Autophagy in HIV-induced T cell death

Current Topics in Microbiology and Immunology

Volumn 335, Issue 1, 2009, Pages 307-321

  Espert, Lucile ^a   Biard Piechaczyk, Martine ^a  

^a University of Montpellier I and II   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 12; INTERLEUKIN 2; NELFINAVIR; NONNUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITOR; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR; VIRUS DNA; VIRUS ENVELOPE PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADAPTIVE IMMUNITY; APOPTOSIS; AUTOPHAGY; CANCER CELL; CD4+ T LYMPHOCYTE; CELL DEATH; CLINICAL TRIAL; DYSLIPIDEMIA; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOPATHOGENESIS; INNATE IMMUNITY; INSULIN RESISTANCE; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; VERTICAL TRANSMISSION; VIREMIA; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS TRANSMISSION; DRUG EFFECT; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS 2; IMMUNOLOGY; METABOLISM; VIROLOGY;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; AUTOPHAGY; CD4-POSITIVE T-LYMPHOCYTES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV PROTEASE INHIBITORS; HIV-1; HIV-2; HOST-PATHOGEN INTERACTIONS; HUMANS;

EID: 75649085337     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-642-00302-8_15     Document Type: Review

References (107)

1. Agrawal L, Lu X, Jin Q, Alkhatib G (2006) Anti-HIV therapy: current and future directions. CurrPharm Des 12:2031-55
2. Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, Murphy PM, Berger EA (1996)CC-CKR5: a RANTES, MIP-1a, MIP-1b receptor as a fusion cofactor for macrophage-tropicHIV-1. Science 272:1955-1958
3. Ameisen JC, Capron A (1991) Cell dysfunction and depletion in AIDS: the programmed celldeath hypotheses. Immunol Today 12:102-105
4. Barré-Sinoussi F, Chermann J-C, Rey F, Nugeyre M-T, Chamaret S, Gruest J, Dauget C, Axler-Blin C, Brun-Vezinet F, Rouzioux C, Rozembaum W, Montagnier L (1983) Isolation of aT-lymphotropic retrovirus from patient at risk for acquired immunodeficiency syndrome(AIDS). Science 220:868-870
5. Ben-Romano R, Rudich A, Tirosh A, Potashnik R, Sasaoka T, Riesenberg K, Schlaeffer F, Bashan N(2004) Nelfinavir-induced insulin resistance is associated with impaired plasma membranerecruitment of the PI 3-kinase effectors Akt/PKB and PKC-zeta. Diabetologia 47:1107-17
6. Blanco J, Barretina J, Ferri KF, Jacotot E, Gutierrez A, Armand-Ugon M, Cabrera C, Kroemer G,Clotet B, Este JA (2003) Cell-surface-expressed HIV-1 envelope induces the death of CD4 Tcells during GP41-mediated hemifusion-like events. Virology 305:318-29
7. Bleul C, Wu LHJA, Springer TA, MacKay CR (1997) The HIV coreceptors CXCR4 and CCR5are differencially expressed and regulated on human T lymphocytes. Proc Natl Acad Sci USA94:1925-1930
8. Bleul CC, Farzan M, Choe H, Parolin C, Clark-Lewis I, Sodroski J, Springer TA (1996) Thelymphocyte chemoattractant SDF-1 is a ligand for LESTRE/fusin and blocks HIV-1 entry. Nature 382:829-833
9. Broker LE, Kruyt FA, Giaccone G (2005) Cell death independent of caspases: a review. ClinCancer Res 11(9):3155-3162
10. Bursch W, Ellinger A, Kienzl H, Torok L, Pandey S, Sikorska M, Walker R, Hermann RS (1996) Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 17(8):1595-1607
11. Butler IF, Pandrea I, Marx PA, Apetrei C (2007) HIV genetic diversity: biological and public health consequences. Curr HIV Res 5(1):23-45
