Secretion of IFN-γ but not IL-17 by CD1d-restricted NKT cells enhances rejection of skin grafts expressing epithelial cell-derived antigen

Journal of Immunology

Volumn 184, Issue 10, 2010, Pages 5663-5669

  Mattarollo, Stephen R ^a   Yong, Michelle ^a   Tan, Lieven ^a   Frazer, Ian H ^a   Leggatt, Graham R ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CD1D ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 17; CD1D1 PROTEIN, MOUSE; IL17A PROTEIN, MOUSE; OVALBUMIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS PRESENTATION; EFFECTOR CELL; GRAFT REJECTION; IMMUNE RESPONSE; INTERFERON PRODUCTION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; SKIN GRAFT; TH1 CELL; TH17 CELL; TUMOR IMMUNOLOGY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; EPITHELIUM CELL; GENETICS; IMMUNOLOGY; KERATINOCYTE; LYMPH NODE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SECRETION; SKIN TRANSPLANTATION; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; ANTIGENS, CD1D; EPITHELIAL CELLS; GRAFT REJECTION; INTERFERON-GAMMA; INTERLEUKIN-17; KERATINOCYTES; LYMPH NODES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NATURAL KILLER T-CELLS; OVALBUMIN; SKIN TRANSPLANTATION; UP-REGULATION;

EID: 77954695595     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903730     Document Type: Article

References (39)

