Oral tolerance in the treatment of inflammatory autoimmune diseases

Inflammation Research

Volumn 48, Issue 3, 1999, Pages 106-119

  Wardrop III, R M ^a   Whitacre, C C ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Autoimmune disease; Immunotherapy; Mucosal tolerance; Oral tolerance

Indexed keywords

ANTIGEN;

ALLERGY; ANIMAL MODEL; AUTOIMMUNE DISEASE; CLONAL ANERGY; DIABETES MELLITUS; EXPERIMENTAL MODEL; IMMUNOTHERAPY; INFLAMMATORY DISEASE; MULTIPLE SCLEROSIS; REVIEW; RHEUMATOID ARTHRITIS; UVEITIS;

ADMINISTRATION, ORAL; ANIMALS; ANTIGENS; AUTOIMMUNE DISEASES; CLINICAL TRIALS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, MUCOSAL;

EID: 0033034410     PISSN: 10233830     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000110050433     Document Type: Review

References (154)

1. van Noort JM, van Sechel A, Boon J, Boersma WJ, Polman CH, Lucas CJ. Minor myelin proteins can be major targets for peripheral blood T cells from both multiple sclerosis patients and healthy subjects. J Neuroimmunol 1993;46:67-72.
2. Hermans G, Stinissen P, Hauben L, Van den Berg-Loonen E, Raus J, Zhang J. Cytokine profile of myelin basic protein-reactive T cells in multiple sclerosis and healthy individuals. Ann Neurol 1997;42:18-27.
3. Wells HG. Studies on the chemistry of anaphylaxis. III. Experiments with isolated proteins, especially those of hen's egg. J Infect Dis 1911;9:147-51.
4. Chase M. Inhibition of experimental drug allergy by prior feeding of the sensitizing agent. Proc Soc Exp Biol Med 1946;61:257-9.
5. Mowat AM. The regulation of immune responses to dietary protein antigens. Immunol Today 1987;8:93.
6. Strobel S, Mowat AM. Immune responses to dietary antigens: oral tolerance. Immunol Today 1998;19:173-81.
7. Thompson HS, Staines NA. Gastric administration of type II collagen delays the onset and severity of collagen-induced arthritis in rats. Clin Exp Immunol 1986;64:581-6.
8. Nagler-Anderson C, Bober LA, Robinson ME, Siskind GW, Thorbecke GJ. Suppression of type II collagen-induced arthritis by intragastric administration of soluble type II collagen. Proc Natl Acad Sci USA 1996;83:7443-6.
9. Bitar DM, Whitacre CC. Suppression of experimental autoimmune encephalomyelitis by the oral administration of myelin basic protein. Cell Immunol 1988;112:364-70.
10. Higgins PJ, Weiner HL. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic protein and its fragments. J Immunol 1988;140:440-5.
11. Weiner HL. Oral tolerance: immune mechanisms and treatment of autoimmune diseases. Immunol Today 1997;18:335-43.
12. Martin R, McFarland HF. Immunological aspects of experimental allergic encephalomyelitis and multiple sclerosis. Crit Rev Clin Lab Sci 1995;32:121-82.
13. Miller A, Lider O, Weiner HL. Antigen-driven bystander suppression after oral administration of antigens. J Exp Med 1991;174:791-8.
14. + T lymphocytes. J Immunol 1989;142:748-52.
15. Chen Y, Inobe J, Weiner HL. Induction of oral tolerance to myelin basic protein in CDS-depleted mice: both CD4+ and CD8+ cells mediate active suppression. J Immunol 1995;155:910-6.
16. 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.
17. Gienappl I, Cox K, Javed N, Whitacre C. Oral tolerance in aotuimmune encephalomyelitis. In vivo reversal of anergy. Ann NY Acad Sci 1996;778:382-3.
18. Miller A, Lider O, al-Sabbagh A, Weiner HL. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic protein. V. Hierarchy of suppression by myelin basic protein from different species. J Neuroimmunol 1992;39:243-50.
