Mechanisms of lymphocyte killing by HIV

Current Opinion in Hematology

Volumn 4, Issue 1, 1997, Pages 24-31

  Casella, Carolyn R ^a   Finkel, Terri H ^a  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN;

CELL DEATH; CELL KILLING; CELL PROTECTION; CELL SPECIFICITY; CYTOTOXIC T LYMPHOCYTE; GENE DELETION; GENETIC LINKAGE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOCYTE ACTIVATION; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VIREMIA; VIRUS REPLICATION;

EID: 0031054102     PISSN: 10656251     EISSN: None     Source Type: Journal    
DOI: 10.1097/00062752-199704010-00005     Document Type: Review

References (97)

1. Pantaleo G, Graziozi C, Demarest JF, Butini L, Montroni M, Fox C, Orenstein JM, Kotler DP, Fauci AS: HIV Infection is active and progressive in lymphoid tissue during the clinically latent stages of disease. Nature 1993, 362:355-363.
2. Embertson J, Zupancic M, Ribas JL, Burke A, Racz P, Tenner-Racz K, Hasse AT: Massive covert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS. Nature 1993, 362:359-362.
3. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD: HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span and viral generation time. Science 1996, 271:1582-1586. The virion and infected cell half-lives were calculated by measuring the plasma viral RNA levels after administration of the drug ritonavir to HIV-positive subjects. This study differs from previous studies by Ho et al. (Nature 1995, 373:123-126) and Wei et al. (Nature 1995 373:117-123) by the measurement of plasma virus at earlier time points after drug administration. Measuring the early kinetics of virus allowed for more precise measurements of virion and infected cell half-lives. The authors found the mean virion half-life to be 0.24 days and the mean half-life of a productively infected cell to be 1.55 days.
4. Piatak M, Saag MS, Yang LC, Clark SJ, Kappes JC, Luk K-C, Hahn BH, Shaw GM, Lifson JD: High levels of HIV-1 in plasma during all stages of infection determined by competitive PCR. Science 1993, 259:1749-1754.
5. Ho DD, Neumann AU, Perelson AS, Chen W, Leonard JM, Markowitz M: Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 1995, 373:123-126.
6. Wei X, Ghosh SK, Taylor ME, Johnson VA, Emini EAD, Lifson PJD, Bonhoeffer S, Nowak MA, Hahn BH, Saag MS, Shaw GM: Viral dynamics in human immunodeficiency virus type 1 infection. Nature 1995, 373:117-122.
7. Furtado MR, Kinglsey LA, Wolinsky SM: Changes in the viral mRNA expression pattern correlate with a rapid rate of CD4+ T-cell number decline in human immunodeficiency virus type 1-infected individuals. J Virol 1995, 69:2092-2100.
8. Ioannidis JPA, Cappelleri JC, Lau J, Sacks HS, Skolnik PR: Predictive value of viral load measurements in asymptomatic untreated HIV-1 infection: a mathematical model. AIDS 1996, 10:255-262.
9. O'Brian WA, Hartigan PM, Martin D, Esinhart J, Hill A, Benoit S, Rubin M, Simberkoff MS, Hamilton JD: Changes in plasma HIV-1 RNA and CD4+ lymphocyte counts and the risk of progression to AIDS. N Engl J Med 1996, 334:426-431.
10. + T-cell counts and for viral RNA in the plasma using a sensitive branched polymerase chain reaction method. Baseline levels of viral RNA in the plasma after the initial viremia proved to be a good predictor of the time until progression to AIDS and the time until death. Importantly, the amount of viral RNA in the plasma was a better indicator of time until death than the CD4 counts in the HIV-infected individuals. A relative hazard of death of 1.55 was noted for every three-fold increase in plasma HIV RNA.
11. Su L, Kaneshima H, Bonyhadi M, Salimi S, Kraft D, Rabin L, McCune JM: HIV-1 induced thymocyte depletion is associated with indirect cytopathicity and infection of progenitor cells in vivo. Immunity 1995, 2:25-36.
12. Maldarelli F, Sato H, Berthold E, Orenstein J, Martin MA: Rapid induction of apoptosis by cell-to-cell transmission of human immunodeficiency virus type 1. J Virol 1995, 69:6457-6465.
13. + blood lymphocytes are rapidly killed in vitro by contact with autologous human immunodeficiency virus-Infected cells. Proc Natl Acad Sci U S A 1995, 92:7312-7316.
