Apoptosis and HIV infection: About molecules and genes

Current Pharmaceutical Design

Volumn 14, Issue 3, 2008, Pages 237-244

  Cossarizza, Andrea ^a,b  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b Department of Biomedical Sciences ^*  (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CASPASE 10; CASPASE 8; CHEMOKINE RECEPTOR CXCR4; FAS ANTIGEN; FAS LIGAND; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 160; INTERLEUKIN 1; INTERLEUKIN 15; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; PROTEIN BCL 2; PROTEINASE; PROTEINASE INHIBITOR; TRANSACTIVATOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VIF PROTEIN; VPR PROTEIN; VPU PROTEIN; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; CYTOKINE; VIRUS PROTEIN;

APOPTOSIS; AUTOPHAGY; B LYMPHOCYTE; BYSTANDER EFFECT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DISEASE FREE SURVIVAL; DRUG MECHANISM; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HOMEOSTASIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; MITOCHONDRION; NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVIEW; VIRUS CELL INTERACTION; ANIMAL; DRUG EFFECT; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; PATHOGENICITY;

ANIMALS; ANTI-HIV AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; APOPTOSIS; CYTOKINES; HIV INFECTIONS; HIV-1; HOMEOSTASIS; HUMANS; VIRAL PROTEINS;

EID: 39749189476     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161208783413293     Document Type: Review

References (145)

1. Gottlieb MS, Schroff R, Schanker HM, Weisman JD, Fan PT, Wolf RA, et al. Pneumocystis carinii pneumonia and mucosal candidiasis in previously healthy homosexual men: Evidence of a new acquired cellular immunodeficiency. N Engl J Med 1981; 305: 1425-31.
2. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, et al. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 1983; 220: 868-71.
3. Gallo RC, Sarin PS, Gelmann EP, Robert-Guroff M, Richardson E, Kalyanaraman VS, et al. Isolation of human T-cell leukemia virus in acquired immune deficiency syndrome (AIDS). Science 1983; 220: 865-7.
4. Joint United Nations Programme on HIV/AIDS and World Health Organization. 2006: www.unaids.org
5. Hammer SM, Squires KE, Hughes MD, Grimes JM, Demeter LM, Currier JS, et al. A controlled trial of two nucleoside analogues plus indinavir in persons with human immunodeficiency virus infection and CD4 cell counts of 200 per cubic millimeter or less. AIDS Clinical Trials Group 320 Study Team. N Engl J Med 1997; 337: 725-33.
6. Palella FJ Jr, Delaney KM, Moorman AC, Loveless MO, Fuhrer J, Satten GA, et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med 19981 338: 853-60.
7. Hammer SM, Saag MS, Schechter M, Montaner JS, Schooley RT, Jacobsen DM, et al. International AIDS Society-USA panel. Treatment for adult HIV infection: 2006 recommendations of the International AIDS Society-USA panel. JAMA 2006; 296: 827-43.
8. Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, Weiss RA. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 1984; 312: 763-7.
9. Lifson JD, Reyes GF, McGrath MS, Stein BS, Engleman EG. AIDS retrovirus induced cytopathology: Giant cell formation and involvement of CD4 antigen. Science 1986; 232: 1123-7.
10. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, et al. Identification of a major co-receptor for primary isolates of HIV-1. Nature 1996; 381: 661-6.
11. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, et al. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 1996; 381: 667-73.
12. Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, Ponath PD, et al. The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 1996; 85: 1135-48.
13. Douek DC, Brenchley JM, Betts MR, Ambrozak DR, Hill BJ, Okamoto Y, et al. HIV preferentially infects HIV-specific CD4+ T cells. Nature. 2; 417: 95-8.
14. Chong Y, Ikematsu H, Kikuchi K, Yamamoto M, Murata M, Nishimura M, et al. Selective CD27+ (memory) B cell reduction and characteristic B cell alteration in drug-naive and HAART-treated HIV type 1-infected patients. AIDS Res Hum Retroviruses 2004; 20: 219-26.
15. Seth A, Markee J, Hoering A, Sevin A, Sabath DE, Schmitz JE, et al. Alterations in T cell phenotype and human immunodeficiency virus type 1-specific cytotoxicity after potent antiretroviral therapy. J Infect Dis 2001; 183: 722-9.