19. Javed NH, Gienapp IE, Cox KL, Whitacre CC. Exquisite peptide specificity of oral tolerance in experimental autoimmune encephalomyelitis. J Immunol 1995;155:1599-605.
20. Brod SA, al-Sabbagh A, Sobel RA, Hafler DA, Weiner HL. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin antigens: IV. Suppression of chronic relapsing disease in the Lewis rat and strain 13 guinea pig. Am Neurol 1991;29:615-22.
21. Meyer AL, Benson JM, Gienapp IE, Cox KL, Whitacre CC. Suppression of murine chronic relapsing experimental autoimmune encephalomyelitis by the oral administration of myelin basic protein. J Immunol 1996;157:4230-8.
22. Karpus WJ, Kennedy KJ, Smith WS, Miller SD. Inhibition of relapsing experimental autoimmune encephalomyelitis in SJL mice by feeding the immunodominant PLP139-151 peptide. J Neurosci Res 1996;45:410-23.
23. Goverman J, Woods A, Larson L, Weiner LP, Hood L, Zaller DM. Transgenic mice that express a myelin basic protein-specific T cell receptor develop spontaneous autoimmunity. Cell 1993;72:551-60.
24. Lafaille JJ, Nagashima K, Katsuki M, Tonegawa S. High incidence of spontaneous autoimmune encephalomyelitis in immunodeficient anti-myelin basic protein T cell receptor transgenic mice. Cell 1994;78:399-408.
25. Benson JM, Whitacre CC. The role of clonal deletion and anergy in oral tolerance. Res Immunol 1997;148:533-41.
26. Constantinescu CS, Hilliard B, Fujioka T, Bhopale MK, Calida D, Rostami AM. Pathogenesis of neuroimmunologic diseases. Experimental models. Immunol Res 1998;17:217-27.
27. Gaupp S, Hartung HP, Toyka K, Jung S. Modulation of experimental autoimmune neuritis in Lewis rats by oral application of myelin antigens. J Neuroimmunol 1997;79:129-37.
28. Trentham DE. Collagen arthritis as a relevant model for rheumatoid arthritis. Arthritis Rheum 1982;25:911-6.
29. Courtenay JS, Dallman MJ, Dayan AD, Martin A, Mosedale B. Immunisation against heterologous type II collagen induces arthritis in mice. Nature 1980;283:666-8.
30. Vingsbo C, Sahlstrand P, Brun JG, Jonsson R, Saxne T, Holmdahl R. Pristane-induced arthritis in rats: a new model for rheumatoid arthritis with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. Am J Pathol 1996;149:1675-83.
31. Holmdahl R, Mo J, Nordling C, et al. Collagen induced arthritis: an experimental model for rheumatoid arthritis with involvement of both DTH and immune complex mediated mechanisms. Clin Exp Rheumatol 1989;7:S51-5.
32. Kaklamanis PM. Experimental animal models resembling rheumatoid arthritis. Clin Rheumatol 1992;11:41-7.
33. Brahn E. Animal models of rheumatoid arthritis. Clues to etiology and treatment. Clin Orthop 1991:42-53.
34. Gaston JS. Role of T-cells in the development of arthritis. Clin Sci (Colch) 1998;95:19-31.
35. Khare SD, Krco CJ, Griffiths MM, Luthra HS, David CS. Oral administration of an immunodominant human collagen peptide modulates collagen-induced arthritis. J Immunol 1995;155:3653-9.
36. Zhang ZY, Lee CS, Lider O, Weiner HL. Suppression of adjuvant arthritis in Lewis rats by oral administration of type 11 collagen. J Immunol 1990;145:2489-93.
37. Yoshino S, Quattrocchi E, Weiner HL. Suppression of antigen-induced arthritis in Lewis rats by oral administration of type II collagen. Arthritis Rheum 1995;38:1092-6.
38. Haque MA, Yoshino S, Inada S, Nomaguchi H, Tokunaga O, Kohashi O. Suppression of adjuvant arthritis in rats by induction of oral tolerance to mycobacterial 65-kDa heat shock protein. Eur J Immunol 1996;26:2650-6.
