The density of coreceptors at the surface of CD4+ T cells contributes to the extent of human immunodeficiency virus type 1 viral replication-mediated T cell death

AIDS Research and Human Retroviruses

Volumn 20, Issue 11, 2004, Pages 1230-1243

  Lelièvre, Jean Daniel ^a   Petit, Frédéric ^b   Perrin, Luc ^c   Mammano, Fabrizio ^d   Arnoult, Damien ^e   Ameisen, Jean Claude ^a   Corbeil, Jacques ^f   Gervaix, Alain ^c   Estaquier, Jérome ^b  

^a INSERM   (France)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d BICHAT HOSPITAL   (France)

^e NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR; ZIDOVUDINE;

ARTICLE; CELL DEATH; CELL DENSITY; CELL SURFACE; CONTROLLED STUDY; DISEASE COURSE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; SURFACE PROPERTY; T LYMPHOCYTE; VIRUS REPLICATION;

EID: 9344227326     PISSN: 08892229     EISSN: None     Source Type: Journal    
DOI: 10.1089/0889222042545045     Document Type: Article

References (81)

1. Mellors JW, Rinaldo CR Jr, Gupta P, White RM, Todd JA, and Kingsley LA: Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 1996;272:1167-1170.
2. O'Brien WA, Hartigan PM, Martin D, Esinhart J, Hill A, Benoit S, et al.: Changes in plasma HIV-1 RNA and CD4+ lymphocyte counts and the risk of progression to AIDS. Veterans Affairs Cooperative Study Group on AIDS. N Engl J Med 1996;334:426-431.
3. Gandhi RT, Chen BK, Straus SE, Dale JK, Lenardo MJ, and Baltimore D: HIV-1 directly kills CD4+ T cells by a Fas-independent mechanism. J Exp Med 1998;187:1113-1122.
4. Laurent-Crawford AG, Krust B, Muller S, Riviere Y, Rey-Cuille MA, Bechet JM, et al.: The cytopathic effect of HIV is associated with apoptosis. Virology 1991;185:829-839.
5. Glynn JM, McElligott DL, and Mosier DE: Apoptosis induced by HIV infection in H9 T cells is blocked by ICE- family protease inhibition but not by a Fas(CD95) antagonist. J Immunol 1996;157: 2754-2758.
6. Moutouh L, Estaquier J, Richman DD, and Corbeil J: Molecular and cellular analysis of human immunodeficiency virus-induced apoptosis in lymphoblastoid T-cell-line-expressing wild-type and mutated CD4 receptors. J Virol 1998;72:8061-8072.
7. Terai C, Kornbluth RS, Pauza CD, Richman DD, and Carson DA: Apoptosis as a mechanism of cell death in cultured T lymphoblasts acutely infected with HIV-I. J Clin Invest 1991;87:1710-1715.
8. Petit F, Arnoult D, Lelievre JD, Parseval LM, Hance AJ, Schneider P, et al.: Productive HIV-1 infection of primary CD4+ T cells induces mitochondrial membrane permeabilization leading to a caspase-independent cell death. J Biol Chem 2002;277: 1477-1487.
9. Lifson A, Buchbinder S, Sheppard H, Mawle A, Wilber J, Stanley M, et al.: Long-term human immunodeficiency virus infection in asymptomatic homosexual and bisexual men with normal CD4+ lymphocyte counts: Immunologic and virologic characteristics. J Infect Dis 1991;163:959-965.
10. Pantaleo G, Menzo S, Vaccarezza M, Graziosi C, Cohen O, Demarest J, et al.: Studies in subjects with long-term nonprogressive human immunodeficiency virus infection. N Engl J Med 1995; 332:209-216.
11. Piatak M Jr, Saag MS, Yang LC, Clark SJ, Kappes JC, Luk KC, et al.: High levels of HIV-1 in plasma during all stages of infection determined by competitive PCR. Science 1993;259:1749-1754.
12. + T-lymphocyte decline and clinical progression in human immunodeficiency virus type 1-infected individuals. J Virol 1993;67:1772-1777.
13. Fouchier RA, Meyaard L, Brouwer M, Hovenkamp E, and Schuitemaker H: Broader tropism and higher cytopathicity for CD4+ T cells of a syncytium-inducing compared to a non-syncytium-inducing HIV-1 isolate as a mechanism for accelerated CD4+ T cell decline in vivo. Virology 1996;219:87-95.
14. Koot M, Keet IP, Vos AH, de Goede RE, Roos MT, Coutinho RA, et al.: Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS. Ann Intern Med 1993;118:681-688.
15. Koot M, van 't Wout AB, Kootstra NA, de Goede RE, Tersmette M, and Schuitemaker H: Relation between changes in cellular load, evolution of viral phenotype, and the clonal composition of virus populations in the course of human immunodeficiency virus type 1 infection. J Infect Dis 1996;173:349-354.