16. 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. Exp Med 1992; 175: 331-40.
17. Meyaard L, Otto SA, Jonker RR, Mijnster MJ, Keet RP, Miedema F. Programmed death of T cells in HIV-1 infection. Science 1992; 257: 217-9.
18. Banda NK, Bernier J, Kurahara DK, Kurrle R, Haigwood N, Sekaly RP, et al. Crosslinking CD4 by-human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J Exp Med 1992; 176: 1099-106.
19. Ameisen JC, Capron A. Cell dysfunction and depletion in AIDS: The programmed cell death hypothesis. Immunol Today 1991; 12: 102-5.
20. Lewin SR, Ribeiro RM, Kaufmann GR, Smith D, Zaunders J, Law M, et al. Dynamics of T cells and TCR excision circles differ after treatment of acute and chronic HIV infection. J Immunol 2002; 169: 4657-66.
21. Natarajan V, Lempicki RA, Sereti I, Badralmaa Y, Adelsberger, JW, Metcalf JA, et al. Increased peripheral expansion of naive CD4+ T cells in vivo atter IL-2 treatment of patients with HIV infection. Proc Natl Acad Sci USA 2002; 99: 10712-7
22. Koning FA, Otto SA, Hazenberg MD, Dekker L, Prins M, Miedema F, et al. Low-level CD4+ T cell activation is associated with low susceptibility to HIV-1 infection. J Immunol 2005; 175: 6117-22.
23. Di Mascio M, Sereti I, Matthews LT, Natarajan V, Adelsberger J, Lempicki R, et al. Naive T-cell dynamics in human immunodeficiency virus type 1 infection: Effects of highly active antiretroviral therapy provide insights into the mechanisms of naive T-cell depletion. J Virol 2006; 80: 2665-74.
24. Teixeira L, Valdez H, McCune JM, Koup RA, Badley AD, Hellerstein MK, et al. Poor CD4 T cell restoration after suppression of HIV-1 replication may reflect lower thymic function. AIDS 2001; 15: 1749-56
25. Cohen Stuart J, Hamann D, Borleffs J, Roos V, Miedema F, Boucher C, et al. Reconstitution of naive T cells during antiretroviral treatment of HIV-infected adults is dependent on age. AIDS 2002; 16: 2263-6.
26. Chattopadhyay PK, Douek DC, Gange SJ, Chadwick KR, Hellerstein M, Margolick JB. Longitudinal assessment of de novo T cell production in relation to HIV-associated T cell homeostasis failure. AIDS Res Hum Retroviruses 2006; 22: 501-7.
27. Ott M, Emiliani S, Van Lint C, Herbein G, Lovett J, Chirmule N, McCloskey T, et al. Immune hyperactivation of HIV-1-infected T cells mediated by Tat and the CD28 pathway. Science 1997; 275: 1481-5
28. Hazenberg MD, Otto SA, van Benthem BH, Roos MT, Coutinho RA, Lange JM, et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 2003; 17: 1881-8.
29. Picker LJ. Immunopathogenesis of acute AIDS virus infection. Curr Opin Immunol 2006; 18: 399-405.
30. Gaines H, von Sydow MA, von Stedingk LV, Biberfeld G, Bottiger B, Hansson LO, et al. Immunological changes in primary HIV-1 infection. AIDS 1990;4: 995-9.
31. Cossarizza A, Ortolani C, Mussini C, Borghi V, Guaraldi G, Mongiardo N, et al. Massive activation of immune cells with an intact T cell repertoire in acute human immunodeficiency virus syndrome. J Infect Dis 1995; 172: 105-12.
32. Norris PJ, Pappalardo BL, Custer B, Spotts G, Hecht FM, Busch MP. Elevations in IL-10, TNF-alpha, and IFN-gamma from the earliest point of HIV Type 1 infection. AIDS Res Hum Retroviruses 2006; 22: 757-62.
33. Varbanov M, Espert L, Biard-Piechaczyk M. Mechanisms of CD4 T-cell depletion triggered by HIV-1 viral proteins. AIDS Rev 2006; 8: 221-36
34. Zagury JF, Cahtalloube H, Achour A, Cho YY, Fall L, Lachgar A, et al. Striking similarities between HIV-1 Env protein and the apoptosis mediating cell surface antigen Fas. Role in the pathogenesis of AIDS. Biomed Pharmacother 190; 47: 331-5.
