A distinct tolerogenic subset of splenic IDO+CD11b+ dendritic cells from orally tolerized mice is responsible for induction of systemic immune tolerance and suppression of collagen-induced arthritis

Cellular Immunology

Volumn 278, Issue 1-2, 2012, Pages 45-54

  Park, Min Jung ^a   Park, Kyung Su ^a,b   Park, Hyun Sil ^a   Cho, Mi La ^a   Hwang, Sue Yun ^c   Min, So Youn ^a   Park, Mi Kyung ^a   Park, Sung Hwan ^a,b   Kim, Ho Youn ^a,b  

^a The Catholic University of Korea   (South Korea)

^b The Catholic University of Korea   (South Korea)

^c Hankyong National University   (South Korea)

Author keywords

Collagen induced arthritis; Dendritic cell; Indoleamine 2,3 dioxygenase; Oral tolerance; Regulatory T cell; Spleen

Indexed keywords

B7 ANTIGEN; CD11B ANTIGEN; CD86 ANTIGEN; COLLAGEN TYPE 2; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 21; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE COURSE; IMMUNE DEFICIENCY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SPLEEN; SPLEEN CELL; TH17 CELL;

ADMINISTRATION, ORAL; ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD11B; ANTIGENS, DIFFERENTIATION; ARTHRITIS, EXPERIMENTAL; CELL DIFFERENTIATION; CELL PROLIFERATION; COLLAGEN TYPE II; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION; IMMUNE TOLERANCE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTEGRIN ALPHA4BETA1; LYMPHOCYTE ACTIVATION; MICE; ORGAN SPECIFICITY; SIGNAL TRANSDUCTION; SPLEEN; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; MUS;

EID: 84868281887     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2012.06.009     Document Type: Article

References (37)

