OX40 is required for regulatory T cell-mediated control of colitis

Journal of Experimental Medicine

Volumn 207, Issue 4, 2010, Pages 699-709

  Griseri, Thibault ^a,b   Asquith, Mark ^a   Thompson, Claire ^a   Powrie, Fiona ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

OX40 LIGAND; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; COLITIS; CONTROLLED STUDY; HOMEOSTASIS; INFLAMMATION; LYMPHOID ORGAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; STEADY STATE; T LYMPHOCYTE; TH1 CELL;

ANIMALS; ANTIGENS, CD45; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL COUNT; CELL MOVEMENT; CELL PROLIFERATION; COLITIS; COLON; DISEASE MODELS, ANIMAL; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; HOMEODOMAIN PROTEINS; INTEGRINS; INTERFERON-GAMMA; INTERLEUKIN-17; INTESTINAL MUCOSA; LYMPHOCYTE ACTIVATION; LYMPHOID TISSUE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, OX40; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTORS;

EID: 77951060733     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20091618     Document Type: Article

References (40)

1. Bennett, C.L., J. Christie, F. Ramsdell, M.E. Brunkow, P.J. Ferguson, L. Whitesell, T.E. Kelly, F.T. Saulsbury, P.F. Chance, and H.D. Ochs. 2001. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet. 27:20-21. doi:10.1038/83713
2. Bouma, G., and W. Strober. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3:521-533. doi:10.1038/nri1132 (Pubitemid 37328672)
3. Cederbom, L., H. Hall, and F. Ivars. 2000. CD4+CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur. J. Immunol. 30:1538-1543. doi:10.1002/1521-4141(200006)30:6〈1538::AID- IMMU1538〉3.0.CO;2-X (Pubitemid 30342794)
4. Chaudhry, A., D. Rudra, P. Treuting, R.M. Samstein, Y. Liang, A. Kas, and A.Y. Rudensky. 2009. CD4+ Regulatory T cells control TH17 responses in a Stat3-dependent manner. Science. 326:986-991.
5. Chen, Q., T.S. Davidson, E.N. Huter, and E.M. Shevach. 2009. Engagement of TLR2 does not reverse the suppressor function of mouse regulatory T cells, but promotes their survival. J. Immunol. 183:4458-4466. doi:10.4049/jimmunol. 0901465
6. 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. doi:10.1111/j.0105-2896.2005.00250.x
7. Croft, M. 2003. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat. Rev. Immunol. 3:609-620. doi:10.1038/nri1148 (Pubitemid 37328664)
8. Darrasse-Jèze, G., S. Deroubaix, H. Mouquet, G.D. Victora, T. Eisenreich, K.H. Yao, R.F. Masilamani, M.L. Dustin, A. Rudensky, K. Liu, and M.C. Nussenzweig. 2009. Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J. Exp. Med. 206:1853-1862. doi:10.1084/jem.20090746
9. Fontenot, J.D., J.P. Rasmussen, L.M. Williams, J.L. Dooley, A.G. Farr, and A.Y. Rudensky. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 22:329-341. doi:10.1016/j.immuni.2005.01. 016
10. Golovina, T.N., T. Mikheeva, M.M. Suhoski, N.A. Aqui, V.C. Tai, X. Shan, R. Liu, R.R. Balcarcel, N. Fisher, B.L. Levine, et al. 2008. CD28 costimulation is essential for human T regulatory expansion and function. J. Immunol. 181:2855-2868.
11. Hippen, K.L., P. Harker-Murray, S.B. Porter, S.C. Merkel, A. Londer, D.K. Taylor, M. Bina, A. Panoskaltsis-Mortari, P. Rubinstein, N. Van Rooijen, et al. 2008. Umbilical cord blood regulatory T-cell expansion and functional effects of tumor necrosis factor receptor family members OX40 and 4-1BB expressed on artificial antigen-presenting cells. Blood. 112:2847-2857. doi:10.1182/blood- 2008-01-132951
12. Ito, T., Y.H. Wang, O. Duramad, T. Hori, G.J. Delespesse, N. Watanabe, F.X. Qin, Z. Yao, W. Cao, and Y.J. Liu. 2005. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 202:1213-1223. doi:10.1084/jem.20051135 (Pubitemid 41586952)
13. Izcue, A., S. Hue, S. Buonocore, C.V. Arancibia-Cárcamo, P.P. Ahern, Y. Iwakura, K.J. Maloy, and F. Powrie. 2008. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity. 28:559-570. doi:10.1016/j.immuni.2008.02.019 (Pubitemid 351467043)
14. Izcue, A., J.L. Coombes, and F. Powrie. 2009. Regulatory lymphocytes and intestinal inflammation. Annu. Rev. Immunol. 27:313-338. doi:10.1146/annurev. immunol.021908.132657
15. Koch, M.A., G. Tucker-Heard, N.R. Perdue, J.R. Killebrew, K.B. Urdahl, and D.J. Campbell. 2009. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10:595-602. doi:10.1038/ni.1731
16. Malmström, V., D. Shipton, B. Singh, A. Al-Shamkhani, M.J. Puklavec, A.N. Barclay, and F. Powrie. 2001. CD134L expression on dendritic cells in the mesenteric lymph nodes drives colitis in T cell-restored SCID mice. J. Immunol. 166:6972-6981. (Pubitemid 32467245)
17. + T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197:111-119. doi:10.1084/jem.20021345
