Protective efficacy of individual CD8+ T cell specificities in chronic viral infection

Journal of Immunology

Volumn 194, Issue 4, 2015, Pages 1755-1762

  Johnson, Susan ^a   Bergthaler, Andreas ^a,b   Graw, Frederik ^c,d,e   Flatz, Lukas ^a,f   Bonilla, Weldy V ^a,g   Siegrist, Claire Anne ^a   Lambert, Paul Henri ^a   Regoes, Roland R ^e   Pinschewer, Daniel D ^a,g  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d LOS ALAMOS NATIONAL LABORATORY   (United States)

^e ETH ZURICH   (Switzerland)

^f LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^g UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARENAVIRUS INFECTION; ARTICLE; CD8+ T LYMPHOCYTE; CELL SELECTION; CELL SPECIFICITY; CELLULAR IMMUNITY; CONTROLLED STUDY; GENETIC ENGINEERING; IMMUNOTHERAPY; INFECTION CONTROL; INFECTION PREVENTION; LYMPHOCYTE FUNCTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS INFECTION; NONHUMAN; REVERSE GENETICS; VIRUS CELL INTERACTION; VIRUS LOAD; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CYTOTOXIC T LYMPHOCYTE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTIC CHORIOMENINGITIS; MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; EPITOPES, T-LYMPHOCYTE; LYMPHOCYTIC CHORIOMENINGITIS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84922573073     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401771     Document Type: Article

References (52)