35. Zauli G, Gibellini D, Secchiero P, Dutartre H, Olive D, Capitani S, et al. Human immunodeficiency virus type 1 Nef protein sensitizes CD4(+) T lymphoid cells to apoptosis via functional upregulation of the CD95/CD95 ligand pathway. Blood 1999; 93: 1000-10.
36. Xu XN, Laffert B, Screaton GR, Kraft M, Wolf D, Kolanus W, et al. Induction of Fas ligand expression by HIV involves the interaction of Nef with the T cell receptor zeta chain. J Exp Med 1999; 189: 1489-96
37. Westendorp MO, Frank R, Ochsenbauer C, Stricker K, Dhein J, Walczak H, et al. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 1995; 375: 497-500.
38. McCloskey TW, Ott M, Tribble E, Khan SA, Teichberg S, Paul MO, et al. Dual role of HIV Tat in regulation of apoptosis in T cells. J Immunol 1997; 158: 1014-9.
39. Herbein G, Mahiknecht U, Batliwalla F, Gregersen P, Pappas T, Butler J, et al. Apoptosis of CD8+ T cells is mediated by macrophages through interaction of HIV gp 120 with chemokine receptor CXCR4. Nature 1998; 395: 189-94.
40. James CO, Huang MB, Khan M, Garcia-Barrio M, Powell MD, Bond VC. Extracellular Nef protein targets CD4+ T cells for apoptosis by interacting with CXCR4 surface receptors. J Virol 2004; 78: 3099-109
41. Chen D, Wang M, Zhou S, Zhou Q. HIV-1 Tat targets microtubules to induce apoptosis, a process promoted by the pro-apoptotic Bcl-2 relative Bim. EMBO J 2002; 21: 6801-10.
42. Deniaud A, Brenner C, Kroemer G. Mitochondrial membrane permeabilization by HIV-1 Vpr. Mitochondrion 2004; 4: 223-33.
43. Garg H, Blumenthal R. HIV gp41-induced apoptosis is mediated by caspase-3-dependent mitochondrial depolarization, which is inhibited by HIV protease inhibitor nelfinavir. J Leukoc Biol 2006; 79: 351-62.
44. Jacotot E, kavagnan L, Loeffler M, Ferri KF, Vieira HL, Zamzami N, et al. The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J Exp Med 2000; 191: 33-46.
45. Macho A, Calzado MA, Jimenez-Reina L, Ceballos E, Leon J, Munoz E. Susceptibility of HIV-1-TAT transfected cells to undergo apoptosis. Biochemical mechanisms. Oncogene 1999; 18: 7543-51.
46. Sastry KJ, Marin MC, Nehete PN, McConnell K, el-Naggar AK, McDonnell TJ. Expression of human immunodeficiency virus type I tat results in down-regulation of bcl-2 and induction of apoptosis in hematopoietic cells. Oncogene 1996; 13: 487-93.
47. Wang Z, Morris GF, Reed JC, Kelly GD, Morris CB. Activation of Bcl-2 promoter-directed gene expression by the human immunodeficiency virus type-1 Tat protein. Virology 1999; 257: 502-10.
48. Bartz SR, Emerman M. Human immunodeficiency virus type I Tat induces apoptosis and increases sensitivity to apoptotic signals by up-regulating FLICE/caspase-8. J Virol 1999; 73: 1956-63.
49. Strack PR, Frey MW, Rizzo CJ, Cordova B, George HJ, Meade R, et al. Apoptosis mediated by HIV protease is preceded by cleavage of Bcl-2. Proc Natl Acad Sci USA 1996; 93: 9571-6.
50. Nie Z, Bren GD, Vlahakis SR, Schimnich AA, Brenchley JM, Trushin SA, et al. HIV-1 protease cleaves procaspase 8 in vivo. J. Virol 2007; 81: 6947-56.
51. Gibellini D, Re MC, Ponti C, Vitone F, Bon I, Fabbri G, et al. HIV-1 Tat protein concomitantly down-regulates apical caspase-10 and up-regulates c-FLLP in lymphoid T cells: A potential molecular mechanism to escape TRAIL cytotoxicity. J Cell Physiol 2005; 203: 547-56.
