Immunotherapy of murine retrovirus-induced acquired immunodeficiency by CD4 T regulatory cell depletion and PD-1 blockade

Journal of Virology

Volumn 85, Issue 24, 2011, Pages 13342-13353

  Li, Wen ^a,b   Green, William R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b NANCHANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAG PROTEIN; GAMMA INTERFERON; PROGRAMMED DEATH 1 RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL SPECIFICITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DISEASE ASSOCIATION; DOWN REGULATION; FLOW CYTOMETRY; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; MOUSE; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; NONHUMAN; OPEN READING FRAME; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RETROVIRUS; SIGNAL TRANSDUCTION; T CELL DEPLETION; UPREGULATION; VIRUS LOAD;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANIMALS; ANTIGENS, DIFFERENTIATION; CD4-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; IMMUNOTHERAPY; LYMPHOCYTE DEPLETION; MALE; MICE; MICE, INBRED C57BL; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; RETROVIRIDAE; SIGNAL TRANSDUCTION; SPLEEN; T-LYMPHOCYTES, REGULATORY;

MURINAE; MUS;

EID: 84862969052     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00120-11     Document Type: Article

References (68)

1. Aandahl, E. M., J. Michaelsson, W. J. Moretto, F. M. Hecht, and D. F. Nixon. 2004. Human CD4+ CD25+ regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens. J. Virol. 78:2454-2459.
2. Agata, Y., et al. 1996. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int. Immunol. 8:765-772.
3. Aziz, D. C., Z. Hanna, and P. Jolicoeur. 1989. Severe immunodeficiency disease induced by a defective murine leukaemia virus. Nature 338:505-508.
4. Barber, D. L., et al. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:682-687.
5. Beilharz, M. W., et al. 2004. Timed ablation of regulatory CD4+ T cells can prevent murine AIDS progression. J. Immunol. 172:4917-4925.
6. Cook, W. J., K. A. Green, J. J. Obar, and W. R. Green. 2003. Quantitative analysis of LP-BM5 murine leukemia retrovirus RNA using real-time RTPCR. J. Virol. Methods 108:49-58.
7. Day, C. L., et al. 2006. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443:350-354.
8. Dietze, K. K., et al. 2011. Transient depletion of regulatory T cells in transgenic mice reactivates virus-specific CD8+ T cells and reduces chronic retroviral set points. Proc. Natl. Acad. Sci. U. S. A. 108:2420-2425.
9. Dittmer, U., et al. 2004. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity 20:293-303.
10. Elrefaei, M., C. A. Baker, N. G. Jones, D. R. Bangsberg, and H. Cao. 2008. Presence of suppressor HIV-specific CD8+ T cells is associated with increased PD-1 expression on effector CD8+ T cells. J. Immunol. 180:7757-7763.
11. Erbe, J. G., K. A. Green, K. M. Crassi, H. C. Morse III, and W. R. Green. 1992. Cytolytic T lymphocytes specific for tumors and infected cells from mice with a retrovirus-induced immunodeficiency syndrome. J. Virol. 66: 3251-3256.
12. Fontenot, J. D., J. P. Rasmussen, M. A. Gavin, and A. Y. Rudensky. 2005. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6:1142-1151.
13. Fontenot, J. D., et al. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22:329-341.
14. Fontenot, J. D., and A. Y. Rudensky. 2005. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat. Immunol. 6:331-337.
15. Fredrickson, T. N., et al. 1985. Multiparameter analyses of spontaneous nonthymic lymphomas occurring in NFS/N mice congenic for ecotropic murine leukemia viruses. Am. J. Pathol. 121:349-360.
16. Freeman, G. J., E. J. Wherry, R. Ahmed, and A. H. Sharpe. 2006. Reinvigorating exhausted HIV-specific T cells via PD-1-PD-1 ligand blockade. J. Exp. Med. 203:2223-2227.
17. Gaur, A., and W. R. Green. 2003. Analysis of the helper virus in murine retrovirus-induced immunodeficiency syndrome: evidence for immunoselection of the dominant and subdominant CTL epitopes of the BM5 ecotropic virus. Viral Immunol. 16:203-212.
18. Green, K. A., C. L. Ahonen, W. J. Cook, and W. R. Green. 2004. CD40- associated TRAF 6 signaling is required for disease induction in a retrovirusinduced murine immunodeficiency. J. Virol. 78:6055-6060.
