Reprogrammed FoxP3+ T regulatory cells become IL-17+ antigen-specific autoimmune effectors in vitro and in vivo

Journal of Immunology

Volumn 181, Issue 5, 2008, Pages 3137-3147

  Radhakrishnan, Suresh ^a   Cabrera, Rosalyn ^a   Schenk, Erin L ^a   Nava Parada, Pilar ^a   Bell, Michael P ^a   Van Keulen, Virginia P ^a   Marler, Ronald J ^a   Felts, Sara J ^a   Pease, Larry R ^a  

^a MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; ANTIBODY; B7 ANTIGEN; B7 DC ANTIGEN; B7-DC ANTIGEN; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; T LYMPHOCYTE RECEPTOR; VACCINE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; CD25+ T LYMPHOCYTE; CELL INTERACTION; CELL LINEAGE; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; DIABETES MELLITUS; DOWN REGULATION; EFFECTOR CELL; HYPOTHESIS; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; LETHALITY; MALE; MELANOMA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; ANIMAL; BIOSYNTHESIS; CELL COMMUNICATION; CYTOLOGY; DRUG EFFECT; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MULTIPLE MYELOMA;

ANIMALS; ANTIBODIES; ANTIGENS, CD80; AUTOIMMUNITY; CELL COMMUNICATION; CYTOKINES; DENDRITIC CELLS; FORKHEAD TRANSCRIPTION FACTORS; IMMUNE TOLERANCE; INTERLEUKIN-17; MICE; MULTIPLE MYELOMA; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES, REGULATORY; VACCINES;

EID: 51549097819     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.5.3137     Document Type: Article

References (60)

1. + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22: 531-562.
2. Ziegler, S. F. 2006. FoxP3: of mice and men. Annu. Rev. Immunol. 24: 209-226.
3. Zheng, Y., and A. Y. Rudensky. 2007. Foxp3 in control of the regulatory T cell lineage. Nat. Immunol. 8: 457-462. (Pubitemid 46605910)
4. Miyara, M., and S. Sakaguchi. 2007. Natural regulatory T cells: mechanisms of suppression. Trends Mol. Med. 13: 108-116. (Pubitemid 46341958)
5. Bonomo, A., P. J. Kehn, E. Payer, L. Rizzo, A. W. Cheever, and E. M. Shevach. 1995. Pathogenesis of post-thymectomy autoimmunity: role of syngeneic MLR-reactive T cells. J. Immunol. 154: 6602-6611.
6. Asano, M., M. Toda, N. Sakaguchi, and S. Sakaguchi. 1996. Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J. Exp. Med. 184: 387-396. (Pubitemid 26324092)
7. + T regulatory cells. Nat. Immunol. 4: 337-342.
8. + regulatory T cells. Nat. Immunol. 4: 330-336.
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. (Pubitemid 40387475)
10. + regulatory T cells specific for a neo-self-antigen develop at the doublepositive thymic stage. Proc. Natl. Acad. Sci. USA 103: 8453-8458.
11. Campbell, D. J., and S. F. Ziegler. 2007. FoxP3 modifies the phenotypic and functional properties of regulatory T cells. Nat. Rev. Immunol. 7: 305-310.
12. + regulatory T cell: a jack of all trades, master of regulation. Nat. Immunol. 9: 239-244.
13. Wan, Y. Y., and R. A. Flavell. 2007. "Yin-Yang" functions of transforming growth factor-β and T regulatory cells in immune regulation. Immunol. Rev. 220: 199-213. (Pubitemid 350064011)
14. Liston, A., and A. Y. Rudensky. 2007. Thymic development and peripheral homeostasis of regulatory T cells. Curr. Opin. Immunol. 19: 176-185. (Pubitemid 46356966)
15. 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. (Pubitemid 32044513)
16. + suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2: 389-400.
17. Gambineri, E., T. R. Torgerson, and H. D. Ochs. 2003. Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FoxP3, a critical regulator of T-cell homeostasis. Curr. Opin. Rheumatol. 15: 430-435. (Pubitemid 36774255)
18. Pardoll, D. 2003. Does the immune system see tumors as foreign or self? Annu. Rev. Immunol. 21: 807-839. (Pubitemid 37174548)
19. Colombo, M. P., and S. Piconese. 2007. Regulatory T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat. Rev. Cancer 7: 880-887.
20. Radhakrishnan, S., L. T. Nguyen, B. Ciric, D. R. Ure, B. Zhou, K. Tamada, H. Dong, S. Y. Tseng, T. Shin, D. M. Pardoll, et al. 2003. Naturally occurring human IgM antibody that binds B7-DC and potentiates T cell stimulation by dendritic cells. J. Immunol. 170: 1830-1838. (Pubitemid 36197399)
21. Radhakrishnan, S., K. R. Wiehagen, V. Pulko, V. Van Keulen, W. A. Faubion, K. L. Knutson, and L. R. Pease. 2007. Induction of a Th1 response from Th2- polarized T cells by activated dendritic cells: dependence on TCR:peptide-MHC interaction, ICAM-1, IL-12, and IFN-γ. J. Immunol. 178: 3583-3592. (Pubitemid 46417625)
22. Radhakrishnan, S., L. T. Nguyen, B. Ciric, D. Flies, V. P. Van Keulen, K. Tamada, L. Chen, M. Rodriguez, and L. R. Pease. 2004. Immunotherapeutic potential of B7-DC (PD-L2) cross-linking antibody in conferring antitumor immunity. Cancer Res. 64: 4965-4972. (Pubitemid 38924544)
23. Radhakrishnan, S., K. Iijima, T. Kobayashi, M. Rodriguez, H. Kita, and L. R. Pease. 2004. Blockade of allergic airway inflammation following systemic treatment with a B7-DC (PD-L2) cross-linking human antibody. J. Immunol. 173: 1360-1365. (Pubitemid 38924316)
24. Radhakrishnan, S., K. Iijima, T. Kobayashi, H. Kita, and L. R. Pease. 2005. Dendritic cells activated by cross-linking B7-DC (PD-L2) block inflammatory airway disease. J. Allergy Clin. Immunol. 116: 668-674. (Pubitemid 41267145)
25. Van Keulen, V. P., B. Ciric, S. Radhakrishnan, K. L. Heckman, Y. Mitsunaga, K. Iijima, H. Kita, M. Rodriguez, and L. R. Pease. 2006. Immunomodulation using the recombinant monoclonal human B7-DC cross-linking antibody rHIgM12. Clin. Exp. Immunol. 143: 314-321.
26. + T cell-mediated suppression by dendritic cells. Science 299: 1033-1036.
27. Kurts, C., W. R. Heath, F. R. Carbone, J. Allison, J. F. Miller, and H. Kosaka. 1996. Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184: 923-930. (Pubitemid 26313550)
28. Nava-Parada, P., G. Forni, K. L. Knutson, L. R. Pease, and E. Celis. 2007. Peptide vaccine given with a Toll-like receptor agonist is effective for the treatment and prevention of spontaneous breast tumors. Cancer Res. 67: 1326-1334. (Pubitemid 46270793)
29. Lucchini, F., M. G. Sacco, N. Hu, A. Villa, J. Brown, L. Cesano, L. Mangiarini, G. Rindi, S. Kindl, F. Sessa, et al. 1992. Early and multifocal tumors in breast, salivary, harderian and epididymal tissues developed in MMTY-Neu transgenic mice. Cancer Lett. 64: 203-209.
