Dominant role of antigen dose in CD4+Foxp3+ regulatory T cell induction and expansion

Journal of Immunology

Volumn 183, Issue 8, 2009, Pages 4895-4903

  Turner, Michael S ^a   Kane, Lawrence P ^a   Morel, Penelope A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIBODY; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; MONOCLONAL ANTIBODY CD28; PROTEIN KINASE B; T LYMPHOCYTE ANTIGEN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIBODIES; ANTIGENS; ANTIGENS, CD28; ANTIGENS, CD3; CARRIER PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; DIABETES MELLITUS, TYPE 1; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-6; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; ONCOGENE PROTEIN V-AKT; OVALBUMIN; PEPTIDES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TOR SERINE-THREONINE KINASES;

EID: 77954104660     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901459     Document Type: Article

References (54)

1. Castano, L., and G. S. Eisenbarth. 1990. Type-I diabetes: a chronic autoimmune disease of human, mouse and rat. Annu. Rev. Immunol. 8: 647-679. (Pubitemid 20135642)
2. Leiter, E. L., M. Prochazka, and D. L. Coleman. 1987. Animal model of human disease, the nonobese diabetic (NOD) mouse. Am. J. Pathol. 128: 380.
3. + regulatory T-cells contributes to the onset of autoimmune diabetes. Diabetes 57: 113-123.
4. Gregori, S., N. Giarratana, S. Smiroldo, and L. Adorini. 2003. Dynamics of pathogenic and suppressor T cells in autoimmune diabetes development. J. Immunol. 171: 4040-4047.
5. + regulatory T cells. J. Immunol. 180: 858-869.
6. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
7. + regulatory T cells from nonobese diabetic mice. J. Immunol. 175: 3053-3059.
8. Bour-Jordan, H., B. L. Salomon, H. L. Thompson, G. L. Szot, M. R. Bernhard, and J. A. Bluestone. 2004. Costimulation controls diabetes by altering the balance of pathogenic and regulatory T cells. J. Clin. Invest. 114: 979-987.
9. Jonuleit, H., E. Schmitt, K. Steinbrink, and A. H. Enk. 2001. Dendritic cells as a tool to induce anergic and regulatory T cells. Trends Immunol. 22: 394-400.
10. Roncarolo, M. G., M. K. Levings, and C. Traversari. 2001. Differentiation of T regulatory cells by immature dendritic cells. J. Exp. Med. 193: F5-F9. (Pubitemid 32524446)
11. + immunoregulatory T cells that control autoimmune diabetes. Immunity 12: 431-440.
12. + T regulatory cells. J. Immunol. 177: 5115-5121.
13. + T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192: 1213-1222.
14. Wakkach, A., N. Fournier, V. Brun, J. P. Breittmayer, F. Cottrez, and H. Groux. 2003. Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 18: 605-617.
15. Rulifson, I. C., A. I. Sperling, P. E. Fields, F. W. Fitch, and J. A. Bluestone. 1997. CD28 costimulation promotes the production of Th2 cytokines. J. Immunol. 158: 658-665.
16. Feili-Hariri, M., X. Dong, S. M. Alber, S. C. Watkins, R. D. Salter, and P. A. Morel. 1999. Immunotherapy of NOD mice with bone marrow-derived dendritic cells. Diabetes 48: 2300-2308.
17. Feili-Hariri, M., D. H. Falkner, A. Gambotto, G. D. Papworth, S. C. Watkins, P. D. Robbins, and P. A. Morel. 2003. Dendritic cells transduced to express interleukin-4 prevent diabetes in nonobese diabetic mice with advanced insulitis. Hum. Gene Ther. 14: 13-23.
18. Feili-Hariri, M., D. H. Falkner, and P. A. Morel. 2002. Regulatory Th2 response induced following adoptive transfer of dendritic cells in prediabetic NOD mice. Eur. J. Immunol. 32: 2021-2030.
19. Feili-Hariri, M., R. R. Flores, A. C. Vasquez, and P. A. Morel. 2006. Dendritic cell immunotherapy for autoimmune diabetes. Immunol. Res. 36: 167-173. (Pubitemid 46398593)
20. + regulatory T cells restore normoglycemia in diabetic NOD mice. J. Exp. Med. 204: 191-201.
21. + T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J. Exp. Med. 199: 1467-1477.
22. Judkowski, V., C. Pinilla, K. Schroder, L. Tucker, N. Sarvetnick, and D. B. Wilson. 2001. Identification of MHC class II-restricted peptide ligands, including a glutamic acid decarboxylase 65 sequence, that stimulate diabetogenic T cells from transgenic BDC2.5 nonobese diabetic mice. J. Immunol. 166: 908-917.
23. Feili-Hariri, M., D. H. Falkner, and P. A. Morel. 2005. Polarization of naive T cells into Th1 or Th2 by distinct cytokine-driven murine dendritic cell populations: implications for immunotherapy. J. Leukocyte Biol. 78: 656-664.
24. Wallace, P. K., J. D. T. Jr., J. L. Fisher, S. S. Wallace, M. S. Ernstoff, and K. A. Muirhead. 2008. Tracking antigen-driven responses by flow cytometry: Monitoring proliferation by dye dilution. Cytometry 73A: 1019-1034.
