Functional skewing of the global CD8 T cell population in chronic hepatitis B virus infection

Journal of Experimental Medicine

Volumn 205, Issue 9, 2008, Pages 2111-2124

  Das, Abhishek ^a   Hoare, Matthew ^b   Davies, Nathan ^a   Lopes, A Ross ^a   Dunn, Claire ^a   Kennedy, Patrick T F ^a   Alexander, Graeme ^b   Finney, Helene ^c   Lawson, Alistair ^c   Plunkett, Fiona J ^a   Bertoletti, Antonio ^a,d   Akbar, Arne N ^a   Maini, Mala K ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c UCB PHARMA   (Belgium)

^d AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GAMMA INTERFERON; INTERLEUKIN 2; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL POPULATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; HEPATITIS B; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRUS LOAD;

ADULT; AGED; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HLA-A2 ANTIGEN; HUMANS; INTERFERON TYPE II; INTERLEUKIN-2; MALE; MIDDLE AGED; MODELS, BIOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA; VIRAL LOAD;

EID: 51049123791     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20072076     Document Type: Article

References (60)

1. Thimme, R., S. Wieland, C. Steiger, J. Ghrayeb, K.A. Reimann, R.H. Purcell, and F.V. Chisari. 2003. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J. Virol. 77:68-76.
2. Chisari, F.V. 1997. Cytotoxic T cells and viral hepatitis. J. Clin. Invest. 99:1472-1477.
3. + cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 191:1269-1280.
4. Reignat, S., G.J. Webster, D. Brown, G.S. Ogg, A. King, S.L. Seneviratne, G. Dusheiko, R. Williams, M.K. Maini, and A. Bertoletti. 2002. Escaping high viral load exhaustion: CD8 cells with altered tetramer binding in chronic hepatitis B virus infection. J. Exp. Med. 195:1089-1101.
5. Bertoletti, A., and M.K. Maini. 2000. Protection or damage: a dual role for the virus-specific cytotoxic T lymphocyte response in hepatitis B and C infection? Curr. Opin. Immunol. 12:403-408.
6. Tsuzaka, K., I. Fukuhara, Y. Setoyama, K. Yoshimoto, K. Suzuki, T. Abe, and T. Takeuchi. 2003. TCR zeta mRNA with an alternatively spliced 3′-untranslated region detected in systemic lupus erythematosus patients leads to the down-regulation of TCR zeta and TCR/CD3 complex. J. Immunol. 171:2496-2503.
7. Krishnan, S., J.G. Kiang, C.U. Fisher, M.P. Nambiar, H.T. Nguyen, V.C. Kyttaris, B. Chowdhury, V. Rus, and G.C. Tsokos. 2005. Increased caspase-3 expression and activity contribute to reduced CD3zeta expression in systemic lupus erythematosus T cells. J. Immunol. 175:3417-3423.
8. Nakagomi, H., M. Petersson, I. Magnusson, C. Juhlin, M. Matsuda, H. Mellstedt, J.L. Taupin, E. Vivier, P. Anderson, and R. Kiessling. 1993. Decreased expression of the signal-transducing zeta chains in tumorinfiltrating T-cells and NK cells of patients with colorectal carcinoma. Cancer Res. 53:5610-5612.
9. Trimble, L.A., and J. Lieberman. 1998. Circulating CD8 T lymphocytes in human immunodeficiency virus-infected individuals have impaired function and downmodulate CD3 zeta, the signaling chain of the T-cell receptor complex. Blood. 91:585-594.
10. Trimble, L.A., P. Shankar, M. Patterson, J.P. Daily, and J. Lieberman. 2000. Human immunodeficiency virus-specific circulating CD8 T lymphocytes have down-modulated CD3zeta and CD28, key signaling molecules for T-cell activation. J. Virol. 74:7320-7330.