12. Chun TW, Davey RT Jr, Ostrowski M, Shawn Justement J, Engel D, Mullins JI, Fauci AS (2000) Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nat Med 6(7):757-761
13. Chun TW, Finzi D, Margolick J, Chadwick K, Schwartz D, Siliciano RF (1995) In vivo fate of HIV-1-infected T cells: quantitative analysis of the transition to stable latency. Nat Med 1(12):1284-1290
14. Chun TW, Stuyver L, Mizell SB, Ehler LA, Mican JA, Baseler M, Lloyd AL, Nowak MA, Fauci AS (1997) Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci \USA 94(24):13193-13197
15. Davey RT Jr, Bhat N, Yoder C, Chun TW, Metcalf JA, Dewar R, Natarajan V, Lempicki RA, Adelsberger JW, Miller KD, Kovacs JA, Polis MA, Walker RE, Falloon J, Masur H, Gee D, Baseler M, Dimitrov DS, Fauci AS, Lane HC (1999) HIV-1 and T cell dynamics after interruption of highly active antiretroviral therapy (HAART) in patients with a history of sustained viral suppression. Proc Natl Acad Sci USA 96(26):15109-15114
16. Davis CB, Dikic I, Unutmaz D, Hill CM, Arthos J, Siani MA, Thompson DA, Schlessinger J, Littman DR (1997) Signal transduction due to HIV-1 envelope interactions with chemokine receptors CXCR4 or CCR5. J Exp Med 186(10):1793-1798
17. Debnath J, Baehrecke EH, Kroemer G (2005) Does autophagy contribute to cell death? Autophagy 1(2):e10-e18
18. Deeks SG, Walker BD (2004) The immune response to AIDS virus infection: good, bad, or both? J Clin Invest 113(6):808-810
19. Deeks SG, Walker BD (2007) Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 27(3):406-416
20. Delgado M, Singh S, De Haro S, Master S, Ponpuak M, Dinkins C, Ornatowski W, Vergne I, Deretic V (2009) Autophagy and pattern recognition receptors in innate immunity. Immunol Rev 227(1):189-202
21. Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M, Kreymborg K, Altenberend F, Brandenburg J, Kalbacher H, Brock R, Driessen C, Rammensee HG, Stevanovic S (2005) Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci USA 102(22):7922-7927
22. Denizot M, Varbanov M, Espert L, Robert-Hebmann V, Sagnier S, Garcia E, Curriu M, Mamoun R, Blanco J, Biard-Piechaczyk M (2008) HIV-1 gp41 fusogenic function triggers autophagy in uninfected cells. Autophagy 4(8):998-1008
23. Deretic V (2005) Autophagy in innate and adaptive immunity. Trends Immunol 26(10):523-528
24. Djavaheri-Mergny M, Amelotti M, Mathieu J, Besancon F, Bauvy C, Souquere S, Pierron G, Codogno P (2006) NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J Biol Chem 281(41):30373-30382
25. Dunne M (2007) Antiretroviral drug development: the challenge of cost and access. Aids 21(Suppl 4):S73-79
26. Espert L, Codogno P, Biard-Piechaczyk M (2007) Involvement of autophagy in viral infections: antiviral function and subversion by viruses. J Mol Med 85(8):811-823
27. Espert L, Denizot M, Grimaldi M, Robert-Hebmann V, Gay B, Varbanov M, Codogno P, Biard-Piechaczyk M (2006) Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 116(8):2161-2172
28. Fauci AS (1988) The human immunodeficiency virus: infectivity and mechanisms of pathogene-sis. Science 239(4840):617-622
29. Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-877
30. Finkel TH, Tudor-Williams G, Banda NK, Cotton MF, Curiel T, Monks C, Baba TW, Ruprecht RM,Kupfer A (1995) Apoptosis occurs predominantly in bystander cells and not in productivelyinfected cells of HIV-and SIV-infected lymph nodes. Nat Med 1(2):129-134