52. Collins KL, Chen BK, Kalams SA, Walker BD, Baltimore D. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 1998; 391: 397-401.
53. Cefai D, Ferrer M, Serpente N, Idziorek T, Dautry-Varsat A, Debre P, et al. Internalization of HIV glycoprotein gp120 is associated with down-modulation of membrane CD4 and p561ck together with impairment of T cell activation. J Immunol 1992; 149: 285-94.
54. Willey RL, Maldarelli F, Martin MA, Strebel K. Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J Virol 1992; 66: 7193-200.
55. Inoue M, Koga Y, Djordjijevic D, Fukuma T, Reddy EP, Yokoyama MM, et al. Down-regulation of CD4 molecules by the expression of Nef: A quantitative analysis of CD4 antigens on the cell surfaces. Int Immunol 1993; 5: 1067-73.
56. Lindwasser OW, Chaudhuri R, Bonifacino JS. Mechanisms of CD4 downregulation by the Nef and Vpu proteins of primate immunodeficiency viruses. Curr Mol Med 2007; 7: 171-84.
57. Vaux DL, Strasser A. The molecular biology of apoptosis. Proc Natl Acad Sci USA 1996; 93: 2239-44.
58. Villa P, Kaufmann SH, Earnshaw WC. Caspases and caspase inhibitors. Trends Biochem Sci 1997; 22: 388-93
59. Broker LE, Kruyt FA, Giaccone G. Cell death independent of caspases: A review. Clin Cancer Res 2005; 11: 3155-62.
60. Barbieri D, Troiano L, Grassilli E, Agnesini C, Cristofalo EA, Monti D, et al. Inhibition of apoptosis by zinc: A reappraisal. Biochem Biophys Res Commun 1992; 187: 1256-61.
61. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005; 434: 1093-7.
62. Mattapallil JJ, Letvin NL, Roederer M. T-cell dynamics during acute SIV infection. AIDS 2004; 18: 13-23.
63. Miller CJ, Li Q, Abel K, Kim EY, Ma ZM, Wietgrefe S, et al. Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J Virol 2005; 79: 9217-27.
64. Wang X, Rasmussen T, Pahar B. Poonia B, Alvarez X, Lackner AA, et al. Massive infection and loss of CD4+ T cells occurs in the intestinal tract of neonatal rhesus macaques in acute SIV infection. Blood 2007; 109: 1174-81.
65. Bosinger SE, Hosiawa KA, Cameron MJ, Persad D, Ran L, Xu L, et al. Gene expression profiling of host response in models of acute HIV infection. J Immunol 2004; 173: 6858-63.
66. Cossarizza A. T-cell repertoire and HIV infection: Facts and perspectives (Editorial Review). AIDS 1997; 11: 1075-88.
67. Cossarizza A, Mussini C, Mongiardo N, Borghi V, Sabbatini A, De Rienzo B, et al. Mitochondria alterations and dramatic tendency to undergo apoptosis in peripheral blood lymphocytes during acute HIV syndrome. AIDS 1997; 11: 19-26.
68. Cossarizza A, Mussini C, Borghi V, Mongiardo N, Nuzzo C, Pedrazzi J, et al. Apoptotic features of peripheral blood granulocytes and monocytes during primary, acute HIV infection. Exp Cell Res 1999; 247: 304-11.
69. Cossarizza A, Stent G, Mussini C, Paganelli R, Borghi V, Nuzzo C, et al. Deregulation of the CD95/CD95L system in lymphocytes from patients with primary acute HIV infection. AIDS 2000; 14: 345-55.
70. Ahr B, Robert-Hebmann V, Devaux C, Biard-Piechaczyk M. Apoptosis of uninfected cells induced by HIV envelope glycoproteins. Retrovirology 2004; 1: 12.
71. Holm GH, Zhang C, Gorry PR, Peden K, Schols D, De Clercq E, et al. Apoptosis of bystander T cells induced by human immunodeficiency virus type 1 with increased envelope/receptor affinity and coreceptor binding site exposure. J Virol 2004; 78: 4541-51.