1. Mowat A.M. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol 2003, 3:331-341.
2. Mowat A.M., Parker L.A., Beacock-Sharp H., Millington O.R., Chirdo F. Oral tolerance. overview and historical perspectives. Ann N Y Acad Sci 2004, 1029:1-8.
3. Faria A.M., Weiner H.L. Oral tolerance. Immunol Rev 2005, 206:232-259.
4. Mayer L., Shao L. Therapeutic potential of oral tolerance. Nat Rev Immunol 2004, 4:407-419.
5. Sakaguchi S., Yamaguchi T., Nomura T., Ono M. Regulatory T cells and immune tolerance. Cell 2008, 133:775-787.
6. Tsuji N.M., Kosaka A. Oral tolerance. intestinal homeostasis and antigen-specific regulatory T cells. Trends Immunol 2008, 29:532-540.
7. Hauet-Broere F., Unger W.W., Garssen J., Hoijer M.A., Kraal G., Samsom J.N. Functional CD25- and CD25+ mucosal regulatory T cells are induced in gut-draining lymphoid tissue within 48 h after oral antigen application. Eur J Immunol 2003, 33:2801-2810.
8. Min S.Y., Park K.S., Cho M.L., Kang J.W., Cho Y.G., Hwang S.Y., Park M.J., Yoon C.H., Min J.K., Lee S.H., Park S.H., Kim H.Y. Antigen-induced, tolerogenic CD11c+, CD11b+ 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 2006, 54:887-898.
9. Steinman R.M., Hawiger D., Nussenzweig M.C. Tolerogenic dendritic cells. Annu Rev Immunol 2003, 21:685-711.
10. Iwasaki A., Kelsall B.L. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J Exp Med 1999, 190:229-239.
11. Iwasaki A., Kelsall B.L. Unique functions of CD11b+, CD8 alpha+, and double-negative Peyer's patch dendritic cells. J Immunol 2001, 166:4884-4890.
12. Nagatani K., Dohi M., To Y., Tanaka R., Okunishi K., Nakagome K., Sagawa K., Tanno Y., Komagata Y., Yamamoto K. Splenic dendritic cells induced by oral antigen administration are important for the transfer of oral tolerance in an experimental model of asthma. J Immunol 2006, 176:1481-1489.
13. Park M.J., Min S.Y., Park K.S., Cho Y.G., Cho M.L., Jung Y.O., Park H.S., Chang S.H., Cho S.G., Min J.K., Park S.H., Kim H.Y. Indoleamine 2,3-dioxygenase-expressing dendritic cells are involved in the generation of CD4+CD25+ regulatory T cells in Peyer's patches in an orally tolerized, collagen-induced arthritis mouse model. Arthritis Res Ther 2008, 10:R11.
14. Puccetti P., Grohmann U. IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation. Nat Rev Immunol 2007, 7:817-823.
15. Mellor A.L., Munn D.H. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 2004, 4:762-774.
16. Matteoli G., Mazzini E., Iliev I.D., Mileti E., Fallarino F., Puccetti P., Chieppa M., Rescigno M. Gut CD103+ dendritic cells express indoleamine 2,3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction. Gut 2010, 59:595-604.
17. Sharma M.D., Baban B., Chandler P., Hou D.Y., Singh N., Yagita H., Azuma M., Blazar B.R., Mellor A.L., Munn D.H. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest 2007, 117:2570-2582.
18. Onodera T., Jang M.H., Guo Z., Yamasaki M., Hirata T., Bai Z., Tsuji N.M., Nagakubo D., Yoshie O., Sakaguchi S., Takikawa O., Miyasaka M. Constitutive expression of IDO by dendritic cells of mesenteric lymph nodes: functional involvement of the CTLA-4/B7 and CCL22/CCR4 interactions. J Immunol 2009, 183:5608-5614.
19. Szanto S., Koreny T., Mikecz K., Glant T.T., Szekanecz Z., Varga J. Inhibition of indoleamine 2,3-dioxygenase-mediated tryptophan catabolism accelerates collagen-induced arthritis in mice. Arthritis Res Ther 2007, 9:R50.
20. Criado G., Simelyte E., Inglis J.J., Essex D., Williams R.O. Indoleamine 2,3 dioxygenase-mediated tryptophan catabolism regulates accumulation of Th1/Th17 cells in the joint in collagen-induced arthritis. Arthritis Rheum 2009, 60:1342-1351.
21. Stuart J.M., Cremer M.A., Kang A.H., Townes A.S. Collagen-induced arthritis in rats. Evaluation of early immunologic events, Arthritis Rheum 1979, 22:1344-1351.
22. Braun D., Longman R.S., Albert M.L. A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood 2005, 106:2375-2381.
23. Baban B., Chandler P.R., Sharma M.D., Pihkala J., Koni P.A., Munn D.H., Mellor A.L. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol 2009, 183:2475-2483.
24. Gutgemann I., Fahrer A.M., Altman J.D., Davis M.M., Chien Y.H. Induction of rapid T cell activation and tolerance by systemic presentation of an orally administered antigen. Immunity 1998, 8:667-673.
25. Li W., Chou S.T., Wang C., Kuhr C.S., Perkins J.D. Role of the liver in peripheral tolerance. induction through oral antigen feeding. Am J Transplant 2004, 4:1574-1582.
26. Taylor M.W., Feng G.S. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J 1991, 5:2516-2522.
27. Adikari S.B., Lian H., Link H., Huang Y.M., Xiao B.G. Interferon-gamma-modified dendritic cells suppress B cell function and ameliorate the development of experimental autoimmune myasthenia gravis. Clin Exp Immunol 2004, 138:230-236.
28. Ehirchiou D., Xiong Y., Xu G., Chen W., Shi Y., Zhang L. CD11b facilitates the development of peripheral tolerance by suppressing Th17 differentiation. J Exp Med 2007, 204:1519-1524.
29. Leipe J., Grunke M., Dechant C., Reindl C., Kerzendorf U., Schulze-Koops H., Skapenko A. Th17 cells in autoimmune arthritis. Arthritis Rheum. 2010.
30. Sato K., Suematsu A., Okamoto K., Yamaguchi A., Morishita Y., Kadono Y., Tanaka S., Kodama T., Akira S., Iwakura Y., Cua D.J., Takayanagi H. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 2006, 203:2673-2682.
31. Xu L., Kitani A., Fuss I., Strober W. Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol 2007, 178:6725-6729.
32. Zhou L., Chong M.M., Littman D.R. Plasticity of CD4+ T cell lineage differentiation. Immunity 2009, 30:646-655.
33. Sharma M.D., Hou D.Y., Liu Y., Koni P.A., Metz R., Chandler P., Mellor A.L., He Y., Munn D.H. Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes. Blood 2009, 113:6102-6111.
34. Pallotta M.T., Orabona C., Volpi C., Vacca C., Belladonna M.L., Bianchi R., Servillo G., Brunacci C., Calvitti M., Bicciato S., Mazza E.M., Boon L., Grassi F., Fioretti M.C., Fallarino F., Puccetti P., Grohmann U. Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat Immunol 2011, 12:870-878.
35. Fallarino F., Grohmann U., Hwang K.W., Orabona C., Vacca C., Bianchi R., Belladonna M.L., Fioretti M.C., Alegre M.L., Puccetti P. Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol 2003, 4:1206-1212.
36. Goubier A., Dubois B., Gheit H., Joubert G., Villard-Truc F., Asselin-Paturel C., Trinchieri G., Kaiserlian D. Plasmacytoid dendritic cells mediate oral tolerance. Immunity 2008, 29:464-475.
37. Coombes J.L., Siddiqui K.R., Arancibia-Carcamo C.V., Hall J., Sun C.M., Belkaid Y., Powrie F. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 2007, 204:1757-1764.