31. Finzi A, Orthwein A, Mercier J, Cohen EA (2007) Productive human immunodeficiency virustype 1 assembly takes place at the plasma membrane. J Virol 81(14):7476-7490
32. Frankel SS, Wenig BM, Burke AP, Mannan P, Thompson LD, Abbondanzo SL, Nelson AM, Pope M,Steinman RM (1996) Replication of HIV-1 in dendritic cell-derived syncytia at the mucosalsurface of the adenoid. Science 272(5258):115-117
33. Gallo RC, Sarin PS, Gelmann EP, Robert-Guroff M, Richardson E, Kalyanaraman VS, Mann D,Sidhu GD, Stahl RE, Zolla-Pazner S, Leibowitch J, Popovic M (1983) Isolation of humanT-cell leukemia virus in acquired immune deficiency syndrome (AIDS). Science220(4599):865-867
34. Garg H, Blumenthal R (2006) HIV gp41-induced apoptosis is mediated by caspase-3-dependentmitochondrial depolarization, which is inhibited by HIV protease inhibitor nelfinavir. JLeukoc Biol 79(2):351-362
35. Gendelman HE, Orenstein JM, Baca LM, Weiser B, Burger H, Kalter DC, Meltzer MS (1989) Themacrophage in the persistence and pathogenesis of HIV infection. Aids 3(8):475-495
36. Gills JJ, Lopiccolo J, Dennis PA (2008a) Nelfinavir, a new anti-cancer drug with pleiotropiceffects and many paths to autophagy. Autophagy 4(1):107-9
37. Gills JJ, Lopiccolo J, Tsurutani J, Shoemaker RH, Best CJ, Abu-Asab MS, Borojerdi J, Warfel NA,Gardner ER, Danish M, Hollander MC, Kawabata S, Tsokos M, Figg WD, Steeg PS, DennisPA (2007b) Nelfinavir, A lead HIV protease inhibitor, is a broad-spectrum, anticancer agentthat induces endoplasmic reticulum stress, autophagy, and apoptosis in vitro and in vivo. ClinCancer Res 13(17):5183-5194
38. Gkrania-Klotsas E, Klotsas AE (2007) HIV and HIV treatment: effects on fats, glucose and lipids. Br Med Bull 84:49-68
39. Gonzalez-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquere S, Eskelinen EL, Pierron G,Saftig P, Kroemer G (2005) The apoptosis/autophagy paradox: autophagic vacuolizationbefore apoptotic death. J Cell Sci 118(Pt 14):3091-102
40. Goodenow MM, Collman RG (2006) HIV-1 coreceptor preference is distinct from target celltropism: a dual-parameter nomenclature to define viral phenotypes. J Leukoc Biol80(5):965-972
41. Grivel JC, Margolis LB (1999) CCR5-and CXCR4-tropic HIV-1 are equally cytopathic for theirT-cell targets in human lymphoid tissue. Nat Med 5(3):344-346
42. + T-celldepletion in HIV infection: are we closer to understanding the cause? Nat Med 8(4):319-323
43. Hammer SM, Saag MS, Schechter M, Montaner JS, Schooley RT, Jacobsen DM, Thompson MA,Carpenter CC, Fischl MA, Gazzard BG, Gatell JM, Hirsch MS, Katzenstein DA, Richman DD,Vella S, Yeni PG, Volberding PA (2006) Treatment for adult HIV infection: 2006 recommendations of the International AIDS Society\-USA panel. Top HIV Med 14(3):827-843
44. + T lymphocytes is highly cytolytic for both cells. J Virol69(11):6925-6931
45. Hisatomi T, Nakazawa T, Noda K, Almulki L, Miyahara S, Nakao S, Ito Y, She H, Kohno R,Michaud N, Ishibashi T, Hafezi-Moghadam A, Badley AD, Kroemer G, Miller JW (2008) HIVprotease inhibitors provide neuroprotection through inhibition of mitochondrial apoptosis inmice. J Clin Invest 118(6):2025-2038
46. Ho DD, Neumann AU, Perelson AS, Chen W, Leonard JM, Markowitz M (1995) Rapid turnoverof plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373:123-126
