A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β -and retinoic acid-dependent mechanism

Journal of Experimental Medicine

Volumn 204, Issue 8, 2007, Pages 1757-1764

  Coombes, Janine L ^a   Siddiqui, Karima R R ^a   Arancibia Cárcamo, Carolina V ^a   Hall, Jason ^b   Sun, Cheng Ming ^b   Belkaid, Yasmine ^b   Powrie, Fiona ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; RETINOIC ACID; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL REGENERATION; CONTROLLED STUDY; DENDRITIC CELL; LYMPHOCYTE SUBPOPULATION; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD; CD4-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; DENDRITIC CELLS; FORKHEAD TRANSCRIPTION FACTORS; INTEGRIN ALPHA CHAINS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; MICE, INBRED BALB C; MICE, SCID; MICE, TRANSGENIC; MODELS, BIOLOGICAL; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA; TRETINOIN;

EID: 34547788180     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20070590     Document Type: Article

References (28)

1. Coombes, J.L., N.J. Robinson, K.J. Maloy, H.H. Uhlig, and F. Powrie. 2005. Regulatory T cells and intestinal homeostasis. Immunol. Rev. 204:184-194.
2. Kretschmer, K., I. Apostolou, D. Hawiger, K. Khazaie, M.C. Nussenzweig, and H. von Boehmer. 2005. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6:1219-1227.
3. Sun, J.B., S. Raghavan, A. Sjoling, S. Lundin, and J. Holmgren. 2006. Oral tolerance induction with antigen conjugated to cholera toxin B subunit generates both Foxp3+CD25+ and Foxp3-CD25- CD4+ regulatory T cells. J. Immunol. 177:7634-7644.
4. Thorstenson, K.M., and A. Khoruts. 2001. Generation of anergic CD25+ CD4+ T cells with immunoregulatory potential in vivo following induction of peripheral tolerance with intravenous or oral antigen. J. Immunol. 167:188-195.
5. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198:1875-1886.
6. Cobbold, S.P., R. Castejon, E. Adams, D. Zelenika, L. Graca, S. Humm, and H. Waldmann. 2004. Induction of foxP3+ regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J. Immunol. 172:6003-6010.
7. Fantini, M.C., C. Becker, G. Monteleone, F. Pallone, P.R. Galle, and M.F. Neurath. 2004. Cutting edge: TGF-beta induces a regulatory phenotype in CD4+CD25- T cells through Foxp3 induction and downregulation of Smad7. J. Immunol. 172:5149-5153.
8. Fu, S., N. Zhang, A.C. Yopp, D. Chen, M. Mao, H. Zhang, Y. Ding, and J.S. Bromberg. 2004. TGF-beta induces Foxp3+ T-regulatory cells from CD4+ CD25- precursors. Am. J. Transplant. 4:1614-1627.
9. Rao, P.E., A.L. Petrone, and P.D. Ponath. 2005. Differentiation and expansion of T cells with regulatory function from human peripheral lymphocytes by stimulation in the presence of TGF-{beta}. J. Immunol. 174:1446-1455.
10. Wan, Y.Y., and R.A. Flavell. 2005. Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA. 102:5126-5131.
11. Chirdo, F.G., O.R. Millington, H. Beacock-Sharp, and A.M. Mowat. 2005. Immunomodulatory dendritic cells in intestinal lamina propria. Eur. J. Immunol. 35:1831-1840.
12. Johansson, C., and B.L. Kelsall. 2005. Phenotype and function of intestinal dendritic cells. Semin. Immunol. 17:284-294.
13. Zhang, X., L. Izikson, L. Liu, and H.L. Weiner. 2001. Activation of CD25(+)CD4(+) regulatory T cells by oral antigen administration. J. Immunol. 167:4245-4253.
14. Bilsborough, J., T.C. George, A. Norment, and J.L. Viney. 2003. Mucosal CD8alpha+ DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology. 108:481-492.
15. Worbs, T., U. Bode, S. Yan, M.W. Hoffmann, G. Hintzen, G. Bernhardt, R. Forster, and O. Pabst. 2006. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203:519-527.
16. Annacker, O., J.L. Coombes, V. Malmstrom, H.H. Uhlig, T. Bourne, B. Johansson-Lindbom, W.W. Agace, C.M. Parker, and F. Powrie. 2005. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 202:1051-1061.
17. Kilshaw, P.J. 1993. Expression of the mucosal T cell integrin alpha M290 beta 7 by a major subpopulation of dendritic cells in mice. Eur. J. Immunol. 23:3365-3368.
18. Brenan, M., and M. Puklavec. 1992. The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J. Exp. Med. 175:1457-1465.
19. + dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202:1063-1073.
20. + regulatory T cells. J. Exp. Med. 201:1061-1067.
21. Annes, J.P., J.S. Munger, and D.B. Rifkin. 2003. Making sense of latent TGFbeta activation. J. Cell Sci. 116:217-224.
22. Iwata, M., A. Hirakiyama, Y. Eshima, H. Kagechika, C. Kato, and S.Y. Song. 2004. Retinoic acid imprints gut-homing specificity on T cells. Immunity. 21:527-538.
23. Gavin, M.A., T.R. Torgerson, E. Houston, P. DeRoos, W.Y. Ho, A. Stray-Pedersen, E.L. Ocheltree, P.D. Greenberg, H.D. Ochs, and A.Y. Rudensky. 2006. Single-cell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc. Natl. Acad. Sci. USA. 103:6659-6664.
24. Rimoldi, M., M. Chieppa, V. Salucci, F. Avogadri, A. Sonzogni, G.M. Sampietro, A. Nespoli, G. Viale, P. Allavena, and M. Rescigno. 2005. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 6:507-514.
25. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T.B. Strom, M. Oukka, H.L. Weiner, and V.K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 441:235-238.
26. Powrie, F., M.W. Leach, S. Mauze, L.B. Caddle, and R.L. Coffman. 1993. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int. Immunol. 5:1461-1471.
27. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188:287-296.
28. Pfaffl, M.W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.