Vγ4 γδ T cell-derived IL-17A negatively regulates NKT cell function in con A-induced fulminant hepatitis

Journal of Immunology

Volumn 187, Issue 10, 2011, Pages 5007-5014

  Zhao, Na ^a,b   Hao, Jianlei ^a   Ni, Yuanyuan ^a   Luo, Wei ^a   Liang, Ruifang ^a   Cao, Guangchao ^a   Zhao, Yapu ^a   Wang, Puyue ^a   Zhao, Liqing ^a   Tian, Zhigang ^c   Flavell, Richard ^d   Hong, Zhangyong ^a   Han, Jihong ^a   Yao, Zhi ^b   Wu, Zhenzhou ^a   Yin, Zhinan ^a  

^a NANKAI UNIVERSITY   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONCANAVALIN A; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 17F; T LYMPHOCYTE RECEPTOR DELTA CHAIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; FEMALE; GAMMA DELTA T LYMPHOCYTE; HEPATITIS; IMMUNOREGULATION; MALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; VGAMMA1 GAMMA DELTA T CELL; VGAMMA4 GAMMA DELTA T CELL;

ANIMALS; CONCANAVALIN A; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; INTERFERON-GAMMA; INTERLEUKIN-17; LIVER FAILURE, ACUTE; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NATURAL KILLER T-CELLS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS;

EID: 81455141970     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101315     Document Type: Article

References (44)

