Pivotal roles of the interleukin-23/T helper 17 cell axis in hepatitis B

Liver International

Volumn 32, Issue 6, 2012, Pages 894-901

  Huang, Zemin ^a   van Velkinburgh, Jennifer C ^b   Ni, Bing ^a   Wu, Yuzhang ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b Van Velkinburgh Initiative for Collaboratory BioMedical Research   (United States)

Author keywords

Hepatitis B; IL 21; IL 22; IL 23; Th17

Indexed keywords

CYTOKINE; INTERLEUKIN 17; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23;

HEPATITIS; HEPATITIS B; HUMAN; MOLECULAR MECHANICS; PATHOGENESIS; PROTEIN FUNCTION; REVIEW; TH17 CELL;

ANIMALS; HEPATITIS B; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTERLEUKIN-23; INTERLEUKINS; LIVER; SIGNAL TRANSDUCTION; TH17 CELLS;

EID: 84862822148     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/j.1478-3231.2012.02764.x     Document Type: Review

References (56)

1. Calvaruso V, Craxi A. Fibrosis in chronic viral hepatitis. Best Pract Res Clin Gastroenterol 2011; 25: 219-30.
2. Di Bisceglie AM. Hepatitis B and hepatocellular carcinoma. Hepatology 2009; 49(5 Suppl.): S56-60.
3. Rehermann B. Intrahepatic T cells in hepatitis B: viral control versus liver cell injury. J Exp Med 2000; 191: 1263-8.
4. + T cells clearly discriminate between patients with acute and chronic hepatitis B infection. Hepatology 2009; 49: 781-90.
5. Alatrakchi N, Koziel M. Regulatory T cells and viral liver disease. J Viral Hepat 2009; 16: 223-9.
6. Zhang JY, Zhang Z, Lin F, et al. Interleukin-17-producing CD4(+) T cells increase with severity of liver damage in patients with chronic hepatitis B. Hepatology 2010; 51: 81-91.
7. Ye Y, Xie X, Yu J, et al. Involvement of Th17 and Th1 effector responses in patients with Hepatitis B. J Clin Immunol 2010; 30: 546-55.
8. Dong C. Regulation and pro-inflammatory function of interleukin-17 family cytokines. Immunol Rev 2008; 226: 80-6.
9. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006; 24: 179-89.
10. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441: 235-8.
11. Mangan PR, Harrington LE, O'quinn DB, et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006; 441: 231-4.
12. Duvallet E, Semerano L, Assier E, Falgarone G, Boissier MC. Interleukin-23: a key cytokine in inflammatory diseases. Ann Med 2011; 43: 503-11.
13. Wu W, Li J, Chen F, et al. Circulating Th17 cells frequency is associated with the disease progression in HBV infected patients. J Gastroenterol Hepatol 2010; 25: 750-7.
14. Ge J, Wang K, Meng QH, et al. Implication of Th17 and Th1 cells in patients with chronic active hepatitis B. J Clin Immunol 2010; 30: 60-7.
15. Li J, Wu W, Peng G, et al. HBcAg induces interleukin-10 production, inhibiting HBcAg-specific Th17 responses in chronic hepatitis B patients. Immunol Cell Biol 2010; 88: 834-41.
16. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27: 485-517.
17. Ivanov II, Mckenzie BS, Zhou L, et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006; 126: 1121-33.
18. O'quinn DB, Palmer MT, Lee YK, Weaver CT. Emergence of the Th17 pathway and its role in host defense. Adv Immunol 2008; 99: 115-63.
19. Ge D, You Z. Expression of interleukin-17RC protein in normal human tissues. Int Arch Med 2008; 1: 19.
20. Patel DN, King CA, Bailey SR, et al. Interleukin-17 stimulates C-reactive protein expression in hepatocytes and smooth muscle cells via p38 MAPK and ERK1/2-dependent NF-kappaB and C/EBPbeta activation. J Biol Chem 2007; 282: 27229-38.
21. Lafdil F, Wang H, Park O, et al. Myeloid STAT3 inhibits T cell-mediated hepatitis by regulating T helper 1 cytokine and interleukin-17 production. Gastroenterology 2009; 137: 2125-35 e1-2.
22. Lemmers A, Moreno C, Gustot T, et al. The interleukin-17 pathway is involved in human alcoholic liver disease. Hepatology 2009; 49: 646-57.
23. Harada K, Shimoda S, Sato Y, et al. Periductal interleukin-17 production in association with biliary innate immunity contributes to the pathogenesis of cholangiopathy in primary biliary cirrhosis. Clin Exp Immunol 2009; 157: 261-70.
24. Moseley TA, Haudenschild DR, Rose L, Reddi AH. Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev 2003; 14: 155-74.
25. Toy D, Kugler D, Wolfson M, et al. Cutting edge: interleukin 17 signals through a heteromeric receptor complex. J Immunol 2006; 177: 36-9.
26. Gaffen SL. An overview of IL-17 function and signaling. Cytokine 2008; 43: 402-7.
27. Wang Q, Zheng Y, Huang Z, et al. Activated IL-23/IL-17 pathway closely correlates with increased Foxp3 expression in livers of chronic hepatitis B patients. BMC Immunol 2011; 12: 25.