18. Onishi, Y., Z. Fehervari, T. Yamaguchi, and S. Sakaguchi. 2008. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA. 105:10113-10118. doi:10.1073/pnas.0711106105
19. Pfaffl, M.W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. doi:10.1093/nar/29.9.e45
20. Piconese, S., B. Valzasina, and M.P. Colombo. 2008. OX40 triggering blocks suppression by regulatory T cells and facilitates tumor rejection. J. Exp. Med. 205:825-839. doi:10.1084/jem.20071341 (Pubitemid 351549881)
21. Pippig, S.D., C. Peña-Rossi, J. Long, W.R. Godfrey, D.J. Fowell, S.L. Reiner, M.L. Birkeland, R.M. Locksley, A.N. Barclay, and N. Killeen. 1999. Robust B cell immunity but impaired T cell proliferation in the absence of CD134 (OX40). J. Immunol. 163:6520-6529.
22. Powrie, F., M.W. Leach, S. Mauze, S. Menon, L.B. Caddle, and R.L. Coffman. 1994. Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity. 1:553-562. doi:10.1016/1074-7613(94)90045-0 (Pubitemid 2156906)
23. Ruby, C.E., R. Montler, R. Zheng, S. Shu, and A.D. Weinberg. 2008. IL-12 is required for anti-OX40-mediated CD4 T cell survival. J. Immunol. 180:2140-2148.
24. Sakaguchi, S., T. Yamaguchi, T. Nomura, and M. Ono. 2008. Regulatory T cells and immune tolerance. Cell. 133:775-787. doi:10.1016/j.cell.2008.05.009
25. + regulatory T cells results in tissue-specific inflammatory disease. J. Exp. Med. 204:1335-1347. doi:10.1084/jem.20070081
26. Shevach, E.M. 2009. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity. 30:636-645. doi:10.1016/j.immuni.2009.04.010
27. Shevach, E.M., and G.L. Stephens. 2006. The GITR-GITRL interaction: co-stimulation or contrasuppression of regulatory activity? Nat. Rev. Immunol. 6:613-618. doi:10.1038/nri1867
28. Shimizu, J., S. Yamazaki, T. Takahashi, Y. Ishida, and S. Sakaguchi. 2002. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 3:135-142. doi:10.1038/ni759 (Pubitemid 34141443)
29. Song, J., T. So, M. Cheng, X. Tang, and M. Croft. 2005. Sustained survivin expression from OX40 costimulatory signals drives T cell clonal expansion. Immunity. 22:621-631. doi:10.1016/j.immuni.2005.03.012 (Pubitemid 40719197)
30. Souza, H.S., C.C. Elia, J. Spencer, and T.T. MacDonald. 1999. Expression of lymphocyte-endothelial receptor-ligand pairs, alpha4beta7/MAdCAM-1 and OX40/OX40 ligand in the colon and jejunum of patients with inflammatory bowel disease. Gut. 45:856-863.
31. Sugamura, K., N. Ishii, and A.D. Weinberg. 2004. Therapeutic targeting of the effector T-cell co-stimulatory molecule OX40. Nat. Rev. Immunol. 4:420-431. doi:10.1038/nri1371 (Pubitemid 38745554)
32. Takeda, I., S. Ine, N. Killeen, L.C. Ndhlovu, K. Murata, S. Satomi, K. Sugamura, and N. Ishii. 2004. Distinct roles for the OX40-OX40 ligand interaction in regulatory and nonregulatory T cells. J. Immunol. 172:3580-3589. (Pubitemid 38337939)
33. Tang, Q., J.Y. Adams, C. Penaranda, K. Melli, E. Piaggio, E. Sgouroudis, C.A. Piccirillo, B.L. Salomon, and J.A. Bluestone. 2008. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity. 28:687-697. doi:10.1016/j.immuni.2008.03.016
34. Valzasina, B., C. Guiducci, H. Dislich, N. Killeen, A.D. Weinberg, and M.P. Colombo. 2005. Triggering of OX40 (CD134) on CD4(+)CD25+ T cells blocks their inhibitory activity: a novel regulatory role for OX40 and its comparison with GITR. Blood. 105:2845-2851. doi:10.1182/blood-2004-07-2959 (Pubitemid 40446278)
35. van Olffen, R.W., N. Koning, K.P. van Gisbergen, F.M. Wensveen, R.M. Hoek, L. Boon, J. Hamann, R.A. van Lier, and M.A. Nolte. 2009. GITR triggering induces expansion of both effector and regulatory CD4+ T cells in vivo. J. Immunol. 182:7490-7500. doi:10.4049/jimmunol.0802751
36. Vu, M.D., X. Xiao, W. Gao, N. Degauque, M. Chen, A. Kroemer, N. Killeen, N. Ishii, and X. Chang Li. 2007. OX40 costimulation turns off Foxp3+ Tregs. Blood. 110:2501-2510. doi:10.1182/blood-2007-01-070748
37. Wan, Y.Y., and R.A. Flavell. 2007. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature. 445:766-770. doi:10.1038/nature05479
38. Watts, T.H. 2005. TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23:23-68. doi:10.1146/annurev.immunol.23.021704. 115839 (Pubitemid 40563164)
39. Yuan, Q., S.K. Bromley, T.K. Means, K.J. Jones, F. Hayashi, A.K. Bhan, and A.D. Luster. 2007. CCR4-dependent regulatory T cell function in inflammatory bowel disease. J. Exp. Med. 204:1327-1334. doi:10.1084/jem.20062076 (Pubitemid 46919871)
40. Zheng, Y., A. Chaudhry, A. Kas, P. deRoos, J.M. Kim, T.T. Chu, L. Corcoran, P. Treuting, U. Klein, and A.Y. Rudensky. 2009. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature. 458:351-356. doi:10.1038/nature07674