19. Green, K. A., W. J. Cook, A. H. Sharpe, and W. R. Green. 2002. The CD154/CD40 interaction required for retrovirus-induced murine immunodeficiency syndrome is not mediated by upregulation of the CD80/CD86 costimulatory molecules. J. Virol. 76:13106-13110.
20. Green, K. A., et al. 1996. Antibody to the ligand for CD40 (gp39) inhibits murine AIDS-associated splenomegaly, hypergammaglobulinemia, and immunodeficiency in disease-susceptible C57BL/6 mice. J. Virol. 70:2569-2575.
21. Green, K. A., R. J. Noelle, B. G. Durell, and W. R. Green. 2001. Characterization of the CD154-positive and CD40-positive cellular subsets required for pathogenesis in retrovirus-induced murine immunodeficiency. J. Virol. 75:3581-3589.
22. Green, K. A., R. J. Noelle, and W. R. Green. 1998. Evidence for a continued requirement for CD40/CD40 ligand (CD154) interactions in the progression of LP-BM5 retrovirus-induced murine AIDS. Virology 241:260-268.
23. Green, K. A., T. Okazaki, T. Honjo, W. J. Cook, and W. R. Green. 2008. The programmed death-1 and interleukin-10 pathways play a down-modulatory role in LP-BM5 retrovirus-induced murine immunodeficiency syndrome. J. Virol. 82:2456-2469.
24. Green, W. R., K. M. Crassi, D. A. Schwarz, and K. A. Green. 1994. Cytotoxic T lymphocytes directed against MAIDS-associated tumors and cells from mice infected by the LP-BM5 MAIDS defective retrovirus. Virology 200: 292-296.
25. Green, W. R., K. A. Green, and K. M. Crassi. 1994. Adoptive transfer of polyclonal and cloned cytolytic T lymphocytes (CTL) specific for mouse AIDS-associated tumors is effective in preserving CTL responses: a measure of protection against LP-BM5 retrovirus-induced immunodeficiency. J. Virol. 68:4679-4684.
26. Greenwald, R. J., G. J. Freeman, and A. H. Sharpe. 2005. The B7 family revisited. Annu. Rev. Immunol. 23:515-548.
27. Hasenkrug, K. J., and U. Dittmer. 2010. Comment on "Premature terminal exhaustion of Friend virus-specific effector CD8+ T cells by rapid induction of multiple inhibitory receptors." J. Immunol. 185:1349. (Author's reply, 185:1349-1350.).
28. Ho, O., and W. R. Green. 2006. Cytolytic CD8+ T cells directed against a cryptic epitope derived from a retroviral alternative reading frame confer disease protection. J. Immunol. 176:2470-2475.
29. Ishida, Y., Y. Agata, K. Shibahara, and T. Honjo. 1992. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11:3887-3895.
30. Iwai, Y., S. Terawaki, M. Ikegawa, T. Okazaki, and T. Honjo. 2003. PD-1 inhibits antiviral immunity at the effector phase in the liver. J. Exp. Med. 198:39-50.
31. Iwashiro, M., et al. 2001. Immunosuppression by CD4+ regulatory T cells induced by chronic retroviral infection. Proc. Natl. Acad. Sci. U. S. A. 98:9226-9230.
32. Jolicoeur, P. 1991. Murine acquired immunodeficiency syndrome (MAIDS): an animal model to study the AIDS pathogenesis. FASEB J. 5:2398-2405.
33. Kinter, A., et al. 2007. Suppression of HIV-specific T cell activity by lymph node CD25+ regulatory T cells from HIV-infected individuals. Proc. Natl. Acad. Sci. U. S. A. 104:3390-3395.
34. Kinter, A. L., et al. 2007. CD25+ regulatory T cells isolated from HIVinfected individuals suppress the cytolytic and nonlytic antiviral activity of HIV-specific CD8+ T cells in vitro. AIDS Res. Hum. Retroviruses 23:438-450.
35. Klinken, S. P., T. N. Fredrickson, J. W. Hartley, R. A. Yetter, and H. C. Morse III. 1988. Evolution of B cell lineage lymphomas in mice with a retrovirus-induced immunodeficiency syndrome, MAIDS. J. Immunol. 140: 1123-1131.
36. Klinman, D. M., and H. C. Morse III. 1989. Characteristic of B cell proliferation and action in murine AIDS. J. Immunol. 142:1144-1149.
37. Latarjet, R., and J. F. Duplan. 1962. Experiments and discussion on leukamogenesis by cell-free extracts of radiation-induced leukemia in mice. Int. J. Radiat. Biol. 5:339-344.
38. Latchman, Y. E., et al. 2004. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc. Natl. Acad. Sci. U. S. A. 101:10691-10696.
39. Li, W., and W. R. Green. 2007. Murine AIDS requires CD154/CD40L expression by the CD4 T cells that mediate retrovirus-induced disease: is CD4 T cell receptor ligation needed? Virology 360:58-71.
40. Li, W., and W. R. Green. 2006. The role of CD4 T cells in the pathogenesis of murine AIDS. J. Virol. 80:5777-5789.
41. Li, Y. N., et al. 2010. CD4+CD25+ regulatory T cells suppress the immune responses of mouse embryo fibroblasts to murine cytomegalovirus infection. Immunol. Lett. 131:131-138.