11. Bronstein-Sitton, N., L. Cohen-Daniel, I. Vaknin, A.V. Ezernitchi, B. Leshem, A. Halabi, Y. Houri-Hadad, E. Greenbaum, Z. Zakay-Rones, L. Shapira, and M. Baniyash. 2003. Sustained exposure to bacterial antigen induces interferon-gamma-dependent T cell receptor zeta downregulation and impaired T cell function. Nat. Immunol. 4:957-964.
12. Baniyash, M. 2004. TCR zeta-chain downregulation: curtailing an excessive inflammatory immune response. Nat. Rev. Immunol. 4:675-687.
13. Sussman, J.J., J.S. Bonifacino, J. Lippincott-Schwartz, A.M. Weissman, T. Saito, R.D. Klausner, and J.D. Ashwell. 1988. Failure to synthesize the T cell CD3-zeta chain: structure and function of a partial T cell receptor complex. Cell. 52:85-95.
14. Pitcher, L.A., and N.S. van Oers. 2003. T-cell receptor signal transmission: who gives an ITAM? Trends Immunol. 24:554-560.
15. Trimble, L.A., L.W. Kam, R.S. Friedman, Z. Xu, and J. Lieberman. 2000. CD3zeta and CD28 down-modulation on CD8 T cells during viral infection. Blood. 96:1021-1029.
16. Kaech, S.M., E.J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2:251-262.
17. Wherry, E.J., J.N. Blattman, K. Murali-Krishna, R. Van Der Most, and R. Ahmed. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77:4911-4927.
18. Zimmerli, S.C., A. Harari, C. Cellerai, F. Vallelian, P.A. Bart, and G. Pantaleo. 2005. HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc. Natl. Acad. Sci. USA. 102:7239-7244.
19. Crispe, I.N. 2003. Hepatic T cells and liver tolerance. Nat. Rev. Immunol. 3:51-62.
20. Bronte, V., and P. Zanovello. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5:641-654.
21. Frumento, G., R. Rotondo, M. Tonetti, G. Damonte, U. Benatti, and G.B. Ferrara. 2002. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J. Exp. Med. 196:459-468.
22. Fallarino, F., U. Grohmann, S. You, B.C. McGrath, D.R. Cavener, C. Vacca, C. Orabona, R. Bianchi, M.L. Belladonna, C. Volpi, et al. 2006. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J. Immunol. 176:6752-6761.
23. + T cells. J. Exp. Med. 186:1407-1418.
24. Doherty, D.G., S. Norris, L. Madrigal-Estebas, G. McEntee, O. Traynor, J.E. Hegarty, and C. O'Farrelly. 1999. The human liver contains multiple populations of NK cells, T cells, and CD3+CD56+ natural T cells with distinct cytotoxic activities and Th1, Th2, and Th0 cytokine secretion patterns. J. Immunol. 163:2314-2321.
25. Chang, J.J., F. Wightman, A. Bartholomeusz, A. Ayres, S.J. Kent, J. Sasadeusz, and S.R. Lewin. 2005. Reduced hepatitis B virus (HBV)-specific CD4+ T-cell responses in human immunodeficiency virus type 1-HBV-coinfected individuals receiving HBV-active antiretroviral therapy. J. Virol. 79:3038-3051.
26. Boni, C., P. Fisicaro, C. Valdatta, B. Amadei, P. Di Vincenzo, T. Giuberti, D. Laccabue, A. Zerbini, A. Cavalli, G. Missale, et al. 2007. Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J. Virol. 81:4215-4225.
27. Almanzar, G., S. Schwaiger, B. Jenewein, M. Keller, D. Herndler-Brandstetter, R. Wurzner, D. Schonitzer, and B. Grubeck-Loebenstein. 2005. Long-term cytomegalovirus infection leads to significant changes in the composition of the CD8+ T-cell repertoire, which may be the basis for an imbalance in the cytokine production profile in elderly persons. J. Virol. 79:3675-3683.
28. Zhang, Z., C.L. Gorman, A.C. Vermi, C. Monaco, A. Foey, S. Owen, P. Amjadi, A. Vallance, C. McClinton, F. Marelli-Berg, et al. 2007. TCRzetadim lymphocytes define populations of circulating effector cells that migrate to inflamed tissues. Blood. 109:4328-4335.
