Bim-mediated deletion of antigen-specific CD8+ T cells in patients unable to control HBV infection

Journal of Clinical Investigation

Volumn 118, Issue 5, 2008, Pages 1835-1845

  Lopes, A Ross ^a   Kellam, Paul ^a   Das, Abhishek ^a   Dunn, Claire ^a   Kwan, Antonia ^a   Turner, Joanna ^a,b   Peppa, Dimitra ^a,b   Gilson, Richard J ^a,b   Gehring, Adam ^c   Bertoletti, Antonio ^c   Maini, Mala K ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Camden Primary Care Trust   (United Kingdom)

^c AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 7 RECEPTOR; PROTEIN BCL 2; PROTEIN MCL 1;

ADULT; AGED; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CLINICAL ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; GENE CLUSTER; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; MALE; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION;

ADULT; AGED; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; GENE EXPRESSION PROFILING; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; MEMBRANE PROTEINS; MIDDLE AGED; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 43049112084     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI33402     Document Type: Article

References (47)

1. Reignat, S., et al. 2002. Escaping high viral load exhaustion: CD8 cells with altered tetramer binding in chronic hepatitis B virus infection. J. Exp. Med. 195:1089-1101.
2. Chen, M.T., et al. 2004. A function of the hepatitis B virus precore protein is to regulate the immune response to the core antigen. Proc. Natl. Acad. Sci. U. S. A. 101:14913-14918.
3. Thimme, R., et al. 2003. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J. Virol. 77:68-76.
4. Maini, M.K., et al. 2000. The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 191:1269-1280.
5. Webster, G.J., et al. 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.
6. Boni, C., et al. 2007. Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J. Virol. 81:4215-4225.
7. Maini, M.K., et al. 1999. Direct ex vivo analysis of hepatitis B virus-specific CD8(+) T cells associated with the control of infection. Gastroenterology. 117:1386-1396.
8. Moskophidis, D., Lechner, F., Pircher, H., and Zinkernagel, R.M. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature. 362:758-761.
9. Rehermann, B., Lau, D., Hoofnagle, J.H., and Chisari, F.V. 1996. Cytotoxic T lymphocyte responsiveness after resolution of chronic hepatitis B virus infection. J. Clin. Invest. 97:1655-1665.
10. Boni, C., et al. 2001. Lamivudine treatment can overcome cytotoxic T-cell hyporesponsiveness in chronic hepatitis B: new perspectives for immune therapy. Hepatology. 33:963-971.
11. Boni, C., et al. 2003. Transient restoration of antiviral T cell responses induced by lamivudine therapy in chronic hepatitis B. J. Hepatol. 39:595-605.
12. Vine, A.M., et al. 2004. The role of CTLs in persistent viral infection: cytolytic gene expression in CD8+ lymphocytes distinguishes between individuals with a high or low proviral load of human T cell lymphotropic virus type 1. J. Immunol. 173:5121-5129.
13. Teague, T.K., et al. 1999. Activation changes the spectrum but not the diversity of genes expressed by T cells. Proc. Natl. Acad. Sci. U. S. A. 96:12691-12696.
14. Abdalla, A.O., et al. 2003. Kinetics of cytokine gene expression in human CD4+ and CD8+ T-lymphocyte subsets using quantitative real-time PCR. Scand. J. Immunol. 58:601-606.
15. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868.
16. Tusher, V.G., Tibshirani, R., and Chu, G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98:5116-5121.
17. Grayson, J.M., Weant, A.E., Holbrook, B.C., and Hildeman, D. 2006. Role of Bim in regulating CD8+ T-cell responses during chronic viral infection. J. Virol. 80:8627-8638.
18. Davey, G.M., et al. 2002. Peripheral deletion of autoreactive CD8 T cells by cross presentation of self-antigen occurs by a Bcl-2-inhibitable pathway mediated by Bim. J. Exp. Med. 196:947-955.
19. Weber, A., et al. 2007. BimS-induced apoptosis requires mitochondrial localization but not interaction with anti-apoptotic Bcl-2 proteins. J. Cell Biol. 177:625-636.
20. Sawada, M., Hayes, P., and Matsuyama, S. 2003. Cytoprotective membrane-permeable peptides designed from the Bax-binding domain of Ku70. Nat. Cell Biol. 5:352-357.
