Dendritic cell inhibition is connected to exhaustion of CD8+ T cell polyfunctionality during chronic hepatitis C virus infection

Journal of Immunology

Volumn 184, Issue 6, 2010, Pages 3134-3144

  Rodrigue Gervais, Ian Gaël ^a,b,d   Rigsby, Hawley ^b   Jouan, Loubna ^a,b   Sauvé, Dominike ^a,b   Sékaly, Rafick Pierre ^a,b,d   Willems, Bernard ^a,b   Lamarre, Daniel ^a,b,c,d  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^d UNIVERSITY OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 12; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MONTIRELIN; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; APOPTOSIS REGULATORY PROTEIN; MEMBRANE ANTIGEN; PATTERN RECOGNITION RECEPTOR; PDCD1 PROTEIN, MOUSE;

ADULT; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; HELPER CELL; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; LYMPHOCYTE FUNCTION; MALE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRUS LOAD; BIOSYNTHESIS; BONE MARROW CELL; DEGRANULATION; DRUG ANTAGONISM; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; LONGITUDINAL STUDY; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; VIROLOGY; VIRUS ACTIVATION;

ANTIGENS, SURFACE; APOPTOSIS REGULATORY PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; CELL DEGRANULATION; DENDRITIC CELLS; FEMALE; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; IMMUNOSUPPRESSION; INTERLEUKIN-2; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; MYELOID CELLS; RECEPTORS, PATTERN RECOGNITION; VIRAL LOAD; VIRUS ACTIVATION;

EID: 77951881216     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902522     Document Type: Article

References (46)

