SIV-specific CD8+ T cells express high levels of PD1 and cytokines but have impaired proliferative capacity in acute and chronic SIVmac251 infection

Blood

Volumn 110, Issue 3, 2007, Pages 928-936

  Petrovas, Constantinos ^a   Price, David A ^a,b   Mattapallil, Joseph ^c   Ambrozak, David R ^a   Geldmacher, Christof ^a   Cecchinato, Valentina ^d   Vaccari, Monica ^d   Tryniszewska, Elzbieta ^d   Gostick, Emma ^b   Roederer, Mario ^a   Douek, Daniel C ^a   Morgan, Sara H ^b   Davis, Simon J ^b   Franchini, Genoveffa ^d   Koup, Richard A ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 2; PROGRAMMED DEATH 1 PROTEIN; PROTEIN; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOPATHOGENESIS; IMMUNOPHENOTYPING; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROVIRUS INFECTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS PATHOGENESIS;

EID: 34547931898     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-01-069112     Document Type: Article

References (60)

1. Barouch DH, Letvin NL. CD8+ cytotoxic T lymphocyte responses to lentiviruses and herpesviruses. Curr Opin Immunol. 2001;13:479-482.
2. Tough DF, Sprent J. Anti-viral immunity: spotting virus-specific T cells. Curr Biol. 1998;8:R498-R501.
3. Altfeld M, Kalife ET, Qi Y, et al. HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLoS Med. 2006;3:1851-1863.
4. Barouch DH, Kunstman J, Kuroda MJ, et al. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature. 2002;415:335-339.
5. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol. 1994;68:6103-6110.
6. Geldmacher C, Currier JR, Herrmann E, et al. CD8 T cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in HIV-1 seropositives. J Virol. 2006;81:2440-2448.
7. McMichael AJ, Rowland-Jones SL. Cellular immune responses to HIV. Nature. 2001;410:980-987.
8. Ogg GS, Jin X, Bonhoeffer S, et al. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science. 1998;279:2103-2106.
9. Pantaleo G, Koup RA. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat Med. 2004;10:806-810.
10. Walker CM, Moody DJ, Stites DP, Levy JA. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science. 1986;234:1563-1566.
11. Appay V, Nixon DF, Donahoe SM, et al. HIV-specific CD8(+) T cells produce antiviral cytokines but are impaired in cytolytic function. J Exp Med. 2000;192:63-75.
12. Champagne P, Ogg GS, King AS, et al. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature. 2001;410:106-111.
13. Gougeon ML. Apoptosis as an HIV strategy to escape immune attack. Nat Rev Immunol. 2003;3:392-404.
14. Xu XN, Screaton GR, McMichael AJ. Virus infections: escape, resistance, and counterattack. Immunity. 2001;15:867-870.
15. Jin X, Bauer DE, Tuttleton SE, et al. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med. 1999;189:991-998.
16. Schmitz JE, Kuroda MJ, Santra S, et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science. 1999;283:857-860.
17. Kuroda MJ, Schmitz JE, Charini WA, et al. Emergence of CTL coincides with clearance of virus during primary simian immunodeficiency virus infection in rhesus monkeys. J Immunol. 1999;162:5127-5133.
18. McKay PF, Schmitz JE, Barouch DH, et al. Vaccine protection against functional CTL abnormalities in simian human immunodeficiency virus-infected rhesus monkeys. J Immunol. 2002;168:332-337.
19. Vogel TU, Allen TM, Altman JD, Watkins DI. Functional impairment of simian immunodeficiency virus-specific CD8+ T cells during the chronic phase of infection. J Virol. 2001;75:2458-2461.
20. Xiong Y, Luscher MA, Altman JD, et al. Simian immunodeficiency virus (SIV) infection of a rhesus macaque induces SIV-specific CD8(+) T cells with a defect in effector function that is reversible on extended interleukin-2 incubation. J Virol. 2001;75:3028-3033.
21. Moskophidis D, Lechner F, Pircher H, Zinkernagel RM. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature. 1993;362:758-761.
22. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol. 2003;77:4911-4927.
23. Wherry EJ, Barber DL, Kaech SM, Blattman JN, Ahmed R. Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc Natl Acad Sci U S A. 2004;101:16004-16009.
24. Marrack P, Kappler J. Control of T cell viability. Annu Rev Immunol. 2004;22:765-787.
25. Betts MR, Nason MC, West SM, et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood. 2006;107:4781-4789.
26. Mueller YM, De Rosa SC, Hutton JA, et al. Increased CD95/Fas-induced apoptosis of HIVspecific CD8(+) T cells. Immunity. 2001;15:871-882.
27. Arnoult D, Petit F, Lelievre JD, et al. Caspase-dependent and -independent T-cell death pathways in pathogenic simian immunodeficiency virus infection: relationship to disease progression. Cell Death Differ. 2003;10:1240-1252.
28. Viollet L, Monceaux V, Petit F, et al. Death of CD4+ T cells from lymph nodes during primary SIVmac251 infection predicts the rate of AIDS progression. J Immunol. 2006;177:6685-6694.
29. Finkel TH, Tudor-Williams G, Banda NK, et al. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV-and SIV-infected lymph nodes. Nat Med. 1995;1:129-134.
30. Donahoe SM, Moretto WJ, Samuel RV, et al. Direct measurement of CD8+ T cell responses in macaques infected with simian immunodeficiency virus. Virology. 2000;272:347-356.
