Tissue-specific differences in PD-1 and PD-L1 expression during chronic viral infection: Implications for CD8 T-cell exhaustion

Journal of Virology

Volumn 84, Issue 4, 2010, Pages 2078-2089

  Blackburn, Shawn D ^b   Crawford, Alison ^b   Shin, Haina ^b   Polley, Antonio ^b   Freeman, Gordon J ^a   Wherry, E John ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11 ANTIGEN; CD19 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN PD L1; PROTEIN PD L2; REGULATOR PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CD8+ T LYMPHOCYTE; CELL KILLING; CELL SUBPOPULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRANULATION; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOREGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TISSUE SPECIFICITY; VIRUS INFECTION;

ANIMALS; ANTIGENS, CD80; ANTIGENS, SURFACE; APOPTOSIS REGULATORY PROTEINS; BONE MARROW; CD8-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; CHRONIC DISEASE; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; ORGAN SPECIFICITY; PEPTIDES; SIGNAL TRANSDUCTION; SPLEEN; TIME FACTORS; VIRUS REPLICATION;

ANIMALIA;

EID: 75449110618     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01579-09     Document Type: Article

References (43)

1. + T-cell population in chronic hepatitis C virus infection. J. Clin. Invest. 113:963-972.
2. Ahmed, R., A. Salmi, L. D. Butler, J. M. Chiller, and M. B. Oldstone. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice: role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160:521-540.
3. Barber, D. L., E. J. Wherry, D. Masopust, B. Zhu, J. P. Allison, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:682-687.
4. Blackburn, S. D., H. Shin, G. J. Freeman, and E. J. Wherry. 2008. Selective expansion of a subset of exhausted CD8 T cells by αPD-L1 blockade. Proc. Natl. Acad. Sci. U. S. A. 39:15016-15021.
5. + T-cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10:29-37.
6. + T cells identifies functionally and phenotypically defined memory T cells during acute resolving hepatitis B virus infection. J. Virol. 80:3532-3540.
7. Boni, C., P. Fisicaro, C. Valdatta, B. Amadei, P. Di Vincenzo, T. Giuberti, D. Laccabue, A. Zerbini, A. Cavalli, G. Missale, A. Bertoletti, and C. Ferrari. 2007. Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J. Virol. 81:4215-4225.
8. Day, C. L., D. E. Kaufmann, P. Kiepiela, J. A. Brown, E. S. Moodley, S. Reddy, E. W. Mackey, J. D. Miller, A. J. Leslie, C. Depierres, Z. Mncube, J. Duraiswamy, B. Zhu, Q. Eichbaum, M. Altfeld, E. J. Wherry, H. M. Coovadia, P. J. Goulder, P. Klenerman, R. Ahmed, G. J. Freeman, and B. D. Walker. 2006. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443:350-354.
9. + T cells associated with reversible immune dysfunction. J. Virol. 81:9249-9258.
10. Ha, S. J., S. N. Mueller, E. J. Wherry, D. L. Barber, R. D. Aubert, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2008. Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. J. Exp. Med. 205:543-555.
11. + T cells in peripheral blood and liver using peptide-MHC tetramers. Proc. Natl. Acad. Sci. U. S. A. 96:5692-5697.
12. Hermans, I. F., J. D. Silk, J. Yang, M. J. Palmowski, U. Gileadi, C. Mc-Carthy, M. Salio, F. Ronchese, and V. Cerundolo. 2004. The VITAL assay: a versatile fluorometric technique for assessing CTL- and NKT-mediated cytotoxicity against multiple targets in vitro and in vivo. J. Immunol. Methods 285:25-40.
13. + T cells with an effector phenotype and control of viral replication. Lancet 363:863-866.
14. Jeong, H. Y., Y. J. Lee, S. K. Seo, S. W. Lee, S. J. Park, J. N. Lee, H. S. Sohn, S. Yao, L. Chen, and I. Choi. 2008. Blocking of monocyte-associated B7-H1 (CD274) enhances HCV-specific T-cell immunity in chronic hepatitis C infection. J. Leukoc. Biol. 83:755-764.
15. + T cells correlates with disease progression and defines a reversible immune dysfunction. Nat. Immunol. 8:1246-1254.
16. Kaufmann, D. E., and B. D. Walker. 2009. PD-1 and CTLA-4 inhibitory cosignaling pathways in HIV infection and the potential for therapeutic intervention. J. Immunol. 182:5891-5897.
17. Keir, M. E., M. J. Butte, G. J. Freeman, and A. H. Sharpe. 2008. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26:677-704.
18. Kinter, A. L., E. J. Godbout, J. P. McNally, I. Sereti, G. A. Roby, M. A. O'Shea, and A. S. Fauci. 2008. The common gamma-chain cytokines IL-2, IL-7, IL-15, and IL-21 induce the expression of programmed death-1 and its ligands. J. Immunol. 181:6738-6746.