1. Neumann-Haefelin, C., H. C. Spangenberg, H. E. Blum, and R. Thimme. 2007. Host and viral factors contributing to CD8+ T cell failure in hepatitis C virus infection. World J. Gastroenterol. 13: 4839-4847.
2. Grakoui, A., N. H. Shoukry, D. J. Woollard, J. H. Han, H. L. Hanson, J. Ghrayeb, K. K. Murthy, C. M. Rice, and C. M. Walker. 2003. HCV persistence and immune evasion in the absence of memory T cell help. Science 302: 659-662. (Pubitemid 37310924)
3. Bowen, D. G., and C. M. Walker. 2005. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 436: 946-952. (Pubitemid 41191670)
4. Golden-Mason, L., B. Palmer, J. Klarquist, J. A. Mengshol, N. Castelblanco, and H. R. Rosen. 2007. Upregulation of PD-1 expression on circulating and intrahepatic hepatitis C virus-specific CD8+ T cells associated with reversible immune dysfunction. J. Virol. 81: 9249-9258.
5. Nakamoto, N., D. E. Kaplan, J. Coleclough, Y. Li, M. E. Valiga, M. Kaminski, A. Shaked, K. Olthoff, E. Gostick, D. A. Price, et al. 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, 1937.e1-2.
6. Fuse, S., C. Y. Tsai, M. J. Molloy, S. R. Allie, W. Zhang, H. Yagita, and E. J. Usherwood. 2009. Recall responses by helpless memory CD8+ T cells are restricted by the up-regulation of PD-1. J. Immunol. 182: 4244-4254.
7. Velu, V., K. Titanji, B. Zhu, S. Husain, A. Pladevega, L. Lai, T. H. Vanderford, L. Chennareddi, G. Silvestri, G. J. Freeman, et al. 2009. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458: 206-210.
8. Kasprowicz, V., J. Schulze Zur Wiesch, T. Kuntzen, B. E. Nolan, S. Longworth, A. Berical, J. Blum, C. McMahon, L. L. Reyor, N. Elias, et al. 2008. High level of PD-1 expression on hepatitis C virus (HCV)-specific CD8+ and CD4+ T cells during acute HCV infection, irrespective of clinical outcome. J. Virol. 82: 3154-3160.
9. Wherry, E. J., S. J. Ha, S. M. Kaech, W. N. Haining, S. Sarkar, V. Kalia, S. Subramaniam, J. N. Blattman, D. L. Barber, and R. Ahmed. 2007. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
10. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426.
11. Li, K., E. Foy, J. C. Ferreon, M. Nakamura, A. C. Ferreon, M. Ikeda, S. C. Ray, M. Gale, Jr., and S. M. Lemon. 2005. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. USA 102: 2992-2997.
12. Loo, Y. M., D. M. Owen, K. Li, A. K. Erickson, C. L. Johnson, P. M. Fish, D. S. Carney, T. Wang, H. Ishida, M. Yoneyama, et al. 2006. Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc. Natl. Acad. Sci. USA 103: 6001-6006.
13. Wang, N., Y. Liang, S. Devaraj, J. Wang, S. M. Lemon, and K. Li. 2009. Toll-like receptor 3 mediates establishment of an antiviral state against hepatitis C virus in hepatoma cells. J. Virol. 83: 9824-9834.
14. Rodrigue-Gervais, I. G., L. Jouan, G. Beaulé, D. Sauvé, J. Bruneau, B. Willems, R. P. Sékaly, and D. Lamarre. 2007. Poly(I:C) and lipopolysaccharide innate sensing functions of circulating human myeloid dendritic cells are affected in vivo in hepatitis C virus-infected patients. J. Virol. 81: 5537-5546.
15. Averill, L., W. M. Lee, and N. J. Karandikar. 2007. Differential dysfunction in dendritic cell subsets during chronic HCV infection. Clin. Immunol. 123: 40-49.
16. Miyazaki, M., T. Kanto, M. Inoue, I. Itose, H. Miyatake, M. Sakakibara, T. Yakushijin, N. Kakita, N. Hiramatsu, T. Takehara, et al. 2008. Impaired cytokine response in myeloid dendritic cells in chronic hepatitis C virus infection regardless of enhanced expression of Toll-like receptors and retinoic acid inducible gene-I. J. Med. Virol. 80: 980-988.
17. Palm, N. W., and R. Medzhitov. 2009. Pattern recognition receptors and control of adaptive immunity. Immunol. Rev. 227: 221-233.
18. Shiina, M., and B. Rehermann. 2008. Cell culture-produced hepatitis C virus impairs plasmacytoid dendritic cell function. Hepatology 47: 385-395.
19. Trifilo, M. J., B. Hahm, E. I. Zuniga, K. H. Edelmann, and M. B. Oldstone. 2006. Dendritic cell inhibition: memoirs from immunosuppressive viruses. J. Infect. Dis. 194(Suppl. 1): S3-10.
20. 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.
21. Trautmann, L., L. Janbazian, N. Chomont, E. A. Said, S. Gimmig, B. Bessette, M. R. Boulassel, E. Delwart, H. Sepulveda, R. S. Balderas, et al. 2006. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat. Med. 12: 1198-1202.
22. Saito, T., D. M. Owen, F. Jiang, J. Marcotrigiano, and M. Gale, Jr. 2008. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454: 523-527.
23. Pause, A., G. Kukolj, M. Bailey, M. Brault, F. Dô, T. Halmos, L. Lagacé, R. Maurice, M. Marquis, G. McKercher, et al. 2003. An NS3 serine protease inhibitor abrogates replication of subgenomic hepatitis C virus RNA. J. Biol. Chem. 278: 20374-20380.
24. Marukian, S., C. T. Jones, L. Andrus, M. J. Evans, K. D. Ritola, E. D. Charles, C. M. Rice, and L. B. Dustin. 2008. Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Hepatology 48: 1843-1850.
