Dendritic cells induce antigen-specific regulatory T cells that prevent graft versus host disease and persist in mice

Journal of Experimental Medicine

Volumn 208, Issue 12, 2011, Pages 2489-2496

  Sela, Uri ^a   Olds, Peter ^a   Park, Andrew ^a   Schlesinger, Sarah J ^a   Steinman, Ralph M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

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

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GRAFT VERSUS HOST REACTION; INFLAMMATORY DISEASE; INTRON; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE TRANSFER; MIXED LYMPHOCYTE REACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL;

ANIMALS; ANTIGENS, CD11C; DENDRITIC CELLS; EPITOPES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GRAFT VS HOST DISEASE; LYMPHOCYTE CULTURE TEST, MIXED; MICE; MICE, INBRED BALB C; T-LYMPHOCYTES, REGULATORY;

EID: 84855472967     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20110466     Document Type: Article

References (36)

1. Benson, M.J., K. Pino-Lagos, M. Rosemblatt, and R.J. Noelle. 2007. Alltrans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 204:1765-1774. http://dx.doi.org/10.1084/jem.20070719
2. Blazar, B.R., P.A. Taylor, R. McElmurry, L. Tian, A. Panoskaltsis-Mortari, S. Lam, C. Lees, T. Waldschmidt, and D.A. Vallera. 1998. Engraftment of severe combined immune deficient mice receiving allogeneic bone marrow via in utero or postnatal transfer. Blood. 92:3949-3959.
3. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198:1875-1886. http://dx.doi.org/10.1084/jem.20030152
4. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204:1757-1764. http://dx.doi.org/10.1084/jem.20070590
5. Edinger, M. 2009. Regulatory T cells for the prevention of graft-versushost disease: professionals defeat amateurs. Eur. J. Immunol. 39:2966-2968. http://dx.doi.org/10.1002/eji.200940030
6. Floess, S., J. Freyer, C. Siewert, U. Baron, S. Olek, J. Polansky, K. Schlawe, H.D. Chang, T. Bopp, E. Schmitt, et al. 2007. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol. 5:e38. http://dx.doi.org/10.1371/journal.pbio.0050038
7. Grinberg-Bleyer, Y., A. Baeyens, S. You, R. Elhage, G. Fourcade, S. Gregoire, N. Cagnard, W. Carpentier, Q. Tang, J. Bluestone, et al. 2010. IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatory T cells. J. Exp. Med. 207:1871-1878. http://dx.doi.org/10.1084/jem.20100209
8. hi Cells. Immunity. 29:758-770. http://dx.doi.org/10.1016/j.immuni.2008.09.018
9. Horwitz, D.A., S.G. Zheng, J.D. Gray, J.H. Wang, K. Ohtsuka, and S. Yamagiwa. 2004. Regulatory T cells generated ex vivo as an approach for the therapy of autoimmune disease. Semin. Immunol. 16:135-143. http://dx.doi.org/10.1016/j.smim.2003.12.009
10. Joffre, O., T. Santolaria, D. Calise, T. Al Saati, D. Hudrisier, P. Romagnoli, and J.P. van Meerwijk. 2008. Prevention of acute and chronic allograft rejection with CD4+CD25+Foxp3+ regulatory T lymphocytes. Nat. Med. 14:88-92. http://dx.doi.org/10.1038/nm1688
11. Kim, H.P., and W.J. Leonard. 2007. CREB/ATF-dependent T cell receptorinduced FoxP3 gene expression: a role for DNA methylation. J. Exp. Med. 204:1543-1551.
12. Koenecke, C., N. Czeloth, A. Bubke, S. Schmitz, A. Kissenpfennig, B. Malissen, J. Huehn, A. Ganser, R. Forster, and I. Prinz. 2009. Alloantigen-specific de novo-induced Foxp3+ Treg revert in vivo and do not protect from experimental GVHD. Eur. J. Immunol. 39:3091-3096. http://dx.doi.org/10.1002/eji.200939432
13. 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. http://dx.doi.org/10.1038/ni1265
14. Luo, X., K.V. Tarbell, H. Yang, K. Pothoven, S.L. Bailey, R. Ding, R.M. Steinman, and M. Suthanthiran. 2007. Dendritic cells with TGF-β1 differentiate naive CD4+CD25-T cells into islet-protective Foxp3+ regulatory T cells. Proc. Natl. Acad. Sci. USA. 104:2821-2826. http://dx.doi.org/10.1073/pnas.0611646104
15. + regulatory T cells. J. Exp. Med. 201:1061-1067. http://dx.doi.org/10.1084/jem.20042276
16. H17 and regulatory T cell differentiation mediated by retinoic acid. Science. 317:256-260. http://dx.doi.org/10.1126/science.1145697