14. Heinkelein M, Sopper S, Jassoy C: Contact of human immunodeficiency virus type 1-infected and uninfected CD4+ T lymphocytes is highly cytolytic for both cells. J Virol 1995, 69:6925-6931.
15. Finkel TH, Tudor-Williams G, Banda NK, Cotton MF, Curiel T, Monks C, Baba TW, Ruprecht RM, Kupfer A: 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. The amounts of apoptosis and infection were measured in the lymph nodes of HIV-infected children and SIV-infected macaques. Apoptosis was measured by in situ nick translation and infection was measured by in situ hybridization for full-length HIV RNA. The authors found that the infected cells were rarely apoptotic. A correlation between apoptosis and infection was also reported.
16. Feinberg MB: Changing the natural history of HIV disease. Lancet 1996, 348:239-246.
17. Touchette N: Evolutions: apoptosis. J Natl Inst Health Res 1995, 7:9193.
18. Estaquier J, Idziorek B, Barre-Sinoussi FDF, Hurtrel B, Aubertin A-M, Venet A, Mehtali M, Muchmore E, Michel P, Mouton Y, Girard M, Ameisen JC: Programmed cell death and AIDS: significance of T-cell apoptosis in pathogenic and nonpathogenic primate lentiviral infection. Proc Natl Acad Sci U S A 1994, 91:9431-9435.
19. Carbonari M, Cibati M, Pesce AM, Sbarigia D, Grossi PDO, Luzi GG, Fiorilli M: Frequency of provirus-bearing CD4+ cells in HIV type 1 infection correlates with extent of in vitro apoptosis of CD8+ but not of CD4+ cells. AIDS Res Hum Retroviruses 1995, 11:789-794.
20. Cotton MF, Casella C, Rapaport ER, Marschner S, Finkel TH: Apoptosis in HIV-1 infection. In Mechanisms of Cell Death and Apoptosis, No. 97. Edited by Krammer PH, Nagaata S. Marburg, Germany: Behring Institute Mitteilungen; 1996:1-12.
21. Gougeon M-L, Garcia S, Heeney J, Tschopp R, Lecoeur H, Guetard D, Rame V. Dauguet C, Montagnier L: Programmed death of T cells in AIDS-related HIV and SIV infection. AIDS Res Hum Retroviruses 1993, 9:553-563.
22. +) from HIV-positive individuals were more prone to apoptosis than were activated T cells from uninfected control subjects. In addition, the authors showed that the amount of Fas expressed per cell is higher in HIV-positive people.
23. Groux H, Torpier G, Monte D, Mouton Y, Capron A, Ameisen JC: Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. J Exp Med 1992, 175:331-340.
24. Meyarrd L, Otto SA, Keet PM, Roos MTL, Miedema F: Programmed death of T cells in human immunodeficiency virus infection: no correlation with progression to disease. J Clin Invest 1994, 93:982-988.
25. Muro-Cacho CA, Pantaleo G, Fauci AS: Analysis of apoptosis in lymph nodes of HIV-infected persons: intensity of apoptosis correlates with the general state of activation of the lymphoid tissue and not with stage of disease or viral burden. J Immunol 1995, 154:5555-5566.
26. Sarin A, Clerici M, Blatt SP, Hendrix CW, Shearer GM, Henkart PA: Inhibition of activation-induced programmed cell death and restoration of defective immune responses of HIV+ donors by cysteine protease inhibitors. J Immunol 1994, 153:862-872.
27. + patients. Am J Pathol 1995, 146:1542-1555.
28. Anderson MR, Armitage RJ, Naraskovsky E, Tough TW, Roux E, Schooley K, Ramsdell F, Lynch DH: Fas transduces activating signals in normal human T lymphocytes. J Exp Med 1993, 178:2231-2235.
29. Brunner T, Mogil RJ, LaFace D, Yoo NJ, Mahboubi A, Echeverri F, Martin SJ, Force WR, Lynch DH, Ware CF, Green DR: Cell autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T cell hybridomas. Nature 1995, 373:441-444.
30. Dhien J, Walczak H, Baumler C, Debatin K-M, Krammer PH: Autocrine T cell suicide mediated by APO-1 (Fas/CD95). Nature 1995, 373:438-441.
31. Ju S-T, Panka DJ, Cui H, Ettinger R, El-Khatib M, Sherr DH, Stanger BZ, Marchak-Rothstein A: Fas (CD95)/FasL interactions required for programmed cell death after activation. Nature 1995, 373:444-448.
32. Katsikis PD, Wunderlich ES, Smith CA, Herzenberg LA: Fas antigen stimulation induces marked apoptosis of T lymphocytes in human immunodeficiency virus-infected individuals. J Exp Med 1995, 181:2029-2036.