47. + T cells and viremia: who's incontrol? Trends Immunol 27(3):119-124
48. Katz RA, Greger JG, Skalka AM (2005) Effects of cell cycle status on early events in retroviralreplication. J Cell Biochem 94(5):880-889
49. Kondo Y, Kanzawa T, Sawaya R, Kondo S (2005) The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 5(9):726-734
50. LaBonte J, Lebbos J, Kirkpatrick P (2003) Enfuvirtide. Nat Rev Drug Discov 2(5):345-346
51. Langford SE, Ananworanich J, Cooper DA (2007) Predictors of disease progression in HIV infection: a review. AIDS Res Ther 4:11
52. Laurent-Crawford AG, Krust B, Riviere Y, Desgranges C, Muller S, Kieny MP, Dauguet C, Hovanessian AG (1993) Membrane expression of HIV envelope glycoproteins triggers apop-tosis in CD4 cells. AIDS Res Hum Retroviruses 9(8):761-773
53. Lee HK, Iwasaki A (2008) Autophagy and antiviral immunity. Curr Opin Immunol 20(1):23-29
54. Lee HK, Lund JM, Ramanathan B, Mizushima N, Iwasaki A (2007) Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315(5817):1398-1401
55. Leligdowicz A, Yindom LM, Onyango C, Sarge-Njie R, Alabi A, Cotten M, Vincent T, da Costa C, Aaby P, Jaye A, Dong T, McMichael A, Whittle H, Rowland-Jones S (2007) Robust Gag-specific T cell responses characterize viremia control in HIV-2 infection. J Clin Invest 117(10):3067-3074
56. Levine B, Deretic V (2007) Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 7(10):767-777
57. Levy JA (1993) Pathogenesis of human immunodeficiency virus infection. Microbiol Rev 57(1):183-289
58. Lifson JD, Feinberg MB, Reyes GR, Rabin L, Banapour B, Chakrabarti S, Moss B, Wong-Staal F, Steimer KS, Engleman EG (1986) Induction of CD4-dependent cell fusion by the HTLV-III/ L AV envelope glycoprotein. Nature 323(6090):725-728
59. Liu R, Paxon WA, Choe S, Ceradini D, Martin SR, Horuk R, MacDonald ME, Stuhlmann H, Koup RA, Landau NR (1996) Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367-377
60. Macias J, Palomares JC, Mira JA, Torres MJ, Garcia-Garcia JA, Rodriquez JM, Vergera S, Pineda JA (2005) Transient rebounds of HIV plasma viremia are associated with the emergence of drug resistance mutations in patients on highly active antiretroviral therapy. J Infect 51(3):195-200
61. Margolis L, Shattock R (2006) Selective transmission of CCR5-utilizing HIV-1: the 'gatekeeper' problem resolved? Nat Rev Microbiol 4(4):312-317
62. McCune JM (2001) The dynamics of CD4+ T-cell depletion in HIV disease. Nature 410(6831):974-979
63. Misse D, Cerutti M, Noraz N, Jourdan P, Favero J, Devauchelle G, Yssel H, Taylor N, Veas F (1999) A CD4-independent interaction of human immunodeficiency virus-1 gp120 with CXCR4 induces their cointernalization, cell signaling, and T-cell chemotaxis. Blood 93(8):2454-2462
64. Molina L, Grimaldi M, Robert-Hebmann V, Espert L, Varbanov M, Devaux C, Granier C, Biard-Piechaczyk M (2007) Proteomic analysis of the cellular responses induced in uninfected immune cells by cell-expressed X4 HIV-1 envelope. Proteomics 7(17):3116-3130
65. Monini P, Sgadari C, Toschi E, Barillari G, Ensoli B (2004) Antitumour effects of antiretroviral therapy. Nat Rev Cancer 4(11):861-875
66. Munoz-Barroso I, Durell S, Sakaguchi K, Appella E, Blumenthal R (1998) Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41. J Cell Biol 140(2):315-323
