Cytokines induced during chronic hepatitis B virus infection promote a pathway for NK cell-mediated liver damage

Journal of Experimental Medicine

Volumn 204, Issue 3, 2007, Pages 667-680

  Dunn, Claire ^a   Brunetto, Maurizia ^b   Reynolds, Gary ^c   Christophides, Theodoros ^a   Kennedy, Patrick T ^a   Lampertico, Pietro ^d   Das, Abhishek ^a   Lopes, A Ross ^a   Borrow, Persephone ^e   Williams, Kevin ^c   Humphreys, Elizabeth ^c   Afford, Simon ^c   Adams, David H ^c   Bertoletti, Antonio ^a,f   Maini, Mala K ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Spedali Riuniti di Santa Chiara   (Italy)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF MILAN   (Italy)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; INTERLEUKIN 8; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CHRONIC HEPATITIS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; EXPERIMENTAL MODEL; HEPATITIS B; HUMAN; INNATE IMMUNITY; LIVER CELL; LIVER DISEASE; LIVER INJURY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; VIRUS REPLICATION;

CELL LINE, TUMOR; CELLS, CULTURED; CROSS-SECTIONAL STUDIES; CYTOKINES; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; INTERFERON-ALPHA; INTERLEUKIN-8; KILLER CELLS, NATURAL; LIVER; LONGITUDINAL STUDIES; SIGNAL TRANSDUCTION;

EID: 33947411395     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20061287     Document Type: Article

References (55)

