CD8+ T cell exhaustion during persistent viral infection is regulated independently of the virus-specific T cell receptor

Immunological Investigations

Volumn 42, Issue 3, 2013, Pages 204-220

  Jackson, Stephanie R ^a   Berrien Elliott, Melissa M ^a   Meyer, Jennifer M ^a   Wherry, E John ^b   Teague, Ryan M ^a,c  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c SAINT LOUIS UNIVERSITY CANCER CENTER   (United States)

Author keywords

CD8+ T cells; Chronic Viral Infection; Dual T cell Receptor; Exhaustion; Tolerance

Indexed keywords

EPITOPE; GAMMA INTERFERON; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN RECOGNITION; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FRIEND LEUKEMIA VIRUS; IMMUNIZATION; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; HUMANS; IMMUNIZATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL;

EID: 84874835222     PISSN: 08820139     EISSN: 15324311     Source Type: Journal    
DOI: 10.3109/08820139.2012.751397     Document Type: Article

References (44)

1. Agnellini, P., Wolint, P., Rehr, M., Cahenzli, J., Karrer, U., Oxenius, A. 2007 Impaired NFAT nuclear translocation results in split exhaustion of virus-specific CD8 T cell functions during chronic viral infection. Proc. Natl. Acad. Sci. U S A 104 4565-4570.
2. Barber, D. L., Wherry, E. J., Masopust, D., Zhu, B., Allison, J. P., Sharpe, A. H., Freeman,G. J., Ahmed, R. 2006 Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439 682-687.
3. Blackburn, S. D., Shin, H., Haining, W. N., Zou, T., Workman, C. J., Polley, A., Betts,M. R., Freeman, G. J., Vignali, D. A., Wherry, E. J. 2009 Coregulation of CD8 T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10 29-37.
4. Blattman, J. N., Grayson, J. M., Wherry, E. J., Kaech, S. M., Smith, K. A., Ahmed, R. 2003 Therapeutic use of IL-2 to enhance antiviral T-cell responses in vivo. Nat. Med. 9 540-547.
5. Bollard, C. M., Rossig, C., Calonge, M. J., Huls, M. H., Wagner, H. J., Massague, J.,Brenner, M. K., Heslop, H. E., Rooney, C. M. 2002 Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood 99 3179-3187.
6. Boni, C., Fisicaro, P., Valdatta, C., Amadei, B., Di Vincenzo, P., Giuberti, T., Laccabue, D.,Zerbini, A., Cavalli, A., Missale, G., Bertoletti, A., Ferrari, C. 2007 Characterization of hepatitis B virus HBV-specific T-cell dysfunction in chronic HBV infection. J. Virol. 81 4215-4225.
7. Brooks, D. G., Lee, A. M., Elsaesser, H., McGavern, D. B., Oldstone, M. B. 2008 IL-10 blockade facilitates DNA vaccine-induced T cell responses and enhances clearance of persistent virus infection. J. Exp. Med. 205 533-541.
8. Cecchinato, V., Tryniszewska, E., Ma, Z. M., Vaccari, M., Boasso, A., Tsai, W. P.,Petrovas, C., Fuchs, D., Heraud, J. M., Venzon, D., Shearer, G. M., Koup, R. A.,Lowy, I., Miller, C. J., Franchini, G. 2008 Immune activation driven by CTLA-4 blockade augments viral replication at mucosal sites in simian immunodeficiency virus infection. J. Immunol. 180 5439-5447.
9. Curran, M. A., Allison, J. P. 2009 Tumor vaccines expressing flt3 ligand synergize with ctla-4 blockade to reject preimplanted tumors. Cancer Res 69 7747-7755.
10. Day, C. L., Kaufmann, D. E., Kiepiela, P., Brown, J. A., Moodley, E. S., Reddy, S., Mackey,E. W., Miller, J. D., Leslie, A. J., DePierres, C., Mncube, Z., Duraiswamy, J., Zhu, B.,Eichbaum, Q., Altfeld, M., Wherry, E. J., Coovadia, H. M., Goulder, P. J., Klenerman,P., Ahmed, R., Freeman, G. J., Walker, B. D. 2006 PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443 350-354.
11. Eggena, M. PP., Barugahare, B., Jones, N., Okello, M., Mutalya, S., Kityo, C., Mugyenyi,P., Cao, H. 2005 Depletion of regulatory T cells in HIV infection is associated with immune activation. J. Immunol. 174 4407-4414.