39. van Eden W, Hogervorst EJ, van der Zee R, van Embden JD, Hensen EJ, Cohen IR. The mycobacterial 65 kD heat-shock protein and autoimmune arthritis. Rheumatol Int 1989;9:187-91.
40. Panchapakesan J, Daglis M, Gatenby P. Antibodies to 65 kDa and 70 kDa heat shock proteins in rheumatoid arthritis and systemic lupus erythematous. Immunol Cell Biol 1992;70:295-300.
41. Karopoulos C, Rowley MJ, Handley CJ, Strugnell RA. Antibody reactivity to mycobacterial 65 kDa heat shock protein: relevance to autoimmunity. J Autoimmun 1995;8:235-48.
42. Inada S, Yoshino S, Haque MA, Ogata Y, Kohashi O. 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. Cell Immunol 1997;175:67-75.
43. Wicker LS, Todd JA, Peterson LB. Genetic control of autoimmune diabetes in the NOD mouse. Annu Rev Immunol 1995;13:179-200.
44. Zhang ZJ, Davidson L, Eisenbarth G, Weiner HL. Suppression of diabetes in nonobese diabetic mice by oral administration of porcine insulin. Proc Natl Acad Sci USA 1991;88:10252-6.
45. + T cells that suppress adoptive transfer of diabetes. J Autoimmun 1994;7:655-63.
46. von Herrath MG, Dyrberg T, Oldstone MB. Oral insulin treatment suppresses virus-induced antigen-specific destruction of beta cells and prevents autoimmune diabetes in transgenic mice. J Clin Invest 1996;98:1324-31.
47. Polanski M, Melican NS, Zhang J, Weiner HL. Oral administration of the immunodominant B-chain of insulin diabetes in a co-transfer model of diabetes in the NOD mouse and is associated with a switch from Th1 to Th2 cytokines. J Autoimmun 1997;10:339-46.
48. Ma SW, Zhao DL, Yin ZQ, et al. Transegnic plants expressing autoantigens fed to mice to induce oral immune tolerance. Nat Med 1997;3:793-6.
49. Caspi RR, Roberge FG, McAllister CG, et al. T cell lines mediating experimental autoimmune uveoretinitis (EAU) in the rat. J Immunol 1986;136:928-33.
50. Caspi RR, Roberge FG, Chan CC, et al. A new model of autoimmune disease. Experimental autoimmune uveoretinitis induced in mice with two different retinal antigens. J Immunol 1988;140:1490-5.
51. Faure JP. Autoimmunity and the retina. Curr Top Eye Res 1980;2:215-302.
52. Nussenblatt RB, Caspi RR, Mahdi R, et al. Inhibition of S-antigen induced experimental autoimmune uveoretinitis by oral induction of tolerance with S-antigen. J Immunol 1990;144:1689-95.
53. Gregerson DS, Obritsch WF, Donoso LA. Oral tolerance in experimental autoimmune uveoretinitis. Distinct mechanisms of resistance are induced by low dose vs high dose feeding protocols. J Immunol 1993;151:5751-61.
54. Rizzo LV, Miller-Rivero NE, Chan CC, Wiggert B, Nussenblatt RB, Caspi RR. Interleukin-2 treatment potentiates induction of oral tolerance in a murine model of autoimmunity. J Clin Invest 1994;94:1668-72.
55. Wildner G, Hunig T, Thurau SR. Orally induced, peptide-specific gamma/delta TCR+ cells suppress experimental autoimmune uveitis. Eur J Immunol 1996;26:2140-8.
56. Thurau SR, Diedrichs-Mohring M, Fricke H, Arbogast S, Wildner G. Molecular mimicry as a therapeutic approach for an autoimmune disease: oral treatment of uveitis-patients with an MHC-peptide crossreactive with autoantigen-first results. Immunol Lett 1997;57:193-201.
