
32. McMenamin C, Pimm C, McKersey M, Holt PG. Regulation of IgE responses to inhaled antigen in mice by antigen-specific gamma delta T cells. Science 1994; 265:1869-71.
33. Peng HJ, Turner MW, Strobel S. Failure to induce oral tolerance to protein antigens in neonatal mice can be corrected by transfer of adult spleen cells. Pediatr Res 1989; 26:486-90.
34. Strobel S, Mowat AM, Drummond HE, Pickering MG, Ferguson A. Immunological responses to fed protein antigens in mice. II. Oral tolerance for CMI is due to activation of cyclophosphamide-sensitive cells by gut-processed antigen. Immunology 1983; 49:451-6.
35. Furrie E, Turner M, Strobel S. The absence of gut flora has no effect on the induction of oral tolerance to ovalbumin. Adv Exp Med Biol 1995; 371B:1239-41.
36. Peng HJ, Turner MW, Strobel S. The generation of a 'tolerogen' after the ingestion of ovalbumin is time-dependent and unrelated to serum levels of immunoreactive antigen. Clin Exp Immunol 1990; 81:510-5.
37. Bruce MG, Strobel S, Hanson DG, Ferguson A. Irradiated mice lose the capacity to 'process' fed antigen for systemic tolerance of delayed-type hypersensitivity. Clin Exp Immunol 1987; 70:611-8.
38. Bruce MG, Ferguson A. Oral tolerance induced by gut-processed antigen. Adv Exp Med Biol 1987; 216A:721-31.
39. Ward PP, Uribe-Luna S, Conneely OM. Lactoferrin and host defense. Biochem Cell Biol, 2002; 80:95-102.
40. Conneely OM. Antiinflammatory activities of lactoferrin. J Am Coll Nutr, 2001; 20:3895-975.
41. Artym J, Zimecki M, Paprocka M, Kruzel ML. Orally administered lactoferrin restores humoral immune response in immunocompromised mice. Immunol Lett, 2003; 89:9-15.
42. Artym J, Zimecki M, Kruzel ML. Reconstitution of the cellular immune response by lactoferrin in cyclophosphamide-treated mice is correlated with renewal of T cell compartment. Immunobiology, 2003; 207:197-205.
43. Zimecki M, Kruzel ML. Systemic or local co-administration of lactoferrin with sensitizing dose of antigen enhances delayed type hypersensitivity in mice. Immunol Lett, 2000; 74:183-8.
44. Actor JK, Hwang SA, Olsen M, Zimecki M, Hunter RL Jr, Kruzel ML. Lactoferrin immunomodulation of DTH response in mice. Int Immunopharmacol, 2002; 2:475-86.
45. Kruzel ML, Harari Y, Chen CY, Castro GA. Lactoferrin protects gut mucosal integrity during endotoxemia induced by lipopolysaccharide in mice. Inflammation, 2000; 24:33-44.
46. Wakabayashi H, Takakura N, Teraguchi S, Tamura Y. Lactoferrin feeding augments peritoneal macrophage activities in mice intraperitoneally injected with inactivated Candida albicans. Microbiol Immunol, 2003; 47:37-43.
47. Mowat AM, Steel M, Worthey EA, Kewin PJ, Garside P. Inactivation of Th1 and Th2 cells by feeding ovalbumin. Ann N Y Acad Sci 1996; 778:122-32.
48. Garside P, Steel M, Worthey EA, Satoskar A, Alexander J, Bluethmann H, Liew FY, Mowat AM. T helper 2 cells are subject to high dose oral tolerance and are not essential for its induction. J Immunol 1995; 154:5649-55.