Oral tolerance: intestinal homeostasis and antigen-specific regulatory T cells

Trends in Immunology

Volumn 29, Issue 11, 2008, Pages 532-540

  Tsuji, Noriko M ^a   Kosaka, Akemi ^a  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ANTIGEN; INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA;

CELL LINE; GASTROINTESTINAL TRACT; HEALTH; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNITY; INTERVENTION STUDY; INTESTINE; MICROENVIRONMENT; NONHUMAN; PHYSIOLOGY; REGULATORY T LYMPHOCYTE; REVIEW;

ANIMALS; ANTIGENS; HOMEOSTASIS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, MUCOSAL; INTESTINES; MOUTH MUCOSA; T-LYMPHOCYTES, REGULATORY;

EID: 53849125398     PISSN: 14714906     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.it.2008.09.002     Document Type: Review

References (107)

1. Faria A.M., and Weiner H.L. Oral tolerance. Immunol. Rev. 206 (2005) 232-259
2. Faria A.M., and Weiner H.L. Oral tolerance: therapeutic implications for autoimmune diseases. Clin. Dev. Immunol. 13 (2006) 143-157
3. Kraal G., et al. The importance of regional lymph nodes for mucosal tolerance. Immunol. Rev. 213 (2006) 119-130
4. + regulatory T cells in the intestine. Inflamm. Allergy Drug Targets 5 (2006) 191-201
5. Dubois B., et al. Oral tolerance and regulation of mucosal immunity. Cell. Mol. Life Sci. 62 (2005) 1322-1332
6. Sakaguchi S., et al. Regulatory T cells and immune tolerance. Cell 133 (2008) 775-787
7. Hauet-Broere F., et al. New cohorts of naive T cells exacerbate ongoing allergy but can be suppressed by regulatory T cells. Allergy 60 (2005) 1530-1536
8. + mucosal regulatory T cells are induced in gut-draining lymphoid tissue within 48 h after oral antigen application. Eur. J. Immunol. 33 (2003) 2801-2810
9. + T cell behavior in mucosal and systemic lymphoid tissues during the induction of oral priming and tolerance. J. Exp. Med. 201 (2005) 1815-1823
10. + regulatory T cell clones induced in Peyer's patches. Int. Immunol. 15 (2003) 525-534
11. Worbs T., et al. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203 (2006) 519-527
12. Worbs T., and Förster R. A key role for CCR7 in establishing central and peripheral tolerance. Trends Immunol. 28 (2007) 274-280
13. Tsuji N.M., et al. Interleukin-10-secreting Peyer's patch cells are responsible for active suppression in low-dose oral tolerance. Immunology 103 (2001) 458-464
14. Bäckström N.F., and Dahlgren U.I. Bystander suppression of collagen-induced arthritis in mice fed ovalbumin. Arthritis Res. Ther. 6 (2004) R151-R160
15. Millington O.R., et al. Induction of bystander suppression by feeding antigen occurs despite normal clonal expansion of the bystander T cell population. J. Immunol. 173 (2004) 6059-6064
16. Kraus T.A., et al. Evidence for a genetic defect in oral tolerance induction in inflammatory bowel disease. Inflamm. Bowel Dis. 12 (2006) 82-88
17. Nagata S., et al. Human Peyer's Patch T Cells are sensitized to dietary antigen and display a Th cell Type 1 cytokine profile. J. Immunol. 165 (2000) 5315-5321
18. + regulatory T cells in the small intestinal lamina propria show and effector /memory phenotype. Int. Immunol. 20 (2008) 307-315
19. Lund J.M., et al. Coordination of early protective immunity to viral infection by regulatory T cells. Science 320 (2008) 1220-1224
20. Mach J., et al. Development of intestinal M cells. Immunol. Rev. 206 (2005) 177-189
21. Jang M.H., et al. Intestinal villous M cells: an antigen entry site in the mucosal epithelium. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 6110-6115
22. Rescigno M., et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2 (2001) 361-367
23. Takayama N., et al. Regulatory role of Peyer's patches for the inhibition of OVA-induced allergic diarrhea. Clin. Immunol. 123 (2007) 199-208
24. Kelsall B.L., and Leon F. Involvement of intestinal dendritic cells in oral tolerance, immunity to pathogens, and inflammatory bowel disease. Immunol. Rev. 206 (2005) 132-148
25. + DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology 108 (2003) 481-492
26. Contractor N., et al. Peyer's patch plasmacytoid dendritic cells (pDC) produce low levels of type I interferons: possible role for IL-10, TGFβ, and prostaglandin E2 in conditioning a unique mucosal pDC phenotype. J. Immunol. 179 (2007) 2690-2694
27. Bryn T., et al. LPS-activated monocytes suppress T-cell immune responses and induce FOXP3+ T cells through a COX-2-PGE2-dependent mechanism. Int. Immunol. 20 (2008) 235-245
28. + dendritic cells are abundant in Peyer's patches during the induction of oral tolerance to type II collagen and suppress experimental collagen-induced arthritis. Arthritis Rheum. 54 (2006) 887-898