1. Bonino, F., and M.R. Brunetto. 2003. Chronic hepatitis B e antigen (HBeAg) negative, anti-HBe positive hepatitis B: an overview. J. Hepatol. 39:S160-S163.
2. Brunetto, M.R., F. Oliveri, B. Coco, G. Leandro, P. Colombatto, J.M. Gorin, and F. Bonino. 2002. Outcome of anti-HBe positive chronic hepatitis B in alpha-interferon treated and untreated patients: a long term cohort study. J. Hepatol. 36:263-270.
3. + cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 191:1269-1280.
4. Kakimi, K., T.E. Lane, S. Wieland, V.C. Asensio, I.L. Campbell, F.V. Chisari, and L.G. Guidotti. 2001. Blocking chemokine responsive to γ-2/interferon (IFN)-γ inducible protein and monokine induced by IFN-γ activity in vivo reduces the pathogenetic but not the antiviral potential of hepatitis B virus-specific cytotoxic T lymphocytes. J. Exp. Med. 194:1755-1766.
5. Sitia, G., M. Isogawa, M. Iannacone, I.L. Campbell, F.V. Chisari, and L.G. Guidotti. 2004. MMPs are required for recruitment of antigen-nonspecific mononuclear cells into the liver by CTLs. J. Clin. Invest. 113:1158-1167.
6. Ando, K., T. Moriyama, L.G. Guidotti, S. Wirth, R.D. Schreiber, H.J. Schlicht, S.N. Huang, and F.V. Chisari. 1993. Mechanisms of class I restricted immunopathology. A transgenic mouse model of fulminant hepatitis. J. Exp. Med. 178:1541-1554.
7. Norris, S., C. Collins, D.G. Doherty, F. Smith, G. McEntee, O. Traynor, N. Nolan, J. Hegarty, and C. O'Farrelly. 1998. Resident human hepatic lymphocytes are phenotypically different from circulating lymphocytes. J. Hepatol. 28:84-90.
8. Webster, G.J., S. Reignat, M.K. Maini, S.A. Whalley, G.S. Ogg, A. King, D. Brown, P.L. Amlot, R. Williams, D. Vergani, et al. 2000. Incubation phase of acute hepatitis B in man: dynamic of cellular immune mechanisms. Hepatology. 32:1117-1124.
9. Tay, C.H., and R.M. Welsh. 1997. Distinct organ-dependent mechanisms for the control of murine cytomegalovirus infection by natural killer cells. J. Virol. 71:267-275.
10. Kafrouni, M.I., G.R. Brown, and D.L. Thiele. 2001. Virally infected hepatocytes are resistant to perforin-dependent CTL effector mechanisms. J. Immunol. 167:1566-1574.
11. Galle, P.R., W.J. Hofmann, H. Walczak, H. Schaller, G. Otto, W. Stremmel, P.H. Krammer, and L. Runkel. 1995. Involvement of the CD95 (APO-1/Fas) receptor and ligand in liver damage. J. Exp. Med. 182:1223-1230.
12. Balkow, S., A. Kersten, T.T. Tran, T. Stehle, P. Grosse, C. Museteanu, O. Utermohlen, H. Pircher, F. von Weizsacker, R. Wallich, et al. 2001. Concerted action of the FasL/Fas and perforin/granzyme A and B pathways is mandatory for the development of early viral hepatitis but not for recovery from viral infection. J. Virol. 75:8781-8791.
13. Wiley, S.R., K. Schooley, P.J. Smolak, W.S. Din, C.P. Huang, J.K. Nicholl, G.R. Sutherland, T.D. Smith, C. Rauch, C.A. Smith, et al. 1995. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity. 3:673-682.
14. Sheridan, J.P., S.A. Marsters, R.M. Pitti, A. Gurney, M. Skubatch, D. Baldwin, L. Ramakrishnan, C.L. Gray, K. Baker, W.I. Wood, et al. 1997. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science. 277:818-821.
15. Zheng, S.J., P. Wang, G. Tsabary, and Y.H. Chen. 2004. Critical roles of TRAIL in hepatic cell death and hepatic inflammation. J. Clin. Invest. 113:58-64.
16. Takeda, K., Y. Hayakawa, M.J. Smyth, N. Kayagaki, N. Yamaguchi, S. Kakuta, Y. Iwakura, H. Yagita, and K. Okumura. 2001. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat. Med. 7:94-100.
17. Jo, M., T.H. Kim, D.W. Seol, J.E. Esplen, K. Dorko, T.R. Billiar, and S.C. Strom. 2000. Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat. Med. 6:564-567.
18. Lawrence, D., Z. Shahrokh, S. Marsters, K. Achilles, D. Shih, B. Mounho, K. Hillan, K. Totpal, L. DeForge, P. Schow, et al. 2001. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat. Med. 7:383-385.
19. Mundt, B., F. Kuhnel, L. Zender, Y. Paul, H. Tillmann, C. Trautwein, M.P. Manns, and S. Kubicka. 2003. Involvement of TRAIL and its receptors in viral hepatitis. FASEB J. 17:94-96.