67. Murphy KM, Sweet MJ, Ross IL, Hume DA (1993) Effects of the tat and nef gene products of human immunodeficiency virus type 1 (HIV-1) on transcription controlled by the HIV-1 long terminal repeat and on cell growth in macrophages. J Virol 67(12):6956-6964
68. Nair D (2005) Antiretroviral therapy-induced hyperlipidaemia. Int J STD AIDS 16(Suppl 1):2-10; discussion 10-13, 41-13
69. Navia BA, Cho ES, Petito CK, Price RW (1986) The AIDS dementia complex: II. Neuropathology. Ann Neurol 19(6):525-535
70. Noursadeghi M, Katz DR, Miller RF (2006) HIV-1 infection of mononuclear phagocytic cells: the case for bacterial innate immune deficiency in AIDS. Lancet Infect Dis 6(12):794-804
71. + T lymphocytes with HIV glycoprotein-expressing cells is mediated by caspases but bypasses CD95 (Fas/Apo-1) and TNF receptor 1. J Immunol 159(11):5246-5252
72. Orvedahl A, Levine B (2008) Eating the enemy within: autophagy in infectious diseases. Cell Death Differ 16(1):57-69
73. Paludan C, Schmid D, Landthaler M, Vockerodt M, Kube D, Tuschl T, Munz C (2005) Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307(5709):593-596
74. Pelchen-Matthews A, Kramer B, Marsh M (2003) Infectious HIV-1 assembles in late endosomes in primary macrophages. J Cell Biol 162(3):443-455
75. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD (1996) HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271(5255):1582-1586
76. Phenix BN, Angel JB, Mandy F, Kravcik S, Parato K, Chambers KA, Gallicano K, Hawley-Foss N, Cassol S, Cameron DW, Badley AD (2000) Decreased HIV-associated T cell apoptosis by HIV protease inhibitors. AIDS Res Hum Retroviruses 16(6):559-567
77. Piguet V, Sattentau Q (2004) Dangerous liaisons at the virological synapse. J Clin Invest 114(5):605-610
78. Popovic M, Sarngadharan MG, Read E, Gallo RC (1984) Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science 224(4648):497-500
79. Pyrko P, Kardosh A, Wang W, Xiong W, Schonthal AH, Chen TC (2007) HIV-1 protease inhibitors nelfinavir and atazanavir induce malignant glioma death by triggering endoplasmic reticu-lum stress. Cancer Res 67(22):10920-10928
80. Raposo G, Moore M, Innes D, Leijendekker R, Leigh-Brown A, Benaroch P, Geuze H (2002) Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic 3(10):718-729
81. Roshal M, Zhu Y, Planelles V (2001) Apoptosis in AIDS. Apoptosis 6(1-2):103-116
82. Rowland-Jones SL, Whittle HC (2007) Out of Africa: what can we learn from HIV-2 about protective immunity to HIV-1? Nat Immunol 8(4):329-331
83. Samara C, Syntichaki P, Tavernarakis N (2007) Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 15(1):105-12
84. Samson M, Libert F, Doran BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C, Muyldermans G, Verhofstede C, Bourtonboy G, Georges M, Imai T, Rana S, Yi Y, Smyth RJ, Collman RG, Doms RW, Vassart G, Parmentier M (1996) Resistance to HIV-1 infection in caucasien individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382:722-725
85. Schmid D, Dengjel J, Schoor O, Stevanovic S, Munz C (2006) Autophagy in innate and adaptive immunity against intracellular pathogens. J Mol Med 84(3):194-202
86. Schmid D, Munz C (2007) Innate and adaptive immunity through autophagy. Immunity 27(1):11-21
87. Schutt M, Zhou J, Meier M, Klein HH (2004) Long-term effects of HIV-1 protease inhibitors on insulin secretion and insulin signaling in INS-1 beta cells. J Endocrinol 183(3):445-454