25. Kishimoto, H., and J. Sprent. 2001. A defect in central tolerance in NOD mice. Nat. Immunol. 2: 1025-1031.
26. + cells. J. Exp. Med. 205: 565-574.
27. Sauer, S., L. Bruno, A. Hertweck, D. Finlay, M. Leleu, M. Spivakov, Z. A. Knight, B. S. Cobb, D. Cantrell, E. O'Connor, et al. 2008. T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc. Natl. Acad. Sci. USA 105: 7797-7802.
28. Ruvinsky, I., N. Sharon, T. Lerer, H. Cohen, M. Stolovich-Rain, T. Nir, Y. Dor, P. Zisman, and O. Meyuhas. 2005. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev. 19: 2199-2211.
29. 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.
30. + regulatory T cells. Proc. Natl. Acad. Sci. USA 105: 18460-18465.
31. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189.
32. Jiang, K., B. Zhong, C. Ritchey, D. L. Gilvary, E. Hong-Geller, S. Wei, and J. Y. Djeu. 2003. Regulation of Akt-dependent cell survival by Syk and Rac. Blood 101: 236-244.
33. Lin, S. J., C. Chang, A. K. Ng, S. H. Wang, J. J. Li, and C. P. Hu. 2007. Prevention of TGF-β-induced apoptosis by interlukin-4 through Akt activation and p70S6K survival signaling pathways. Apoptosis 12: 1659-1670.
34. Tu, Y., A. Gardner, and A. Lichtenstein. 2000. The phosphatidylinositol 3-kinase/AKT kinase pathway in multiple myeloma plasma cells: roles in cytokine-dependent survival and proliferative responses. Cancer Res. 60: 6763-6770.
35. - effector T cells. Int. Immunol. 20: 421-431.
36. + regulatory T cells. Proc. Natl. Acad. Sci. USA 104: 2821-2826.
37. + regulatory T cells from peripheral Foxp3- precursors. Blood 110: 4293-4302.
38. + CD25 T cells. J. Immunol. 179: 2041-2045.
39. Calderon, B., A. Suri, X. O. Pan, J. C. Mills, and E. R. Unanue. 2008. IFN-γ-dependent regulatory circuits in immune inflammation highlighted in diabetes. J. Immunol. 181: 6964-6974.
40. Hideshima, T., N. Nakamura, D. Chauhan, and K. C. Anderson. 2001. Biologic sequelae of interleukin-6 induced PI3-K/Akt signaling in multiple myeloma. Oncogene 20: 5991-6000. (Pubitemid 32955041)
41. Kim, J.-H., J. E. Kim, H.-Y. Liu, W. Cao, and J. Chen. 2008. Regulation of interleukin-6-induced hepatic insulin resistance by mammalian target of rapamycin through the STAT3-SOCS3 pathway. J. Biol. Chem. 283: 708-715.
42. Lutz, M. B., and G. Schuler. 2002. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 23: 445-449.
43. Morel, P. A., M. Feili-Hariri, P. T. Coates, and A. W. Thomson. 2003. Dendritic cells, T cell tolerance and therapy of adverse immune reactions. Clin. Exp. Immunol. 133: 1-10.
44. Morelli, A. E., and A. W. Thomson. 2007. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat. Rev. Immunol. 7: 610-621. (Pubitemid 47123548)
45. Szeles, L., G. Keresztes, D. Torocsik, Z. Balajthy, L. Krenacs, S. Poliska, A. Steinmeyer, U. Zuegel, M. Pruenster, A. Rot, and L. Nagy. 2009. 1,25-Dihydroxyvitamin D3 is an autonomous regulator of the transcriptional changes leading to a tolerogenic dendritic cell phenotype. J. Immunol. 182: 2074-2083.
46. Steinman, R. M., and M. C. Nussenzweig. 2002. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99: 351-358.
47. + regulatory T cells are activated in vivo by recognition of self. Int. Immunol. 19: 557-566.
48. Apostolou, I., and H. von Boehmer. 2004. In vivo instruction of suppressor commitment in naive T cells. J. Exp. Med. 199: 1401-1408.
49. 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.
50. Kang, H. K., M. Liu, and S. K. Datta. 2007. Low-dose peptide tolerance therapy of lupus generates plasmacytoid dendritic cells that cause expansion of autoantigen- specific regulatory T cells and contraction of inflammatory Th17 cells. J. Immunol. 178: 7849-7858.
51. Kang, H. K., M. A. Michaels, B. R. Berner, and S. K. Datta. 2005. Very low-dose tolerance with nucleosomal peptides controls lupus and induces potent regulatory T cell subsets. J. Immunol. 174: 3247-3255.
52. Liu, E., H. Moriyama, N. Abiru, D. Miao, L. Yu, R. M. Taylor, F. D. Finkelman, and G. S. Eisenbarth. 2002. Anti-peptide autoantibodies and fatal anaphylaxis in NOD mice in response to insulin self-peptides B:9-23 and B:13-23. J. Clin. Invest. 110: 1021-1027.
53. Pedotti, R., M. Sanna, M. Tsai, J. DeVoss, L. Steinman, H. McDevitt, and S. J. Galli. 2003. Severe anaphylactic reactions to glutamic acid decarboxylase (GAD) self peptides in NOD mice that spontaneously develop autoimmune type 1 diabetes mellitus. BMC Immunol. 4: 2.
54. Pedotti, R., D. Mitchell, J. Wedemeyer, M. Karpuj, D. Chabas, E. M. Hattab, M. Tsai, S. J. Galli, and L. Steinman. 2001. An unexpected version of horror autotoxicus: anaphylactic shock to a self-peptide. Nat. Immunol. 2: 216-222.