A role for IL-27 in limiting T regulatory cell populations

Journal of Immunology

Volumn 187, Issue 1, 2011, Pages 266-273

  Wojno, Elia D Tait ^a   Hosken, Nancy ^b   Stumhofer, Jason S ^a   O'Hara, Aisling C ^a   Mauldin, Elizabeth ^a   Fang, Qun ^a   Turka, Laurence A ^c   Levin, Steven D ^b   Hunter, Christopher A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Zymogenetics ^*  (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2; INTERLEUKIN 27; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CELL ACTIVATION; CELL DIFFERENTIATION; CELL POPULATION; CHIMERA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DOWN REGULATION; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE;

ANIMALS; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; GROWTH INHIBITORS; INFLAMMATION; INTERLEUKIN-2; INTERLEUKINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN SUBUNITS; RADIATION CHIMERA; RECEPTORS, CYTOKINE; T-LYMPHOCYTES, REGULATORY;

EID: 79960400849     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1004182     Document Type: Article

References (61)

1. Boulay, J. L., J. J. O'Shea, and W. E. Paul. 2003. Molecular phylogeny within type I cytokines and their cognate receptors. Immunity 19: 159-163.
2. Hunter, C. A. 2005. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat. Rev. Immunol. 5: 521-531.
3. Kastelein, R. A., C. A. Hunter, and D. J. Cua. 2007. Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu. Rev. Immunol. 25: 221-242.
4. +) T cells. Immunity 16: 779-790.
5. Pflanz, S., L. Hibbert, J. Mattson, R. Rosales, E. Vaisberg, J. F. Bazan, J. H. Phillips, T. K. McClanahan, R. de Waal Malefyt, and R. A. Kastelein. 2004. WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J. Immunol. 172: 2225-2231.
6. Hibbert, L., S. Pflanz, R. De Waal Malefyt, and R. A. Kastelein. 2003. IL-27 and IFN-a signal via Stat1 and Stat3 and induce T-Bet and IL-12Rbeta2 in naive T cells. J. Interferon Cytokine Res. 23: 513-522.
7. + T cells through Stat1-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. USA 100: 15047-15052.
8. Takeda, A., S. Hamano, A. Yamanaka, T. Hanada, T. Ishibashi, T. W. Mak, A. Yoshimura, and H. Yoshida. 2003. Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1 commitment. J. Immunol. 170: 4886-4890. (Pubitemid 36554716)
9. Villarino, A., L. Hibbert, L. Lieberman, E. Wilson, T. Mak, H. Yoshida, R. A. Kastelein, C. Saris, and C. A. Hunter. 2003. The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity 19: 645-655.
10. Hamano, S., K. Himeno, Y. Miyazaki, K. Ishii, A. Yamanaka, A. Takeda, M. Zhang, H. Hisaeda, T. W. Mak, A. Yoshimura, and H. Yoshida. 2003. WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production. Immunity 19: 657-667. (Pubitemid 37490791)
11. Rosas, L. E., A. A. Satoskar, K. M. Roth, T. L. Keiser, J. Barbi, C. Hunter, F. J. de Sauvage, and A. R. Satoskar. 2006. Interleukin-27R (WSX-1/T-cell cytokine receptor) gene-deficient mice display enhanced resistance to leishmania donovani infection but develop severe liver immunopathology. Am. J. Pathol. 168: 158-169.
12. Wirtz, S., I. Tubbe, P. R. Galle, H. J. Schild, M. Birkenbach, R. S. Blumberg, and M. F. Neurath. 2006. Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27. J. Exp. Med. 203: 1875-1881.
13. Sonoda, K. H., T. Yoshimura, A. Takeda, T. Ishibashi, S. Hamano, and H. Yoshida. 2007. WSX-1 plays a significant role for the initiation of experimental autoimmune uveitis. Int. Immunol. 19: 93-98.
14. Artis, D., A. Villarino, M. Silverman,W. He, E. M. Thornton, S. Mu, S. Summer, T. M. Covey, E. Huang, H. Yoshida, et al. 2004. The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. J. Immunol. 173: 5626-5634. (Pubitemid 39392150)