72. Holm GH, Gabuzda D. Distinct mechanisms of CD4+ and CD8+ T-cell activation and bystander apoptosis induced by human immunodeficiency virus type 1 virions. J Virol 2005; 79: 6299-311.
73. Moon HS, Yang JS. Role of HIV Vpr as a regulator of apoptosis and an effector on bystander cells. Mol Cells 2006; 21: 7-20
74. Badley 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.
75. Badley AD, Dockrell D, Simpson M, Schut R, Lynch DH, Leibson P, et al. Macrophage-dependent apoptosis of CD4+ T lymphocytes from HIV-infected individuals is mediated by FasL and tumor necrosis factor. J Exp Med 1997; 185: 55-64.
76. Clerici M. Sarin A, Coffman RE, Wynn TA, Blatt SP, Hendrix CW, et al., Type 1/type 2 cytokine modulation of T-cell programmed cell death as a model for human immunodeficiency virus pathogenesis. Proc Natl Acad Sci USA 1994; 91: 11811-5.
77. Ledru E, Fevrier M, Lecoeur H, Garcia S, Boullier S, Gougeon ML. A nonsecreted variant of interleukin-4 is associated with apoptosis: implication for the T helper-2 polarization in HIV infection. Blood 2003; 101: 3102-5.
78. Schnittman SM, Denning SM, Greenhouse JJ, Justement JS, Baseler M, Kurtzberg J, et al. Evidence for susceptibility of intrathymic T-cell precursors and their progeny carrying T-cell antigen receptor phenotypes TCR alpha beta + and TCR gamma delta + to human immunodeficiency virus infection: A mechanism for CD4+ (T4) lymphocyte depletion. Proc Natl Acad Sci USA 1990; 87: 7727-31.
79. McCune JM. Thymic function in HIV-1 disease. Semin Immunol 1997; 9: 397-404.
80. Haynes BF, Markert ML, Sempowski GD, Patel DD, Hale LP. The role of the thymus in immune reconstitution in aging, bone marrow transplantation, and HIV-1 infection. Annu Rev Immunol 2000; 18: 529-60.
81. McCune JM, Loftus R, Schmidt DK, Carroll P, Webster D, Swor-Yim LB, et al. High prevalence of thymic tissue in adults with human immunodeficiency virus-1 infection. J Clin Invest 1998; 101: 2301-8
82. Viganò A, Vella S, Principi N, Bricalli D, Sala N, Salvaggio A, et al. Thymus volume correlates with the progression of vertical HIV infection. AIDS 1999; 13: F29-34.
83. Viganò A, Vella S, Saresella M, Vanzulli A, Bricalli D, Di Fabio S, et al. Early immune reconstitution after potent antiretroviral therapy in HIV-infected children correlates with the increase in thymus volume. AIDS 2000; 14: 251-61.
84. Stoddart CA, Liegler TJ, Mammano F, Linquist-Stepps VD, Hayden MS, Deeks SG, et al. Impaired replication of protease inhibitor-resistant HIV-1 in human thymus. Nat Med 2001; 7: 712-8.
85. Franceschi C, Franceschini MG, Boschini A, Trenti T, Nuzzo C, Castellani G, et al. Phenotypic characteristics and tendency to apoptosis of peripheral blood mononuclear cells from HIV+ long term non progressors. Cell Death Differ 1997; 4: 815-23.
86. Liegler TJ, Yonemoto W, Elbeik T, Vittinghoff E, Buchbinder SP, Greene WC. Diminished spontaneous apoptosis in lymphocytes from human immunodeficiency virus-infected long-term nonprogressors. J Infect Dis 1998; 178: 669-79.
87. Gougeon ML, Lecoeur H, Sasaki Y. Apoptosis and the CD95 system in HIV disease: Impact of highly active anti-retroviral therapy (HAART). Immunol Lett 1999; 66): 97-103.
88. Roger PM, Breittmayer JP, Arlotto C, Pugliese P, Pradier C, Bernard-Pomier G, et al. Highly active anti-retroviral therapy (HAART) is associated with a lower level of CD4+ T cell apoptosis in HIV-infected patients. Clin Exp Immunol 1999; 118: 412-6.
89. Caggiari L, Zanussi S, Bortolin MT, D'andrea M, Nasti G, Simonelli C, et al. Effects of therapy with highly active anti-retroviral therapy (HAART) and IL-2 on CD4+ and CD8+ lymphocyte apoptosis in HIV+ patients. Clin Exp Immumol 2000; 120: 101-6.
