Human immunodeficiency virus (HIV-1) infection selectively downregulates PD-1 expression in infected cells and protects the cells from early apoptosis in vitro and in vivo

Virology

Volumn 376, Issue 1, 2008, Pages 140-153

  Venkatachari, Narasimhan J ^a   Buchanan, William G ^a   Ayyavoo, Velpandi ^a  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Apoptosis; HIV 1; Infection; PD 1

Indexed keywords

CELL PROTEIN; PROTEIN PROGRAMMED DEATH 1;

APOPTOSIS; ARTICLE; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CELL PROTECTION; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS LOAD;

ANTI-RETROVIRAL AGENTS; ANTIGENS, CD; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; HIV CORE PROTEIN P24; HIV INFECTIONS; HIV-1; HUMANS; VIRAL LOAD;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 43749122339     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.03.015     Document Type: Article

References (41)

1. Ameisen J.C. Apoptosis subversion: HIV-Nef provides both armor and sword. Nat. Med. 7 11 (2001) 1181-1182
2. Arlen P.A., Brooks D.G., Gao L.Y., Vatakis D., Brown H.J., and Zack J.A. Rapid expression of human immunodeficiency virus following activation of latently infected cells. J. Virol. 80 3 (2006) 1599-1603
3. Azad A.A. Could Nef and Vpr proteins contribute to disease progression by promoting depletion of bystander cells and prolonged survival of HIV-infected cells?. Biochem. Biophys. Res. Commun. 267 3 (2000) 677-685
4. Bahbouhi B., Landay A., and Al-Harthi L. Dynamics of cytokine expression in HIV productively infected primary CD4+ T cells. Blood 103 12 (2004) 4581-4587
5. Barber D.L., Wherry E.J., Masopust D., Zhu B., Allison J.P., Sharpe A.H., Freeman G.J., and Ahmed R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439 7077 (2006) 682-687
6. Carbonari M., Pesce A.M., Cibati M., Modica A., Dell'Anna L., D'Offizi G., Angelici A., Uccini S., Modesti A., and Fiorilli M. Death of bystander cells by a novel pathway involving early mitochondrial damage in human immunodeficiency virus-related lymphadenopathy. Blood 90 1 (1997) 209-216
7. Chun T.W., Justement J.S., Lempicki R.A., Yang J., Dennis Jr. G., Hallahan C.W., Sanford C., Pandya P., Liu S., McLaughlin M., Ehler L.A., Moir S., and Fauci A.S. Gene expression and viral production in latently infected, resting CD4+ T cells in viremic versus aviremic HIV-infected individuals. Proc. Natl. Acad. Sci. U. S. A. 100 4 (2003) 1908-1913
8. Conti L., Rainaldi G., Matarrese P., Varano B., Rivabene R., Columba S., Sato A., Belardelli F., Malorni W., and Gessani S. The HIV-1 vpr protein acts as a negative regulator of apoptosis in a human lymphoblastoid T cell line: possible implications for the pathogenesis of AIDS. J. Exp. Med. 187 3 (1998) 403-413
9. Cotton M.F., Cassella C., Rapaport E.L., Tseng P.O., Marschner S., and Finkel T.H. Apoptosis in HIV-1 Infection. Behring-Inst.-Mitt. 97 (1996) 220-231
10. D'Souza M., Fontenot A.P., Mack D.G., Lozupone C., Dillon S., Meditz A., Wilson C.C., Connick E., and Palmer B.E. Programmed death 1 expression on HIV-specific CD4+ T cells is driven by viral replication and associated with T cell dysfunction. J. Immunol. 179 3 (2007) 1979-1987
11. 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., and Walker B.D. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443 7109 (2006) 350-354
12. Dong H., Strome S.E., Salomao D.R., Tamura H., Hirano F., Flies D.B., Roche P.C., Lu J., Zhu G., Tamada K., Lennon V.A., Celis E., and Chen L. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8 8 (2002) 793-800
13. Esumi S., Kaneko R., Kawamura Y., and Yagi T. Split single-cell RT-PCR analysis of Purkinje cells. Nat. Protoc. 1 4 (2006) 2143-2151
14. Finkel T.H., Tudor-Williams G., Banda N.K., Cotton M.F., Curiel T., Monks C., Baba T.W., Ruprecht R.M., and Kupfer A. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat. Med. 1 2 (1995) 129-134
15. Freeman G.J., Wherry E.J., Ahmed R., and Sharpe A.H. Reinvigorating exhausted HIV-specific T cells via PD-1-PD-1 ligand blockade. J. Exp. Med. 203 10 (2006) 2223-2227
16. Gougeon M.L. Apoptosis as an HIV strategy to escape immune attack. Nat. Rev. Immunol. 3 5 (2003) 392-404
17. Grakoui A., John Wherry E., Hanson H.L., Walker C., and Ahmed R. Turning on the off switch: regulation of anti-viral T cell responses in the liver by the PD-1/PD-L1 pathway. J. Hepatol. 45 4 (2006) 468-472
18. Greenwald R.J., Freeman G.J., and Sharpe A.H. The B7 family revisited. Annu. Rev. Immunol. 23 (2005) 515-548
19. Holm G.H., and Gabuzda D. Distinct mechanisms of CD4+ and CD8+ T-cell activation and bystander apoptosis induced by human immunodeficiency virus type 1 virions. J. Virol. 79 10 (2005) 6299-6311
