Oral tolerance to food protein

Mucosal Immunology

Volumn 5, Issue 3, 2012, Pages 232-239

  Pabst, O ^a   Mowat, A M ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CX3CR1; IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; RETINOIC ACID; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANTIBODY RESPONSE; CELIAC DISEASE; CLONAL ANERGY; CYTOKINE PRODUCTION; DELAYED HYPERSENSITIVITY; DENDRITIC CELL; FOOD ALLERGY; IMMUNOLOGICAL TOLERANCE; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; LAMINA PROPRIA; LYMPHOCYTE PROLIFERATION; MESENTERY LYMPH NODE; MUCOSAL IMMUNITY; NONHUMAN; ORAL TOLERANCE; PEYER PATCH; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW;

EID: 84859808080     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2012.4     Document Type: Review

References (88)

1. Molodecky , N. A. et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142 , 46-54.e42 ( 2011 ).
2. Meresse , B. , Ripoche , J. , Heyman , M. & Cerf-Bensussan , N. Celiac disease: From oral tolerance to intestinal inflammation, autoimmunity and lymphomagenesis. Mucosal Immunol. 2 , 8-23 ( 2009 ).
3. Wells , H. G. & Osborne , T. B. The biological reactions of the vegetable proteins. I: Anaphylaxis. J. Infect. Dis. 8 , 66-124 ( 1911 ).
4. Weiner , H. L. , da Cunha , A. P. , Quintana , F. & Wu , H. Oral tolerance. Immunol. Rev. 241 , 241-259 ( 2011 ).
5. Faria , A. M. & Weiner , H. L. Oral tolerance: Therapeutic implications for autoimmune diseases. Clin. Dev. Immunol. 13 , 143-157 ( 2006 ).
6. Kapp , K. et al. Modulation of systemic antigen-specific immune responses by oral antigen in humans. Eur. J. Immunol. 40 , 3128-3137 ( 2010 ).
7. Kraus , T. A. , Toy , L. , Chan , L. , Childs , J. & Mayer , L. Failure to induce oral tolerance to a soluble protein in patients with inflammatory bowel disease. Gastroenterology 126 , 1771-1778 ( 2004 ).
8. Husby , S. , Mestecky , J. , Moldoveanu , Z. , Holland , S. & Elson , C. O. Oral tolerance in humans. T cell but not B cell tolerance after antigen feeding. J. Immunol. 152 , 4663-4670 ( 1994 ).
9. Higgins , P. J. & Weiner , H. L. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic protein and its fragments. J. Immunol. 140 , 440-445 ( 1988 ).
10. Nagler-Anderson , C. , Bober , L. A. , Robinson , M. E. , Siskind , G. W. & Thorbecke , G. J. Suppression of type II collagen-induced arthritis by intragastric administration of soluble type II collagen. Proc. Natl. Acad. Sci. USA 83 , 7443-7446 ( 1986 ).
11. Zhang , Z. J. , Davidson , L. , Eisenbarth , G. & Weiner , H. L. Suppression of diabetes in nonobese diabetic mice by oral administration of porcine insulin. Proc. Natl. Acad. Sci. USA 88 , 10252-10256 ( 1991 ).
12. Mowat , A. M. , Faria , A. M. & Weiner , H. L. Oral tolerance: Basic mechanisms and clinical implications. In Mucosal Immunology ( Mestecky J., Bienenstock J., Lamm M.E., Strober W., McGhee J.R., Mayer L., eds). 3rd edn (487-538) (Academic Press, San Diego, 2005 ).
13. Brandtzaeg , P. , Kiyono , H. , Pabst , R. & Russell , M. W. Terminology: Nomenclature of mucosa-associated lymphoid tissue. Mucosal Immunol. 1 , 31-37 ( 2008 ).
14. Macpherson , A. J. , McCoy , K. D. , Johansen , F. E. & Brandtzaeg , P. The immune geography of IgA induction and function. Mucosal Immunol. 1 , 11-22 ( 2008 ).
15. Suzuki , H. et al. Ovalbumin-protein sigma 1 M-cell targeting facilitates oral tolerance with reduction of antigen-specific CD4+ T cells. Gastroenterology 135 , 917-925 ( 2008 ).
16. Fujihashi , K. et al. Peyer's patches are required for oral tolerance to proteins. Proc. Natl. Acad. Sci. USA 98 , 3310-3315 ( 2001 ).