31. Kuroda MJ, Schmitz JE, Barouch DH, et al. Analysis of Gag-specific cytotoxic T lymphocytes in simian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J Exp Med. 1998;187:1373-1381.
32. Mothe BR, Horton H, Carter DK, et al. Dominance of CD8 responses specific for epitopes bound by a single major histocompatibility complex class I molecule during the acute phase of viral infection. J Virol. 2002;76:875-884.
33. Hel Z, Nacsa J, Kelsall B, et al. Impairment of Gag-specific CD8(+) T-cell function in mucosal and systemic compartments of simian immunodeficiency virus mac251- and simian-human immunodeficiency virus KU2-infected macaques. J Virol. 2001;75:11483-11495.
34. Nacsa J, Radaelli A, Edghill-Smith Y, et al. Avipox-based simian immunodeficiency virus (SIV) vaccines elicit a high frequency of SIV-specific CD4+ and CD8+ T-cell responses in vaccinia-experienced SIVmac251-infected macaques. Vaccine. 2004;22:597-606.
35. Hel Z, Tsai WP, Thornton A, et al. Potentiation of simian immunodeficiency virus (SIV)-specific CD4(+) and CD8(+) T cell responses by a DNA-SIV and NYVAC-SIV prime/boost regimen. J Immunol. 2001;167:7180-7191.
36. Sun Y, Schmitz JE, Buzby AP, et al. Virus-specific cellular immune correlates of survival in vaccinated monkeys after simian immunodeficiency virus challenge. J Virol. 2006;80:10950-10956.
37. Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature. 2006;439:682-687.
38. Day CL, Kaufmann DE, Kiepiela P, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature. 2006;443:350-354.
39. Petrovas C, Casazza JP, Brenchley JM, et al. PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J Exp Med. 2006;203:2281-2292.
40. Trautmann L, Janbazian L, Chomont N, et al. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat Med. 2006;12:1198-1202.
41. Greenwald RJ, Freeman GJ, Sharpe AH. The B7 family revisited. Annu Rev Immunol. 2005;23:515-548.
42. Ishida Y, Agata Y, Shibahara K, Honjo T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 1992;11:3887-3895.
43. Dong H, Strome SE, Salomao DR, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8:793-800.
44. Hori J, Wang M, Miyashita M, et al. B7-H1-induced apoptosis as a mechanism of immune privilege of corneal allografts. J Immunol. 2006;177:5928-5935.
45. Muhlbauer M, Fleck M, Schutz C, et al. PD-L1 is induced in hepatocytes by viral infection and by interferon-alpha and -gamma and mediates T cell apoptosis. J Hepatol. 2006;45:520-528.
46. Nacsa J, Stanton J, Kunstman KJ, et al. Emergence of cytotoxic T lymphocyte escape mutants following antiretroviral treatment suspension in rhesus macaques infected with SIVmac251. Virology. 2003;305:210-218.
47. Tryniszewska E, Nacsa J, Lewis MG, et al. Vaccination of macaques with long-standing SIVmac251 infection lowers the viral set point after cessation of antiretroviral therapy. J Immunol. 2002;169:5347-5357.
48. Mattapallil JJ, Douek DC, Buckler-White A, et al. Vaccination preserves CD4 memory T cells during acute simian immunodeficiency virus challenge. J Exp Med. 2006;203:1533-1541.
49. Mattapallil JJ, Smit-McBride Z, McChesney M, Dandekar S. Intestinal intraepithelial lymphocytes are primed for gamma interferon and MIP-1beta expression and display antiviral cytotoxic activity despite severe CD4(+) T-cell depletion in primary simian immunodeficiency virus infection. J Virol. 1998;72:6421-6429.
50. Price DA, West SM, Betts MR, et al. T cell receptor recognition motifs govern immune escape patterns in acute SIV infection. Immunity. 2004;21:793-803.
51. Zhang X, Schwartz JC, Guo X, et al. Structural and functional analysis of the costimulatory receptor programmed death-1. Immunity. 2004;20:337-347.
52. Freeman GJ, Wherry EJ, Ahmed R, Sharpe AH. Reinvigorating exhausted HIV-specific T cells via PD-1-PD-1 ligand blockade. J Exp Med. 2006;203:2223-2227.
53. Allen TM, O'Connor DH, Jing P, et al. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature. 2000;407:386-390.
54. Cai G, Karni A, Oliveira EM, Weiner HL, Hafler DA, Freeman GJ. PD-1 ligands, negative regulators for activation of naive, memory, and recently activated human CD4+ T cells. Cell Immunol. 2004;230:89-98.
55. Migliaccio M, Alves PM, Romero P, Rufer N. Distinct mechanisms control human naive and antigen-experienced CD8+ T lymphocyte proliferation. J Immunol. 2006;176:2173-2182.
56. Perfetto SP, Chattopadhyay PK, Lamoreaux L, et al. Amine reactive dyes: an effective tool to discriminate live and dead cells in polychromatic flow cytometry. J Immunol Methods. 2006;313:199-208.
57. Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12:1365-1371.
58. Silvestri G, Sodora DL, Koup RA, et al. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity. 2003;18:441-452.
59. Veazey RS, DeMaria M, Chalifoux LV, et al. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science. 1998;280:427-431.
60. Choi YK, Whelton KM, Mlechick B, Murphey-Corb MA, Reinhart TA. Productive infection of dendritic cells by simian immunodeficiency virus in macaque intestinal tissues. J Pathol. 2003;201:616-628.