33. Silvestris F, Carrorio P, Frassanito MA, Tucci M, Romito A, Nagata S, Dammacco F: Overexpression of Fas antigen of T cells in advanced HIV-1 infection: differential ligation constantly induced apoptosis. AIDS 1996, 10:131-141.
34. + T cells from human immunodeficiency virus-infected persons. J Exp Med 1995, 182:1759-1767.
35. Bradley AD, McElhinny JA, Leibson PJ, Lynch DH, Alderson MR, Paya CV: Upregulation of Fas ligand expression by human immunodeficiency virus in human macrophages mediates apoptosis of uninfected T lymphocytes. J Virol 1996, 70:199-206. Primary monocyte-derived macrophages were found to contain Fas ligand mRNA. The level of Fas ligand mRNA increased fourfold upon infection with a macrophage-tropic stain of HIV. Coculture of infected monocyte-derived macrophages and an uninfected Fas-positive T-cell line caused the death of the uninfected T-cell line. Infected monocyte-derived macrophages also caused the apoptosis of activated PBLs. Interestingly, uninfected monocyte-derived macrophages also induced the death of activated PBLs, although slightly less efficiently than infected monocyte-derived macrophages. This death appeared to be caused by Fas-Fas ligand interaction because an antibody that blocks this interaction inhibited death.
36. 2 anti-Fas antibody fragments. Interestingly, the amount of death in the infected cultures was 10-fold higher than the number of infected cells, indicating that the uninfected cells were also dying.
37. Ensoli B, Barillari G, Salahluddin SZ, Gallo RC, Wong-Staal F: Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature 1990, 345:84-86.
38. Lynch DH, Ramsdell F, Alderson MR: Fas and FasL in the homeostatic regulation of immune responses, Immunol Today 1995, 16:569-574.
39. Oyaizu N, McCloskey TW, Than S, Hu R, Kalyanaraman VS, Pahwa S: Cross-linking of CD4 molecules upregulates Fas antigen expression in lymphocytes by inducing interferon-gamma and tumor necrosis factor-alpha secretion. Blood 1994, 84:2622-2631.
40. + T cells. J Gen Virol 1995, 76:681-690.
41. Cohen DI, Tani Y, Tian H, Boone E, Samelson LE, Lane HC: Participation of tyrosine phosphorylation in the cytopathic effect of human immunodeficiency virus-1. Science 1992, 256:542-545.
42. Kolesnitchenko V, Wahl LM, Tian H, Sunila I, Tani Y, Hartmann C-P, Cossman J, Raffeld M, Orenstein J, Samelson LE, Cohen DJ: Human immunodeficiency virus 1 envelope-initiated G2-phase programmed cell death. Proc Natl Acad Sci U S A 1995, 92:11889-11893.
43. Forster S, Berverley P, Aspinall R: gp120-induced programmed cell death in recently activated T cells without subsequent ligation of the T cell receptor. Eur J Immunol 1995, 25:1778-1782.
44. Banda NK, Bernier J, Kurahara DK, Kurrle R, Haigwood N, Sekaly RP, Finkel TH: Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J Exp Med 1992, 176:1099-1106.
45. Radrizzani M, Accornero P, Amidei A, Aiello A, Delia D, Kurrle R, Colombo MP: IL-12 inhibits apoptosis induced in a human Th1 clone by gp120/CD4 cross-linking and CD3/TCR activation or by IL-2 deprivation. Cell Immunol 1995, 161:14-21.
46. lck. J Exp Med 1996, 183:39-48.
47. + T cells. J Biol Chem 1995, 270:19364-19369.
48. Kabelitz D, Pohl T, Pechhold K: Activation-induced cell death (apoptosis) of mature peripheral T lymphocytes. Immunol Today 1993, 14:338-339.
49. Green DR, Scott DW: Activation-induced apoptosis in lymphocytes. Curr Opin Immunol 1994, 6:476-487.
50. Li CJ, Friedman DJ, Wang C, Metelev V, Pardee AB: Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science 1995, 268:429-431.
51. + progenitor cells from asymptomatic patients are not a major reservoir for human immunodeficiency virus-1. Blood 1995, 86:1749-1756.
52. +) cells purified from the bone marrow of AIDS patients are committed to apoptotic cell death in culture. AIDS 1993, 7:1049-1055.
53. - and "activating" memory T cells. Clin Exp Immunol 1994, 95:195-200.