15. Miyazaki, Y., H. Inoue, M. Matsumura, K. Matsumoto, T. Nakano, M. Tsuda, S. Hamano, A. Yoshimura, and H. Yoshida. 2005. Exacerbation of experimental allergic asthma by augmented Th2 responses in WSX-1-deficient mice. J. Immunol. 175: 2401-2407. (Pubitemid 41113850)
16. Shimizu, S., N. Sugiyama, K. Masutani, A. Sadanaga, Y. Miyazaki, Y. Inoue, M. Akahoshi, R. Katafuchi, H. Hirakata, M. Harada, et al. 2005. Membranous glomerulonephritis development with Th2-type immune deviations in MRL/lpr mice deficient for IL-27 receptor (WSX-1). J. Immunol. 175: 7185-7192. (Pubitemid 41713412)
17. Batten, M., J. Li, S. Yi, N. M. Kljavin, D. M. Danilenko, S. Lucas, J. Lee, F. J. de Sauvage, and N. Ghilardi. 2006. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7: 929-936.
18. Stumhofer, J. S., A. Laurence, E. H. Wilson, E. Huang, C. M. Tato, L. M. Johnson, A. V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, et al. 2006. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7: 937-945.
19. Fitzgerald, D. C., G. X. Zhang, M. El-Behi, Z. Fonseca-Kelly, H. Li, S. Yu, C. J. Saris, B. Gran, B. Ciric, and A. Rostami. 2007. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat. Immunol. 8: 1372-1379.
20. + regulatory T cells control autoimmunity? Curr. Opin. Immunol. 17: 638-642.
21. Miyara, M., and S. Sakaguchi. 2007. Natural regulatory T cells: mechanisms of suppression. Trends Mol. Med. 13: 108-116.
22. Wing, K., and S. Sakaguchi. 2010. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 11: 7-13.
23. Belkaid, Y., and G. Oldenhove. 2008. Tuning microenvironments: induction of regulatory T cells by dendritic cells. Immunity 29: 362-371.
24. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
25. + T regulatory cells. J. Immunol. 178: 4022-4026.
26. 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.
27. Kim, J. M., and A. Rudensky. 2006. The role of the transcription factor Foxp3 in the development of regulatory T cells. Immunol. Rev. 212: 86-98.
28. Neufert, C., C. Becker, S. Wirtz, M. C. Fantini, B. Weigmann, P. R. Galle, and M. F. Neurath. 2007. IL-27 controls the development of inducible regulatory T cells and Th17 cells via differential effects on STAT1. Eur. J. Immunol. 37: 1809-1816.
29. Stumhofer, J. S., J. S. Silver, A. Laurence, P. M. Porrett, T. H. Harris, L. A. Turka, M. Ernst, C. J. Saris, J. J. O'Shea, and C. A. Hunter. 2007. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat. Immunol. 8: 1363-1371.
30. Huber, M., V. Steinwald, A. Guralnik, A. Brüstle, P. Kleemann, C. Rosenplänter, T. Decker, and M. Lohoff. 2008. IL-27 inhibits the development of regulatory T cells via STAT3. Int. Immunol. 20: 223-234.
31. Villarino, A. V., J. Larkin, III, C. J. Saris, A. J. Caton, S. Lucas, T. Wong, F. J. de Sauvage, and C. A. Hunter. 2005. Positive and negative regulation of the IL-27 receptor during lymphoid cell activation. J. Immunol. 174: 7684-7691.
32. Owaki, T., M. Asakawa, S. Kamiya, K. Takeda, F. Fukai, J. Mizuguchi, and T. Yoshimoto. 2006. IL-27 suppresses CD28-mediated IL-2 production through suppressor of cytokine signaling 3. J. Immunol. 176: 2773-2780.
33. Villarino, A. V., J. S. Stumhofer, C. J. Saris, R. A. Kastelein, F. J. de Sauvage, and C. A. Hunter. 2006. IL-27 limits IL-2 production during Th1 differentiation. J. Immunol. 176: 237-247.
34. + T cell numbers. J. Immunol. 169: 4850-4860.
35. Malek, T. R., A. Yu, V. Vincek, P. Scibelli, and L. Kong. 2002. CD4 regulatory T cells prevent lethal autoimmunity in IL-2Rbeta-deficient mice. Implications for the nonredundant function of IL-2. Immunity 17: 167-178.
36. + regulatory T cell function. Eur. J. Immunol. 34: 2480-2488.
37. Fontenot, J. D., J. P. Rasmussen, M. A. Gavin, and A. Y. Rudensky. 2005. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6: 1142-1151.
38. +) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J. Exp. Med. 201: 723-735.
39. + T regulatory cells. J. Immunol. 177: 5115-5121.