1. Virgin, H. W., E. J. Wherry, and R. Ahmed. 2009. Redefining chronic viral infection. Cell 138: 30-50.
2. Fung-Leung, W. P., T. M. Kündig, R. M. Zinkernagel, and T. W. Mak. 1991. Immune response against lymphocytic choriomeningitis virus infection in mice without CD8 expression. J. Exp. Med. 174: 1425-1429.
3. Matloubian, M., R. J. Concepcion, and R. Ahmed. 1994. CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. J. Virol. 68: 8056-8063.
4. Koup, R. A., J. T. Safrit, Y. Cao, C. A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D. D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68: 4650-4655.
5. Borrow, P., H. Lewicki, B. H. Hahn, G. M. Shaw, and M. B. Oldstone. 1994. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68: 6103-6110.
6. Thimme, R., D. Oldach, K. M. Chang, C. Steiger, S. C. Ray, and F. V. Chisari. 2001. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 194: 1395-1406.
7. Goulder, P. J., and D. I. Watkins. 2008. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat. Rev. Immunol. 8: 619-630.
8. McKiernan, S. M., R. Hagan, M. Curry, G. S. McDonald, A. Kelly, N. Nolan, A. Walsh, J. Hegarty, E. Lawlor, and D. Kelleher. 2004. Distinct MHC class I and II alleles are associated with hepatitis C viral clearance, originating from a single source. Hepatology 40: 108-114.
9. Schmitz, J. E., M. J. Kuroda, S. Santra, V. G. Sasseville, M. A. Simon, M. A. Lifton, P. Racz, K. Tenner-Racz, M. Dalesandro, B. J. Scallon, et al. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283: 857-860.
10. 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.
11. Moskophidis, D., F. Lechner, H. Pircher, and R. M. Zinkernagel. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362: 758-761.
12. 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.
13. 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.
14. Agnellini, P., P. Wolint, M. Rehr, J. Cahenzli, U. Karrer, and A. Oxenius. 2007. Impaired NFAT nuclear translocation results in split exhaustion of virus-specific CD8+ T cell functions during chronic viral infection. Proc. Natl. Acad. Sci. USA 104: 4565-4570.
15. 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.
16. Rehermann, B., and M. Nascimbeni. 2005. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 5: 215-229.
17. Bergthaler, A., L. Flatz, A. Verschoor, A. N. Hegazy, M. Holdener, K. Fink, B. Eschli, D. Merkler, R. Sommerstein, E. Horvath, et al. 2009. Impaired antibody response causes persistence of prototypic T cell-contained virus. PLoS Biol. 7: e1000080.
18. Harker, J. A., G. M. Lewis, L. Mack, and E. I. Zuniga. 2011. Late interleukin-6 escalates T follicular helper cell responses and controls a chronic viral infection. Science 334: 825-829.
19. Kotturi, M. F., B. Peters, F. Buendia-Laysa, Jr., J. Sidney, C. Oseroff, J. Botten, H. Grey, M. J. Buchmeier, and A. Sette. 2007. The CD8+ T-cell response to lymphocytic choriomeningitis virus involves the L antigen: uncovering new tricks for an old virus. J. Virol. 81: 4928-4940.
20. Fuller, M. J., A. Khanolkar, A. E. Tebo, and A. J. Zajac. 2004. Maintenance, loss, and resurgence of T cell responses during acute, protracted, and chronic viral infections. J. Immunol. 172: 4204-4214.
21. Blattman, J. N., E. J. Wherry, S. J. Ha, R. G. van der Most, and R. Ahmed. 2009. Impact of epitope escape on PD-1 expression and CD8 T-cell exhaustion during chronic infection. J. Virol. 83: 4386-4394.
22. Brooks, D. G., D. B. McGavern, and M. B. Oldstone. 2006. Reprogramming of antiviral T cells prevents inactivation and restores T cell activity during persistent viral infection. J. Clin. Invest. 116: 1675-1685.
23. 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 epi-tope presentation or chronic antigenic stimulation. Virology 315: 93-102.
24. Matano, T., R. Shibata, C. Siemon, M. Connors, H. C. Lane, and M. A. Martin. 1998. Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J. Virol. 72: 164-169.
25. Frahm, N., P. Kiepiela, S. Adams, C. H. Linde, H. S. Hewitt, K. Sango, M. E. Feeney, M. M. Addo, M. Lichterfeld, M. P. Lahaie, et al. 2006. Control of human immunodeficiency virus replication by cytotoxic T lymphocytes targeting subdominant epitopes. Nat. Immunol. 7: 173-178.
26. Paley, M. A., D. C. Kroy, P. M. Odorizzi, J. B. Johnnidis, D. V. Dolfi, B. E. Barnett, E. K. Bikoff, E. J. Robertson, G. M. Lauer, S. L. Reiner, and E. J. Wherry. 2012. Progenitor and terminal subsets of CD8+ T cells cooperate to contain chronic viral infection. Science 338: 1220-1225.
27. Graw, F., K. Richter, A. Oxenius, and R. R. Regoes. 2011. Comparison of cy-totoxic T lymphocyte efficacy in acute and persistent lymphocytic choriomen-ingitis virus infection. Proc. Biol. Sci. 278: 3395-3402.
28. Utzschneider, D. T., A. Legat, S. A. Fuertes Marraco, L. Carrié, I. Luescher, D. E. Speiser, and D. Zehn. 2013. T cells maintain an exhausted phenotype after antigen withdrawal and population reexpansion. Nat. Immunol. 14: 603-610.
