IL-23 drives pathogenic IL-17-producing CD8+ T cells

Journal of Immunology

Volumn 182, Issue 9, 2009, Pages 5296-5305

  Ciric, Bogoljub ^a   El behi, Mohamed ^a   Cabrera, Rosalyn ^b   Zhang, Guang Xian ^a   Rostami, Abdolmohamad ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 AMINODACTINOMYCIN; GRANZYME B; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 6; IONOMYCIN; PHORBOL 13 ACETATE 12 MYRISTATE; STAT1 PROTEIN; STAT4 PROTEIN; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA1;

ADOPTIVE TRANSFER; ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOLYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HYPERGLYCEMIA; LYMPHOCYTE PROLIFERATION; LYMPHOCYTOTOXICITY; MOUSE; NONHUMAN; PATHOGENICITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN CELL; TC17 CELL; TH17 CELL; TUMOR ASSOCIATED LEUKOCYTE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CYTOTOXICITY TEST; EXPERIMENTAL DIABETES MELLITUS; HELPER CELL; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SECRETION; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELLS, CULTURED; CYTOTOXICITY TESTS, IMMUNOLOGIC; DIABETES MELLITUS, EXPERIMENTAL; IMMUNOPHENOTYPING; INTERLEUKIN-17; INTERLEUKIN-23; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 66949180111     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900036     Document Type: Article

References (63)

