High susceptibility to liver injury in IL-27 p28 conditional knockout mice involves intrinsic interferon-γ dysregulation of CD4+ T cells

Hepatology

Volumn 57, Issue 4, 2013, Pages 1620-1631

  Zhang, Song ^a   Liang, Ruifang ^a   Luo, Wei ^a   Liu, Chang ^a   Wu, Xiaoli ^a   Gao, Yanan ^b   Hao, Jianlei ^a   Cao, Guangchao ^a   Chen, Xi ^a   Wei, Jun ^a   Xia, Siyuan ^a   Li, Zheng ^a   Wen, Ti ^a   Wu, Yunyun ^a   Zhou, Xinglong ^a   Wang, Puyue ^a   Zhao, Liqing ^a   Wu, Zhengzhou ^a   Xiong, Sidong ^c   Gao, Xiaoming ^c   Gao, Xiang ^d   Chen, Yongyan ^e   Ge, Qing ^b   Tian, Zhigang ^e   Yin, Zhinan ^a   more..

^a NANKAI UNIVERSITY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c SOOCHOW UNIVERSITY   (China)

^d NANJING UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

CONCANAVALIN A; GAMMA INTERFERON; INTERLEUKIN 27; MESSENGER RNA; NEUTRALIZING ANTIBODY; PROTEIN P28;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE PREDISPOSITION; FEMALE; GENE INACTIVATION; IMMUNE DYSREGULATION; INFLAMMATION; KNOCKOUT MOUSE; LIVER INJURY; MALE; MOLECULAR PATHOLOGY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; THYMUS; WILD TYPE;

ANIMALS; ANTIGENS, CD11C; CD4-POSITIVE T-LYMPHOCYTES; CONCANAVALIN A; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG-INDUCED LIVER INJURY; FEMALE; INTERFERON-GAMMA; INTERLEUKIN-17; KILLER CELLS, NATURAL; MALE; MICE; MICE, KNOCKOUT;

EID: 84876129756     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26166     Document Type: Article

References (33)