42. Liang, B., et al. 1996. Murine AIDS, a key to understanding retrovirusinduced immunodeficiency. Viral Immunol. 9:225-239.
43. MacDonald, A. J., et al. 2002. CD4 T helper type 1 and regulatory T cells induced against the same epitopes on the core protein in hepatitis C virusinfected persons. J. Infect. Dis. 185:720-727.
44. Mayrand, S. M., P. A. Healy, B. E. Torbett, and W. R. Green. 2000. Anti-Gag cytolytic T lymphocytes specific for an alternative translational reading frame-derived epitope and resistance versus susceptibility to retrovirus-induced murine AIDS in F(1) mice. Virology 272:438-449.
45. Mayrand, S. M., D. A. Schwarz, and W. R. Green. 1998. An alternative translational reading frame encodes an immunodominant retroviral CTL determinant expressed by an immunodeficiency-causing retrovirus. J. Immunol. 160:39-50.
46. Morse, H. C., III, et al. 1992. Retrovirus-induced immunodeficiency in the mouse: MAIDS as a model for AIDS. AIDS 6:607-621.
47. Mosier, D. E., R. A. Yetter, and H. C. Morse III. 1987. Functional T lymphocytes are required for a murine retrovirus-induced immunodeficiency disease (MAIDS). J. Exp. Med. 165:1737-1742.
48. Mosier, D. E., R. A. Yetter, and H. C. Morse III. 1985. Retroviral induction of acute lymphoproliferative disease and profound immunosuppression in adult C57BL/6 mice. J. Exp. Med. 161:766-784.
49. Okazaki, T., and T. Honjo. 2006. The PD-1-PD-L pathway in immunological tolerance. Trends Immunol. 27:195-201.
50. Petrovas, C., et al. 2006. PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J. Exp. Med. 203:2281-2292.
51. Piccirillo, C. A., and E. M. Shevach. 2004. Naturally-occurring CD4+CD25+ immunoregulatory T cells: central players in the arena of peripheral tolerance. Semin. Immunol. 16:81-88.
52. Rouse, B. T., P. P. Sarangi, and S. Suvas. 2006. Regulatory T cells in virus infections. Immunol. Rev. 212:272-286.
53. Rowe, W. P., W. E. Pugh, and J. W. Hartley. 1970. Plaque assay techniques for murine leukemia viruses. Virology 42:1136-1139.
54. Rutkowski, M. R., O. Ho, and W. R. Green. 2009. Defining the mechanism(s) of protection by cytolytic CD8 T cells against a cryptic epitope derived from a retroviral alternative reading frame. Virology 390:228-238.
55. Rutkowski, M. R., C. A. Stevens, and W. R. Green. 2011. Impaired memory CD8 T cell responses against an immunodominant retroviral cryptic epitope. Virology 412:256-268.
56. Sakaguchi, S. 2004. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22:531-562.
57. Sakaguchi, S., et al. 2001. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol. Rev. 182:18-32.
58. Schwarz, D. A., and W. R. Green. 1994. CTL responses to the gag polyprotein encoded by the murine AIDS defective retrovirus are strain dependent. J. Immunol. 153:436-441.
59. Shevach, E. M. 2004. Regulatory/suppressor T cells in health and disease. Arthritis Rheum. 50:2721-2724.
60. Siliciano, R. F., et al. 1988. Analysis of host-virus interactions in AIDS with anti-gp120 T cell clones: effect of HIV sequence variation and a mechanism for CD4+ cell depletion. Cell 54:561-575.
61. Takamura, S., et al. 2010. Premature terminal exhaustion of Friend virusspecific effector CD8+ T cells by rapid induction of multiple inhibitory receptors. J. Immunol. 184:4696-4707.
62. Trautmann, L., et al. 2006. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat. Med. 12:1198-1202.
63. Vahlenkamp, T. W., M. B. Tompkins, and W. A. Tompkins. 2004. Feline immunodeficiency virus infection phenotypically and functionally activates immunosuppressive CD4+CD25+ T regulatory cells. J. Immunol. 172:4752-4761.
64. Velu, V., et al. 2009. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458:206-210.
65. Weiss, L., et al. 2004. Human immunodeficiency virus-driven expansion of CD4+CD25+ regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood 104:3249-3256.
66. Wherry, E. J., et al. 2007. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27:670-684.
67. Yetter, R. A., et al. 1988. CD4+ T cells are required for development of a murine retrovirus-induced immunodeficiency syndrome (MAIDS). J. Exp. Med. 168:623-635.
68. Zelinskyy, G., et al. 2009. The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood 114:3199-3207.