29. Krymskaya, L., W.H. Lee, L. Zhong, and C.P. Liu. 2005. Polarized development of memory cell-like IFN-gamma-producing cells in the absence of TCR zeta-chain. J. Immunol. 174:1188-1195.
30. Finney, H.M., A.N. Akbar, and A.D. Lawson. 2004. Activation of resting human primary T cells with chimeric receptors: costimulation from CD28, inducible costimulator, CD134, and CD137 in series with signals from the TCRzeta chain. J. Immunol. 172:104-113.
31. Plunkett, F.J., O. Franzese, H.M. Finney, J.M. Fletcher, L.L. Belaramani, M. Salmon, I. Dokal, D. Webster, A.D. Lawson, and A.N. Akbar. 2007. The loss of telomerase activity in highly differentiated CD8+CD28-CD27- T cells is associated with decreased Akt (Ser473) phosphorylation. J. Immunol. 178:7710-7719.
32. Rodriguez, P.C., A.H. Zea, K.S. Culotta, J. Zabaleta, J.B. Ochoa, and A.C. Ochoa. 2002. Regulation of T cell receptor CD3zeta chain expression by L-arginine. J. Biol. Chem. 277:21123-21129.
33. Rodriguez, P.C., D.G. Quiceno, and A.C. Ochoa. 2007. L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood. 109:1568-1573.
34. Roth, E., R. Steininger, S. Winkler, F. Langle, T. Grunberger, R. Fugger, and F. Muhlbacher. 1994. L-Arginine deficiency after liver transplantation as an effect of arginase efflux from the graft. Influence on nitric oxide metabolism. Transplantation. 57:665-669.
35. Modolell, M., I.M. Corraliza, F. Link, G. Soler, and K. Eichmann. 1995. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur. J. Immunol. 25:1101-1104.
36. Kropf, P., D. Baud, S.E. Marshall, M. Munder, A. Mosley, J.M. Fuentes, C.R. Bangham, G.P. Taylor, S. Herath, B.S. Choi, et al. 2007. Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur. J. Immunol. 37:935-945.
37. 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.
38. Webster, G.J., S. Reignat, D. Brown, G.S. Ogg, L. Jones, S.L. Seneviratne, R. Williams, G. Dusheiko, and A. Bertoletti. 2004. Longitudinal analysis of CD8+ T cells specific for structural and nonstructural hepatitis B virus proteins in patients with chronic hepatitis B: implications for immunotherapy. J. Virol. 78:5707-5719.
39. Lopes, A.R., P. Kellam, A. Das, C. Dunn, A. Kwan, J. Turner, D. Peppa, R.J. Gilson, A. Gehring, A. Bertoletti, and M.K. Maini. 2008. Bim-mediated deletion of antigen-specific CD8 T cells in patients unable to control HBV infection. J. Clin. Invest. 118:1835-1845.
40. Karrer, U., S. Sierro, M. Wagner, A. Oxenius, H. Hengel, U.H. Koszinowski, R.E. Phillips, and P. Klenerman. 2003. Memory inflation: continuous accumulation of antiviral CD8+ T cells over time. J. Immunol. 170:2022-2029.
41. Adams, D.H., S.G. Hubscher, J.M. Neuberger, P. McMaster, E. Elias, and J.A. Buckels. 1991. Reduced incidence of rejection in patients undergoing liver transplantation for chronic hepatitis B. Transplant. Proc. 23:1436-1437.
42. Farges, O., F. Saliba, H. Farhamant, D. Samuel, A. Bismuth, M. Reynes, and H. Bismuth. 1996. Incidence of rejection and infection after liver transplantation as a function of the primary disease: possible influence of alcohol and polyclonal immunoglobulins. Hepatology. 23:240-248.
43. Guidotti, L.G., T. Ishikawa, M.V. Hobbs, B. Matzke, R. Schreiber, and F.V. Chisari. 1996. Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity. 4:25-36.