90. Grelli S, Campagna S, Lichtner M, Ricci G. Vella S, Vullo V, et al. Spontaneous and anti-Fas-induced apoptosis in lymphocytes from HIV-infected patients undergoing highly active anti-retroviral therapy. AIDS 2000; 14: 939-49.
91. Cossarizza A, Pinti M, Moretti L, Bricalli D, Bianchi R, Troiano L, et al. Mitochondrial functionality and mitochondrial DNA content in lymphocytes of vertically infected human immunodeficiency virus-positive children with highly active antiretroviral therapy-related lipodystrophy. J Infect Dis 2002; 185: 299-305.
92. Gozuacik D, Kimchi A. Autophagy and cell death. Curr Top Dev Biol 2007; 78: 217-45.
93. Jin S, DiPaola RS, Mathew R, White E. Metabolic catastrophe as a means to cancer cell death. J Cell Sci 2007; 120 (3): 379-83.
94. Espert L, Denizot M, Grimaldi M, Robert-Hebmann V, Gay B, Varbanov M, et al. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 2006; 116: 2161-72.
95. Espert L, Denizot M, Grimaldi M, Robert-Hebmann V, Gay B, Varbanov M, et al. Autophagy and CD4+ T lymphocyte destruction by HIV-1. Autophagy 2007; 3: 32-4.
96. Richter C, Schweizer M, Cossarizza A, Franceschi C. Control of apoptosis by the cellular ATP level. FEBS Lett 1996; 378: 107-10.
97. Eguchi Y, Shimizu S, Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 1997; 57: 1835-40.
98. Vercammen D, Brouckaert G, Denecker G, Van de Craen M, Declercq W, Fiers W, et al. Dual signaling of the Fas receptor: Initiation of both apoptotic and necrotic cell death pathways. J Exp Med 1998; 188: 919-30.
99. McConkey DJ. Biochemical determinants of apoptosis and necrosis. Toxicol Lett 1998; 99: 157-68.
100. Fulda S, Debatin KM. Exploiting death receptor signaling pathways for tumor therapy. Biochim Biophys Acta 2004; 1705: 27-41.
101. Schreck R, Rieber P, Baeuerle PA. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 1991; 10: 2247-58.
102. Papp B, Zhang D, Groopman JE, Byrn RA. Stimulation of human immunodeficiency virus type 1 expression by ceramide. AIDS Res Hum Retroviruses 1994; 10: 775-80.
103. Schwarz KB. Oxidative stress during viral infection: A review. Free Radic Biol Med 1996; 21: 641-9
104. Richard A, Robichaud G, Lapointe R, Bourgoin S, Darveau A, Poulin L. Interference of HIV-1 Nef in the sphingomyelin transduction pathway activated by tumour necrosis factor-alpha in human glial cells. AIDS 1997; 11: F1-7.
105. Hersey P, Zhang XD. Overcoming resistance of cancer cells to apoptosis. J Cell Physiol 2003; 196: 9-18.
106. Bofill M, Gombert W, Borthwick NJ, Akbar AN, McLaughlin JE, Lee CA, et al. Presence of CD3+CD8+Bcl-2(low) lymphocytes undergoing apoptosis and activated macrophages in lymph nodes of HIV-1+ patients. Am J Pathol 1995; 146: 1542-55.
107. Strack PR, Frey MW, Rizzo CJ, Cordova B, George HJ, Meade R, et al. Apoptosis mediated by HIV protease is preceded by cleavage of Bcl-2. Proc Natl Acad Sci USA 1996; 93: 9571-6.
108. Korant BD, Strack PR, Frey MW, Rizzo CJ. A cellular anti-apoptosis protein is cleaved by the HIV-1 protease. Adv Exp Med Biol 1998; 436: 27-9.
109. Shoeman RL, Honer B, Stoller TJ, Kesselmeier C, Miedel MC, Traub P, et al. Human immunodeficiency virus type 1 protease cleaves the intermediate filament proteins vimentin, desmin, and glial fibrillary acidic protein. Proc Natl Acad Sci USA 1990; 87: 6336-40.
