Proliferation capacity and cytotoxic activity are mediated by functionally and phenotypically distinct virus-specific CD8 t cells defined by interleukin-7Rα (CD127) and perforin expression

Journal of Virology

Volumn 84, Issue 8, 2010, Pages 3868-3878

  Cellerai, Cristina ^a   Perreau, Matthieu ^a   Rozot, Virginie ^a   Enders, Felicitas Bellutti ^a   Pantaleo, Giuseppe ^a   Harari, Alexandre ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD57 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 7 RECEPTOR ALPHA; PERFORIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOMEGALOVIRUS; CYTOTOXICITY; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INFLUENZA VIRUS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; BIOSYNTHESIS; CELL CULTURE; CELL PROLIFERATION; DEGRANULATION; FLOW CYTOMETRY; IMMUNOLOGY; T LYMPHOCYTE SUBPOPULATION; VIRUS INFECTION;

CYTOMEGALOVIRUS; ORTHOMYXOVIRIDAE;

CD8-POSITIVE T-LYMPHOCYTES; CELL DEGRANULATION; CELL PROLIFERATION; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; FLOW CYTOMETRY; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-2; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; PERFORIN; T-LYMPHOCYTE SUBSETS; TUMOR NECROSIS FACTOR-ALPHA; VIRUS DISEASES;

EID: 77950510141     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02565-09     Document Type: Article

References (69)