1. Tiegs, G., J. Hentschel, and A. Wendel. 1992. A T cell-dependent experimental liver injury in mice inducible by concanavalin A. J. Clin. Invest. 90: 196-203.
2. Takeda, K., Y. Hayakawa, L. Van Kaer, H. Matsuda, H. Yagita, and K. Okumura. 2000. Critical contribution of liver natural killer T cells to a murine model of hepatitis. Proc. Natl. Acad. Sci. USA 97: 5498-5503. (Pubitemid 30313747)
3. Jaruga, B., F. Hong, W. H. Kim, and B. Gao. 2004. IFN-gamma/STAT1 acts as a proinflammatory signal in T cell-mediated hepatitis via induction of multiple chemokines and adhesion molecules: a critical role of IRF-1. Am. J. Physiol. Gastrointest. Liver Physiol. 287: G1044-G1052. (Pubitemid 39423697)
4. Kaneko, Y., M. Harada, T. Kawano, M. Yamashita, Y. Shibata, F. Gejyo, T. Nakayama, and M. Taniguchi. 2000. Augmentation of Valpha14 NKT cellmediated cytotoxicity by interleukin 4 in an autocrine mechanism resulting in the development of concanavalin A-induced hepatitis. J. Exp. Med. 191: 105-114. (Pubitemid 30043652)
5. Küsters, S., F. Gantner, G. Künstle, and G. Tiegs. 1996. Interferon gamma plays a critical role in T cell-dependent liver injury in mice initiated by concanavalin A. Gastroenterology 111: 462-471.
6. Siebler, J., S. Wirtz, S. Klein, M. Protschka, M. Blessing, P. R. Galle, and M. F. Neurath. 2003. A key pathogenic role for the STAT1/T-bet signaling pathway in T-cell-mediated liver inflammation. Hepatology 38: 1573-1580. (Pubitemid 37466983)
7. -/-) mice: role for IFN-gamma in activating apoptosis of hepatocytes. J. Immunol. 159: 1418-1428.
8. Carding, S. R., and P. J. Egan. 2002. Gammadelta T cells: functional plasticity and heterogeneity. Nat. Rev. Immunol. 2: 336-345. (Pubitemid 37328756)
9. Born, W. K., Z. Yin, Y. S. Hahn, D. Sun, and R. L. O'Brien. 2010. Analysis of gamma delta T cell functions in the mouse. J. Immunol. 184: 4055-4061.
10. Hao, J., X.Wu, S. Xia, Z. Li, T.Wen, N. Zhao, Z.Wu, P.Wang, L. Zhao, and Z. Yin. 2010. Current progress in γδ T-cell biology. Cell. Mol. Immunol. 7: 409-413.
11. O'Brien, R. L., M. P. Happ, A. Dallas, E. Palmer, R. Kubo, and W. K. Born. 1989. Stimulation of a major subset of lymphocytes expressing T cell receptor gamma delta by an antigen derived from Mycobacterium tuberculosis. Cell 57: 667-674. (Pubitemid 19140647)
12. Hiromatsu, K., Y. Yoshikai, G. Matsuzaki, S. Ohga, K. Muramori, K. Matsumoto, J. A. Bluestone, and K. Nomoto. 1992. A protective role of gamma/delta T cells in primary infection with Listeria monocytogenes in mice. J. Exp. Med. 175: 49-56.
13. Chien, Y. H., and Y. Konigshofer. 2007. Antigen recognition by gammadelta T cells. Immunol. Rev. 215: 46-58.
14. Jensen, K. D., X. Su, S. Shin, L. Li, S. Youssef, S. Yamasaki, L. Steinman, T. Saito, R. M. Locksley, M. M. Davis, et al. 2008. Thymic selection determines gammadelta T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon gamma. Immunity 29: 90-100.
15. Yin, Z., D. H. Zhang, T. Welte, G. Bahtiyar, S. Jung, L. Liu, X. Y. Fu, A. Ray, and J. Craft. 2000. Dominance of IL-12 over IL-4 in gamma delta T cell differentiation leads to default production of IFN-gamma: failure to down-regulate IL-12 receptor beta 2-chain expression. J. Immunol. 164: 3056-3064. (Pubitemid 30148965)
16. Yin, Z., C. Chen, S. J. Szabo, L. H. Glimcher, A. Ray, and J. Craft. 2002. T-Bet expression and failure of GATA-3 cross-regulation lead to default production of IFN-gamma by gammadelta T cells. J. Immunol. 168: 1566-1571. (Pubitemid 34135750)
17. Chen, L., W. He, S. T. Kim, J. Tao, Y. Gao, H. Chi, A. M. Intlekofer, B. Harvey, S. L. Reiner, Z. Yin, et al. 2007. Epigenetic and transcriptional programs lead to default IFN-gamma production by gammadelta T cells. J. Immunol. 178: 2730-2736. (Pubitemid 46333149)
18. Gao, Y., W. Yang, M. Pan, E. Scully, M. Girardi, L. H. Augenlicht, J. Craft, and Z. Yin. 2003. Gamma delta T cells provide an early source of interferon gamma in tumor immunity. J. Exp. Med. 198: 433-442. (Pubitemid 36976054)
19. He, W., J. Hao, S. Dong, Y. Gao, J. Tao, H. Chi, R. Flavell, R. L. O'Brien, W. K. Born, J. Craft, et al. 2010. Naturally activated V gamma 4 gamma delta T cells play a protective role in tumor immunity through expression of eomesodermin. J. Immunol. 185: 126-133.
20. Heilig, J. S., and S. Tonegawa. 1986. Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature 322: 836-840. (Pubitemid 16055256)
21. Ito, K., M. Bonneville, Y. Takagaki, N. Nakanishi, O. Kanagawa, E. G. Krecko, and S. Tonegawa. 1989. Different gamma delta T-cell receptors are expressed on thymocytes at different stages of development. Proc. Natl. Acad. Sci. USA 86: 631-635. (Pubitemid 19037794)