44. Toyonaga, T., O. Hino, S. Sugai, S. Wakasugi, K. Abe, M. Shichiri, and K. Yamamura. 1994. Chronic active hepatitis in transgenic mice expressing interferon-gamma in the liver. Proc. Natl. Acad. Sci. USA. 91:614-618.
45. Morita, M., Y. Watanabe, and T. Akaike. 1995. Protective effect of hepatocyte growth factor on interferon-gamma-induced cytotoxicity in mouse hepatocytes. Hepatology. 21:1585-1593.
46. Maeda, S., L. Chang, Z.W. Li, J.L. Luo, H. Leffert, and M. Karin. 2003. IKKbeta is required for prevention of apoptosis mediated by cell-bound but not by circulating TNFalpha. Immunity. 19:725-737.
47. Su, F., and R.J. Schneider. 1997. Hepatitis B virus HBx protein sensitizes cells to apoptotic killing by tumor necrosis factor alpha. Proc. Natl. Acad. Sci. USA. 94:8744-8749.
48. 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 a 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.
49. Shields, P.L., C.M. Morland, M. Salmon, S. Qin, S.G. Hubscher, and D.H. Adams. 1999. Chemokine and chemokine receptor interactions provide a mechanism for selective T cell recruitment to specific liver compartments within hepatitis C-infected liver. J. Immunol. 163:6236-6243.
50. + cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J. Exp. Med. 188:223-232.
51. Lang, K.S., P. Georgiev, M. Recher, A.A. Navarini, A. Bergthaler, M. Heikenwalder, N.L. Harris, T. Junt, B. Odermatt, P.A. Clavien, et al. 2006. Immunoprivileged status of the liver is controlled by Toll-like receptor 3 signaling. J. Clin. Invest. 116:2456-2463.
52. Poli, G., and C. Bordignon. 2003. Unplugging the T cell receptor. Nat. Immunol. 4:943-944.
53. Ezernitchi, A.V., I. Vaknin, L. Cohen-Daniel, O. Levy, E. Manaster, A. Halabi, E. Pikarsky, L. Shapira, and M. Baniyash. 2006. TCR zeta down-regulation under chronic inflammation is mediated by myeloid suppressor cells differentially distributed between various lymphatic organs. J. Immunol. 177:4763-4772.
54. Sitia, G., M. Isogawa, K. Kakimi, S.F. Wieland, F.V. Chisari, and L.G. Guidotti. 2002. Depletion of neutrophils blocks the recruitment of antigen-nonspecific cells into the liver without affecting the antiviral activity of hepatitis B virus-specific cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA. 99:13717-13722.
55. 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.
56. Rodriguez, P.C., A.H. Zea, J. DeSalvo, K.S. Culotta, J. Zabaleta, D.G. Quiceno, J.B. Ochoa, and A.C. Ochoa. 2003. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J. Immunol. 171:1232-1239.
57. Rodriguez, P.C., C.P. Hernandez, D. Quiceno, S.M. Dubinett, J. Zabaleta, J.B. Ochoa, J. Gilbert, and A.C. Ochoa. 2005. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J. Exp. Med. 202:931-939.
58. Dunn, C., M. Brunetto, G. Reynolds, T. Christophides, P.T. Kennedy, P. Lampertico, A. Das, A.R. Lopes, P. Borrow, K. Williams, et al. 2007. Cytokines induced during chronic hepatitis B virus infection promote a pathway for NK cell-mediated liver damage. J. Exp. Med. 204:667-680.
59. Lucas, M., A.L. Vargas-Cuero, G.M. Lauer, E. Barnes, C.B. Willberg, N. Semmo, B.D. Walker, R. Phillips, and P. Klenerman. 2004. Pervasive influence of hepatitis C virus on the phenotype of antiviral CD8+ T cells. J. Immunol. 172:1744-1753.
60. Wherry, E.J., J.N. Blattman, and R. Ahmed. 2005. Low CD8 T-cell proliferative potential and high viral load limit the effectiveness of therapeutic vaccination. J. Virol. 79:8960-8968.