Critical role of interleukin-17/interleukin-17 receptor axis in mediating Con A-induced hepatitis

Immunology and Cell Biology

Volumn 90, Issue 4, 2012, Pages 421-428

  Yan, Shu ^a   Wang, Luman ^a   Liu, Nan ^a   Wang, Ying ^a   Chu, Yiwei ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

concanavalin A; hepatitis; interleukin 17; Kupffer cell; T cells

Indexed keywords

ALANINE AMINOTRANSFERASE; CONCANAVALIN A; GADOLINIUM CHLORIDE; HYBRID PROTEIN; IMMUNOGLOBULIN G1; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ACUTE HEPATITIS; ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; INJURY SEVERITY; KUPFFER CELL; LIVER CELL; LIVER HISTOLOGY; LIVER INJURY; LIVER NECROSIS; MONONUCLEAR CELL; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CONCANAVALIN A; HEPATITIS; HUMANS; IMMUNOGLOBULIN G; INFLAMMATION; INTERLEUKIN-17; KUPFFER CELLS; LIVER; MICE; RECEPTORS, INTERLEUKIN-17; SIGNAL TRANSDUCTION;

MUS;

EID: 84859948273     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2011.59     Document Type: Article

References (52)

1. Kern M, Popov A, Scholz K, Schumak B, Djandji D, Limmer A et al. Virally infected mouse liver endothelial cells trigger CD8+ T-cell immunity. Gastroenterology 2010; 138: 336-346.
2. Park EJ, Lee JH, Yu GY, He G, Ali SR, Holzer RG et al. Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 2010; 140: 197-208.
3. Wang H, Park O, Lafdil F, Shen K, Horiguchi N, Yin S et al. Interplay of hepatic and myeloid signal transducer and activator of transcription 3 in facilitating liver regeneration via tempering innate immunity. Hepatology 2010; 51: 1354-1362.
4. Bird L. T cell responses: IL-2 overrules tolerogenic liver responses. Nat Rev Immunol 2010; 10: 289.
5. 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.
6. Nakaya M, Hashimoto M, Nakagawa R,Wakabayashi Y, Ishizaki T, Takada I et al. SOCS3 in T and NKT cells negatively regulates cytokine production and ameliorates ConA-induced hepatitis. J Immunol 2009; 183: 7047-7053.
7. Mizuhara H, Uno M, Seki N, Yamashita M, Yamaoka M, Ogawa T et al. Critical involvement of interferon gamma in the pathogenesis of T-cell activation-associated hepatitis and regulatory mechanisms of interleukin-6 for the manifestations of hepatitis. Hepatology 1996; 23: 1608-1615. (Pubitemid 26181246)
8. Schumann J, Wolf D, Pahl A, Brune K, Papadopoulos T, van Rooijen N et al. Importance of Kupffer cells for T-cell-dependent liver injury in mice. Am J Pathol 2000; 157: 1671-1683.
9. Russell JQ, Morrissette GJ, Weidner M, Vyas C, Aleman-Hoey D, Budd RC. Liver damage preferentially results from CD8(+) T cells triggered by high affinity peptide antigens. J Exp Med 1998; 188: 1147-1157. (Pubitemid 28443338)
10. Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol 1991; 260: G355-G362.
11. Decker K. The response of liver macrophages to inflammatory stimulation. Keio J Med 1998; 47: 1-9. (Pubitemid 128473325)
12. Arii S, Imamura M. Physiological role of sinusoidal endothelial cells and Kupffer cells and their implication in the pathogenesis of liver injury. J Hepatobiliary Pancreat Surg 2000; 7: 40-48.
13. Nakashima H, Kinoshita M, Nakashima M, Habu Y, Shono S, Uchida T et al. Superoxide produced by Kupffer cells is an essential effector in concanavalin A-induced hepatitis in mice. Hepatology 2008; 48: 1979-1988.
14. Gantner F, Leist M, Lohse AW, Germann PG, Tiegs G. Concanavalin A-induced T-cell-mediated hepatic injury in mice: the role of tumor necrosis factor. Hepatology 1995; 21: 190-198.
15. MacDonald HR. NK1.1+ T cell receptor-alpha/beta+ cells: new clues to their origin, specificity, and function. J Exp Med 1995; 182: 633-638.
16. Subleski JJ, Wiltrout RH, Weiss JM. Application of tissue-specific NK and NKT cell activity for tumor immunotherapy. J Autoimmun 2009; 33: 275-281.
17. 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 USA 2000; 97: 5498-5503. (Pubitemid 30313747)
18. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004; 21: 467-476. (Pubitemid 39370503)
19. Hamada S, Umemura M, Shiono T, Tanaka K, Yahagi A, Begum MD et al. IL-17A produced by gammadelta T cells plays a critical role in innate immunity against listeria monocytogenes infection in the liver. J Immunol 2008; 181: 3456-3463.
20. Dardalhon V, Korn T, Kuchroo VK, Anderson AC. Role of Th1 and Th17 cells in organ-specific autoimmunity. J Autoimmun 2008; 31: 252-256.
21. Ogura H, Murakami M, Okuyama Y, Tsuruoka M, Kitabayashi C, Kanamoto M et al. Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction. Immunity 2008; 29: 628-636.
22. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH et al. A distinct lineage of CD4T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6: 1133-1141. (Pubitemid 41541791)
23. Yao Z, Fanslow WC, Seldin MF, Rousseau AM, Painter SL, Comeau MR et al. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 1995; 3: 811-821. (Pubitemid 26091152)
24. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001; 194: 519-527. (Pubitemid 32835046)
25. Kramer JM, Yi L, Shen F, Maitra A, Jiao X, Jin T et al. Evidence for ligand-independent multimerization of the IL-17 receptor. J Immunol 2006; 176: 711-715. (Pubitemid 43099664)
26. Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Karow M, Flavell RA. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 2007; 27: 647-659. (Pubitemid 47615503)
27. Nagata T, McKinley L, Peschon JJ, Alcorn JF, Aujla SJ, Kolls JK. Requirement of IL-17RA in Con A induced hepatitis and negative regulation of IL-17 production in mouse T cells. J Immunol 2008; 181: 7473-7479.
28. Lafdil F, Wang H, Park O, Zhang W, Moritoki Y, Yin S et al. Myeloid STAT3 inhibits T cell-mediated hepatitis by regulating T helper 1 cytokine and interleukin-17 production. Gastroenterology 2009; 137: 2125-2135.e1-2.
29. Rachitskaya AV, Hansen AM, Horai R, Li Z, Villasmil R, Luger D et al. 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 2008; 180: 5167-5171.
30. Lan RY, Salunga TL, Tsuneyama K, Lian ZX, Yang GX, Hsu W et al. Hepatic IL-17 responses in human and murine primary biliary cirrhosis. J Autoimmun 2009; 32: 43-51.
31. Yasumi Y, Takikawa Y, Endo R, Suzuki K. Interleukin-17 as a new marker of severity of acute hepatic injury. Hepatol Res 2007; 37: 248-254. (Pubitemid 46505838)
32. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 2009; 31: 331-341.
33. Biswas PS, Gupta S, Chang E, Song L, Stirzaker RA, Liao JK et al. Phosphorylation of IRF4 by ROCK2 regulates IL-17 and IL-21 production and the development of autoimmunity in mice. J Clin Invest 2010; 120: 3280-3295.
34. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201: 233-240. (Pubitemid 40189432)
35. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003; 421: 744-748. (Pubitemid 36227625)
36. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6: 1123-1132. (Pubitemid 41541790)
37. Jaeschke H. Neutrophil-mediated tissue injury in alcoholic hepatitis. Alcohol 2002; 27: 23-27. (Pubitemid 34626480)
38. Bonder CS, Ajuebor MN, Zbytnuik LD, Kubes P, Swain MG. Essential role for neutrophil recruitment to the liver in concanavalin A-induced hepatitis. J Immunol 2004; 172: 45-53. (Pubitemid 38020454)
39. Stark MA, Huo Y, Burcin TL, Morris MA, Olson TS, Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 2005; 22: 285-294. (Pubitemid 40387471)
40. Ley K, Smith E, Stark MA. IL-17A-producing neutrophil-regulatory Tn lymphocytes. Immunol Res 2006; 34: 229-242. (Pubitemid 44195938)
41. Smith E, Stark MA, Zarbock A, Burcin TL, Bruce AC, Vaswani D et al. IL-17A inhibits the expansion of IL-17A-producing T cells in mice through 'short-loop' inhibition via IL-17 receptor. J Immunol 2008; 181: 1357-1364.
42. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med 2007; 13: 139-145.
43. Dong C. Diversification of T-helper-cell lineages: finding the family root of IL-17-producing cells. Nat Rev Immunol 2006; 6: 329-333.
44. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A et al. Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 2010; 32: 681-691.
45. Trautwein C, Rakemann T, Brenner DA, Streetz K, Licato L, Manns MP et al. Concanavalin A-induced liver cell damage: activation of intracellular pathways triggered by tumor necrosis factor in mice. Gastroenterology 1998; 114: 1035-1045. (Pubitemid 28217571)
46. Kono H, Fujii H, Asakawa M, Yamamoto M, Maki A, Matsuda M et al. Functional heterogeneity of the kupffer cell population is involved in the mechanism of gadolinium chloride in rats administered endotoxin. J Surg Res 2002; 106: 179-187.
47. Li B, Sun R, Wei H, Gao B, Tian Z. Interleukin-15 prevents concanavalin A-induced liver injury in mice via NKT cell-dependent mechanism. Hepatology 2006; 43: 1211-1219. (Pubitemid 43980099)
48. Sun R, Tian Z, Kulkarni S, Gao B. IL-6 prevents T cell-mediated hepatitis via inhibition of NKT cells in CD4+ T cell- and STAT3-dependent manners. J Immunol 2004; 172: 5648-5655. (Pubitemid 38542068)
49. Holub M, Cheng CW, Mott S, Wintermeyer P, van Rooijen N, Gregory SH. Neutrophils sequestered in the liver suppress the proinflammatory response of Kupffer cells to systemic bacterial infection. J Immunol 2009; 183: 3309-3316.
50. Pillarisetty VG, Shah AB, Miller G, Bleier JI, DeMatteo RP. Liver dendritic cells are less immunogenic than spleen dendritic cells because of differences in subtype composition. J Immunol 2004; 172: 1009-1017. (Pubitemid 38113760)
51. Gehring S, Dickson EM, San Martin ME, van Rooijen N, Papa EF, Harty MW et al. Kupffer cells abrogate cholestatic liver injury in mice. Gastroenterology 2006; 130: 810-822. (Pubitemid 43374530)
52. West MA, Billiar TR, Curran RD, Hyland BJ, Simmons RL. Evidence that rat Kupffer cells stimulate and inhibit hepatocyte protein synthesis in vitro by different mechanisms. Gastroenterology 1989; 96: 1572-1582. (Pubitemid 19138703)