1. Ma, H. L., S. Liang, J. Li, L. Napierata, T. Brown, S. Benoit, M. Senices, D. Gill, K. Dunussi-Joannopoulos, M. Collins, et al. 2008. IL-22 is required for Th17 cell-mediated pathology in a mouse model of psoriasis-like skin inflammation. J. Clin. Invest. 118: 597-607.
2. van Beelen, A. J., M. B. Teunissen, M. L. Kapsenberg, and E. C. de Jong. 2007. Interleukin-17 in inflammatory skin disorders. Curr. Opin. Allergy Clin. Immunol. 7: 374-381.
3. Zheng, Y., D. M. Danilenko, P. Valdez, I. Kasman, J. Eastham-Anderson, J. Wu, and W. Ouyang. 2007. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445: 648-651. (Pubitemid 46232884)
4. Awasthi, A., and V. K. Kuchroo. 2009. IL-17A directly inhibits TH1 cells and thereby suppresses development of intestinal inflammation. Nat. Immunol. 10: 568-570.
5. Cruz, A., S. A. Khader, E. Torrado, A. Fraga, J. E. Pearl, J. Pedrosa, A. M. Cooper, and A. G. Castro. 2006. Cutting edge: IFN-gamma regulates the induction and expansion of IL-17-producing CD4 T cells during mycobacterial infection. J. Immunol. 177: 1416-1420.
6. Irmler, I. M., M. Gajda, and R. Bräuer. 2007. Exacerbation of antigen-induced arthritis in IFN-gamma-deficient mice as a result of unrestricted IL-17 response. J. Immunol. 179: 6228-6236.
7. Kelchtermans, H., E. Schurgers, L. Geboes, T. Mitera, J. Van Damme, J. Van Snick, C. Uyttenhove, and P. Matthys. 2009. Effector mechanisms of interleukin-17 in collagen-induced arthritis in the absence of interferon-gamma and counteraction by interferon-gamma. Arthritis Res. Ther. 11: R122.
8. Kryczek, I., A. T. Bruce, J. E. Gudjonsson, A. Johnston, A. Aphale, L. Vatan, W. Szeliga, Y. Wang, Y. Liu, T. H. Welling, et al. 2008. Induction of IL-17+ T cell trafficking and development by IFN-gamma: mechanism and pathological relevance in psoriasis. J. Immunol. 181: 4733-4741.
9. Xiao, M., C. Wang, J. Zhang, Z. Li, X. Zhao, and Z. Qin. 2009. IFNgamma promotes papilloma development by up-regulating Th17-associated inflammation. Cancer Res. 69: 2010-2017.
10. He, D., L. Wu, H. K. Kim, H. Li, C. A. Elmets, and H. Xu. 2009. IL-17 and IFN-gamma mediate the elicitation of contact hypersensitivity responses by different mechanisms and both are required for optimal responses. J. Immunol. 183: 1463-1470.
11. Balato, A., D. Unutmaz, and A. A. Gaspari. 2009. Natural killer T cells: an unconventional T-cell subset with diverse effector and regulatory functions. J. Invest. Dermatol. 129: 1628-1642.
12. Coquet, J. M., K. Kyparissoudis, D. G. Pellicci, G. Besra, S. P. Berzins, M. J. Smyth, and D. I. Godfrey. 2007. IL-21 is produced by NKT cells and modulates NKT cell activation and cytokine production. J. Immunol. 178: 2827-2834. (Pubitemid 46333160)
13. Goto, M., M. Murakawa, K. Kadoshima-Yamaoka, Y. Tanaka, K. Nagahira, Y. Fukuda, and T. Nishimura. 2009. Murine NKT cells produce Th17 cytokine interleukin-22. Cell. Immunol. 254: 81-84.
14. Coquet, J. M., S. Chakravarti, K. Kyparissoudis, F. W. McNab, L. A. Pitt, B. S. McKenzie, S. P. Berzins, M. J. Smyth, and D. I. Godfrey. 2008. Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc. Natl. Acad. Sci. USA 105: 11287-11292.
15. Doisne, J. M., C. Becourt, L. Amniai, N. Duarte, J. B. Le Luduec, G. Eberl, and K. Benlagha. 2009. Skin and peripheral lymph node invariant NKT cells are mainly retinoic acid receptor-related orphan receptor (gamma)t+ and respond preferentially under inflammatory conditions. J. Immunol. 183: 2142-2149.
16. Lee, K. A., M. H. Kang, Y. S. Lee, Y. J. Kim, D. H. Kim, H. J. Ko, and C. Y. Kang. 2008. A distinct subset of natural killer T cells produces IL-17, contributing to airway infiltration of neutrophils but not to airway hyperreactivity. Cell. Immunol. 251: 50-55.
17. Rachitskaya, A. V., A. M. Hansen, R. Horai, Z. Li, R. Villasmil, D. Luger, R. B. Nussenblatt, and R. R. Caspi. 2008. Cutting edge: NKT cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J. Immunol. 180: 5167-5171.
18. Yoshiga, Y., D. Goto, S. Segawa, Y. Ohnishi, I. Matsumoto, S. Ito, A. Tsutsumi, M. Taniguchi, and T. Sumida. 2008. Invariant NKT cells produce IL-17 through IL-23-dependent and -independent pathways with potential modulation of Th17 response in collagen-induced arthritis. Int. J. Mol. Med. 22: 369-374.