1. Ahmed, R., and D. Gray. 1996. Immunological memory and protective immunity: understanding their relation. Science 272: 54-60.
2. + T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8: 379-385.
3. + T cells produce antiviral cytokines but are impaired in cytolytic function. J. Exp. Med. 192: 63-75.
4. Appay, V., R. A. van Lier, F. Sallusto, and M. Roederer. 2008. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73: 975-983.
5. Ashton-Rickardt, P. G. 2005. The granule pathway of programmed cell death. Crit. Rev. Immunol. 25: 161-182.
6. + T cells are programmed by prolonged antigen exposure and low levels of cellular activation. Eur. J. Immunol. 36: 842-854.
7. Barry, M., and R. C. Bleackley. 2002. Cytotoxic T lymphocytes: all roads lead to death. Nat. Rev. Immunol. 2: 401-409.
8. Bart, P. A., A. Harari, and G. Pantaleo. 2006. Clinical studies of experimental vaccines. Curr. Opin. HIV AIDS 1: 286-293.
9. Bart, P. A., G. P. Rizzardi, G. Tambussi, J. P. Chave, A. G. Chapuis, C. Graziosi, J. M. Corpataux, N. Halkic, J. Y. Meuwly, M. Munoz, P. Meylan, W. Spreen, H. McDade, S. Yerly, L. Perrin, A. Lazzarin, and G. Pantaleo. 2000. Immunological and virological responses in HIV-1-infected adults at early stage of established infection treated with highly active antiretroviral therapy. AIDS 14: 1887-1897.
10. Berke, G. 1995. The CTL's kiss of death. Cell 81: 9-12.
11. + T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281: 65-78.
12. Betts, M. R., and A. Harari. 2008. Phenotype and function of protective T-cell immune responses in HIV. Curr. Opin. HIV AIDS 3: 349-355.
13. + T cells. Blood 107: 4781-4789.
14. + T cells identifies functionally and phenotypically defined memory T cells during acute resolving hepatitis B virus infection. J. Virol. 80: 3532-3540.
15. Bots, M., and J. P. Medema. 2006. Granzymes at a glance. J. Cell Sci. 119: 5011-5014.
16. Boutboul, F., D. Puthier, V. Appay, O. Pelle, H. Ait-Mohand, B. Combadiere, G. Carcelain, C. Katlama, S. L. Rowland-Jones, P. Debre, C. Nguyen, and B. Autran. 2005. Modulation of interleukin-7 receptor expression characterizes differentiation of CD8 T cells specific for HIV, EBV, and CMV. AIDS 19: 1981-1986.
17. + T cells. Blood 101: 2711-2720.
18. Champagne, P., G. S. Ogg, A. S. King, C. Knabenhans, K. Ellefsen, M. Nobile, V. Appay, G. P. Rizzardi, S. Fleury, M. Lipp, R. Forster, S. Rowland- Jones, R. P. Sekaly, A. J. McMichael, and G. Pantaleo. 2001. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410: 106-111.
19. Chattopadhyay, P. K., M. R. Betts, D. A. Price, E. Gostick, H. Horton, M. Roederer, and S. C. De Rosa. 2009. The cytolytic enzymes granzyme A, granzyme B, and perforin: expression patterns, cell distribution, and their relationship to cell maturity and bright CD57 expression. J. Leukoc. Biol. 85: 88-97.
20. Chowdhury, D., and J. Lieberman. 2008. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu. Rev. Immunol. 26: 389-420.
21. Colle, J. H., J. L. Moreau, A. Fontanet, O. Lambotte, M. Joussemet, J. F. Delfraissy, and J. Theze. 2006. CD127 expression and regulation are altered in the memory CD8 T cells of HIV-infected patients: reversal by highly active anti-retroviral therapy (HAART). Clin. Exp. Immunol. 143: 398-403.
22. Colle, J. H., J. L. Moreau, A. Fontanet, O. Lambotte, M. Joussemet, S. Jacod, J. F. Delfraissy, and J. Theze. 2006. Regulatory dysfunction of the interleukin-7 receptor in CD4 and CD8 lymphocytes from HIV-infected patients: effects of antiretroviral therapy. J. Acquir. Immune. Defic. Syndr. 42: 277-285.
23. 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.
24. Doherty, P. C., and J. P. Christensen. 2000. Accessing complexity: the dynamics of virus-specific T-cell responses. Annu. Rev. Immunol. 18: 561-592.
25. Dutoit, V., V. Rubio-Godoy, P. Y. Dietrich, A. L. Quiqueres, V. Schnuriger, D. Rimoldi, D. Lienard, D. Speiser, P. Guillaume, P. Batard, J. C. Cerottini, P. Romero, and D. Valmori. 2001. Heterogeneous T-cell response to MAGE-A10 (254-262) : high avidity-specific cytolytic T lymphocytes show superior antitumor activity. Cancer Res. 61: 5850-5856.
26. + memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 101: 4260-4266.
27. Harari, A., C. Cellerai, F. B. Enders, J. Kostler, L. Codarri, G. Tapia, O. Boyman, E. Castro, S. Gaudieri, I. James, M. John, R. Wagner, S. Mallal, and G. Pantaleo. 2007. Skewed association of polyfunctional antigen-specific CD8 T-cell populations with HLA-B genotype. Proc. Natl. Acad. Sci. U. S. A. 104: 16233-16238.
28. Harari, A., V. Dutoit, C. Cellerai, P. A. Bart, R. A. Du Pasquier, and G. Pantaleo. 2006. Functional signatures of protective antiviral T-cell immunity in human virus infections. Immunol. Rev. 211: 236-254.