16. Richman DD and Bozzette SA: The impact of the syncytium-inducing phenotype of human immunodeficiency virus on disease progression. J Infect Dis 1994;169:968-974.
17. Tersmette M, Lange JM, de Goede RE, de Wolf F, Eeftink-Schattenkerk JK, Schellekens PT, et al.: Association between biological properties of human immunodeficiency virus variants and risk for AIDS and AIDS mortality. Lancet 1989;1:983-985.
18. Berger EA: HIV entry and tropism: The chemokine receptor connection. AIDS 1997;11:S3-16.
19. Berkowitz RD, Alexander S, Bare C, Linquist-Stepps V, Bogan M, Moreno ME, et al.: CCR5- and CXCR4-utilizing strains of human immunodeficiency virus type 1 exhibit differential tropism and pathogenesis in vivo. J Virol 1998;72:10108-10117.
20. Grivel JC and Margolis LB: CCR5- and CXCR4-tropic HIV-1 are equally cytopathic for their T-cell targets in human lymphoid tissue. Nat Med 1999;5:344-346.
21. Penn ML, Grivel JC, Schramm B, Goldsmith MA, and Margolis L: CXCR4 utilization is sufficient to trigger CD4+ T cell depletion in HIV-1-infected human lymphoid tissue. Proc Natl Acad Sci USA 1999;96:663-668.
22. Kreisberg JF, Kwa D, Schramm B, Trautner V, Connor R, Schuitemaker H, et al.: Cytopathicity of human immunodeficiency virus type 1 primary isolates depends on coreceptor usage and not patient disease status. J Virol 2001;75:8842-8847.
23. Malkevich N, Womack C, Pandya P, Grivel JC, Fauci AS, and Margolis L: Human immunodeficiency virus type 1 (HIV-1) non-B subtypes are similar to HIV-1 subtype B in that coreceptor specificity is a determinant of cytopathicity in human lymphoid tissue infected ex vivo. J Virol 2001;75:10520-10522.
24. Kwa D, Vingerhoed J, Boeser-Nunnink B, Broersen S, and Schuitemaker H: Cytopathic effects of non-syncytium-inducing and syncytium-inducing human immunodeficiency virus type 1 variants on different CD4(+)-T-cell subsets are determined only by coreceptor expression. J Virol 2001;75:10455-10459.
25. Kaneshima H, Su L, Bonyhadi ML, Connor RI, Ho DD, and McCune JM: Rapid-high, syncytium-inducing isolates of human immunodeficiency virus type 1 induce cytopathicity in the human thymus of the SCID-hu mouse. J Virol 1994;68:8188-8192.
26. Camerini D, Su HP, Gamez-Torre G, Johnson ML, Zack JA, and Chen IS: Human immunodeficiency virus type 1 pathogenesis in SCID-hu mice correlates with syncytium-inducing phenotype and viral replication. J Virol 2000;74:3196-3204.
27. Mosier DE, Gulizia RJ, MacIsaac PD, Torbett BE, and Levy JA: Rapid loss of CD4+ T cells in human-PBL-SCID mice by non-cytopathic HIV isolates. Science 1993;260:689-692.
28. Huang Y, Paxton W, Wolinsky S, Neumann A, Zhang L, He T, et al.: The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat Med 1996;2:1240-1243.
29. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, et al.: Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 1996;382:722-725.
30. Zimmerman P, Buckler-White A, Alkhatib G, Spalding T, Kubofcik J, Combadiere C, et al.: Inherited resistance to HIV-1 conferred by an inactivating mutation in CC chemokine receptor 5: Studies in populations with contrasting clinical phenotypes, defined racial background, and quantified risk. Mol Med 1997;3:23-36.
31. Edelstein R, Arcuino L, Hughes J, Melvin A, Mohan K, King P, et al.: Risk of mother-to-infant transmission of HIV-1 is not reduced in CCR5/delta32ccr5 heterozygotes. J Acquir Immune Defic Syndr Hum Retrovirol 1997;16:243-246.
32. Hoffman T, MacGregor R, Burger H, Mick R, Doms R, and Collman R: CCR5 genotypes in sexually active couples discordant for human immunodeficiency virus type 1 infection status. J Infect Dis 1997;176:1093-1096.
33. Smith M, Dean M, Carrington M, Winkler C, Huttley G, Lomb D, et al.: Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC), ALIVE Study. Science 1997;277: 959-965.
34. Wu L, Paxton W, Kassam N, Ruffing N, Rottman J, Sullivan N, et al.: CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J Exp Med 1997; 185:1681-1691.