29. + regulatory T cells in Peyer's patches in an orally tolerized, collagen-induced arthritis mouse model. Arthritis Res. Ther. 10 (2008) R11
30. Miyamoto K., et al. The ICOS molecule plays a crucial role in the development of mucosal tolerance. J. Immunol. 175 (2005) 7341-7347
31. Ito T., et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulatory ligand. J. Exp. Med. 204 (2007) 105-115
32. Zhang Y., et al. Regulation of T cell activation and tolerance by PDL2. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 11695-11700
33. Keir M., et al. PD-1 and its ligands in T-cell immunity. Curr. Opin. Immunol. 19 (2007) 309-314
34. Kweon M.N., et al. Mucosally induced systemic T cell unresponsiveness to ovalbumin requires CD40 ligand-CD40 interactions. J. Immunol. 162 (1999) 1904-1909
35. Ehirchiou D., et al. CD11b facilitates the development of peripheral tolerance by suppressing Th17 differentiation. J. Exp. Med. 204 (2007) 1519-1524
36. Denning T.L., et al. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8 (2007) 1086-1094
37. +, and double-negative Peyer's patch dendritic cells. J. Immunol. 166 (2001) 4884-4890
38. Tsuji N.M., and Nowak B. IL-18 and antigen-specific CD4+ regulatory T cells in Peyer's patches. Ann. N. Y. Acad. Sci. 1029 (2004) 413-415
39. Samsom J.N., et al. FcgRIIB regulates nasal and oral tolerance: a role for dendritic cells. J. Immunol. 174 (2005) 5279-5287
40. Monteleone I., et al. IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur. J. Immunol. 38 (2008) 1533-1547
41. Uematsu S., et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9 (2008) 769-776
42. Zheng Y., and Rudensky A.Y. Foxp3 in control of the regulatory T cell lineage. Nat. Immunol. 8 (2007) 457-462
43. Faria A.M., and Weiner H.L. Oral tolerance and TGF-β-producing cells. Inflamm. Allergy Drug Targets 5 (2006) 179-190
44. Macpherson A.J., and Slack E. The functional interaction of commensal bacteria with intestinal secretory IgA. Curr. Opin. Gastroenterol. 23 (2007) 673-678
45. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198 (2003) 1875-1886
46. + T cell subsets. J. Leukoc. Biol. 82 (2007) 335-346
47. Selvaraj R.K., and Geiger T.L. A kinetic and dynamic analysis of Foxp3 induced in T cells by TGF-β. J. Immunol. 178 (2007) 7667-7677
48. +CD25- cells to develop suppressive activity: The role of IL-2, TGF-b, and IL-10. J. Immunol. 172 (2004) 5213-5221
49. +CD25- T cells through Foxp3 induction and down-regulation of Smad7. J. Immunol. 172 (2004) 5149-5153
50. Ono M., et al. Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 446 (2007) 685-689
51. Wu Y., et al. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 126 (2006) 375-387
52. Wan Y.Y., and Flavell R.A. 'Yin-Yang' functions of transforming growth factor-beta and T regulatory cells in immune regulation. Immunol. Rev. 220 (2007) 199-213
53. Sun C.M., et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204 (2007) 1775-1785
54. + regulatory T cells is mediated by cell surface-bound transforming growth factor β. J. Exp. Med. 194 (2001) 629-644
55. +CD45RBhigh-induced colitis by a TGF-β-dependent mechanism. J. Immunol. 170 (2003) 2516-2522
56. + regulatory T cell subset with TGFβ-mediated function and enhanced suppression of experimental autoimmune encephalomyelitis. J. Immunol. 180 (2008) 7327-7337
57. Wan Y.Y., and Flavell R.A. Regulatory T cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 445 (2007) 766-770
58. Li M.O., et al. Transforming growth factor-β controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 25 (2006) 455-471
59. Marie J.C., et al. Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-beta receptor. Immunity 25 (2006) 441-454
60. Awasthi A., et al. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat. Immunol. 8 (2007) 1380-1389
61. Stumhofer J.S., et al. Interleukins 27 and 6 induce STAT-3-mediated T cell production of interleukin 10. Nat. Immunol. 8 (2007) 1363-1371
62. H-17 cell-mediated pathology. Nat. Immunol. 8 (2007) 1390-1397
63. Kamanaka M., et al. Expression of Interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knock in tiger mouse. Immunity 25 (2006) 941-952
64. + and Foxp3- precursor cells in the absence of interleukin 10. Nat. Immunol. 8 (2007) 931-941
65. Rubtsov Y.P., et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28 (2008) 546-558
66. Roncarolo M.G., et al. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol. Rev. 212 (2006) 28-50
67. McGeachy M.J., and Cua D.J. Th17 cell differentiation: The long and winding road. Immunity 28 (2008) 445-453