110. Tomasselli AG, Hui JO, Adams L, Chosay J, Lowery D, Greenberg B, et al. Actin, troponin C, alzheimer amyloid precursor protein and pro-interleukin 1-beta as substrates of the protease from human immunodeficiency virus. J Biol Chem 1991; 266: 14548-53.
111. Adams LD, Tomasselli AG, Robbins P, Moss B, Heinrikson RL. HIV-1 protease cleaves actin during acute infection of human T-lymphocytes. AIDS Res Hum Retroviruses 1992; 8: 291-5.
112. Shoeman RL, Sachse C, Honer B, Mothes E, Kaufmann M, Traub P. Cleavage of human and mouse cytoskeletal and sarcomeric proteins by human immunodeficiency virus type 1 protease. Actin, desmin, myosin, and tropomyosin. Am J Pathol 1993; 142: 221-30.
113. Ventoso I, Blanco R, Perales C, Carrasco L. HIV-1 protease cleaves eukaryotic initiation factor 4G and inhibits cap-dependent translation. Proc Natl Acad Sci USA 2001; 98: 12966-71.
114. Perales C, Carrasco L, Ventoso I. Cleavage of eIF4G by HIV-1 protease: effects on translation. FEBS Lett 2003; 533: 89-94.
115. Nie Z, Phenix BN, Lum J, Alam A, Lynch DH, Beckett B, et al. HIV-1 protease processes procaspase 8 to cause mitochondrial release of chtychrome c, caspase cleavage and nuclear fragmentation. Cell Death Differ 2002; 9: 1172-84.
116. Staszewski S, Morales-Ramirez J, Tashima KT, Rachlis A, Skiest D, Stanford J, et al. Study 006 Team. Efavirenz plus zidovudine and lamivudine, efavirenz plus indinavir, and indinavir plus zidovudine and lamivudine in the treatment of HIV-1 infection in adults. N Engl J Med 1999; 341: 1865-73.
117. Kravcik S, Magill A, Sanghvi B, Ogden R, Cameron DW, Lewis R, et al. Comparative CD4 T cell responses of protease inhibitor containing and sparing antiretroviral regimens. HIV Clin Trials 2001; 2: 160-70
118. Meroni L, Varchetta S, Manganaro D, Gatti N, Riva A, Mondorte A, et al. Reduced levels of CD4 cell spontaneous apoptosis in human immundeficiency virus-infected patients with discordant response to protease inhibitors. J Infect Dis 2002; 186: 143-4.
119. Vlahakis SR, Bennett SA, Whitehead SN, Badley AD. HIV protease inhibitors modulate apoptosis signaling in vitro and in vivo. Apoptosis 2007; 12: 969-77.
120. Carr A, Emery $, Kelleher A, Law M, Cooper DA. CD8+ lymphocyte responses to antiretroviral therapy of HIV infection. J Acq Immun Def Synd 1996; 13: 320-6.
121. Badley AD. In vitro and in vivo effects of HIV protease inhibitors on apoptosis. Cell Death Differ 2005; 12(Suppl 1): 924-31.
122. Fry TJ, Connick E, Falloon J, Lederman MM, Liewehr DJ, Spritzler J, et al. A potential role for interleukin-7 in T-cell homeostasis. Blood 2001; 97: 2983-90.
123. Bolotin E, Annett G, Parkman R, Weinberg K. Serum levels of IL-7 in bone marrow transplant recipients: Relationship to clinical characteristics and lymphocyte count. Bone Marrow Transplant 1999; 23: 783-8.
124. Nemes E, Lugli E, Nasi M, Ferraresi R, Pinti M, Bugarini R, et al. Immunophenotype of HIV+ patients during CD4 cell-monitored treatment interruption: Role of the IL-7/IL-7 receptor system. AIDS 2006; 20: 2021-32.
125. Wang FX, Xu Y, Sullivan J, Souder E, Argyris EG, Acheampong EA, et al. IL-7 is a potent and proviral strain-specific inducer of latent HIV-1 cellular reservoirs of infected individuals on virally suppressive HAART. J Clin Invest 2005; 115: 128-37.
126. Nunnari G, Xu Y, Acheampong EA, Fang J, Daniel R, Zhang C, et al. Exogenous IL-7 induces Fas-mediated human neuronal apoptosis: Potential effects during human immunodeficiency virus type 1 infection. J Neurovirol 2005; 11: 319-28.