40. 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.
41. Iritani, B. M., K. A. Forbush, M. A. Farrar, and R. M. Perlmutter. 1997. Control of B cell development by Ras-mediated activation of Raf. EMBO J. 16: 7019-7031.
42. Hogan, B., R. Beddington, F. Constantini, and E. Lacy. 1994. Manipulating the Mouse Embryo. A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Godfrey, V. L., J. E. Wilkinson, and L. B. Russell. 1991. X-linked lymphoreticular disease in the scurfy (sf) mutant mouse. Am. J. Pathol. 138: 1379-1387.
44. Clark, L. B., M. W. Appleby, M. E. Brunkow, J. E. Wilkinson, S. F. Ziegler, and F. Ramsdell. 1999. Cellular and molecular characterization of the scurfy mouse mutant. J. Immunol. 162: 2546-2554. (Pubitemid 29309272)
45. Brunkow, M. E., E. W. Jeffery, K. A. Hjerrild, B. Paeper, L. B. Clark, S. A. Yasayko, J. E. Wilkinson, D. Galas, S. F. Ziegler, and F. Ramsdell. 2001. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27: 68-73.
46. + regulatory T cells. Nat. Immunol. 4: 330-336.
47. 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.
48. Rivera, A., C. C. Chen, J. P. Dougherty, A. Ben-Nun, and Y. Ron. 2003. Host stem cells can selectively reconstitute missing lymphoid lineages in irradiation bone marrow chimeras. Blood 101: 4347-4354. (Pubitemid 36873767)
49. Komatsu, N., and S. Hori. 2007. Full restoration of peripheral Foxp3+ regulatory T cell pool by radioresistant host cells in scurfy bone marrow chimeras. Proc. Natl. Acad. Sci. USA 104: 8959-8964.
50. Kim, J. M., J. P. Rasmussen, and A. Y. Rudensky. 2007. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8: 191-197.
51. Seita, J., M. Asakawa, J. Ooehara, S. Takayanagi, Y. Morita, N. Watanabe, K. Fujita, M. Kudo, J. Mizuguchi, H. Ema, et al. 2008. Interleukin-27 directly induces differentiation in hematopoietic stem cells. Blood 111: 1903-1912. (Pubitemid 351451499)
52. Cox, J. H., N. M. Kljavin, N. Ramamoorthi, L. Diehl, M. Batten, and N. Ghilardi. 2011. IL-27 promotes T cell-dependent colitis through multiple mechanisms. J. Exp. Med. 208: 115-123.
53. Hoyer, K. K., H. Dooms, L. Barron, and A. K. Abbas. 2008. Interleukin-2 in the development and control of inflammatory disease. Immunol. Rev. 226: 19-28.
54. Malek, T. R. 2008. The biology of interleukin-2. Annu. Rev. Immunol. 26: 453-479.
55. + T cells: a common basis between tumor immunity and autoimmunity. J. Immunol. 163: 5211-5218.
56. Dannull, J., Z. Su, D. Rizzieri, B. K. Yang, D. Coleman, D. Yancey, A. Zhang, P. Dahm, N. Chao, E. Gilboa, and J. Vieweg. 2005. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J. Clin. Invest. 115: 3623-3633.
57. Sakaguchi, S., and F. Powrie. 2007. Emerging challenges in regulatory T cell function and biology. Science 317: 627-629. (Pubitemid 47229955)
58. Yamaguchi, T., K. Hirota, K. Nagahama, K. Ohkawa, T. Takahashi, T. Nomura, and S. Sakaguchi. 2007. Control of immune responses by antigen-specific regulatory T cells expressing the folate receptor. Immunity 27: 145-159. (Pubitemid 47089022)
59. reg during BCG immunization on anti-mycobacterial Th1 responses and protection against Mycobacterium tuberculosis. PLoS ONE 3: e2833.
60. Ruter, J., B. G. Barnett, I. Kryczek, M. J. Brumlik, B. J. Daniel, G. Coukos, W. Zou, and T. J. Curiel. 2009. Altering regulatory T cell function in cancer immunotherapy: a novel means to boost the efficacy of cancer vaccines. Front. Biosci. 14: 1761-1770.
61. Salcedo, R., J. A. Hixon, J. K. Stauffer, R. Jalah, A. D. Brooks, T. Khan, R. M. Dai, L. Scheetz, E. Lincoln, T. C. Back, et al. 2009. Immunologic and therapeutic synergy of IL-27 and IL-2: enhancement of T cell sensitization, tumor-specific CTL reactivity and complete regression of disseminated neuroblastoma metastases in the liver and bone marrow. J. Immunol. 182: 4328-4338.