12. Ejrnaes, M., Filippi, C. M., Martinic, M. M., Ling, E. M., Togher, L. M., Crotty, S., von Herrath, M. G. 2006 Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203 2461-2472.
13. Ercolini, A. M., Ladle, B. H., Manning, E. A., Pfannenstiel, L. W., Armstrong, T. D.,Machiels, J. P., Bieler, J. G., Emens, L. A., Reilly, R. T., Jaffee, E. M. 2005 Recruitment of latent pools of high-avidity CD8 T cells to the antitumor immune response. J. Exp. Med. 201 1591-1602.
14. Fujio, K., Okamura, T., Yamamoto, K. 2010 The Family of IL-10-secreting CD4 T cells. Adv. Immunol. 105 99-130.
15. Goldberg, M. V., Maris, C. H., Hipkiss, E. L., Flies, A. S., Zhen, L., Tuder, R. M., Grosso,J. F., Harris, T. J., Getnet, D., Whartenby, K. A., Brockstedt, D. G., Dubensky, T. W.,Jr., Chen, L., Pardoll, D. M., Drake, C. G. 2007. Role of PD-1 and its ligand, B7H1, in early fate decisions of CD8 T cells. Blood 110 186-192.
16. Grosso, J. F., Kelleher, C. C., Harris, T. J., Maris, C. H., Hipkiss, E. L., De Marzo, A.,Anders, R., Netto, G., Getnet, D., Bruno, T. C., Goldberg, M. V., Pardoll, D. M., Drake,C. G. 2007 LAG-3 regulates CD8 T cell accumulation and effector function in murine self-and tumor-tolerance systems. J. Clin. Invest. 117 3383-3392.
17. Ha, S. J.,Mueller, S. N.,Wherry, E. J.,Barber, D. L.,Aubert, R. D., Sharpe, A. H., Freeman,G. J., Ahmed, R. 2008 Enhancing therapeutic vaccination by blocking PD-1- mediated inhibitory signals during chronic infection. J. Exp. Med. 205 543-555.
18. Hernandez, J., Aung, S., Redmond, W. L., Sherman, L. A. 2001 Phenotypic and functional analysis of CD8 T cells undergoing peripheral deletion in response to crosspresentation of self-antigen. J. Exp. Med. 194 707-717.
19. Kim, P. S., Ahmed, R. 2010 Features of responding T cells in cancer and chronic infection. Curr. Opin. Immunol. 22 223-230.
20. Lucas, C. L., Workman, C. J., Beyaz, S., LoCascio, S., Zhao, G., Vignali, D. A., Sykes,M. 2011 LAG-3, TGF-beta, and cell-intrinsic PD-1 inhibitory pathways contribute to CD8 but not CD4 T-cell tolerance induced by allogeneic BMT with anti-CD40L. Blood 117 5532-5540.
21. Martin-Orozco, N., Wang, Y. H., Yagita, H., Dong, C. 2006 Cutting Edge Programmed death PD ligand-1/PD-1 interaction is required for CD8 T cell tolerance to tissue antigens. J. Immunol. 177 8291-8295.
22. Moskophidis, D., Lechner, F., Pircher, H., Zinkernagel, R. M. 1993 Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362 758-761.
23. Mueller, K., Schweier, O., Pircher, H. 2008 Efficacy of IL-2-versus IL-15-stimulated CD8 T cells in adoptive immunotherapy. Eur. J. Immunol. 38 2874-2885.
24. Ohlen, C., Kalos, M., Cheng, L. E., Shur, A. C., Hong, D. J., Carson, B. D., Kokot, N. C.,Lerner, C. G., Sather, B. D., Huseby, E. S., Greenberg, P. D. 2002 CD8 T cell tolerance to a tumor-associated antigen is maintained at the level of expansion rather than effector function. J. Exp. Med. 195 1407-1418.
25. Pablo Penaloza-MacMaster, K. A., Alice Kamphorst, A., Smita Iyer, S., Erin West, E.,.Bogna Konieczny, B.,Gordon Freeman, G., Alexander Rudenski, A., and Rafi Ahmed,.R. 2011 FoxP3 CD4 cells promote CD8 T cell exhaustion during chronic infection The J. Immunol. 186 105.5.
26. Probst, H. C., McCoy, K., Okazaki, T., Honjo, T., van den Broek, M. 2005 Resting dendritic cells induce peripheral CD8 T cell tolerance through PD-1 and CTLA-4. Nat. Immunol. 6 280-286.
27. Quezada, S. A., Peggs, K. S., Curran, M. A., Allison, J. P. 2006 CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J. Clin. Invest. 116 1935-1945.
28. Radziewicz, H., Ibegbu, C. C., Fernandez, M. L., Workowski, K. A., Obideen, K., Wehbi,M., Hanson, H. L., Steinberg, J. P., Masopust, D., Wherry, E. J., Altman, J. D., Rouse,B. T., Freeman, G. J., Ahmed, R., Grakoui, A. 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.