17. Spahn , T. W. et al. Induction of oral tolerance to cellular immune responses in the absence of Peyer's patches. Eur. J. Immunol. 31 , 1278-1287 ( 2001 ).
18. Spahn , T. W. et al. Mesenteric lymph nodes are critical for the induction of high-dose oral tolerance in the absence of Peyer's patches. Eur. J. Immunol. 32 , 1109-1113 ( 2002 ).
19. Kraus , T. A. et al. Induction of mucosal tolerance in Peyer's patch-deficient, ligated small bowel loops. J. Clin. Invest. 115 , 2234-2243 ( 2005 ).
20. Goubier , A. et al. Plasmacytoid dendritic cells mediate oral tolerance. Immunity 29 , 464-475 ( 2008 ).
21. Chirdo , F. G. , Millington , O. R. , Beacock-Sharp , H. & Mowat , A. M. Immunomodulatory dendritic cells in intestinal lamina propria. Eur. J. Immunol. 35 , 1831-1840 ( 2005 ).
22. Menard , S. , Cerf-Bensussan , N. & Heyman , M. Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunol. 3 , 247-259 ( 2010 ).
23. Karlsson , M. et al. "Tolerosomes" are produced by intestinal epithelial cells. Eur. J. Immunol. 31 , 2892-2900 ( 2001 ).
24. Niess , J. H. et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307 , 254-258 ( 2005 ).
25. Rescigno , M. et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2 , 361-367 ( 2001 ).
26. Chieppa , M. , Rescigno , M. , Huang , A. Y. & Germain , R. N. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203 , 2841-2852 ( 2006 ).
27. Vallon-Eberhard , A. , Landsman , L. , Yogev , N. , Verrier , B. & Jung , S. Transepithelial pathogen uptake into the small intestinal lamina propria. J. Immunol. 176 , 2465-2469 ( 2006 ).
28. Bain , C. C. & Mowat , A. M. Intestinal macrophages-specialised adaptation to a unique environment. Eur. J. Immunol. 41 , 2494-2498 ( 2011 ).
29. Schulz , O. et al. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 206 , 3101-3114 ( 2009 ).
30. Bogunovic , M. et al. Origin of the lamina propria dendritic cell network. Immunity 31 , 513-525 ( 2009 ).
31. Hapfelmeier , S. et al. Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step in DeltainvG S. Typhimurium colitis. J. Exp. Med. 205 , 437-450 ( 2008 ).
32. Shreedhar , V. K. , Kelsall , B. L. & Neutra , M. R. Cholera toxin induces migration of dendritic cells from the subepithelial dome region to T-and B-cell areas of Peyer's patches. Infect. Immun. 71 , 504-509 ( 2003 ).
33. Macpherson , A. J. & Uhr , T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303 , 1662-1665 ( 2004 ).
34. Walker , W. A. & Isselbacher , K. J. Uptake and transport of macromolecules by the intestine. Possible role in clinical disorders. Gastroenterology 67 , 531-550 ( 1974 ).
35. Husby , S. , Jensenius , J. C. & Svehag , S. E. Passage of undegraded dietary antigen into the blood of healthy adults. Quantification, estimation of size distribution, and relation of uptake to levels of specific antibodies. Scand. J. Immunol. 22 , 83-92 ( 1985 ).
36. Smith , K. M. , Davidson , J. M. & Garside , P. T-cell activation occurs simultaneously in local and peripheral lymphoid tissue following oral administration of a range of doses of immunogenic or tolerogenic antigen although tolerized T cells display a defect in cell division. Immunology 106 , 144-158 ( 2002 ).
37. Zinselmeyer , B. H. et al. In situ characterization of CD4+ T cell behavior in mucosal and systemic lymphoid tissues during the induction of oral priming and tolerance. J. Exp. Med. 201 , 1815-1823 ( 2005 ).
38. Peng , H. J. , Turner , M. W. & 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. 81 , 510-515 ( 1990 ).
39. Thomson , A. W. & Knolle , P. A. Antigen-presenting cell function in the tolerogenic liver environment. Nat. Rev. Immunol. 10 , 753-766 ( 2010 ).
40. Callery , M. P. , Kamei , T. & Flye , M. W. The effect of portacaval shunt on delayed-hypersensitivity responses following antigen feeding. J. Surg. Res. 46 , 391-394 ( 1989 ).