54. lck protein-tyrosine kinase interact with a common element in CD4 cytoplasmic tall. Proc Natl Acad Sci U S A 1995, 92:349-353.
55. Ameisen JC, Estaquier J, Idziorek T: From AIDS to parasite infection: pathogen-mediated subversion of programmed cell death as a mechanism for immune dysregulation. Immunol Rev 1994, 142:13-50.
56. Crise B, Buonocore L, Rose JK: CD4 is retained in the endoplasmic reticulum by the human immunodeficiency virus type 1 glycoprotein precursor. J Virol 1990, 64:5585-5593.
57. Willey RL, Maldarelli F, Martin MA, Strebel K: Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J Virol 1992, 66:7193-7200.
58. Zauli G, Gibelini D, Milani D, Mazzoni M, Borgatti P, La Placa M, Capitani S: Human immunodeficiency virus type 1 Tat protein protects lymphoid, epithelial, and neuronal cell lines from death by apoptosis. Cancer Res 1993, 53:4481-4485.
59. Caputo A, Sodroski JG, Haseltine WA: Constitutive expression of HIV-1 tat protein in human Jurkat T cells using a BK virus vector. J AIDS 1990, 3:372-329.
60. Gibellini D, Caputo A, Celeghini C, Bassini A, La Placa M: Tat-expressing Jurkat cells show an increased resistance to different apoptotic stimuli, including acute human immunodeficiency virus-type 1 (HIV-1) infection. Br J Haematol 1995, 89:24-44.
61. Li CJ, Wang C, Friedman DJ, Pardee AB: Reciprocal modulations between p53 and Tat of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 1995, 92:5461-5464. This study showed a reciprocal relationship in the ability to downregulate promoters between Tat and p53. p53 was able to suppress CAT protein expression from an HIV long terminal repeat CAT expression construct. Tat was able to suppress CAT protein expression from a CAT expression construct driven by the p53 promoter. In a productive infection where levels of Tat are high and transcription from the HIV long terminal repeat is necessary, Tat may reduce p53 expression.
62. Zauli G, Gibellini D, Caputo A, Bassini A, Negrini M, Monne M, Mazzoni M, Capitani S: The human immunodeficiency virus type-1 Tat protein upregulates Bcl-2 gene expression in Jurkat T-cell lines and primary peripheral blood mononuclear cells. Blood 1995, 86:3823-3834. The ability of Tat to increase bcl-2 expression is examined in this paper. The authors found that both intra- and extracellular Tat can increase bcl-2 mRNA. Furthermore, a T-cell line stably transfected with Tat showed increased bcl-2 mRNA and resistance to apoptosis induced by serum withdrawal.
63. Green way A, Azad A, McPhee D: Human immunodeficiency virus type 1 Nef protein inhibits activation pathways in peripheral blood mononuclear cells and T-cell lines. J Virol 1995, 69:1842-1850.
64. Penninger JM, Mak TW: Signal transduction, mitotic catastrophes, and death in T-cell development. Immunol Rev 1994, 142:231-272.
65. Solary E, Dubrez L, Eymin B: The role of apoptosis in the pathogenesis and treatment of diseases. Eur Respir J 1996, 9:1293-1305.
66. Schwartz O, Marechal V, Le Gall S, Lemonnier F, Heard JM: Endocytosis of major histocompatibillty complex class I molecules is induced by the HIV-1 Nef protein. Nat Med 1996, 2:338-342.
67. Howcroft TK, Strebel K, Martin MA, Singer DS: Repression of MHC class I gene promoter activity by two-exon Tat of HIV. Science 1993, 260:1320-1322.
68. Thompson CB: Apoptosis in the pathogenesis and treatment of disease. Science 1995, 267:1456-1462.
69. Hill AB, Barnett BC, McMichael AJ, McGeoch DJ: HLA class I molecules are not transported to the cell surface in cells infected with Herpes simplex virus types 1 and 2. J Immunol 1994, 152:2736-2741.
70. cdc2 activity. J Virol 1995, 69:6703-6711.
71. Jowett JBJ, Planelles V, Poon B, Shah NP, Chen M-L, Chen ISY: The human immunodeficiency virus type 1 vpr gene arrests infected T cells In the G2 + M phase of the cell cycle. J Virol 1995, 69:6304-6313.
72. cdc2.
73. Rogel ME, Wu LI, Emmerman M: The human Immunodeficiency virus type 1 vpr gene prevents cell proliferation during chronic infection. J Virol 1995, 96:882-888.
74. cdc2 activation required for apoptosis. Science 1994, 263:1143-1145.