21. Pellegrini, M., et al. 2004. Loss of Bim increases T cell production and function in interleukin 7 receptor-deficient mice. J. Exp. Med. 200:1189-1195.
22. Wojciechowski, S., et al. 2006. Bim mediates apoptosis of CD127(lo) effector T cells and limits T cell memory. Eur. J. Immunol. 36:1694-1706.
23. Kaech, S.M., et al. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4:1191-1198.
24. Paiardini, M., et al. 2005. Loss of CD127 expression defines an expansion of effector CD8+ T cells in HIV-infected individuals. J. Immunol. 174:2900-2909.
25. van Leeuwen, E.M., et al. 2005. IL-7 receptor alpha chain expression distinguishes functional subsets of virus-specific human CD8+ T cells. Blood. 106:2091-2098.
26. Opferman, J.T., et al. 2003. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature. 426:671-676.
27. O'Connor, L., et al. 1998. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17:384-395.
28. Bouillet, P., et al. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 286:1735-1738.
29. Hildeman, D.A., et al. 2002. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity. 16:759-767.
30. Pellegrini, M., Belz, G., Bouillet, P., and Strasser, A. 2003. Shutdown of an acute T cell immune response to viral infection is mediated by the proapoptotic Bcl-2 homology 3-only protein Bim. Proc. Natl. Acad. Sci. U. S. A. 100:14175-14180.
31. Sabbagh, L., et al. 2006. A critical role for TNF receptor-associated factor 1 and Bim down-regulation in CD8 memory T cell survival. Proc. Natl. Acad. Sci. U. S. A. 103:18703-18708.
32. Bengsch, B., et al. 2007. Analysis of CD127 and KLRG1 expression on hepatitis C virus-specific CD8+ T cells reveals the existence of different memory T-cell subsets in the peripheral blood and liver. J. Virol. 81:945-953.
33. Radziewicz, H., et al. 2007. Liver-infiltrating lymphocytes in chronic human hepatitis C virus infection display an exhausted phenotype with high levels of PD-1 and low levels of CD127 expression. J. Virol. 81:2545-2553.
34. Penna, A., et al. 2007. Dysfunction and functional restoration of HCV-specific CD8 responses in chronic hepatitis C virus infection. Hepatology. 45:588-601.
35. Bosque, A., et al. 2007. The induction of Bim expression in human T-cell blasts is dependent on nonapoptotic Fas/CD95 signaling. Blood. 109:1627-1635.
36. Vezys, V., et al. 2006. Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J. Exp. Med. 203:2263-2269.
37. Sandalova, E., Wei, C.H., Masucci, M.G., and Levitsky, V. 2004. Regulation of expression of Bcl-2 protein family member Bim by T cell receptor triggering. Proc. Natl. Acad. Sci. U. S. A. 101:3011-3016.
38. Sandalova, E., Hislop, A.D., and Levitsky, V. 2006. T-cell receptor triggering differentially regulates bim expression in human lymphocytes from healthy individuals and patients with infectious mononucleosis. Hum. Immunol. 67:958-965.
39. Jin, Y., Shih, W.K., and Berkower, I. 1988. Human T cell response to the surface antigen of hepatitis B virus (HBsAg). Endosomal and nonendosomal processing pathways are accessible to both endogenous and exogenous antigen. J. Exp. Med. 168:293-306.
40. Limmer, A., et al. 2000. Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat. Med. 6:1348-1354.
41. Albert, M.L., Sauter, B., and Bhardwaj, N. 1998. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature. 392:86-89.
42. Berg, M., et al. 2006. Cross-presentation of antigens from apoptotic tumor cells by liver sinusoidal endothelial cells leads to tumor-specific CD8+ T cell tolerance. Eur. J. Immunol. 36:2960-2970.
43. Dunn, C., 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.
44. Bertolino, P., Trescol-Biemont, M.C., and Rabourdin-Combe, C. 1998. Hepatocytes induce functional activation of naive CD8+ T lymphocytes but fail to promote survival. Eur. J. Immunol. 28:221-236.
45. Morimoto, J., Tan, X., Teague, R.M., Ohlen, C., and Greenberg, P.D. 2007. Induction of tolerance in CD8+ T cells to a transgenic autoantigen expressed in the liver does not require cross-presentation. J. Immunol. 178:6849-6860.
46. Gehring, A.J., et al. 2007. The level of viral antigen presented by hepatocytes influences CD8 T-cell function. J. Virol. 81:2940-2949.
47. Baugh, L.R., Hill, A.A., Brown, E.L., and Hunter, C.P. 2001. Quantitative analysis of mRNA amplification by in vitro transcription. Nucleic Acids Res. 29:E29.