29. Pérarnau, B., M. F. Saron, B. Reina San Martin, N. Bervas, H. Ong, M. J. Soloski, A. G. Smith, J. M. Ure, J. E. Gairin, and F. A. Lemonnier. 1999. Single H2Kb, H2Db and double H2KbDb knockout mice: peripheral CD8+ T cell repertoire and anti-lymphocytic choriomeningitis virus cytolytic responses. Eur. J. Immunol. 29: 1243-1252.
30. Flatz, L., A. Bergthaler, J. C. de la Torre, and D. D. Pinschewer. 2006. Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc. Natl. Acad. Sci. USA 103: 4663-4668.
31. Battegay, M., S. Cooper, A. Althage, J. Bänziger, H. Hengartner, and R. M. Zinkernagel. 1991. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J. Virol. Methods 33: 191-198.
32. Bergthaler, A., L. Flatz, A. N. Hegazy, S. Johnson, E. Horvath, M. Löhning, and D. D. Pinschewer. 2010. Viral replicative capacity is the primary determinant of lymphocytic choriomeningitis virus persistence and immunosuppression. Proc. Natl. Acad. Sci. USA 107: 21641-21646.
33. Pinschewer, D. D., L. Flatz, R. Steinborn, E. Horvath, M. Fernandez, H. Lutz, M. Suter, and A. Bergthaler. 2010. Innate and adaptive immune control of genetically engineered live-attenuated arenavirus vaccine prototypes. Int. Immunol. 22: 749-756.
34. Ganusov, V. V., and R. J. De Boer. 2006. Estimating costs and benefits of CTL escape mutations in SIV/HIV infection. PLOS Comput. Biol. 2: e24.
35. Schuler, M. M., M. D. Nastke, and S. Stevanovikć. 2007. SYFPEITHI: database for searching and T-cell epitope prediction. Methods Mol. Biol. 409: 75-93.
36. Betts, M. R., D. R. Ambrozak, D. C. Douek, S. Bonhoeffer, J. M. Brenchley, J. P. Casazza, R. A. Koup, and L. J. Picker. 2001. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 75: 11983-11991.
37. Addo, M. M., X. G. Yu, A. Rathod, D. Cohen, R. L. Eldridge, D. Strick, M. N. Johnston, C. Corcoran, A. G. Wurcel, C. A. Fitzpatrick, et al. 2003. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J. Virol. 77: 2081-2092.
38. Horiike, N., S. M. Fazle Akbar, K. Michitaka, K. Joukou, K. Yamamoto, N. Kojima, Y. Hiasa, M. Abe, and M. Onji. 2005. In vivo immunization by vaccine therapy following virus suppression by lamivudine: a novel approach for treating patients with chronic hepatitis B. J. Clin. Virol. 32: 156-161.
39. Oldstone, M. B., and M. J. Buchmeier. 1982. Restricted expression of viral glycoprotein in cells of persistently infected mice. Nature 300: 360-362.
40. Lin, M. Y., and R. M. Welsh. 1998. Stability and diversity of T cell receptor repertoire usage during lymphocytic choriomeningitis virus infection of mice. J. Exp. Med. 188: 1993-2005.
41. Chen, H., Z. M. Ndhlovu, D. Liu, L. C. Porter, J. W. Fang, S. Darko, M. A. Brockman, T. Miura, Z. L. Brumme, A. Schneidewind, et al. 2012. TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat. Immunol. 13: 691-700.
42. Vezys, V., D. Masopust, C. C. Kemball, D. L. Barber, L. A. O'Mara, C. P. Larsen, T. C. Pearson, R. Ahmed, and A. E. Lukacher. 2006. Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J. Exp. Med. 203: 2263-2269.
43. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4: 630-640.
44. Almeida, J. R., D. Sauce, D. A. Price, L. Papagno, S. Y. Shin, A. Moris, M. Larsen, G. Pancino, D. C. Douek, B. Autran, et al. 2009. Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity. Blood 113: 6351-6360.
45. Migueles, S. A., A. C. Laborico, W. L. Shupert, M. S. Sabbaghian, R. Rabin, C. W. Hallahan, D. Van Baarle, S. Kostense, F. Miedema, M. McLaughlin, et al. 2002. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 3: 1061-1068.
46. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, et al. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789.
47. Migueles, S. A., C. M. Osborne, C. Royce, A. A. Compton, R. P. Joshi, K. A. Weeks, J. E. Rood, A. M. Berkley, J. B. Sacha, N. A. Cogliano-Shutta, et al. 2008. Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29: 1009-1021.
48. Hersperger, A. R., F. Pereyra, M. Nason, K. Demers, P. Sheth, L. Y. Shin, C. M. Kovacs, B. Rodriguez, S. F. Sieg, L. Teixeira-Johnson, et al. 2010. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog. 6: e1000917.
49. Elahi, S., W. L. Dinges, N. Lejarcegui, K. J. Laing, A. C. Collier, D. M. Koelle, M. J. McElrath, and H. Horton. 2011. Protective HIV-specific CD8+ T cells evade Treg cell suppression. Nat. Med. 17: 989-995.
50. Kaufmann, D. E., D. G. Kavanagh, F. Pereyra, J. J. Zaunders, E. W. Mackey, T. Miura, S. Palmer, M. Brockman, A. Rathod, A. Piechocka-Trocha, et al. 2007. Upregulation of CTLA-4 by HIV-specific CD4+ T cells correlates with disease progression and defines a reversible immune dysfunction. Nat. Immunol. 8: 1246-1254.
51. 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, et al. 2006. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443: 350-354.
52. Mueller, S. N., and R. Ahmed. 2009. High antigen levels are the cause of T cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. USA 106: 8623-8628.