29. Harari, A., F. B. Enders, C. Cellerai, P. A. Bart, and G. Pantaleo. 2009. Distinct profiles of cytotoxic granules in memory CD8 T cells correlate with function, differentiation stage, and antigen exposure. J. Virol. 83: 2862-2871.
30. Harari, A., and G. Pantaleo. 2008. HIV-1-specific immune response. Adv. Pharmacol. 56: 75-92.
31. Harari, A., S. Petitpierre, F. Vallelian, and G. Pantaleo. 2004. Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood 103: 966-972.
32. Harari, A., F. Vallelian, P. R. Meylan, and G. Pantaleo. 2005. Functional heterogeneity of memory CD4 T-cell responses in different conditions of antigen exposure and persistence. J. Immunol. 174: 1037-1045.
33. Hersperger, A. R., G. Makedonas, and M. R. Betts. 2008. Flow cytometric detection of perforin upregulation in human CD8 T cells. Cytometry A 11: 1050-1057.
34. + memory T-cell subsets. Proc. Natl. Acad. Sci. U. S. A. 101: 5610-5615.
35. + T cells is associated with diminished interleukin-2 (IL-2) production and is recovered by exogenous IL-2. J. Virol. 77: 10900-10909.
36. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 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.
37. Kaech, S. M., E. J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2: 251-262.
38. Kagi, D., B. Ledermann, K. Burki, R. M. Zinkernagel, and H. Hengartner. 1996. Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu. Rev. Immunol. 14: 207-232.
39. Kaufmann, D. E., and B. D. Walker. 2008. Programmed death-1 as a factor in immune exhaustion and activation in HIV infection. Curr. Opin. HIV AIDS 3: 362-367.
40. Klenerman, P., and A. Hill. 2005. T cells and viral persistence: lessons from diverse infections. Nat. Immunol. 6: 873-879.
41. Lanzavecchia, A., and F. Sallusto. 2005. Understanding the generation and function of memory T-cell subsets. Curr. Opin. Immunol. 17: 326-332.
42. + T cells. AIDS 13: 1649-1658.
43. + T cells. J. Exp. Med. 200: 701-712.
44. Lieberman, J. 2003. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat. Rev. Immunol. 3: 361-370.
45. + T-cell cytotoxic activity. J. Immunol. 182: 5560-5569.
46. + T-cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 3: 1061-1068.
47. + T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29: 1009-1021.
48. + T cells in HIV-infected individuals. J. Immunol. 174: 2900-2909.
49. Pantaleo, G., and A. Harari. 2006. Functional signatures in antiviral T-cell immunity for monitoring virus-associated diseases. Nat. Rev. Immunol. 6: 417-423.
50. Pantaleo, G., and R. A. Koup. 2004. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat. Med. 10: 806-810.
51. + T-cell survival in HIV infection. J. Exp. Med. 203: 2281-2292.
52. + T cells in HIV infection. J. Immunol. 183: 1120-1132.
53. Pipkin, M. E., and J. Lieberman. 2007. Delivering the kiss of death: progress on understanding how perforin works. Curr. Opin. Immunol. 19: 301-308.
54. + T cells after prolonged suppression of human immunodeficiency virus replication by antiretroviral therapy. J. Virol. 82: 3391-3404.
55. Russell, J. H., and T. J. Ley. 2002. Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20: 323-370.
56. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T-cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.
57. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
58. + effector and memory T-cell generation. Nat. Immunol. 4: 835-842.
59. Seder, R. A., P. A. Darrah, and M. Roederer. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8: 247-258.
60. Sprent, J., and C. D. Surh. 2002. T-cell memory. Annu. Rev. Immunol. 20: 551-579.
61. + T cells are a consequence of antigen load. J. Virol. 81: 2713-2725.
62. + T cells leads to reversible immune dysfunction. Nat. Med. 12: 1198-1202.
63. + T cells. Blood 106: 2091-2098.
64. + T-cell differentiation in response to viruses. Nat. Rev. Immunol. 3: 931-939.
65. + T cells. J. Exp. Med. 199: 925-936.
66. Younes, S. A., B. Yassine-Diab, A. R. Dumont, M. R. Boulassel, Z. Grossman, J. P. Routy, and R. P. Sekaly. 2003. HIV-1 viremia prevents the establishment of interleukin 2-producing HIV-specific memory CD4+ T cells endowed with proliferative capacity. J. Exp. Med. 198: 1909-1922.
67. + T-cell exhaustion in typical progressors but not in long-term nonprogressors. Blood 109: 4671-4678.
68. Zimmerli, S. C., A. Harari, C. Cellerai, F. Vallelian, P. A. Bart, and G. Pantaleo. 2005. HIV-1-specific IFN-γ/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc. Natl. Acad. Sci. U. S. A. 102: 7239-7244.
69. Zinkernagel, R. M., M. F. Bachmann, T. M. Kundig, S. Oehen, H. Pirchet, and H. Hengartner. 1996. On immunological memory. Annu. Rev. Immunol. 14: 333-367.