20. Saitou, Y., K. Shiraki, H. Fuke, T. Inoue, K. Miyashita, Y. Yamanaka, Y. Yamaguchi, N. Yamamoto, K. Ito, K. Sugimoto, and T. Nakano. 2005. Involvement of tumor necrosis factor-related apoptosis-inducing ligand and tumor necrosis factor-related apoptosis-inducing ligand receptors in viral hepatic diseases. Hum. Pathol. 36:1066-1073.
21. Nguyen, K.B., T.P. Salazar-Mather, M.Y. Dalod, J.B. Van Deusen, X.Q. Wei, F.Y. Liew, M.A. Caligiuri, J.E. Durbin, and C.A. Biron. 2002. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 169:4279-4287.
22. Sato, K., S. Hida, H. Takayanagi, T. Yokochi, N. Kayagaki, K. Takeda, H. Yagita, K. Okumura, N. Tanaka, T. Taniguchi, and K. Ogasawara. 2001. Antiviral response by natural killer cells through TRAIL gene induction by IFN-alpha/beta. Eur. J. Immunol. 31:3138-3146.
23. Marrack, P., J. Kappler, and T. Mitchell. 1999. Type I interferons keep activated T cells alive. J. Exp. Med. 189:521-530.
24. Dondi, E., L. Rogge, G. Lutfalla, G. Uze, and S. Pellegrini. 2003. Down-modulation of responses to type I IFN upon T cell activation. J. Immunol. 170:749-756.
25. Tian, Z., X. Shen, H. Feng, and B. Gao. 2000. IL-1 beta attenuates IFN-alpha beta-induced antiviral activity and STAT1 activation in the liver: involvement of proteasome-dependent pathway. J. Immunol. 165:3959-3965.
26. Khabar, K.S., F. Al-Zoghaibi, M.N. Al-Ahdal, T. Murayama, M. Dhalla, N. Mukaida, M. Taha, S.T. Al-Sedairy, Y. Siddiqui, G. Kessie, and K. Matsushima. 1997. The α chemokine, interleukin 8, inhibits the antiviral action of interferon α. J. Exp. Med. 186:1077-1085.
27. Polyak, S.J., K.S. Khabar, M. Rezeiq, and D.R. Gretch. 2001. Elevated levels of interleukin-8 in serum are associated with hepatitis C virus infection and resistance to interferon therapy. J. Virol. 75:6209-6211.
28. Guidotti, L.G., R. Rochford, J. Chung, M. Shapiro, R. Purcell, and F.V. Chisari. 1999. Viral clearance without destruction of infected cells during acute HBV infection. Science. 284:825-829.
29. Myers, R.P., M.H. Tainturier, V. Ratziu, A. Piton, V. Thibault, F. Imbert-Bismut, D. Messous, F. Charlotte, V. Di Martino, Y. Benhamou, and T. Poynard. 2003. Prediction of liver histological lesions with biochemical markers in patients with chronic hepatitis B. J. Hepatol. 39:222-230.
30. Kashii, Y., R. Giorda, R.B. Herberman, T.L. Whiteside, and N.L. Vujanovic. 1999. Constitutive expression and role of the TNF family ligands in apoptotic killing of tumor cells by human NK cells. J. Immunol. 163:5358-5366.
31. Mirandola, P., C. Ponti, G. Gobbi, I. Sponzilli, M. Vaccarezza, L. Cocco, G. Zauli, P. Secchiero, F.A. Manzoli, and M. Vitale. 2004. Activated human NK and CD8+ T cells express both TNF-related apoptosis-inducing ligand (TRAIL) and TRAIL receptors but are resistant to TRAIL-mediated cytotoxicity. Blood. 104:2418-2424.
32. Ishiyama, K., H. Ohdan, M. Ohira, H. Mitsuta, K. Arihiro, and T. Asahara. 2006. Difference in cytotoxicity against hepatocellular carcinoma between liver and periphery natural killer cells in humans. Hepatology. 43:362-372.
33. Cooper, M.A., T.A. Fehniger, and M.A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22:633-640.
34. Sprengers, D., R.G. van der Molen, J.G. Kusters, B. Hansen, H.G. Niesters, S.W. Schalm, and H.L. Janssen. 2006. Different composition of intrahepatic lymphocytes in the immune-tolerance and immune-clearance phase of chronic hepatitis B. J. Med. Virol. 78:561-568.
35. Ichikawa, K., W. Liu, L. Zhao, Z. Wang, D. Liu, T. Ohtsuka, H. Zhang, J.D. Mountz, W.J. Koopman, R.P. Kimberly, and T. Zhou. 2001. Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat. Med. 7:954-960.
36. Clancy, L., K. Mruk, K. Archer, M. Woelfel, J. Mongkolsapaya, G. Screaton, M.J. Lenardo, and F.K. Chan. 2005. Preligand assembly domain-mediated ligand-independent association between TRAIL receptor 4 (TR4) and TR2 regulates TRAIL-induced apoptosis. Proc. Natl. Acad. Sci. USA. 102:18099-18104.
37. Rossol, S., G. Marinos, P. Carucci, M.V. Singer, R. Williams, and N.V. Naoumov. 1997. Interleukin-12 induction of Th1 cytokines is important for viral clearance in chronic hepatitis B. J. Clin. Invest. 99:3025-3033.
38. Tsai, S.L., P.J. Chen, M.Y. Lai, P.M. Yang, J.L. Sung, J.H. Huang, L.H. Hwang, T.H. Chang, and D.S. Chen. 1992. Acute exacerbations of chronic type B hepatitis are accompanied by increased T cell responses to hepatitis B core and e antigens. Implications for hepatitis B e antigen seroconversion. J. Clin. Invest. 89:87-96.