25. Smyk-Pearson, S., I. A. Tester, J. Klarquist, B. E. Palmer, J. M. Pawlotsky, L. Golden-Mason, and H. R. Rosen. 2008. Spontaneous recovery in acute human hepatitis C virus infection: functional T-cell thresholds and relative importance of CD4 help. J. Virol. 82: 1827-1837.
26. He, X. S., B. Rehermann, F. X. López-Labrador, J. Boisvert, R. Cheung, J. Mumm, H. Wedemeyer, M. Berenguer, T. L. Wright, M. M. Davis, and H. B. Greenberg. 1999. Quantitative analysis of hepatitis C virus-specific CD8 (+) T cells in peripheral blood and liver using peptide-MHC tetramers. Proc. Natl. Acad. Sci. USA 96: 5692-5697.
27. Lauer, G. M., M. Lucas, J. Timm, K. Ouchi, A. Y. Kim, C. L. Day, J. Schulze Zur Wiesch, G. Paranhos-Baccala, I. Sheridan, D. R. Casson, et al. 2005. Full-breadth analysis of CD8+ T-cell responses in acute hepatitis C virus infection and early therapy. J. Virol. 79: 12979-12988.
28. Spangenberg, H. C., S. Viazov, N. Kersting, C. Neumann-Haefelin, D. McKinney, M. Roggendorf, F. von Weizsäcker, H. E. Blum, and R. Thimme. 2005. Intrahepatic CD8+ T-cell failure during chronic hepatitis C virus infection. Hepatology 42: 828-837. (Pubitemid 41401120)
29. Badr, G., N. Bédard, M. S. Abdel-Hakeem, L. Trautmann, B. Willems, J. P. Villeneuve, E. K. Haddad, R. P. Sékaly, J. Bruneau, and N. H. Shoukry. 2008. Early interferon therapy for hepatitis C virus rescues polyfunctional, long-lived CD8+ memory T Cells. J. Virol. 82: 10017-10031.
30. Almeida, J. R., D. A. Price, L. Papagno, Z. A. Arkoub, D. Sauce, E. Bornstein, T. E. Asher, A. Samri, A. Schnuriger, I. Theodorou, et al. 2007. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204: 2473-2485.
31. Blackburn, S. D., H. Shin, W. N. Haining, T. Zou, C. J. Workman, A. Polley, M. R. Betts, G. J. Freeman, D. A. Vignali, and E. J. Wherry. 2009. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10: 29-37.
32. Nolte, M. A., S. Leibundgut-Landmann, O. Joffre, and C. Reis e Sousa. 2007. Dendritic cell quiescence during systemic inflammation driven by LPS stimulation of radioresistant cells in vivo. J. Exp. Med. 204: 1487-1501.
33. Tinoco, R., V. Alcalde, Y. Yang, K. Sauer, and E. I. Zuniga. 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. Franco, S., M. Parera, E. Aparicio, B. Clotet, and M. A. Martinez. 2007. Genetic and catalytic efficiency structure of an HCV protease quasispecies. Hepatology 45: 899-910. (Pubitemid 46631559)
35. Brooks, D. G., S. J. Ha, H. Elsaesser, A. H. Sharpe, G. J. Freeman, and M. B. Oldstone. 2008. IL-10 and PD-L1 operate through distinct pathways to suppress T-cell activity during persistent viral infection. Proc. Natl. Acad. Sci. USA 105: 20428-20433.
36. Petrovas, C., J. P. Casazza, J. M. Brenchley, D. A. Price, E. Gostick, W. C. Adams, M. L. Precopio, T. Schacker, M. Roederer, D. C. Douek, and R. A. Koup. 2006. PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J. Exp. Med. 203: 2281-2292.
37. Elsaesser, H., K. Sauer, and D. G. Brooks. 2009. IL-21 is required to control chronic viral infection. Science 324: 1569-1572.
38. Fröhlich, A., J. Kisielow, I. Schmitz, S. Freigang, A. T. Shamshiev, J. Weber, B. J. Marsland, A. Oxenius, and M. Kopf. 2009. IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science 324: 1576-1580.
39. Lu, W., L. C. Arraes, W. T. Ferreira, and J. M. Andrieu. 2004. Therapeutic dendritic-cell vaccine for chronic HIV-1 infection. Nat. Med. 10: 1359-1365.
40. 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.
41. Zaks, K., M. Jordan, A. Guth, K. Sellins, R. Kedl, A. Izzo, C. Bosio, and S. Dow. 2006. Efficient immunization and cross-priming by vaccine adjuvants containing TLR3 or TLR9 agonists complexed to cationic liposomes. J. Immunol. 176: 7335-7345. (Pubitemid 43849034)
42. Johnson, S., Y. Zhan, R. M. Sutherland, A. M. Mount, S. Bedoui, J. L. Brady, E. M. Carrington, L. E. Brown, G. T. Belz, W. R. Heath, and A. M. Lew. 2009. Selected Toll-like receptor ligands and viruses promote helper-independent cytotoxic T cell priming by upregulating CD40L on dendritic cells. Immunity 30: 218-227.
43. Schmitt, N., R. Morita, L. Bourdery, S. E. Bentebibel, S. M. Zurawski, J. Banchereau, and H. Ueno. 2009. Human dendritic cells induce the differentiation of interleukin-21-producing T follicular helper-like cells through interleukin-12. Immunity 31: 158-169.
44. Mueller, S., 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.
45. Urbani, S., B. Amadei, D. Tola, G. Pedrazzi, L. Sacchelli, M. C. Cavallo, A. Orlandini, G. Missale, and C. Ferrari. 2008. Restoration of HCV-specific T cell functions by PD-1/PD-L1 blockade in HCV infection: effect of viremia levels and antiviral treatment. J. Hepatol. 48: 548-558.
46. Wang, X., Z. Zhang, S. Zhang, J. Fu, J. Yao, Y. Jiao, H. Wu, and F. S. Wang. 2008. B7-H1 up-regulation impairs myeloid DC and correlates with disease progression in chronic HIV-1 infection. Eur. J. Immunol. 38: 3226-3236.