22. Pereira, P., D. Gerber, S. Y. Huang, and S. Tonegawa. 1995. Ontogenic development and tissue distribution of V gamma 1-expressing gamma/delta T lymphocytes in normal mice. J. Exp. Med. 182: 1921-1930.
23. Hahn, Y. S., C. Taube, N. Jin, L. Sharp, J. M. Wands, M. K. Aydintug, M. Lahn, S. A. Huber, R. L. O'Brien, E. W. Gelfand, and W. K. Born. 2004. Different potentials of gamma delta T cell subsets in regulating airway responsiveness: V gamma 1+ cells, but not V gamma 4+ cells, promote airway hyperreactivity, Th2 cytokines, and airway inflammation. J. Immunol. 172: 2894-2902. (Pubitemid 38263675)
24. Hahn, Y. S., C. Taube, N. Jin, K. Takeda, J. W. Park, J. M. Wands, M. K. Aydintug, C. L. Roark, M. Lahn, R. L. O'Brien, et al. 2003. V gamma 4+ gamma delta T cells regulate airway hyperreactivity to methacholine in ovalbumin-sensitized and challenged mice. J. Immunol. 171: 3170-3178. (Pubitemid 37093542)
25. Huang, Y., N. Jin, C. L. Roark, M. K. Aydintug, J. M. Wands, H. Huang, R. L. O'Brien, and W. K. Born. 2009. The influence of IgE-enhancing and IgEsuppressive gammadelta T cells changes with exposure to inhaled ovalbumin. J. Immunol. 183: 849-855.
26. Huber, S. A., D. Graveline, M. K. Newell, W. K. Born, and R. L. O'Brien. 2000. V gamma 1+ T cells suppress and V gamma 4+ T cells promote susceptibility to coxsackievirus B3-induced myocarditis in mice. J. Immunol. 165: 4174-4181.
27. Roark, C. L., J. D. French, M. A. Taylor, A. M. Bendele, W. K. Born, and R. L. O'Brien. 2007. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gamma delta T cells. J. Immunol. 179: 5576-5583.
28. Hamada, S., M. Umemura, T. Shiono, K. Tanaka, A. Yahagi, M. D. Begum, K. Oshiro, Y. Okamoto, H. Watanabe, K. Kawakami, et al. 2008. IL-17A produced by gammadelta T cells plays a critical role in innate immunity against listeria monocytogenes infection in the liver. J. Immunol. 181: 3456-3463.
29. Nakae, S., Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387. (Pubitemid 35279557)
30. Shi, G., Z. Zhang, D. Feng, Y. Xu, Y. Lu, J. Wang, J. Jiang, Z. Zhang, X. Li, and G. Ning. 2010. Selection of reference genes for quantitative real-time reverse transcription-polymerase chain reaction in concanavalin A-induced hepatitis model. Anal. Biochem. 401: 81-90.
31. Ribot, J. C., A. deBarros, D. J. Pang, J. F. Neves, V. Peperzak, S. J. Roberts, M. Girardi, J. Borst, A. C. Hayday, D. J. Pennington, and B. Silva-Santos. 2009. CD27 is a thymic determinant of the balance between interferon-gamma- and interleukin 17-producing gammadelta T cell subsets. Nat. Immunol. 10: 427-436.
32. Li, B., R. Sun, H. Wei, B. Gao, and Z. Tian. 2006. Interleukin-15 prevents concanavalin A-induced liver injury in mice via NKT cell-dependent mechanism. Hepatology 43: 1211-1219. (Pubitemid 43980099)
33. Bonneville, M., R. L. O'Brien, and W. K. Born. 2010. Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 10: 467-478.
34. Tough, D. F., and J. Sprent. 1998. Lifespan of gamma/delta T cells. J. Exp. Med. 187: 357-365.
35. Kronenberg, M., and L. Gapin. 2002. The unconventional lifestyle of NKT cells. Nat. Rev. Immunol. 2: 557-568. (Pubitemid 37328731)
36. Stetson, D. B., M. Mohrs, R. L. Reinhardt, J. L. Baron, Z. E. Wang, L. Gapin, M. Kronenberg, and R. M. Locksley. 2003. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J. Exp. Med. 198: 1069-1076. (Pubitemid 37248622)
37. Xu, S., Y. Han, X. Xu, Y. Bao, M. Zhang, and X. Cao. 2010. IL-17A-producing gammadeltaT cells promote CTL responses against Listeria monocytogenes infection by enhancing dendritic cell cross-presentation. J. Immunol. 185: 5879-5887.
38. Jin, N., C. L. Roark, N. Miyahara, C. Taube, M. K. Aydintug, J. M. Wands, Y. Huang, Y. S. Hahn, E. W. Gelfand, R. L. O'Brien, and W. K. Born. 2009. Allergic airway hyperresponsiveness-enhancing gammadelta T cells develop in normal untreated mice and fail to produce IL-4/13, unlike Th2 and NKT cells. J. Immunol. 182: 2002-2010.
39. 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.
40. Wondimu, Z., T. Santodomingo-Garzon, T. Le, and M. G. Swain. 2010. Protective role of interleukin-17 in murine NKT cell-driven acute experimental hepatitis. Am. J. Pathol. 177: 2334-2346.
41. 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. (Pubitemid 47615503)
42. Lee, Y. K., J. S. Menezes, Y. Umesaki, and S. K. Mazmanian. 2011. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 108(Suppl. 1): 4615-4622.
43. Esplugues, E., S. Huber, N. Gagliani, A. E. Hauser, T. Town, Y. Y. Wan, W. O'Connor, Jr., A. Rongvaux, N. Van Rooijen, A. M. Haberman, et al. 2011. Control of TH17 cells occurs in the small intestine. Nature 475: 514-518.
44. O'Connor, W., Jr., M. Kamanaka, C. J. Booth, T. Town, S. Nakae, Y. Iwakura, J. K. Kolls, and R. A. Flavell. 2009. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 10: 603-609.