39. Lohr, H.F., W. Weber, J. Schlaak, B. Goergen, K.H. Meyer zum Buschenfelde, and G. Gerken. 1995. Proliferative response of CD4+ T cells and hepatitis B virus clearance in chronic hepatitis with or without hepatitis B e-minus hepatitis B virus mutants. Hepatology. 22:61-68.
40. Sato, K., A. Niessner, S.L. Kopecky, R.L. Frye, J.J. Goronzy, and C.M. Weyand. 2006. TRAIL-expressing T cells induce apoptosis of vascular smooth muscle cells in the atherosclerotic plaque. J. Exp. Med. 203:239-250.
41. Herbeuval, J.P., J.C. Grivel, A. Boasso, A.W. Hardy, C. Chougnet, M.J. Dolan, H. Yagita, J.D. Lifson, and G.M. Shearer. 2005. CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood. 106:3524-3531.
42. Radaeva, S., R. Sun, B. Jaruga, V.T. Nguyen, Z. Tian, and B. Gao. 2006. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factor-related apoptosis-inducing ligand-dependent manners. Gastroenterology. 130:435-452.
43. Ashkenazi, A., R.C. Pai, S. Fong, S. Leung, D.A. Lawrence, S.A. Marsters, C. Blackie, L. Chang, A.E. McMurtrey, A. Hebert, et al. 1999. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104:155-162.
44. Walczak, H., R.E. Miller, K. Ariail, B. Gliniak, T.S. Griffith, M. Kubin, W. Chin, J. Jones, A. Woodward, T. Le, et al. 1999. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5:157-163.
45. Schneider, P., N. Holler, J.L. Bodmer, M. Hahne, K. Frei, A. Fontana, and J. Tschopp. 1998. Conversion of membrane-bound Fas(CD95) ligand to its soluble form is associated with downregulation of its proapoptotic activity and loss of liver toxicity. J. Exp. Med. 187:1205-1213.
46. Higuchi, H., S.F. Bronk, Y. Takikawa, N. Werneburg, R. Takimoto, W. El-Deiry, and G.J. Gores. 2001. The bile acid glycochenodeoxycholate induces trail-receptor 2/DR5 expression and apoptosis. J. Biol. Chem. 276:38610-38618.
47. Janssen, H.L., H. Higuchi, A. Abdulkarim, and G.J. Gores. 2003. Hepatitis B virus enhances tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) cytotoxicity by increasing TRAIL-R1/death receptor 4 expression. J. Hepatol. 39:414-420.
48. Liang, X., Y. Liu, Q. Zhang, L. Gao, L. Han, C. Ma, L. Zhang, Y.H. Chen, and W. Sun. 2007. Hepatitis B virus sensitizes hepatocytes to TRAIL-induced apoptosis through Bax. J. Immunol. 178:503-510.
49. Mahe, Y., N. Mukaida, K. Kuno, M. Akiyama, N. Ikeda, K. Matsushima, and S. Murakami. 1991. Hepatitis B virus X protein transactivates human interleukin-8 gene through acting on nuclear factor kB and CCAAT/enhancer- binding protein-like cis-elements. J. Biol. Chem. 266:13759-13763.
50. Campbell, J.J., S. Qin, D. Unutmaz, D. Soler, K.E. Murphy, M.R. Hodge, L. Wu, and E.C. Butcher. 2001. Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J. Immunol. 166:6477-6482.
51. Salazar-Mather, T.P., C.A. Lewis, and C.A. Biron. 2002. Type I interferons regulate inflammatory cell trafficking and macrophage inflammatory protein 1alpha delivery to the liver. J. Clin. Invest. 110:321-330.
52. Kakimi, K., L.G. Guidotti, Y. Koezuka, and F.V. Chisari. 2000. Natural killer T cell activation inhibits hepatitis B virus replication in vivo. J. Exp. Med. 192:921-930.
53. Kayagaki, N., N. Yamaguchi, M. Nakayama, H. Eto, K. Okumura, and H. Yagita. 1999. Type I interferons (IFNs) regulate tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) expression on human T cells: a novel mechanism for the antitumor effects of type I IFNs. J. Exp. Med. 189:1451-1460.
54. Reynolds, G.M., L.J. Billingham, L.J. Gray, J.R. Flavell, S. Najafipour, J. Crocker, P. Nelson, L.S. Young, and P.G. Murray. 2002. Interleukin 6 expression by Hodgkin/Reed-Sternberg cells is associated with the presence of 'B' symptoms and failure to achieve complete remission in patients with advanced Hodgkin's disease. Br. J. Haematol. 118:195-201.
55. Afford, S.C., S. Randhawa, A.G. Eliopoulos, S.G. Hubscher, L.S. Young, and D.H. Adams. 1999. CD40 activation induces apoptosis in cultured human hepatocytes via induction of cell surface fas ligand expression and amplifies fas-mediated hepatocyte death during allograft rejection. J. Exp. Med. 189:441-446.