1. + T cell pool IL-1 subverts IL-2-mediated suppression. J. Immunol. 179: 1423-1426.
2. Kryczek, I., S. Wei, L. Zou, S. Altuwaijri, W. Szeliga, J. Kolls, A. Chang, and W. Zou. 2007. Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J. Immunol. 178: 6730-6733. (Pubitemid 46847396)
3. Liu, S. J., J. P. Tsai, C. R. Shen, Y. P. Sher, C. L. Hsieh, Y. C. Yeh, A. H. Chou, S. R. Chang, K. N. Hsiao, F. W. Yu, and H. W. Chen. 2007. Induction of a distinct CD8 Tnc17 subset by transforming growth factor-β and interleukin-6. J. Leukocyte Biol. 82: 354-360.
4. 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.
5. 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. (Pubitemid 43214587)
6. + T helper cells. Cell 126: 1121-1133.
7. Nurieva, R., X. O. Yang, G. Martinez, Y. Zhang, A. D. Panopoulos, L. Ma, K. Schluns, Q. Tian, S. S. Watowich, A. M. Jetten, and C. Dong. 2007. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448: 480-483. (Pubitemid 47123514)
8. Korn, T., E. Bettelli, W. Gao, A. Awasthi, A. Jager, T. B. Strom, M. Oukka, and V. K. Kuchroo. 2007. IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature 448: 484-487. (Pubitemid 47123515)
9. + T cells lacking T-bet and eomesodermin. Science 321: 408-411.
10. Caruso, R., D. Fina, O. A. Paoluzi, G. Del Vecchio Blanco, C. Stolfi, A. Rizzo, F. Caprioli, M. Sarra, F. Andrei, M. C. Fantini, et al. 2008. IL-23-mediated regulation of IL-17 production in Helicobacter pylori-infected gastric mucosa. Eur. J. Immunol. 38: 470-478.
11. Vanden Eijnden, S., S. Goriely, D. De Wit, F. Willems, and M. Goldman. 2005. IL-23 up-regulates IL-10 and induces IL-17 synthesis by polyclonally activated naive T cells in human. Eur. J. Immunol. 35: 469-475.
12. Nam, J. S., M. Terabe, M. J. Kang, H. Chae, N. Voong, Y. A. Yang, A. Laurence, A. Michalowska, M. Mamura, S. Lonning, et al. 2008. Transforming growth factor β subverts the immune system into directly promoting tumor growth through interleukin-17. Cancer Res. 68: 3915-3923.
13. Tajima, M., D. Wakita, D. Noguchi, K. Chamoto, Z. Yue, K. Fugo, H. Ishigame, Y. Iwakura, H. Kitamura, and T. Nishimura. 2008. IL-6-dependent spontaneous proliferation is required for the induction of colitogenic IL-17-producing CD8+ T cells. J. Exp. Med. 205: 1019-1027. (Pubitemid 351679678)
14. Tzartos, J. S., M. A. Friese, M. J. Craner, J. Palace, J. Newcombe, M. M. Esiri, and L. Fugger. 2008. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am. J. Pathol. 172: 146-155.
15. + interphotoreceptor retinoid-binding protein-specific T cells in experimental autoimmune uveitis. Invest. Ophthalmol. Visual Sci. 48: 4153-4161.
16. + IL-17-producing T cells are important in effector functions for the elicitation of contact hypersensitivity responses. J. Immunol. 177: 6852-6858.
17. Teunissen, M. B., C. W. Koomen, R. de Waal Malefyt, E. A. Wierenga, and J. D. Bos. 1998. Interleukin-17 and interferon-γ synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J. Invest. Dermatol. 111: 645-649.
18. Taplin, C. E., and J. M. Barker. 2008. Autoantibodies in type 1 diabetes. Autoimmunity 41: 11-18.
19. Itoh, N., T. Hanafusa, A. Miyazaki, J. Miyagawa, K. Yamagata, K. Yamamoto, M. Waguri, A. Imagawa, S. Tamura, M. Inada, et al. 1993. Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients. J. Clin. Invest. 92: 2313-2322. (Pubitemid 23333537)
20. Di Lorenzo, T. P., M. Peakman, and B. O. Roep. 2007. Translational mini-review series on type 1 diabetes: systematic analysis of T cell epitopes in autoimmune diabetes. Clin. Exp. Immunol. 148: 1-16.
21. Kay, T. W., J. L. Parker, L. A. Stephens, H. E. Thomas, and J. Allison. 1996. RIP-beta 2-microglobulin transgene expression restores insulitis, but not diabetes, in beta 2-microglobulin null nonobese diabetic mice. J. Immunol. 157: 3688-3693.
22. + cytotoxic T-cell responses in autoimmune diabetes-prone NOD mice. Diabetes 45: 902-908.
23. + T cells in the initiation of insulin-dependent diabetes mellitus. Eur. J. Immunol. 26: 1762-1769.
24. 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)
25. + T cell deletion induced by cross-presentation of self-antigens and favors autoimmunity. J. Exp. Med. 186: 2057-2062.
26. + T cell tolerance to tissue antigens. J. Immunol. 177: 8291-8295.
27. Zehntner, S. P., C. Brickman, L. Bourbonniere, L. Remington, M. Caruso, and T. Owens. 2005. Neutrophils that infiltrate the central nervous system regulate T cell responses. J. Immunol. 174: 5124-5131. (Pubitemid 40504599)
28. McGeachy, M. J., K. S. Bak-Jensen, Y. Chen, C. M. Tato, W. Blumenschein, T. McClanahan, and D. J. Cua. 2007. TGF-β and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain TH-17 cell-mediated pathology. Nat. Immunol. 8: 1390-1397.
29. Moore, K.W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin- 10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
30. + T and B lymphocytes. J. Immunol. 161: 4420-4427.
31. 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. (Pubitemid 44263906)
32. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132.
33. 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)
34. Kimura, A., T. Naka, and T. Kishimoto. 2007. IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl. Acad. Sci. USA 104: 12099-12104. (Pubitemid 47185636)
35. Asao, H., C. Okuyama, S. Kumaki, N. Ishii, S. Tsuchiya, D. Foster, and K. Sugamura. 2001. Cutting edge: the common γ-chain is an indispensable subunit of the IL-21 receptor complex. J. Immunol. 167: 1-5. (Pubitemid 32567752)