57. Thurau SR, Chan CC, Nussenblatt RB, Caspi RR. Oral tolerance in a murine model of relapsing experimental autoimmune uveoretinitis (EAU): induction of protective tolerance in primed animals. Clin Exp Immunol 1997;109:370-6.
58. Singh VK, Anand R, Sharma K, Agarwal SS. Suppression of experimental autoimmune uveitis in Lewis rats by oral administration of recombinant Escherichia coli expressing retinal S-antigen. Cell Immunol 1996;172:158-62.
59. Vladutiu AO, Rose NR. Autoimmune murine thyroiditis relation to histocompatibility (H-2) type. Science 1971;174:1137-9.
60. Esquivel PS, Rose NR, Kong YC. Induction of autoimmunity in good and poor responder mice with mouse thyroglobulin and lipopolysaccharide. J Exp Med 1997;145:1250-63.
61. Braley-Mullen H, Johnson M, Johnson M, Sharp GC, Kyriakos M. Induction of experimental autoimmune thyroiditis in mice with in vitro activated splenic T cells. Cell Immunol 1985;93:132-43.
62. Sugihara S, Maruo S, Tada T, et al. Autoimmune thyroiditis induced in mice depleted of particular T cell subsets. II. Immunohistochemical studies on the thyroiditis lesion. Reg Immunol 1989;2:345-54.
63. Sugihara S, Fujiwara H, Shearer GM. Autoimmune thyroiditis induced in mice depleted of particular T cell subsets. Characterization of thyroiditis-inducing T cell lines and clones derived from thyroid lesions. J Immunol 1993;150:683-94.
64. Peterson KE, Braley-Mullen H. Suppression of murine experimental autoimmune thyroiditis of oral administration of porcine thyroglobulin. Cell Immunol 1995;166:123-30.
65. Guimaraes VS, Quintans J, Fisfalen ME, et al. Suppression of development of experimental autoimmune thyroiditis by oral administration of thyroglobulin. Endocrinology 1995;136:3353-9.
66. Guimaraes VS, Quintans J, Fisfalen ME, et al. Immunosuppression of thyroiditis. Endocrinology 1996;137:2199-207.
67. Lindstrom J, Shelton D, Fujii Y. Myasthenia gravis. Adv Immunol 1988;42:233-84.
68. Hoedemaekers AC, van Breda Vriesman PJ, De Baets MH. Myasthenia gravis as a prototype autoimmune receptor disease. Immunol Res 1997;16:341-54.
69. Wang ZY, Qiao J, Link H. Suppression of experimental autoimmune myasthenia gravis by oral administration of acetylcholine receptor. J Neuroimmunol 1993;44:209-14.
70. Wang ZY, Link H, Ljungdahl A, et al. Induction of interferon-gamma, interleukin-4, and transforming growth factor-beta in rats orally tolerized against experimental autoimmune myasthenia gravis. Cell Immunol 1994;157:353-68.
71. Wang ZY, Huang J, Olsson T, He B, Link H. B cell responses to acetylcholine receptor in rats orally tolerized against experimental autoimmune myasthenia gravis. J Neurol Sci 1995;128:167-74.
72. Ma CG, Zhang GX, Xiao BE, et al. Mucosal tolerance to experimental autoimmune myasthenia gravis is associated with down-regulation of AChR-specific IFN-gamma-expressing Th1-like cells and up-regulation of TGF-beta mRNA in mononuclear cells. Ann NY Acad Sci 1996;778:273-87.
73. Wang ZY, He B, Qiao J, Link H. Suppression of experimental autoimmune myasthenia gravis and experimental allergic encephalomyelitis by oral administration of acetylcholine receptor and myelin basic protein: double tolerance. J Neuroimmunol 1995;63:79-86.
74. Sayegh MH, Zhang ZJ, Hancock WW, Kwok CA, Carpenter CB, Weiner HL. Down-regulation of the immune response to histocompatibility antigens and prevention of sensitization by skin allografts by orally administered alloantigen. Transplantation 1992;53:163-6.