127. Surh CD, Sprent J. Regulation of mature T cell homeostasis. Semin Immunol 2005; 17: 183-91.
128. Jameson SC. Maintaining the norm: T-cell homeostasis. Nat Rev Immunol 2002; 2: 547-56
129. Waldmann TA. IL-15 in the life and death of lymphocytes: immunotherapeutic implications. Trends Mol Med 2003; 9: 517-21.
130. Alpdogan O, van den Brink MR. IL-7 and IL-15: Therapeutic cytokines for immunodeficiency. Trends Immunol 2005; 26: 56-64.
131. Ahmad A, Ahmad R, Iannello A, Toma E, Morisset R, Sindhu ST. IL-15 and HIV infection: Lessons for immunotherapy and vaccination. Curr HIV Res 2005; 3: 261-70.
132. Petrovas C, Mueller YM, Dimitriou ID, Bojczuk PM, Mounzer KC, Witek J, et al. HIV-specific CD8+ T cells exhibit markedly reduced levels of Bcl-2 and Bcl-xL. J Immunol 2004; 172: 4444-53.
133. Arnoult D, Petit F, Lelievre JD, Lecossier D, Hance A, Monceaux V, 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: 1240-52.
134. Kaslow RA, Dorak T, Tang JJ. Influence of host genetic variation on susceptibility to HIV type 1 infection. J Infect Dis 2005; 191 Suppl 1: S68-77.
135. Haas DW. Human genetic variability and HIV treatment response. Curr HIV/ AIDS Rep 2006; 3: 53-8.
136. Khoo SH, Pepper L, Snowden N, Hajeer Ali, Vallely P, Wilkins EG, et al. Tumour necrosis factor c2 microsatellite allele is associated with the rate of HIV disease progression. AIDS 1997; 11: 423-8.
137. Brinkman BM, Keet IP, Miedema F, Verweij CL, Klein MR. Polymorphisms within the human tamor necrosis factor-alpha. promoter region in human immunodeficiency virus type 1-seropositive persons. J Infect Dis 1997; 175: 188-90.
138. Fellay J, Marzolini C, Meaden EF, Back DJ, Buclin T, Chave JP, et al. Swiss HIV Cohort Study. Response to antiretroviral treatment in HIV-1-infected individuals with allelic variants of the multidrug resistance transporter 1: A pharmacogenetics study. Lancet 2002; 359: 30-6.
139. Brumme ZL, Dong WW, Chan KJ, Hogg RS, Montaner JS, O'Shaughnessy MV, et al. Influence of polymorphisms within the CX3CR1 and MDR-1 genes on initial antiretroviral therapy response. AIDS 2003; 17: 201-8
140. Nasi M, Borghi V, Pinti M, Beliodi C, Lugli F, Maffei S, et al. MDR1 C3435T genetic polymorphism does not influence the response to antiretroviral therapy in drug-naive HIV-positive patients. AIDS 2003; 17: 1696-8.
141. Nasi M, Pinti M, Bugarini R, Troiano L, Lugli F, Bellodi C, et al. Genetic polymorphisms of Fas (CD95) and Fas ligand (CD178) influence the rise in CD4+ T cell count after antiretroviral therapy in drug-naive HIV-positive patients. immunogenetics 2005; 57: 628-35.
142. Haas DW, Geraghty DE, Andersen J, Mar J, Motsinger AA, D'Aquila RT, et al. AIDS Clinical Trials Group. Immunogenetics of CD4 lymphocyte count recovery during antiretroviral therapy: An AIDS Clinical Trials Group study. J Infect Dis 2006; 194: 1098-107.
143. Pohlmann S, Reeves JD. Cellular entry of HIV: Evaluation of therapeutic targets. Curr Pharm Des 2006; 12(16)7 1963-73.
144. Rumbaugh JA, Nath A. Developments in HIV neuropathogenesis. Curr Pharm Des 2006; 12(9): 1023-44.
145. Smith MB, Smith RH Jr, Jorgensen WL. Assault on resistance: The use of computational chemistry in the development of anti-HIV drugs. Curr Pharm Des 2006; 12(15): 1843-56.