36. Mathur, A. N., H. C. Chang, D. G. Zisoulis, G. L. Stritesky, Q. Yu, J. T. O'Malley, R. Kapur, D. E. Levy, G. S. Kansas, and M. H. Kaplan. 2007. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J. Immunol. 178: 4901-4907.
37. Hildner, K. M., P. Schirmacher, I. Atreya, M. Dittmayer, B. Bartsch, P. R. Galle, S. Wirtz, and M. F. Neurath. 2007. Targeting of the transcription factor STAT4 by antisense phosphorothioate oligonucleotides suppresses collagen-induced arthritis. J. Immunol. 178: 3427-3436.
38. Chen, Z., A. Laurence, and J. J. O'Shea. 2007. Signal transduction pathways and transcriptional regulation in the control of Th17 differentiation. Semin. Immunol. 19: 400-408.
39. Mathur, A. N., H. C. Chang, D. G. Zisoulis, R. Kapur, M. L. Belladonna, G. S. Kansas, and M. H. Kaplan. 2006. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood 108: 1595-1601.
40. Rangachari, M., N. Mauermann, R. R. Marty, S. Dirnhofer, M. O. Kurrer, V. Komnenovic, J. M. Penninger, and U. Eriksson. 2006. T-bet negatively regulates autoimmune myocarditis by suppressing local production of interleukin 17. J. Exp. Med. 203: 2009-2019. (Pubitemid 44188474)
41. + T cell function by the transcription factor Eomesodermin. Science 302: 1041-1043.
42. Gocke, A. R., P. D. Cravens, L. H. Ben, R. Z. Hussain, S. C. Northrop, M. K. Racke, and A. E. Lovett-Racke. 2007. T-bet regulates the fate of Th1 and Th17 lymphocytes in autoimmunity. J. Immunol. 178: 1341-1348.
43. Chen, Y., C. L. Langrish, B. McKenzie, B. Joyce-Shaikh, J. S. Stumhofer, T. McClanahan, W. Blumenschein, T. Churakovsa, J. Low, L. Presta, et al. 2006. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Invest. 116: 1317-1326.
44. Vizler, C., N. Bercovici, A. Heurtier, N. Pardigon, K. Goude, K. Bailly, C. Combadiere, and R. S. Liblau. 2000. Relative diabetogenic properties of isletspecific Tc1 and Tc2 cells in immunocompetent hosts. J. Immunol. 165: 6314-6321.
45. McKenzie, M. D., N. L. Dudek, L. Mariana, M. M. Chong, J. A. Trapani, T. W. Kay, and H. E. Thomas. 2006. Perforin and Fas induced by IFNγ and TNFα mediate β cell death by OT-I CTL. Int. Immunol. 18: 837-846.
46. Kagi, D., B. Odermatt, P. Seiler, R. M. Zinkernagel, T. W. Mak, and H. Hengartner. 1997. Reduced incidence and delayed onset of diabetes in perforin- deficient nonobese diabetic mice. J. Exp. Med. 186: 989-997. (Pubitemid 27441144)
47. + T cell-mediated insulin-dependent diabetes mellitus. J. Immunol. 163: 4335-4341.
48. + clones associated with IFN-γ-inducible protein 10 (CXC chemokine ligand 10) production but not cytokine expression, cytolytic activity, or homing characteristics. J. Immunol. 174: 2746-2755.
49. Gajewski, T. F., and F. W. Fitch. 1990. Anti-proliferative effect of IFN-γ in immune regulation: IV. Murine CTL clones produce IL-3 and GM-CSF, the activity of which is masked by the inhibitory action of secreted IFN-γ. J. Immunol. 144: 548-556.
50. Price, P., R. P. Johnson, D. T. Scadden, C. Jassoy, T. Rosenthal, S. Kalams, and B. D. Walker. 1995. Cytotoxic CD8+ T lymphocytes reactive with human immunodeficiency virus-1 produce granulocyte/macrophage colony-stimulating factor and variable amounts of interleukins 2, 3, and 4 following stimulation with the cognate epitope. Clin. Immunol. Immunopathol. 74: 100-106.
51. Ihle, J. N. 1992. Interleukin-3 and hematopoiesis. Chem. Immunol. 51: 65-106.
52. Kindler, V., B. Thorens, S. de Kossodo, B. Allet, J. F. Eliason, D. Thatcher, N. Farber, and P. Vassalli. 1986. Stimulation of hematopoiesis in vivo by recombinant bacterial murine interleukin 3. Proc. Natl. Acad. Sci. USA 83: 1001-1005. (Pubitemid 16086401)
53. Schrader, J. W. 1986. The panspecific hemopoietin of activated T lymphocytes (interleukin-3). Annu. Rev. Immunol. 4: 205-216.
54. Kroenke, M. A., T. J. Carlson, A. V. Andjelkovic, and B. M. Segal. 2008. IL-12-and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 205: 1535-1541.
55. Liang, S. C., X. Y. Tan, D. P. Luxenberg, R. Karim, K. Dunussi-Joannopoulos, M. Collins, and L. A. Fouser. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203: 2271-2279.
56. H17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445: 648-651.
57. Aggarwal, S., M. H. Xie, M. Maruoka, J. Foster, and A. L. Gurney. 2001. Acinar cells of the pancreas are a target of interleukin-22. J. Interferon Cytokine Res. 21: 1047-1053. (Pubitemid 34114283)
58. Kreymborg, K., R. Etzensperger, L. Dumoutier, S. Haak, A. Rebollo, T. Buch, F. L. Heppner, J. C. Renauld, and B. Becher. 2007. IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis. J. Immunol. 179: 8098-8104.
59. Zenewicz, L. A., G. D. Yancopoulos, D. M. Valenzuela, A. J. Murphy, M. Karow, and R. A. Flavell. 2007. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 27: 647-659.
60. Chang, S. H., and C. Dong. 2007. A novel heterodimeric cytokine consisting of IL-17 and IL-17F regulates inflammatory responses. Cell Res. 17: 435-440.
61. Liang, S. C., A. J. Long, F. Bennett, M. J. Whitters, R. Karim, M. Collins, S. J. Goldman, K. Dunussi-Joannopoulos, C. M. M. Williams, J. F. Wright, and L. A. Fouser. 2007. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J. Immunol. 179: 7791-7799.
62. Jain, R., D. M. Tartar, R. K. Gregg, R. D. Divekar, J. J. Bell, H. H. Lee, P. Yu, J. S. Ellis, C. M. Hoeman, C. L. Franklin, and H. Zaghouani. 2008. Innocuous IFNγ induced by adjuvant-free antigen restores normoglycemia in NOD mice through inhibition of IL-17 production. J. Exp. Med. 205: 207-218. (Pubitemid 351185727)
63. + T cells activated in the presence of TGFβ express FoxP3 and mediate linked suppression of primary immune responses and cardiac allograft rejection. Int. Immunol. 18: 1549-1562.