41. Yang , R. , Liu , Q. , Grosfeld , J. L. & Pescovitz , M. D. Intestinal venous drainage through the liver is a prerequisite for oral tolerance induction. J. Pediatr. Surg. 29 , 1145-1148 ( 1994 ).
42. Pabst , O. , Bernhardt , G. & Forster , R. The impact of cell-bound antigen transport on mucosal tolerance induction. J. Leukoc. Biol. 82 , 795-800 ( 2007 ).
43. Forster , R. , Davalos-Misslitz , A. C. & Rot , A. CCR7 and its ligands: Balancing immunity and tolerance. Nat. Rev. Immunol. 8 , 362-371 ( 2008 ).
44. Worbs , T. et al. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203 , 519-527 ( 2006 ).
45. Milling , S. , Yrlid , U. , Cerovic , V. & MacPherson , G. Subsets of migrating intestinal dendritic cells. Immunol. Rev. 234 , 259-267 ( 2010 ).
46. Jaensson , E. et al. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205 , 2139-2149 ( 2008 ).
47. Sun , C. M. et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3T reg cells via retinoic acid. J. Exp. Med. 204 , 1775-1785 ( 2007 ).
48. Iwata , M. et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21 , 527-538 ( 2004 ).
49. Worthington , J. J. , Czajkowska , B. I. , Melton , A. C. & Travis , M. A. Intestinal dendritic cells specialize to activate transforming growth factor-beta and induce Foxp3+ regulatory T cells via integrin alphavbeta8. Gastroenterology 141 , 1802-1812 ( 2011 ).
50. Paidassi , H. et al. Preferential expression of integrin alphavbeta8 promotes generation of regulatory T cells by mouse CD103+ dendritic cells. Gastroenterology 141 , 1813-1820 ( 2011 ).
51. Scott , C. L. , Aumeunier , A. M. & Mowat , A. M. Intestinal CD103+ dendritic cells: Master regulators of tolerance? Trends Immunol. 32 , 412-419 ( 2011 ).
52. Iliev , I. D. et al. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 58 , 1481-1489 ( 2009 ).
53. Iliev , I. D. , Mileti , E. , Matteoli , G. , Chieppa , M. & Rescigno , M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2 , 340-350 ( 2009 ).
54. Agace , W. W. & Persson , E. K. How vitamin A metabolizing dendritic cells are generated in the gut mucosa. Trends Immunol. 33 , 42-48 ( 2011 ).
55. Molenaar , R. et al. Expression of retinaldehyde dehydrogenase enzymes in mucosal dendritic cells and gut-draining lymph node stromal cells is controlled by dietary vitamin A. J. Immunol. 186 , 1934-1942 ( 2011 ).
56. Villablanca , E. J. et al. MyD88 and retinoic acid signaling pathways interact to modulate gastrointestinal activities of dendritic cells. Gastroenterology 141 , 176-185 ( 2011 ).
57. Jaensson-Gyllenback , E. et al. Bile retinoids imprint intestinal CD103+ dendritic cells with the ability to generate gut-tropic T cells. Mucosal Immunol. 4 , 438-447 ( 2011 ).
58. Wang , S. et al. MyD88-dependent TLR1/2 signals educate dendritic cells with gut-specific imprinting properties. J. Immunol. 187 , 141-150 ( 2011 ).
59. Yokota , A. et al. GM-CSF and IL-4 synergistically trigger dendritic cells to acquire retinoic acid-producing capacity. Int. Immunol. 21 , 361-377 ( 2009 ).
60. Annacker , O. et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 202 , 1051-1061 ( 2005 ).
61. Molenaar , R. et al. Lymph node stromal cells support dendritic cellinduced gut-homing of T cells. J. Immunol. 183 , 6395-6402 ( 2009 ).
62. Hammerschmidt , S. I. et al. Stromal mesenteric lymph node cells are essential for the generation of gut-homing T cells in vivo. J. Exp. Med. 205 , 2483-2490 ( 2008 ).
63. Fletcher , A. L. et al. Reproducible isolation of lymph node stromal cells reveals site-dependent differences in fibroblastic reticular cells. Front. Immunol. 2 , 35; doi: 10.3389/fimmu.2011.00035 ( 2011 ).