19. + T-cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 3:1061-1068.
20. + T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29:1009-1021.
21. Nakamoto, N., H. Cho, A. Shaked, K. Olthoff, M. E. Valiga, M. Kaminski, E. Gostick, D. A. Price, G. J. Freeman, E. J. Wherry, and K. M. Chang. 2009. Synergistic reversal of intrahepatic HCV-specific CD8 T-cell exhaustion by combined PD-1/CTLA-4 blockade. PLoS Pathog. 5:e1000313.
22. Nakamoto, N., D. E. Kaplan, J. Coleclough, Y. Li, M. E. Valiga, M. Kaminski, A. Shaked, K. Olthoff, E. Gostick, D. A. Price, G. J. Freeman, E. J. Wherry, and K. M. Chang. 2008. Functional restoration of HCV-specific CD8 T cells by PD-1 blockade is defined by PD-1 expression and compartmentalization. Gastroenterology 134:1927-1937.
23. Oldstone, M. B., and M. J. Buchmeier. 1982. Restricted expression of viral glycoprotein in cells of persistently infected mice. Nature 300:360-362.
24. + T-cell survival in HIV infection. J. Exp. Med. 203:2281-2292.
25. + T cells express high levels of PD1 and cytokines but have impaired proliferative capacity in acute and chronic SIVmac251 infection. Blood 110:928-936.
26. Radziewicz, H., C. C. Ibegbu, M. L. Fernandez, K. A. Workowski, K. Obideen, M. Wehbi, H. L. Hanson, J. P. Steinberg, D. Masopust, E. J. Wherry, J. D. Altman, B. T. Rouse, G. J. Freeman, R. Ahmed, and A. Grakoui. 2006. Liver infiltrating lymphocytes in chronic human HCV infection display an exhausted phenotype with high PD-1 and low CD127 expression. J. Virol. 81:2545-2553.
27. Rodriguez, M., M. J. Buchmeier, M. B. Oldstone, and P. W. Lampert. 1983. Ultrastructural localization of viral antigens in the CNS of mice persistently infected with lymphocytic choriomeningitis virus (LCMV). Am. J. Pathol. 110:95-100.
28. Shacklett, B. L., J. W. Critchfield, A. L. Ferre, and T. L. Hayes. 2009. Mucosal T-cell responses to HIV: responding at the front lines. J. Intern. Med. 265:58-66.
29. Sharpe, A. H., E. J. Wherry, R. Ahmed, and G. J. Freeman. 2007. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat. Immunol. 8:239-245.
30. Shin, H., and E. J. Wherry. 2007. CD8 T-cell dysfunction during chronic viral infection. Curr. Opin. Immunol. 19:408-415.
31. + T cells. PLoS Med. 5:e100.
32. + T cells leads to reversible immune dysfunction. Nat. Med. 12:1198-1202.
33. Urbani, S., B. Amadei, D. Tola, M. Massari, S. Schivazappa, G. Missale, and C. Ferrari. 2006. PD-1 expression in acute hepatitis C virus (HCV) infection is associated with HCV-specific CD8 exhaustion. J. Virol. 80:11398-11403.
34. van der Most, R. G., K. Murali-Krishna, J. G. Lanier, E. J. Wherry, M. T. Puglielli, J. N. Blattman, A. Sette, and R. Ahmed. 2003. Changing immunodominance patterns in antiviral CD8 T-cell responses after loss of epitope presentation or chronic antigenic stimulation. Virology 315:93-102.
35. Velu, V., S. Kannanganat, C. Ibegbu, L. Chennareddi, F. Villinger, G. J. Freeman, R. Ahmed, and R. R. Amara. 2007. Elevated expression levels of inhibitory receptor programmed death 1 on simian immunodeficiency virusspecific CD8 T cells during chronic infection but not after vaccination. J. Virol. 81:5819-5828.
36. Velu, V., K. Titanji, B. Zhu, S. Husain, A. Pladevega, L. Lai, T. H. Vanderford, L. Chennareddi, G. Silvestri, G. J. Freeman, R. Ahmed, and R. R. Amara. 2008. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458:206-210.
37. Welsh, R. M., Jr., and M. J. Buchmeier. 1979. Protein analysis of defective interfering lymphocytic choriomeningitis virus and persistently infected cells. Virology 96:503-515.
38. 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.
39. 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.
40. + T-cell exhaustion during chronic viral infection. Immunity 27:670-684.
41. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. J. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188:2205-2213.
42. + T-cell exhaustion in typical progressors, but not in long-term nonprogressors. Blood 109: 4671-4678.
43. Zhou, S., R. Ou, L. Huang, and D. Moskophidis. 2002. Critical role for perforin-, Fas/FasL-, and TNFR1-mediated cytotoxic pathways in downregulation of antigen-specific T cells during persistent viral infection. J. Virol. 76:829-840.