75. Collette Y, Dutartre H, Benziane A, Roman-Morales, Benarous R, Harris M, Olive D: Physical and functional interaction of Nef with Lck: HIV-1 Nef-induced T-cell signaling defects. J Biol Chem 1996, 271:6333-6341.
76. + viruses but not for down-regulation of CD4. EMBO J 1995, 14:484-491.
77. Ruderman JV: MAP kinases and the activation of quiescent cells. Curr Opin Cell Biol 1993, 5:207-213.
78. Kafalas P, Brown TR, Brickell PM: Signalling by the p60c-src family of protein-tyrosine kinases. Int J Biochem Cell Biol 1995, 27:551-563.
79. Viscidi RP, Mayur K, Lederman HM, Frankel AD: Inhibition of antigen-induced lymphocyte proliferation by Tat protein from HIV-1. Science 1989, 246:1606-1608.
80. Luban J, Bossolt KL, Franke EK, Kalpana GV, Goff SP: Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 1993, 73:1067-1078.
81. Montague JW, Gaido ML, Frye C, Cidlowski JA: A calcium-dependent nuclease from apoptotic rat thymocytes is homologous with cyclophilin: recombinant cyclophilins A, B, and C have nuclease activity. J Biol Chem 1994, 269:18877-18880.
82. Cheynier R, Henrichwark S, Hadida F, Pelletier E, Oksenhendler E, Autran B, Wain-Hobson S: HIV and T cell expansion in splenic white pulps is accompanied by infiltration of HIV-specific cytotoxic T lymphocytes. Cell 1994, 78:373-387.
83. Brenner BG, Gryllis C, Wainberg MA: Role of antibody-dependent cellular cytotoxicity and lymphokine-activated killer cells in AIDS and related diseases. J Leukoc Biol 1990, 50:628-640.
84. Spear GT, Landay AL, Sillivan BL, Dittel B, Lint TF: Activation of complement on the surface of cells infected by human Immunodeficiency virus. J Immunol 1990, 144:1490-1496.
85. Cao J, Park IW, Cooper A, Sodroski J: Molecular determinants of acute single-cell lysis by human Immunodeficiency virus type 1. J Virol 1996, 70:1340-1354.
86. Laurence JA, Gottlieb AB, Kunkel HG: Soluble suppressor factors in patients with acquired immunodeficiency syndrome and its prodrome. J Clin Invest 1983, 72:2072-2081.
87. Walker CM, Moody DJ, Stilles DP, Levy JA: CDB+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 1988, 234:1563-1566.
88. + depleted peripheral blood mononuclear cells.
89. + T cells that suppressed HIV infection were identified. They belong to the CC chemokine family and are RANTES, MIP-1α, and MIP-1β. All three chemokines are needed for efficient suppression of replication of HIV-1. Replication of most but not all laboratory strains was suppressed by the addition of the three chemokines.
90. Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, Murphy PM, Berger EA: CC CKR5: a RANTES, MIP-1α, MIP-1β receptor as a fusin cofactor for macrophage-tropic HIV-1. Science 1996, 272:1955-1958.
91. Deng HK, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Marzio PD, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, Landau NR: Identification of a major co-receptor for primary isolates of HIV-1. Nature 1996, 381:661-666.
92. + cells is mediated by the chemoklne receptor CC-CKR-5. Nature 1996, 381:667-673. Alkhatib et al. (Science 1996, 272:1955-1958), Deng et al. (Nature 1996, 361:661-666), and Dragic et al. all show that the chemokine receptor CC-CKR-5, which is responsive to RANTES, MIP-1α, and MIP-1β, acts as a second cellular receptor for macrophage-tropic strains of HIV. Deng et al. also show that CC-CKR-5 RNA transcripts are found in primary monocyte/macrophages and in macrophage-depleted T cells. All authors entertain the possibility that other second receptors for HIV exist.
93. Tough DF, Borrow P, Sprent J: Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 1996, 272:1947-1949.
94. Bacon KB, Premack BA, Gardner P, Schall TJ: Activation of dual T cell signaling pathways by the chemoklne RANTES. Science 1995, 269:1727-1730.
95. Clerici M, Shearer GM: The Th1-Th-2 hypothesis of HIV infection: new insights, Immunol Today 1994, 15:575-581.
96. Zinkernagel RM, Hengartner H: T-cell-mediated immunopathology versus direct cytolysls by virus: implications for HIV and AIDS. Immunol Today 1994, 15:262-268.
97. + cell subset in HIV disease implicate replicative senescence in HIV pathogenesis. AIDS 1996, 10:F17-F22.