75. Hancock WW, Sayegh MH, Kwok CA, Weiner HL, Carpenter CB. Oral, but not intravenous, alloantigen prevents accelerated allograft rejection by selective intragraft Th2 cell activation. Transplantation 1993;55:1112-8.
76. Sayegh MH, Khoury SJ, Hancock WW, Weiner HL, Carpenter CB. Induction of immunity and oral tolerance with polymorphic class II major histocompatibility complex allopeptides in the rat. Proc Natl Acad Sci USA 1992;89:7762-6.
77. He YG, Mellon J, Niederkorn JY. The effect of oral immunization on corneal allograft survival. Transplantation 1996;61:920-6.
78. Ali M, Lemoine NR, Ring CJ. The use of DNA viruses as vectors for gene therapy. Gene Ther 1994;1:367-84.
79. Yang Y, Li Q, Ertl HC, Wilson JM. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol 1995;59:2004-15.
80. Ilan Y, Prakash R, Davidson A, et al. Oral tolerization to adenoviral antigens permits long-term gene expression using recombinant adenoviral vectors. J Clin Invest 1997;99:1098-106.
81. Ilan Y, Sauter B, Chowdhury NR, et al. Oral tolerization to adenoviral proteins permits repeated adenovirus-mediated gene therapy in rats with pre-existing immunity to adenoviruses. Hepatology 1998;27:1368-76.
82. Husby S, Mestecky J, Moldoveanu Z, Holland S, Elson CO. Oral tolerance in humans. T cell but not B cell tolerance after antigen feeding. J Immunol 1994;152:4663-70.
83. Weiner HL, Mackin GA, Matsui M, et al. Double-blind pilot trial of oral tolerization with myelin antigens in multiple sclerosis [see comments]. Science 1993;259:1321-4.
84. Fukaura H, Kent SC, Pietrusewicz MJ, Khoury SJ, Weiner HL, Hafler DA. Antigen-specific TGF-beta 1 secretion with bovine myelin oral tolerization in multiple sclerosis. Ann NY Acad Sci 1996;778:251-7.
85. Barnett ML, Combitchi D, Trentham DE. A pilot trial of oral type II collagen in the treatment of juvenile rheumatoid arthritis. Arthritis Rheum 1996;39:623-8.
86. Trentham DE, Dynesius-Trentham RA, Orav EJ, et al. Effects of oral administration of type II collagen on rheumatoid arthritis. Science 1993;261:1727-30.
87. Barnett ML, Kremer KM, St. Clair EW, et al. Treatment of rheumatoid arthritis with oral type II collagen. Results of a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum 1998;41:290-7.
88. Sieper J, Kary S, Sorensen H, et al. Oral type II collagen treatment in early rheumatoid arthritis. A double-blind, placebo-controlled, randomized trial. Arthritis Rheum 1996;39:41-51.
89. Nussenblatt RB, Whitcup SM, de Smet MD, et al. Intraocular inflammatory disease (uveitis) and the use of oral tolerance: a status report. Ann NY Acad Sci 1996;778:325-37.
90. Nussenblatt RB, Gery I, Weiner HL, et al. Treatment of uveitis by oral administration of retinal antigens: results of a phase I/II randomized masked trial. Am J Ophthalmol 1997;123:583-92.
91. Schatz R, Rogers DG, Brouhard BH. Prevention of insulin-dependent diabetes mellitus: an overview of three trials. Cleve Clin J Med 1996;63:270-4.
92. Coutant R, Carel JC, Timsit J, Boitard C, Bougneres P. Insulin and the prevention of insulin-dependent diabetes mellitus. Diabetes Metab 1997;23:25-8.
93. Blanas E, Carbone FR, Allison J, Miller JF, Heath WR. Induction of autoimmune diabetes by oral administration of autoantigen. Science 1996;274:1707-9.
94. McFarland HF. Complexities in the treatment of autoimmune disease. Science 1996;274:2037-8.
95. Litwin A, Flanagan M, Entis G, et al. Immunologic effects of encapsulated short ragweed extract: a potent new agent for oral immunotherapy. Ann Allergy Asthma Immunol 1996;77:132-8.