19. Michel, M. L., A. C. Keller, C. Paget, M. Fujio, F. Trottein, P. B. Savage, C. H. Wong, E. Schneider, M. Dy, and M. C. Leite-de-Moraes. 2007. Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J. Exp. Med. 204: 995-1001.
20. Azukizawa, H., H. Kosaka, S. Sano, W. R. Heath, I. Takahashi, X. H. Gao, Y. Sumikawa, M. Okabe, K. Yoshikawa, and S. Itami. 2003. Induction of T-cell-mediated skin disease specific for antigen transgenically expressed in keratinocytes. Eur. J. Immunol. 33: 1879-1888.
21. Matsuda, J. L., O. V. Naidenko, L. Gapin, T. Nakayama, M. Taniguchi, C. R. Wang, Y. Koezuka, and M. Kronenberg. 2000. Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J. Exp. Med. 192: 741-754.
22. Dunn, L. A., M. Evander, R. W. Tindle, A. L. Bulloch, R. L. de Kluyver, G. J. Fernando, P. F. Lambert, and I. H. Frazer. 1997. Presentation of the HPV16E7 protein by skin grafts is insufficient to allow graft rejection in an E7-primed animal. Virology 235: 94-103.
23. Matsumoto, K., G. R. Leggatt, J. Zhong, X. Liu, R. L. de Kluyver, T. Peters, G. J. Fernando, A. Liem, P. F. Lambert, and I. H. Frazer. 2004. Impaired antigen presentation and effectiveness of combined active/passive immunotherapy for epithelial tumors. J. Natl. Cancer Inst. 96: 1611-1619.
24. Kenna, T. J., R. Thomas, and R. J. Steptoe. 2008. Steady-state dendritic cells expressing cognate antigen terminate memory CD8+ T-cell responses. Blood 111: 2091-2100.
25. Narayan, S., A. Choyce, G. J. Fernando, and G. R. Leggatt. 2007. Secondary immunisation with high-dose heterologous peptide leads to CD8 T cell populations with reduced functional avidity. Eur. J. Immunol. 37: 406-415.
26. Crowe, N. Y., J. M. Coquet, S. P. Berzins, K. Kyparissoudis, R. Keating, D. G. Pellicci, Y. Hayakawa, D. I. Godfrey, and M. J. Smyth. 2005. Differential antitumor immunity mediated by NKT cell subsets in vivo. J. Exp. Med. 202: 1279-1288.
27. Gumperz, J. E., S. Miyake, T. Yamamura, and M. B. Brenner. 2002. Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining. J. Exp. Med. 195: 625-636.
28. Godfrey, D. I., K. J. Hammond, L. D. Poulton, M. J. Smyth, and A. G. Baxter. 2000. NKT cells: facts, functions and fallacies. Immunol. Today 21: 573-583.
29. Godfrey, D. I., and M. Kronenberg. 2004. Going both ways: immune regulation via CD1d-dependent NKT cells. J. Clin. Invest. 114: 1379-1388.
30. Guillonneau, C., J. D. Mintern, F. X. Hubert, A. C. Hurt, G. S. Besra, S. Porcelli, I. G. Barr, P. C. Doherty, D. I. Godfrey, and S. J. Turner. 2009. Combined NKT cell activation and influenza virus vaccination boosts memory CTL generation and protective immunity. Proc. Natl. Acad. Sci. USA 106: 3330-3335.
31. Hong, C., H. Lee, Y. K. Park, J. Shin, S. Jung, H. Kim, S. Hong, and S. H. Park. 2009. Regulation of secondary antigen-specific CD8(+) T-cell responses by natural killer T cells. Cancer Res. 69: 4301-4308.
32. Atalar, K., B. Afzali, G. Lord, and G. Lombardi. 2009. Relative roles of Th1 and Th17 effector cells in allograft rejection. Curr. Opin. Organ Transplant. 14: 23-29.
33. Bettelli, E., T. Korn, M. Oukka, and V. K. Kuchroo. 2008. Induction and effector functions of T(H)17 cells. Nature 453: 1051-1057.
34. Chen, Y., and K. J. Wood. 2007. Interleukin-23 and TH17 cells in transplantation immunity: does 23+17 equal rejection? Transplantation 84: 1071-1074.
35. Mills, K. H. 2008. Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 38: 2636-2649.
36. Mattarollo, S. R., A. Rahimpour, A. Choyce, D. I. Godfrey, G. R. Leggatt, and I. H. Frazer. 2010. Invariant NKT cells in hyperplastic skin induce a local immune suppressive environment by IFN-gamma production. J. Immunol. 184: 1242-1250.
37. Dander, E., A. Balduzzi, G. Zappa, G. Lucchini, P. Perseghin, V. Andrè, E. Todisco, D. Rahal, M. Migliavacca, D. Longoni, et al. 2009. Interleukin-17-producing T-helper cells as new potential player mediating graft-versus-host disease in patients undergoing allogeneic stem-cell transplantation. Transplantation 88: 1261-1272.
38. Chang, D. H., H. Deng, P. Matthews, J. Krasovsky, G. Ragupathi, R. Spisek, A. Mazumder, D. H. Vesole, S. Jagannath, and M. V. Dhodapkar. 2008. Inflammation-associated lysophospholipids as ligands for CD1d-restricted T cells in human cancer. Blood 112: 1308-1316.
39. Holleran, W. M., Y. Takagi, and Y. Uchida. 2006. Epidermal sphingolipids: metabolism, function, and roles in skin disorders. FEBS Lett. 580: 5456-5466.