1. Tiegs G, Hentschel J, Wendel A. A T cell-dependent experimental liver injury in mice inducible by concanavalin A. J Clin Invest 1992; 90: 196-203.
2. Mizuhara H, O'Neill E, Seki N, Ogawa T, Kusunoki C, Otsuka K, Satoh S, et al. T cell activation-associated hepatic injury: mediation by tumor necrosis factors and protection by interleukin 6. J Exp Med 1994; 179: 1529-1537.
3. Gao B, Jeong WI, Tian Z. Liver: an organ with predominant innate immunity. HEPATOLOGY 2008; 47: 729-736.
4. Gao B, Radaeva S, Park O. Liver natural killer and natural killer T cells: immunobiology and emerging roles in liver diseases. J Leukoc Biol 2009; 86: 513-528.
5. Takeda K, Hayakawa Y, Van Kaer L, Matsuda H, Yagita H, Okumura K. Critical contribution of liver natural killer T cells to a murine model of hepatitis. Proc Natl Acad Sci U S A 2000; 97: 5498-5503.
6. Kaneko Y, Harada M, Kawano T, Yamashita M, Shibata Y, Gejyo F, et al. Augmentation of Valpha14 NKT cell-mediated cytotoxicity by interleukin 4 in an autocrine mechanism resulting in the development of concanavalin A-induced hepatitis. J Exp Med 2000; 191: 105-114.
7. Kusters S, Gantner F, Kunstle G, Tiegs G. Interferon gamma plays a critical role in T cell-dependent liver injury in mice initiated by concanavalin A. Gastroenterology 1996; 111: 462-471.
8. Tagawa Y, Sekikawa K, Iwakura Y. Suppression of concanavalin A-induced hepatitis in IFN-gamma(-/-) mice, but not in TNF-alpha(-/-) mice: role for IFN-gamma in activating apoptosis of hepatocytes. J Immunol 1997; 159: 1418-1428.
9. Hong F, Jaruga B, Kim WH, Radaeva S, El-Assal ON, Tian Z, et al. Opposing roles of STAT1 and STAT3 in T cell-mediated hepatitis: regulation by SOCS. J Clin Invest 2002; 110: 1503-1513.
10. Pflanz S, Timans JC, Cheung J, Rosales R, Kanzler H, Gilbert J, et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002; 16: 779-790.
11. Villarino AV, Hunter CA. Biology of recently discovered cytokines: discerning the pro- and anti-inflammatory properties of interleukin-27. Arthritis Res Ther 2004; 6: 225-233.
12. Yoshida H, Miyazaki Y. Regulation of immune responses by interleukin-27. Immunol Rev 2008; 226: 234-247.
13. Yoshida H, Nakaya M, Miyazaki Y. Interleukin 27: a double-edged sword for offense and defense. J Leukoc Biol 2009; 86: 1295-1303.
14. Wojno ED, Hunter CA. New directions in the basic and translational biology of interleukin-27. Trends Immunol 2012; 33: 91-97.
15. Nicoletti F, Di Marco R, Zaccone P, Salvaggio A, Magro G, Bendtzen K, et al. Murine concanavalin A-induced hepatitis is prevented by interleukin 12 (IL-12) antibody and exacerbated by exogenous IL-12 through an interferon-gamma-dependent mechanism. HEPATOLOGY 2000; 32: 728-733.
16. Xu M, Morishima N, Mizoguchi I, Chiba Y, Fujita K, Kuroda M, et al. Regulation of the development of acute hepatitis by IL-23 through IL-22 and IL-17 production. Eur J Immunol 2011; 41: 2828-2839.
17. Siebler J, Wirtz S, Frenzel C, Schuchmann M, Lohse AW, Galle PR, et al. Cutting edge: a key pathogenic role of IL-27 in T cell-mediated hepatitis. J Immunol 2008; 180: 30-33.
18. Yamanaka A, Hamano S, Miyazaki Y, Ishii K, Takeda A, Mak TW, et al. Hyperproduction of proinflammatory cytokines by WSX-1-deficient NKT cells in concanavalin A-induced hepatitis. J Immunol 2004; 172: 3590-3596.
19. Stumhofer JS, Tait ED, Quinn WJ 3rd, Hosken N, Spudy B, Goenka R, et al. A role for IL-27p28 as an antagonist of gp130-mediated signaling. Nat Immunol 2010; 11: 1119-1126.
20. Shimozato O, Sato A, Kawamura K, Chiyo M, Ma G, Li Q, et al. The secreted form of p28 subunit of interleukin (IL)-27 inhibits biological functions of IL-27 and suppresses anti-allogeneic immune responses. Immunology 2009; 128: e816-e825.
21. Dibra D, Cutrera J, Xia X, Kallakury B, Mishra L, Li S. Interleukin-30: a novel antiinflammatory cytokine candidate for prevention and treatment of inflammatory cytokine-induced liver injury. HEPATOLOGY 2012; 55: 1204-1214.
22. Toyabe S, Seki S, Iiai T, Takeda K, Shirai K, Watanabe H, et al. Requirement of IL-4 and liver NK1+ T cells for concanavalin A-induced hepatic injury in mice. J Immunol 1997; 159: 1537-1542.
23. Gao B, Wang H, Lafdil F, Feng D. STAT proteins-key regulators of anti-viral responses, inflammation, and tumorigenesis in the liver. J Hepatol 2012; 57: 430-441.
24. Liu J, Guan X, Ma X. Regulation of IL-27 p28 gene expression in macrophages through MyD88- and interferon-gamma-mediated pathways. J Exp Med 2007; 204: 141-152.
25. Liu F, Song Y, Liu D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther 1999; 6: 1258-1266.
26. Lazarevic V, Glimcher LH. T-bet in disease. Nat Immunol 2011; 12: 597-606.
27. Robertson NJ, Fairchild PJ, Waldmann H. Ectopic transplantation of tissues under the kidney capsule. Methods Mol Biol 2007; 380: 347-353.
28. Carpenter AC, Bosselut R. Decision checkpoints in the thymus. Nat Immunol 2010; 11: 666-673.
29. Klein L, Hinterberger M, Wirnsberger G, Kyewski B. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat Rev Immunol 2009; 9: 833-844.
30. Yu W, Nagaoka H, Jankovic M, Misulovin Z, Suh H, Rolink A, et al. Continued RAG expression in late stages of B cell development and no apparent re-induction after immunization. Nature 1999; 400: 682-687.
31. Lucas S, Ghilardi N, Li J, de Sauvage FJ. IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and -independent mechanisms. Proc Natl Acad Sci U S A 2003; 100: 15047-15052.
32. Owaki T, Asakawa M, Morishima N, Hata K, Fukai F, Matsui M, et al. A role for IL-27 in early regulation of Th1 differentiation. J Immunol 2005; 175: 2191-2200.
33. Crabe S, Guay-Giroux A, Tormo AJ, Duluc D, Lissilaa R, Guilhot F, et al. The IL-27 p28 subunit binds cytokine-like factor 1 to form a cytokine regulating NK and T cell activities requiring IL-6R for signaling. J Immunol 2009; 183: 7692-7702.