96. Jain SL, Barone KS, Michael JG. Activation patterns of murine T cells after oral administration of an enterocoated soluble antigen. Cell Immunol 1996;167:170-5.
97. Jain SL, Barone KS, Flanagan MP, Michael JG. Activation patterns of murine B cells after oral administration of an encapsulated soluble antigen. Vaccine 1996;14:1291-7.
98. Litwin A, Flanagan M, Entis G, et al. Oral immunotherapy with short ragweed extract in a novel encapsulated preparation: a double-blind study. J Allergy Clin Immunol 1997;100:30-8.
99. Van Deusen MA, Angelini BL, Cordoro KM, Seiler BA, Wood L, Skoner DP. Efficacy and safety of oral immunotherapy with short ragweed extract. Ann Allergy Asthma Immunol 1997;78:573-80.
100. Warshaw AL, Walker WA, Cornell R, Isselbacher KJ. Small intestinal permeability to macromolecules. Transmission of horseradish peroxidase into mesenteric lymph and portal blood. Lab Invest Lab Invest 1971;25:675-684.
101. Bruce MG, Ferguson A. The influence of intestinal processing on the immunogenicity and molecular size of absorbed, circulating ovalbumin in mice. Immunology 1986;59:295-300.
102. Bjorneboe M, Prytz H, Orskov F. Antibodies to intestinal microbes in serum of patients with cirrhosis of the liver. Lancet 1972;1:58-60.
103. Triger DR, Alp MH, Wright R. Bacterial and dietary antibodies in liver disease. Lancet 1972;1:60-63.
104. Nakano Y, Monden M, Valdivia LA, Gotoh M, Tono T, Mori T. Permanent acceptance of liver allografts by intraportal injection of donor spleen cells in rats. Surgery 1992;111:668-676.
105. Callery MP, Kamei T, Flye MW. The effect of portacaval shunt on delayed-hypersensitivity responses following antigen feeding. J Surg Res 1989;46:391-394.
106. Yang R, Liu Q, Grosfeld JL, Pescovitz MD. Intestional venous drainage through the liver is a prerequisite for oral tolerance induction. J Pediatr Surg 1994;29:1145-1148.
107. Mowat AM, Viney JL. The anatomical basis of intestinal immunity. Immunol Rev 1997;156:145-66.
108. Bland PW, Warren LG. Antigen presentation by epithelial cells of the rat small intestine. I. Kinetics, antigen specificity and blocking by anti-Ia antisera. Immunology 1986;58:1-7.
109. Bland PW, Warren LG. Antigen presentation by epithelial cells of the rat small intestine. I. Selective induction of suppressor T cells. Immunology 1986;58:9-14.
110. Streilein JW. Immunological non-responsiveness and acquisition of tolerance in relation to immune privilege in the eye. Eye 1995;9:236-40.
111. Lu L, McCaslin D, Starzl TE, Thomson AW. Bone marrow-derived dendritic cell progenitors (NLDC 145+, MHC class II+, B7-1dim, B7-2-) induce alloantigen-specific hyporesponsiveness in murine T lymphocytes. Transplantation 1995;60:1539-45.
112. Khoury SJ, Gallon L, Verburg RR, et al. Ex vivo treatment of antigen-presenting cells with CTLA4Ig and encephalitogenic peptide prevents experimental autoimmune encephalomyelitis in the Lewis rat. J Immunol 1996;157:3700-5.
113. Fu F, Li Y, Qian S, et al. Costimulatory molecule-deficient dendritic cell progenitors (MHC class II+, CD80dim, CD86-) prolong cardiac allograft survival in nonimmunosuppressed recipients. Transplantation 1996;62:659-65.
114. Steinbrink K, Wolfl M, Jonuleit H, Knop J, Enk AH. Induction of tolerance by IL-10-treated dendritic cells. J Immunol 1996;159:4772-80.