28. Sonnenberg GF, Fouser LA, Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 2011; 12: 383-90.
29. Wolk K, Kunz S, Witte E, et al. IL-22 increases the innate immunity of tissues. Immunity 2004; 21: 241-54.
30. Kotenko SV, Izotova LS, Mirochnitchenko OV, et al. Identification of the functional interleukin-22 (IL-22) receptor complex: the IL-10R2 chain (IL-10Rbeta) is a common chain of both the IL-10 and IL-22 (IL-10-related T cell-derived inducible factor, IL-TIF) receptor complexes. J Biol Chem 2001; 276: 2725-32.
31. Xie MH, Aggarwal S, Ho WH, et al. Interleukin (IL)-22, a novel human cytokine that signals through the interferon receptor-related proteins CRF2-4 and IL-22R. J Biol Chem 2000; 275: 31335-9.
32. Xu W, Presnell SR, Parrish-Novak J, et al. A soluble class II cytokine receptor, IL-22RA2, is a naturally occurring IL-22 antagonist. Proc Natl Acad Sci USA 2001; 98: 9511-6.
33. Eyerich S, Eyerich K, Cavani A, Schmidt-Weber C. IL-17 and IL-22: siblings, not twins. Trends Immunol 2010; 31: 354-61.
34. Wolk K, Sabat R. Interleukin-22: a novel T- and NK-cell derived cytokine that regulates the biology of tissue cells. Cytokine Growth Factor Rev 2006; 17: 367-80.
35. Radaeva S, Sun R, Pan HN, Hong F, Gao B. Interleukin 22 (IL-22) plays a protective role in T cell-mediated murine hepatitis: IL-22 is a survival factor for hepatocytes via STAT3 activation. Hepatology 2004; 39: 1332-42.
36. Pan H, Hong F, Radaeva S, Gao B. Hydrodynamic gene delivery of interleukin-22 protects the mouse liver from concanavalin A-, carbon tetrachloride-, and Fas ligand-induced injury via activation of STAT3. Cell Mol Immunol 2004; 1: 43-9.
37. Zenewicz LA, Yancopoulos GD, Valenzuela DM, et al. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 2007; 27: 647-59.
38. Ki SH, Park O, Zheng M, et al. Interleukin-22 treatment ameliorates alcoholic liver injury in a murine model of chronic-binge ethanol feeding: role of signal transducer and activator of transcription 3. Hepatology 2010; 52: 1291-300.
39. Zhang Y, Cobleigh MA, Lian JQ, et al. A proinflammatory role for interleukin-22 in the immune response to hepatitis B virus. Gastroenterology 2011; 141: 1897-906.
40. Dambacher J, Beigel F, Zitzmann K, et al. The role of interleukin-22 in hepatitis C virus infection. Cytokine 2008; 41: 209-16.
41. Foster RG, Golden-Mason L, Rutebemberwa A, Rosen HR. Interleukin (IL)-17/IL-22-Producing T cells Enriched Within the Liver of Patients with Chronic Hepatitis C Viral (HCV) Infection. Dig Dis Sci 2011; 57: 381-9.
42. Xiang X, Gui H, King NJ, et al. IL-22 and non-ELR-CXC chemokine expression in chronic hepatitis B virus-infected liver. Immunol Cell Biol 2011; DOI:10.1038/icb.2011.79 [Epub ahead of print].
43. Park O, Wang H, Weng H, et al. In vivo consequences of liver-specific interleukin-22 expression in mice: Implications for human liver disease progression. Hepatology 2011; 54: 252-61.
44. Spolski R, Leonard WJ. The Yin and Yang of interleukin-21 in allergy, autoimmunity and cancer. Curr Opin Immunol 2008; 20: 295-301.
45. Spolski R, Leonard WJ. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu Rev Immunol 2008; 26: 57-79.
46. Zhou L, Ivanov II, Spolski R, et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007; 8: 967-74.
47. Publicover J, Goodsell A, Nishimura S, et al. IL-21 is pivotal in determining age-dependent effectiveness of immune responses in a mouse model of human hepatitis B. J Clin Invest 2011; 121: 1154-62.
48. Franks I. Viral hepatitis: interleukin 21 has a key role in age-dependent response to HBV. Nat Rev Gastroenterol Hepatol 2011; 8: 243.
49. Hu X, Ma S, Huang X, et al. Interleukin-21 is upregulated in hepatitis B-related acute-on-chronic liver failure and associated with severity of liver disease. J Viral Hepat 2011; 18: 458-67.
50. Oppmann B, Lesley R, Blom B, et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000; 13: 715-25.
51. Cua DJ, Sherlock J, Chen Y, et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003; 421: 744-8.
52. Langrish CL, Chen Y, Blumenschein WM, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201: 233-40.
53. Bastos KR, Marinho CR, Barboza R, et al. What kind of message does IL-12/IL-23 bring to macrophages and dendritic cells? Microbes Infect 2004; 6: 630-6.
54. Aggarwal S, Ghilardi N, Xie MH, De Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003; 278: 1910-4.
55. Murphy CA, Langrish CL, Chen Y, et al. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003; 198: 1951-7.
56. Parham C, Chirica M, Timans J, et al. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J Immunol 2002; 168: 5699-708.