20. Ishida Y., Agata Y., Shibahara K., and Honjo T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11 11 (1992) 3887-3895
21. Ji J., Chen J.J., Braciale V.L., and Cloyd M.W. Apoptosis induced in HIV-1-exposed, resting CD4+ T cells subsequent to signaling through homing receptors is Fas/Fas ligand-mediated. J. Leukoc Biol. 81 1 (2007) 297-305
22. Kamp W., Berk M.B., Visser C.J., and Nottet H.S. Mechanisms of HIV-1 to escape from the host immune surveillance. Eur. J. Clin. Invest. 30 8 (2000) 740-746
23. Lelievre J.D., Mammano F., Arnoult D., Petit F., Grodet A., Estaquier J., and Ameisen J.C. A novel mechanism for HIV1-mediated bystander CD4+ T-cell death: neighboring dying cells drive the capacity of HIV1 to kill noncycling primary CD4+ T cells. Cell Death Differ. 11 9 (2004) 1017-1027
24. Majumder B., Venkatachari N.J., Schafer E.A., Janket M.L., and Ayyavoo V. Dendritic cells infected with vpr-positive human immunodeficiency virus type 1 induce CD8+ T-cell apoptosis via upregulation of tumor necrosis factor alpha. J. Virol. 81 14 (2007) 7388-7399
25. Marshall W.L., Datta R., Hanify K., Teng E., and Finberg R.W. U937 cells overexpressing bcl-xl are resistant to human immunodeficiency virus-1-induced apoptosis and human immunodeficiency virus-1 replication. Virology 256 1 (1999) 1-7
26. McCloskey T.W., Ott M., Tribble E., Khan S.A., Teichberg S., Paul M.O., Pahwa S., Verdin E., and Chirmule N. Dual role of HIV Tat in regulation of apoptosis in T cells. J. Immunol. 158 2 (1997) 1014-1019
27. Mehandru S., Poles M.A., Tenner-Racz K., Horowitz A., Hurley A., Hogan C., Boden D., Racz P., and Markowitz M. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200 6 (2004) 761-770
28. Meng Q., Yang P., Li B., Zhou H., Huang X., Zhu L., Ren Y., and Kijlstra A. CD4+PD-1+ T cells acting as regulatory cells during the induction of anterior chamber-associated immune deviation. Invest. Ophthalmol. Vis. Sci. 47 10 (2006) 4444-4452
29. Moon H.S., and Yang J.S. Role of HIV Vpr as a regulator of apoptosis and an effector on bystander cells. Mol. Cells 21 1 (2006) 7-20
30. Nielsen C., Ohm-Laursen L., Barington T., Husby S., and Lillevang S.T. Alternative splice variants of the human PD-1 gene. Cell. Immunol. 235 2 (2005) 109-116
31. Petrovas C., Casazza J.P., Brenchley J.M., Price D.A., Gostick E., Adams W.C., Precopio M.L., Schacker T., Roederer M., Douek D.C., and Koup R.A. PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J. Exp. Med. 203 10 (2006) 2281-2292
32. Petrovas C., Price D.A., Mattapallil J., Ambrozak D.R., Geldmacher C., Cecchinato V., Vaccari M., Tryniszewska E., Gostick E., Roederer M., Douek D.C., Morgan S.H., Davis S.J., Franchini G., and Koup R.A. SIV-specific CD8+ T cells express high levels of PD1 and cytokines but have impaired proliferative capacity in acute and chronic SIVmac251 infection. Blood 110 3 (2007) 928-936
33. Piguet V., Schwartz O., Le Gall S., and Trono D. The downregulation of CD4 and MHC-I by primate lentiviruses: a paradigm for the modulation of cell surface receptors. Immunol. Rev. 168 (1999) 51-63
34. Seelamgari A., Maddukuri A., Berro R., de la Fuente C., Kehn K., Deng L., Dadgar S., Bottazzi M.E., Ghedin E., Pumfery A., and Kashanchi F. Role of viral regulatory and accessory proteins in HIV-1 replication. Front. Biosci. 9 (2004) 2388-2413
35. 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., and Sekaly R.P. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat. Med. 12 10 (2006) 1198-1202
36. Varbanov M., Espert L., and Biard-Piechaczyk M. Mechanisms of CD4 T-cell depletion triggered by HIV-1 viral proteins. AIDS Rev. 8 4 (2006) 221-236
37. Velu V., Kannanganat S., Ibegbu C., Chennareddi L., Villinger F., Freeman G.J., Ahmed R., and Amara R.R. Elevated expression levels of inhibitory receptor programmed death 1 on simian immunodeficiency virus-specific CD8 T cells during chronic infection but not after vaccination. J. Virol. 81 11 (2007) 5819-5828
38. Venkatachari N.J., Majumder B., and Ayyavoo V. Human immunodeficiency virus (HIV) type 1 Vpr induces differential regulation of T cell costimulatory molecules: direct effect of Vpr on T cell activation and immune function. Virology 358 2 (2007) 347-356
39. Yamashita M., and Emerman M. Retroviral infection of non-dividing cells: old and new perspectives. Virology 344 1 (2006) 88-93
40. Zha Y., Blank C., and Gajewski T.F. Negative regulation of T-cell function by PD-1. Crit. Rev. Immunol. 24 4 (2004) 229-237
41. Zhang J.Y., Zhang Z., Wang X., Fu J.L., Yao J., Jiao Y., Chen L., Zhang H., Wei J., Jin L., Shi M., Gao G.F., Wu H., and Wang F.S. PD-1 up-regulation is correlated with HIV-specific memory CD8+ T-cell exhaustion in typical progressors but not in long-term nonprogressors. Blood 109 11 (2007) 4671-4678