115. Croft M, Joseph SB, Miner KT. Partial activation of naive CD4 T cells and tolerance induction in response to peptide presented by resting B cells. J Immunol 1997;159:3257-65.
116. Qin Z, Richter G, Schuler T, Ibe S, Cao X, Blankenstein T. B cells inhibit induction of T cell-dependent tumor immunity [In Process Citation]. Nat Med 1998;4:627-30.
117. Vella AT, Scherer MT, Schultz L, Kappler JW, Marrack P. B cells are not essential for peripheral T-cell tolerance. Proc Natl Acad Sci USA 1996;93:951-5.
118. Zhong G, Sousa CR, Germain RN. Antigen-unspecific B cells and lymphoid dendritic cells both show extensive surface expression of processed antigen-major histocompatibility complex class II complexes after soluble protein exposure in vivo or in vitro. J Exp Med 1997;186:673-82.
119. D'Orazio T, Niederkorn JY. A novel role for TGF-beta and IL-10 in the induction of immune privilege. J Immunol 1998;160:2089-98.
120. Kelsall BL, Strober W. The role of dendritic cells in antigen processing in the Peyer's patch. Am NY Acad Sci 1996;778:47-54.
121. Liu LM, MacPherson GG. Lymph-borne (veiled) dendritic cells can acquire and present intestinally administered antigens. Immunology 1991;73:281-6.
122. Liu LM, MacPherson GG. Antigen acquisition by dendritic cells: intestinal dendritic cells acquire antigen administered orally and can prime naive T cells in vivo. J Exp Med 1993;177:1299-307.
123. Viney JL, Mowat AM, O'Mally JM, Williamson E, Fanger NA. Expanding dendritic cells in vivo enhances the induction of oral tolerance. J Immunol 1998.
124. + but not CD8+ T cells are required for the induction of oral tolerance. Int Immunol 1995;7:501-4.
125. Barone KS, Jain SL, Michael JG. Effect of in vivo depletion of CD4+ and CD8+ cells on the induction and maintenance of oral tolerance. Cell Immunol 1995;163:19-29.
126. Garside P, Mowat AM. Mechanisms of oral tolerance. Crit Rev Immunol 1997;17:119-37.
127. 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.
128. Barone KS, Tolarova DD, Ormsby I, Doetschman T, Michael JG. Induction of oral tolerance in TGF-beta 1 null mice. J Immunol 1998;161:154-60.
129. Whitacre CC, Gienapp IE, Meyer A, Cox KL, Javed N. Oral tolerance in experimental autoimmune encephalomyelitis. Annals of the New York Academy of Sciences 1996;778:217-27.
130. Mowat AM, Steel M, Worthey EA, Kewin PJ, Garside P. Inactivation of Th1 and Th2 cells by feeding ovalbumin. Ann NY Acad Sci 1996;778:122-32.
131. Schwartz RH. A cell culture model for T lymphocyte clonal anergy. Science 1990;248:1349-56.
132. Chen Y, Inobe J, Marks R, Gonnella P, Kuchroo VK, Weiner HL. Peripheral deletion of antigen-reactive T cells in oral tolerance [published erratum appears in Nature 1995 Sep 21;377:257]. Nature 1996;376:177-80.
133. Caspi RR, Stiff LR, Morawetz R, et al. Cytokine-dependent modulation of oral tolerance in a murine model of autoimmune uveitis. Ann NY Acad Sci 1996;778:315-24.
134. Aroeira LS, Cardillo F, De Albuquerque DA, Vaz NM, Mengel J. Anti-IL-10 treatment does not block either the induction or the maintenance of orally induced tolerance to OVA. Scand J Immunol 1995;41:319-23.
135. Garside P, Steel M, Worthey EA, et al. T helper 2 cells are subject to high dose oral tolerance and are not essential for its induction. Journal of Immunology 1995;154:5649-55.
136. Marth T, Strober W, Kelsall BL. High dose oral tolerance in ovalbumin TCR-transgenic mice: systemic neutralization of IL-12 augments TGF-beta secretion and T cell apoptosis. J Immunol 1996;157:2348-57.