29. Schietinger, A., Delrow, J. J., Basom, R. S., Blattman, J. N., Greenberg, P. D. 2012 Rescued tolerant CD8 T cells are preprogrammed to reestablish the tolerant state. Science 335 723-727.
30. Shin, H., Wherry, E. J. 2007 CD8 T cell dysfunction during chronic viral infection. Curr. Opin. Immunol. 19 408-415.
31. Shull, M. M., Ormsby, I., Kier, A. B., Pawlowski, S., Diebold, R. J., Yin, M., Allen, R.,Sidman, C., Proetzel, G., Calvin, D., et al. 1992 Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359 693-699.
32. Teague, R. M., Greenberg, P. D., Fowler, C., Huang, M. Z., Tan, X., Morimoto, J., Dossett,M. L., Huseby, E. S., Ohlen, C. 2008 Peripheral CD8 T cell tolerance to selfproteins is regulated proximally at the T cell receptor. Immunity 28 662-674 .
33. Tinoco, R., Alcalde, V., Yang, Y., Sauer, K., Zuniga, E. I. 2009 Cell-intrinsic transforming growth factor-beta signaling mediates virus-specific CD8 T cell deletion and viral persistence in vivo. Immunity 31 145-157.
34. Trautmann, L., Janbazian, L., Chomont, N., Said, E. A., Gimmig, S., Bessette, B.,Boulassel, M. R., Delwart, E., Sepulveda, H., Balderas, R. S., Routy, J. P., Haddad,E. K., Sekaly, R. P. 2006 Upregulation of PD-1 expression on HIV-specific CD8 T cells leads to reversible immune dysfunction. Nat. Med. 12 1198-1202.
35. Vicari, A. P., Chiodoni, C., Vaure, C., Ait-Yahia, S., Dercamp, C., Matsos, F., Reynard, O.,Taverne, C., Merle, P., Colombo, M. P., O'Garra, A., Trinchieri, G., Caux, C. 2002 Reversal of tumor-induced dendritic cell paralysis by CpG immunostimulatory oligonucleotide and anti-interleukin 10 receptor antibody. J. Exp. Med. 196 541-549.
36. Wherry EJ, Ha SJ, Kaech SM, Haining WN, Sarkar S, Kalia V, Subramaniam S,Blattman JN, Barber DL, Ahmed R. 2007. Molecular signature of CD8 T cell exhaustion during chronic viral infection. Immunity 27 670-84.
37. Wherry, E. J., Blattman, J. N., Ahmed, R. 2005 Low CD8 T-cell proliferative potential and high viral load limit the effectiveness of therapeutic vaccination. J. Virol. 79 8960-8968.
38. Wherry, E. J., Blattman, J. N., Murali-Krishna, K., van der Most, R., Ahmed, R. 2003 Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77 4911-4927.
39. Wilson, E. B., Brooks, D. G. 2010 Translating insights from persistent LCMV infection into anti-HIV immunity. Immunol. Res. 48 3-13.
40. Xie, Z., Chen, Y., Zhao, S., Yang, Z., Yao, X., Guo, S., Yang, C., Fei, L., Zeng, X., Ni, B., Wu,Y. 2009 Intrahepatic PD1/PD-L1 up-regulation closely correlates with inflammation and virus replication in patients with chronic HBV infection. Immunol. Invest. 38 624-638.
41. Yao, Z. Q., Ni, L., Zhang, Y., Ma, C. J., Zhang, C. L., Dong, Z. P., Frazier, A. D., Wu, X. Y.,Thayer, P., Borthwick, T., Chen, X. Y., Moorman, J. P. 2011 Differential regulation of T and B lymphocytes by PD-1 and SOCS-1 signaling in hepatitis C virusassociated non-Hodgkin's lymphoma. Immunol. Invest. 40 243-264.
42. Youngblood B, Oestreich KJ, Ha SJ, Duraiswamy J, Akondy RS, West EE, Wei Z, Lu P,Austin JW, Riley JL, Boss JM, Ahmed R. 2011. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8 T cells. Immunity 35 400-12.
43. Zajac, A. J., Blattman, J. N., Murali-Krishna, K., Sourdive, D. J., Suresh, M., Altman,J. D., Ahmed, R. 1998 Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188 2205-2213.
44. Zhang, Q., Yang, X., Pins, M., Javonovic, B., Kuzel, T., Kim, S. J., Parijs, L. V., Greenberg,N. M., Liu, V., Guo, Y., Lee, C. 2005 Adoptive transfer of tumor-reactive transforming growth factor-beta-insensitive CD8 T cells eradication of autologous mouse prostate cancer. Cancer Res. 65 1761-1769.