30. Lachman, L. B., X. M. Rao, R. H. Kremer, B. Ozpolat, G. Kiriakova, and J. E. Price. 2001. DNA vaccination against neu reduces breast cancer incidence and metastasis in mice. Cancer Gene Ther. 8: 259-268.
31. Fallarino, F., U. Grohmann, K.-W. Hwang, C. Orabona, C. Vacca, R. Bianchi, M. L. Belladonna, M. C. Fioretti, M. L. Alegre, and P. Puccetti. 2003. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol. 4: 1206-1212. (Pubitemid 37547898)
32. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R. M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony- stimulating factor. J. Exp. Med. 176: 1693-1702.
33. Heckman, K. L., E. L. Schenk, S. Radhakrishnan, K. D. Pavelko, M. J. Hansen, and L. R. Pease. 2007. Fast-tracked CTL: rapid induction of potent anti-tumor killer T cells in situ. Eur. J. Immunol. 37: 1827-1835.
34. Xystrakis, E., A. S. Dejean, I. Bernard, P. Druet, R. Liblau, D. Gonzalez-Dunia, and A. Saoudi. 2004. Identification of a novel natural regulatory CD8 T-cell subset and analysis of its mechanism of regulation. Immunobiology 104: 3294-3301.
35. Blocki, F. A., S. Radhakrishnan, V. P. Van Keulen, K. L. Heckman, B. Ciric, C. L. Howe, M. Rodriguez, E. Kwon, and L. R. Pease. 2006. Induction of a gene expression program in dendritic cells with a cross-linking IgM antibody to the co-stimulatory molecule B7-DC. FASEB J. 20: 2408-2410.
36. 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: 166-168.
37. + regulatory T cells from human peripheral blood. J. Immunol. 166: 7282-7289.
38. + T cells through Foxp3 induction and down-regulation of Smad7. J. Immunol. 172: 5149-5153.
39. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
40. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132.
41. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141. (Pubitemid 41541791)
42. 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 cells. Immunity 24: 179-189. (Pubitemid 43214587)
43. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. W. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-β induces development of the TH17 lineage. Nature 441: 231-234.
44. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061. (Pubitemid 36222930)
45. + natural regulatory T cells revealed by DNA microarray analysis. Int. Immunol. 18: 1197-1209.
46. Weaver, C. T., L. E. Harrington, P. R. Mangan, M. Gavrieli, and K. M. Murphy. 2006. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24: 677-688.
47. Weaver, C. T., R. D. Hatton, P. R. Mangan, and L. E. Harrington. 2007. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25: 821-852.
48. Stockinger, B., and M. Veldhoen. 2007. Differentiation and function of Th17 T cells. Curr. Opin. Immunol. 19: 281-286.
49. Reiner, S. L. 2007. Development in motion: helper T cells at work. Cell 129: 33-36. (Pubitemid 46507593)
50. - T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-β. J. Immunol. 178: 6725-6729.
51. Bird, J. J., D. R. Brown, A. C. Mullen, N. H. Moskowitz, M. A. Mahowald, J. R. Sider, T. F. Gajewski, C. R. Wang, and S. L. Reiner. 1998. Helper T cell differentiation is controlled by the cell cycle. Immunity 9: 229-237. (Pubitemid 28400036)
52. Gudmundsdottir, H., A. D. Wells, and L. A. Turka. 1999. Dynamics and requirements of T cell clonal expansion in vivo at the single-cell level: effector function is linked to proliferative capacity. J. Immunol. 162: 5212-5223. (Pubitemid 29307126)
53. Richter, A., M. Lohning, and A. Radbruch. 1999. Instruction for cytokine expression in T helper lymphocytes in relation to proliferation and cell cycle progression. J. Exp. Med. 190: 1439-1450.
54. Chang, J. T., V. R. Palanivel, I. Kinjyo, F. Schambach, A. M. Intlekofer, A. Banerjee, S. A. Longworth, K. E. Vinup, P. Mrass, J. Oliaro, et al. 2007. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315: 1687-1691. (Pubitemid 46515618)
55. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
56. Yang, X. O., B. P. Pappu, R. Nurieva, A. Akimzhanov, H. S. Kang, Y. Chung, L. Ma, B. Shah, A. D. Panopoulos, K. S. Schluns, et al. 2008. T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORα and RORγ. Immunity 28: 29-39.
57. + T helper cells. Cell 126: 1121-1133.
58. Radhakrishnan, S., E. Celis, and L. R. Pease. 2005. B7-DC cross-linking restores antigen uptake and augments antigen-presenting cell function by matured dendritic cells. Proc. Natl. Acad. Sci. USA 102: 11438-11443. (Pubitemid 41153838)
59. Pavelko, K. D., K. L. Heckman, M. J. Hansen, and L. R. Pease. 2008. An effective vaccine strategy protective against antigenically distinct tumor variants. Cancer Res. 68: 2471-2478.
60. Radhakrishnan, S., L. T. Nguyen, B. Ciric, V. P. Van Keulen, and L. R. Pease. 2007. B7-DC/PD-L2 cross-linking induces NF-κ-B-dependent protection of dendritic cells from cell death. J. Immunol. 178: 1426-1432. (Pubitemid 46154613)