137. Karpus WJ, Lukacs NW. The role of chemokines in oral tolerance. Abrogation of nonresponsiveness by treatment with antimonocyte chemotactic protein-1. Ann NY Acad Sci 1996;778:133-44
138. Karpus WJ, Kennedy KJ, Kunkel SL, Lukacs NW. Monocyte chemotactic protein 1 regulates oral tolerance induction by inhibition of T helper cell 1-related cytokines. J Exp Med 1998;187:733-41.
139. Zhang ZY, Michael JG. Orally inducible immune unresponsiveness is abrogated by IFN-gamma treatment. J Immunol 1990;144:4163-5.
140. Marinaro M, Boyaka PN, Finkelman FD, et al. Oral but not parenteral interleukin (IL)-12 redirects T helper 2 (Th2)-type responses to an oral vaccine without altering mucosal IgA responses. J Exp Med 1997;185:415-27.
141. 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;12:809-837.
142. Whitacre CC, Gienapp IE, Meyer A, Cox KL, Javed N. Treatment of autoimmune disease by oral tolerance to autoantigens. Clin Immunol Immunopathol 1996;80:S31-S49.
143. Xu-Amano J, Kiyono H, Jackson RJ, et al. Helper T cell subsets for immunoglobulin A responses: oral immunization with tetanus toxoid and cholera toxin as adjuvant selectively induces Th2 cells in mucosa associated tissues. J Exp Med 1993;178:1309-20.
144. Xu-Amano J, Jackson RJ, Fujihashi K, Kiyono H, Staats HF, McGhee JR. Helper Th1 and Th2 cell responses following mucosal or systemic immunization with cholera toxin. Vaccine 1994;12:903-11.
145. Hornquist E, Lycke N. Cholera toxin adjuvant greatly promotes antigen priming of T cells. Eur J Immunol 1993;23:2136-43.
146. Elson CO, Ealding W. Cholera toxin feeding did not induce oral tolerance in mice and abrogated oral tolerance to an unrelated protein antigen. J Immunol 1984;133:2892-7.
147. Sun JB, Holmgren J, Czerkinsky C. Cholera toxin B subunit: an efficient transmucosal carrier-delivery system for induction of peripheral immunological tolerance. Proc Natl Acad Sci USA 1994;91:10795-9.
148. Sun JB, Rask C, Olsson T, Holmgren J, Czerkinsky C. Treatment of experimental autoimmune encephalomyelitis by feeding myelin basic protein conjugated to cholera toxin B subunit. Proc Natl Acad Sci USA 1996;93:7196-201.
149. Czerkinsky C, Sun JB, Lebens M, et al. Cholera toxin B subunit as transmucosal carrier-delivery and immunomodulating system for induction of antiinfections and antipathological immunity. Ann NY Acad Sci 1996;778:185-93.
150. Bergerot I, Ploix C, Petersen J, et al. A cholera toxoid-insulin conjugate as an oral vaccine against spontaneous autoimmune diabetes. Proc Natl Acad Sci USA 1997;94:4610-4.
151. Khoury SJ, Lider O, al-Sabbagh A, Weiner HL. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic protein. III. Synergistic effect of lipopolysaccharide. Cell Immunol 1990;131:302-10.
152. Mengel J, Cardillo F, Aroeira LS, Williams O, Russo M, Vaz NM. Anti-gamma delta T cell antibody blocks the induction and maintenance of oral tolerance to ovalbumin in mice. Immunol Lett 1995;48:97-102.
153. Ke Y, Pearce K, Lake JP, Ziegler HK, Kapp JA. Gamma delta T lymphocytes regulate the induction and maintenance of oral tolerance. J Immunol 1997;158:3610-8.
154. Harrison LC, Dempsey-Collier M, Kramer DR, Takahashi K. Aerosol insulin induces regulatory CD8 gamma delta T cells that prevent murine insulin-dependent diabetes. J Exp Med 1996;184:2167-74.