17. Murai, M., O. Turovskaya, G. Kim, R. Madan, C.L. Karp, H. Cheroutre, and M. Kronenberg. 2009. 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. http://dx.doi.org/10.1038/ni.1791
18. Oldenhove, G., N. Bouladoux, E.A. Wohlfert, J.A. Hall, D. Chou, L. Dos Santos, S. O'Brien, R. Blank, E. Lamb, S. Natarajan, et al. 2009. Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity. 31:772-786. http://dx.doi.org/10.1016/j.immuni.2009.10.001
19. Polansky, J.K., K. Kretschmer, J. Freyer, S. Floess, A. Garbe, U. Baron, S. Olek, A. Hamann, H. von Boehmer, and J. Huehn. 2008. DNA methylation controls Foxp3 gene expression. Eur. J. Immunol. 38:1654-1663. http://dx.doi.org/10.1002/eji.200838105
20. Roncarolo, M.G., and M. Battaglia. 2007. Regulatory T-cell immunotherapy for tolerance to self antigens and alloantigens in humans. Nat. Rev. Immunol. 7:585-598. http://dx.doi.org/10.1038/nri2138
21. Rubtsov, Y.P., R.E. Niec, S. Josefowicz, L. Li, J. Darce, D. Mathis, C. Benoist, and A.Y. Rudensky. 2010. Stability of the regulatory T cell lineage in vivo. Science. 329:1667-1671. http://dx.doi.org/10.1126/science.1191996
22. Sakaguchi, S. 2005. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6:345-352. http://dx.doi.org/10.1038/ni1178
23. Sakaguchi, S., T. Yamaguchi, T. Nomura, and M. Ono. 2008. Regulatory T cells and immune tolerance. Cell. 133:775-787. http://dx.doi.org/10.1016/j.cell.2008.05.009
24. Shevach, E.M., T.S. Davidson, E.N. Huter, R.A. Dipaolo, and J. Andersson. 2008. Role of TGF-β in the induction of Foxp3 expression and T regulatory cell function. J. Clin. Immunol. 28:640-646. http://dx.doi.org/10.1007/s10875-008-9240-1
25. Steinman, R.M., and M.D. Witmer. 1978. Lymphoid dendritic cells are potent stimulators of the primary mixed leukocyte reaction in mice. Proc. Natl. Acad. Sci. USA. 75:5132-5136. http://dx.doi.org/10.1073/pnas.75.10.5132
26. Sun, C.M., J.A. Hall, R.B. Blank, N. Bouladoux, M. Oukka, J.R. Mora, and Y. Belkaid. 2007. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204:1775-1785. http://dx.doi.org/10.1084/jem.20070602
27. 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. http://dx.doi.org/10.1016/j.immuni.2008.03.016
28. Taylor, P.A., C.J. Lees, and B.R. Blazar. 2002. The infusion of ex vivo activated and expanded CD4(+)CD25(+) immune regulatory cells inhibits graft-versus-host disease lethality. Blood. 99:3493-3499. http://dx.doi.org/10.1182/blood.V99.10.3493
29. von Boehmer, H. 2007. Oral tolerance: is it all retinoic acid? J. Exp. Med. 204:1737-1739. http://dx.doi.org/10.1084/jem.20071251
30. 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. http://dx.doi.org/10.1073/pnas.0501701102
31. 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. http://dx.doi.org/10.1038/nature05479
32. Yamazaki, S., M. Patel, A. Harper, A. Bonito, H. Fukuyama, M. Pack, K.V. Tarbell, M. Talmor, J.V. Ravetch, K. Inaba, and R.M. Steinman. 2006. Effective expansion of alloantigen-specific Foxp3+ CD25+ CD4+ regulatory T cells by dendritic cells during the mixed leukocyte reaction. Proc. Natl. Acad. Sci. USA. 103:2758-2763. http://dx.doi.org/10.1073/pnas.0510606103
33. Yamazaki, S., A.J. Bonito, R. Spisek, M. Dhodapkar, K. Inaba, and R.M. Steinman. 2007. Dendritic cells are specialized accessory cells along with TGF- for the differentiation of Foxp3+ CD4+ regulatory T cells from peripheral Foxp3 precursors. Blood. 110:4293-4302. http://dx.doi.org/10.1182/blood-2007-05-088831
34. Yang, X.O., R. Nurieva, G.J. Martinez, H.S. Kang, Y. Chung, B.P. Pappu, B. Shah, S.H. Chang, K.S. Schluns, S.S. Watowich, et al. 2008. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity. 29:44-56. http://dx.doi.org/10.1016/j.immuni.2008.05.007
35. Zheng, Y., S. Josefowicz, A. Chaudhry, X.P. Peng, K. Forbush, and A.Y. Rudensky. 2010. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature. 463:808-812. http://dx.doi.org/10.1038/nature08750
36. Zhou, X., S.L. Bailey-Bucktrout, L.T. Jeker, C. Penaranda, M. Martínez-Llordella, M. Ashby, M. Nakayama, W. Rosenthal, and J.A. Bluestone. 2009. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 10:1000-1007. http://dx.doi.org/10.1038/ni.1774