88. Seay MD, Dinesh-Kumar SP (2007) Autophagy takes its TOLL on innate immunity. Cell Host Microbe 2(2):69-70
89. Sgadari C, Barillari G, Toschi E, Carlei D, Bacigalupo I, Baccarini S, Palladino C, Leone P, Bugarini R, Malavasi L, Cafaro A, Falchi M, Valdembri D, Rezza G, Bussolino F, Monini P, Ensoli B (2002) HIV protease inhibitors are potent anti-angiogenic molecules and promote regression of Kaposi sarcoma. Nat Med 8(3):225-232
90. Sgadari C, Monini P, Barillari G, Ensoli B (2003) Use of HIV protease inhibitors to block Kaposi's sarcoma and tumour growth. Lancet Oncol 4(9):537-547
91. Sodroski J, Goh WC, Rosen C, Campbell K, Haseltine WA (1986) Role of the HTLV-III/LAV envelope in syncytium formation and cytopathicity. Nature 322(6078):470-474
92. Stocker H, Scheller C, Jassoy C (2000) Destruction of primary CD4(+) T cells by cell-cell interaction in human immunodeficiency virus type 1 infection in vitro. J Gen Virol 81(Pt 8):1907-1911
93. Suzuki Y, Craigie R (2007) The road to chromatin\-nuclear entry of retroviruses. Nat Rev Microbiol 5(3):187-196
94. Swanson MS (2006) Autophagy: eating for good health. J Immunol 177(8):4945-4951
95. Terai C, Kornbluth RS, Pauza CD, Richman DD, Carson DA (1991) Apoptosis as a mechanism of cell death in cultured T lymphoblasts acutely infected with HIV-1. J Clin Invest 87:1710-1715
96. Thorburn A (2007) Apoptosis and autophagy: regulatory connections between two supposedly different processes. Apoptosis 13(1):1-9
97. Varbanov M, Espert L, Biard-Piechaczyk M (2006) Mechanisms of CD4 T-cell depletion triggered by HIV-1 viral proteins. AIDS Rev 8(4):221-236
98. Ventoso I, Navarro J, Munoz MA, Carrasco L (2005) Involvement of HIV-1 protease in virus-induced cell killing. Antiviral Res 66(1):47-55
99. Vlahakis SR, Bennett SA, Whitehead SN, Badley AD (2007) HIV protease inhibitors modulate apoptosis signaling in vitro and in vivo. Apoptosis 12(5):969-977
100. Wei X, Ghosh SK, Taylor ME, Johnson VA, Emini EA, Deutsch P, Lifson JD, Bonhoeffer S, Nowak MA, Hahn BH, Saag MS, Shaw GM (1995) Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373:117-122
101. Weissenhorn W, Dessen A, Harrison SC, Skehel JJ, Wiley DC (1997) Atomic structure of the ectodomain from HIV-1 gp41 [see comments]. Nature 387(6631):426-430
102. Weissman D, Rabin RL, Arthos J, Rubbert A, Dybul M, Swofford R, Venkatesan S, Farber JM, Fauci AS (1997) Macrophage-tropic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor. Nature 389(6654):981-985
103. Welsch S, Keppler OT, Habermann A, Allespach I, Krijnse-Locker J, Krausslich HG (2007) HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLoS Pathog 3(3):e36
104. Wild CT, Shugars DC, Greenwell TK, McDanal CB, Matthews TJ (1994) Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc Natl Acad Sci USA 91(21):9770-9774
105. + lymphocytes and cells infected by human immunodeficiency virus. Proc Natl Acad Sci USA 84:1429-1433
106. Zamborlini A, Lehmann-Che J, Clave E, Giron ML, Tobaly-Tapiero J, Roingeard P, Emiliani S, Toubert A, de The H, Saib A (2007) Centrosomal pre-integration latency of HIV-1 in quiescent cells. Retrovirology 4:63
107. Zhou D, Spector SA (2008) Human immunodeficiency virus type-1 infection inhibits autophagy. AIDS 22(6):695-699