68. H-17 cells requires transforming growth factor-β and induction of the nuclear receptor RORγt. Nat. Immunol. 9 (2008) 641-649
69. Monteleone G., et al. Interleukin-21: a critical regulator of the balance between effector and regulatory T-cell responses. Trends Immunol. 29 (2008) 290-294
70. Hue S., et al. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203 (2006) 2473-2483
71. Izcuel A., et al. Interleukin-23 restrains regulatory T Cell activity to drive T Cell- dependent colitis. Immunity 28 (2008) 559-570
72. Lochner M., et al. In vivo equilibrium of proinflammatory IL-17+ and regulatory IL-10+ Foxp3+ RORgamma t+ T cells. J. Exp. Med. 205 (2008) 1381-1393
73. Bettelli E., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006) 235-238
74. H17 cell differentiation by antagonizing ROR γt function. Nature 453 (2008) 236-240
75. Ichiyama K., et al. Foxp3 inhibits ROR{gamma}t-mediated IL-17A mRNA transcription through direct interaction with ROR{gamma}t. J. Biol. Chem. 283 (2008) 17003-17008
76. Travis M.A., et al. Loss of integrin αvβ8 on dendritic cells causes autoimmunity and colitis in mice. Nature 449 (2007) 361-366
77. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204 (2007) 1757-1764
78. Mucida D., et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317 (2007) 256-260
79. Benson M.J., et al. All-trans retinoic acid mediates enhanced T regulatory cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 204 (2007) 1765-1774
80. Iwata M., et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21 (2004) 527-538
81. Mora J.R., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314 (2006) 1157-1160
82. + T cells. Clin. Exp. Immunol. 153 (2008) 127-135
83. Tanaka K., and Ishikawa H. Role of intestinal bacterial flora in oral tolerance induction. Histol. Histopathol. 19 (2004) 907-914
84. Verginis P., et al. Induction of antigen-specific regulatory T cells in wild-type mice: visualization and targets of suppression. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 3479-3484
85. Kang Y., et al. Immunosuppressant as adjuvant for tolerogenic immunization. J. Immunol. 180 (2008) 5172-5176
86. Battaglia M., et al. Rapamycin and interleukin-10 treatment induces T regulatory type 1 cells that mediate antigen-specific transplantation. Diabetes 55 (2006) 40-49
87. Roncarolo M.G., and Battaglia M. Regulatory T-cell immunotherapy for tolerance to self antigens and alloantigens in humans. Nat. Rev. Immunol. 7 (2007) 585-598
88. Hawrylowicz C.M., and O'Garra A. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol. 5 (2005) 271-283
89. Xystrakis E., et al. Reversing the defective induction of IL-10-secreting regulatory T cells in glucocorticoid-resistant asthma patients. J. Clin. Invest. 116 (2006) 146-155
90. + regulatory cells. J. Immunol. 177 (2006) 7634-7644
91. Huibregtse I.L., et al. Induction of ovalbumin-specific tolerance by oral administration of Lactococcus lactis secreting ovalbumin. Gastroenterology 133 (2007) 517-528
92. Verhasselt V., et al. Brest milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat. Med. 14 (2008) 170-175
93. Akdis C.A., et al. Immunological mechanisms of sublingual immunotherapy. Allergy 61 (2006) 11-14
94. + regulatory T cells. Int. Immunol. 16 (2004) 1189-1201
95. H17 cell differentiation by the aryl hydrocarbon receptor. Nature 453 (2008) 65-71
96. Hauben E., et al. Activation of the aryl hydrocarbon receptor promotes allograft specific tolerance through direct- and DC-mediated effects on regulatory T cells. Blood 112 (2008) 1214-1222
97. + Peyer's patch dendritic cells secrete IL-6 and induce IgA secretion from naive B cells. J. Immunol. 171 (2003) 3684-3690
98. Mora J.R., et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424 (2003) 88-93
99. Annacker O., et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 202 (2005) 1051-1061
100. + dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202 (2005) 1063-1073
101. Blázquez A.B., and Berin M.C. Gastrointestinal dendritic cells promote Th2 skewing via OX40L. J. Immunol. 180 (2008) 4441-4450
102. Becker C., et al. Constitutive p40 promoter activation and IL-23 production in the terminal ileum mediated by dendritic cells. J. Clin. Invest. 112 (2003) 693-706
103. Chirdo F.G., et al. Immunomodulatory dendritic cells in intestinal lamina propria. Eur. J. Immunol. 35 (2005) 1831-1834
104. Tezuka H., et al. Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 448 (2007) 929-933
105. Rimoldi M., et al. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 6 (2005) 507-551
106. + T cells. Nat. Med. 12 (2006) 627-635
107. Izcue A., et al. Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol. Rev. 212 (2006) 256-271