64. Chen , Y. et al. Peripheral deletion of antigen-reactive T cells in oral tolerance. Nature 376 , 177-180 ( 1995 ).
65. Chen , Y. et al. Oral tolerance in myelin basic protein T-cell receptor transgenic mice: Suppression of autoimmune encephalomyelitis and dose-dependent induction of regulatory cells. Proc. Natl. Acad. Sci. USA 93 , 388-391 ( 1996 ).
66. Siewert , C. et al. Experience-driven development: Effector/memory-like alphaE+Foxp3+ regulatory T cells originate from both naive T cells and naturally occurring naive-like regulatory T cells. J. Immunol. 180 , 146-155 ( 2008 ).
67. Dubois , B. et al. Innate CD4+CD25+ regulatory T cells are required for oral tolerance and inhibition of CD8+ T cells mediating skin inflammation. Blood 102 , 3295-3301 ( 2003 ).
68. Maynard , C. L. et al. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3-precursor cells in the absence of interleukin 10. Nat. Immunol. 8 , 931-941 ( 2007 ).
69. Curotto de Lafaille , M. A. & Lafaille , J. J. Natural and adaptive foxp3+ regulatory T cells: More of the same or a division of labor? Immunity 30 , 626-635 ( 2009 ).
70. Rubtsov , Y. P. et al. Stability of the regulatory T cell lineage in vivo. Science 329 , 1667-1671 ( 2010 ).
71. Koenecke , C. et al. Alloantigen-specific de novo-induced Foxp3+ Treg revert in vivo and do not protect from experimental GVHD. Eur. J. Immunol. 39 , 3091-3096 ( 2009 ).
72. Curotto de Lafaille , M. A. et al. Adaptive Foxp3+ regulatory T celldependent and-independent control of allergic inflammation. Immunity 29 , 114-126 ( 2008 ).
73. Hadis , U. et al. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity 34 , 237-246 ( 2011 ).
74. Strobel , S. & Ferguson , A. Persistence of oral tolerance in mice fed ovalbumin is different for humoral and cell-mediated immune responses. Immunology 60 , 317-318 ( 1987 ).
75. Wagner , N. et al. Critical role for beta7 integrins in formation of the gut-associated lymphoid tissue. Nature 382 , 366-370 ( 1996 ).
76. Cassani , B. et al. Gut-tropic T cells that express integrin alpha4beta7 and CCR9 are required for induction of oral immune tolerance in mice. Gastroenterology 141 , 2109-2118 ( 2011 ).
77. Svensson , M. et al. CCL25 mediates the localization of recently activated CD8alphabeta(+) lymphocytes to the small-intestinal mucosa. J. Clin. Invest. 110 , 1113-1121 ( 2002 ).
78. Walton , K. L. , Galanko , J. A. , Balfour Sartor , R. & Fisher , N. C. T cellmediated oral tolerance is intact in germ-free mice. Clin. Exp. Immunol. 143 , 503-512 ( 2006 ).
79. Ishikawa , H. et al. Effect of intestinal microbiota on the induction of regulatory CD25+ CD4+ T cells. Clin. Exp. Immunol. 153 , 127-135 ( 2008 ).
80. Atarashi , K. et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331 , 337-341 ( 2011 ).
81. Murai , M. et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat. Immunol. 10 , 1178-1184 ( 2009 ).
82. Fohse , L. et al. High TCR diversity ensures optimal function and homeostasis of Foxp3+ regulatory T cells. Eur. J. Immunol. 41 , 3101-3113 ( 2011 ).
83. Lathrop , S. K. et al. Peripheral education of the immune system by colonic commensal microbiota. Nature 478 , 250-254 ( 2011 ).
84. Tsuji , M. et al. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 323 , 1488-1492 ( 2009 ).
85. Tomura , M. et al. Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice. J. Clin. Invest. 120 , 883-893 ( 2010 ).
86. Salazar-Gonzalez , R. M. et al. CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches. Immunity 24 , 623-632 ( 2006 ).
87. Lelouard , H. et al. Pathogenic bacteria and dead cells are internalized by a unique subset of Peyer's patch dendritic cells that express lysozyme. Gastroenterology 138 , 173-184 e1-3 ( 2010 ).
88. Jang , M. H. et al. Intestinal villous M cells: An antigen entry site in the mucosal epithelium. Proc. Natl. Acad. Sci. USA 101 , 6110-6115 ( 2004 ).