35. Kostrikis L, Huang Y, Moore J, Wolinsky S, Zhang L, Guo Y, et al.: A chemokine receptor CCR2 allele delays HIV-1 disease progression and is associated with a CCR5 promoter mutation. Nat Med 1998;4:350-353.
36. Gervaix A, Nicolas J, Portales P, Posfay-Barbe K, Wyler CA, Segondy M, et al.: Response to treatment and disease progression linked to CD4+ T cell surface CC chemokine receptor 5 density in human immunodeficiency virus type 1 vertical infection. J Infect Dis 2002;185:1055-1061.
37. Reynes J, Portales P, Segondy M, Baillat V, Andre P, Reant B, et al.: CD4+ T cell surface CCR5 density as a determining factor of virus load in persons infected with human immunodeficiency virus type 1. J Infect Dis 2000;181:927-932.
38. Paxton W, Liu R, Kang S, Wu L, Gingeras T, Landau N, et al.: Reduced HIV-1 infectability of CD4+ lymphocytes from exposed-uninfected individuals: Association with low expression of CCR5 and high production of beta-chemokines. Virology 1998;244: 66-73.
39. Lin YL, Mettling C, Portales P, Reynes J, Clot J, and Corbeau P: Cell surface CCR5 density determines the postentry efficiency of R5 HIV-1 infection. Proc Natl Acad Sci USA 2002;99:15590-15595.
40. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, and Kabat D: Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 1998;72:2855-2864.
41. Kuhmann SE, Platt EJ, Kozak SL, and Kabat D: Cooperation of multiple CCR5 coreceptors is required for infections by human immunodeficiency virus type 1. J Virol 2000;74:7005-7015.
42. Gervaix A, West D, Leoni LM, Richman DD, Wong-Staal F, and Corbeil J: A new reporter cell line to monitor HIV infection and drug susceptibility in vitro. Proc Natl Acad Sci USA 1997;94: 4653-4658.
43. Morgenstern J and Land H: Advanced mammalian gene transfer: High titer retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acid Res 1990;18:3587-3596.
44. Deng H, Liu R, Elimeier W, Choe S, Unumatz D, Burkhart M, Di Marzio P, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, and Landau NR: Identification of a major co-receptor for primary isolates of HIV-1. Nature 1996;381: 661-666.
45. Estaquier J, Monceaux V, Cumont MC, Aubertin AM, Hurtrel B, and Ameisen JC: Early changes in peripheral blood T cells during primary infection of rhesus macaques with a pathogenic SIV. J Med Primatol 2000;29:127-135.
46. Estaquier J, Idziorek T, de Bels F, Barre-Sinoussi F, Hurtrel B, Aubertin AM, et al.: Programmed cell death and AIDS: Significance of T-cell apoptosis in pathogenic and nonpathogenic primate lentiviral infections. Proc Natl Acad Sci USA 1994;91: 9431-9435.
47. Estaquier J, Idziorek T, Zou W, Emilie D, Farber CM, Bourez JM, et al.: T helper type 1/T helper type 2 cytokines and T cell death: Preventive effect of interleukin 12 on activation-induced and CD95 (FAS/APO-1)-mediated apoptosis of CD4+ T cells from human immunodeficiency virus-infected persons. J Exp Med 1995;182: 1759-1767.
48. Estaquier J, Tanaka M, Suda T, Nagata S, Golstein P, and Ameisen JC: Fas-mediated apoptosis of CD4+ and CD8+ T cells from human immunodeficiency virus-infected persons: Differential in vitro preventive effect of cytokines and protease antagonists. Blood 1996;87:4959-4966.
49. Yerly S, Rutschman OT, Opravil M, Marchal F, Hirschel B, Perrin L, et al.: Cell-associated HIV-RNA in blood as indicator of virus load in lymph nodes. J Infect Dis 1999;180:850-853.
50. Dean M, Carrington M, Winkler C, Huttley GA, Smith MW, Allikmets R, et al.: Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Science 1996;273:1856-1862.
51. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, Horuk R, et al.: Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 1996;86:367-377.
52. Michael NL, Chang G, Louie LG, Mascola JR, Dondero D, Birx DL, et al.: The role of viral phenotype and CCR5 gene defects in HIV-1 transmission and disease progression. Nat Med 1997;3: 338-340.
53. Michael NL, Louie LG, Rohrbaugh AL, Schultz KA, Dayhoff DE, Wang CE, et al.: The role of CCR5 and CCR2 polymorphisms in HIV-1 transmission and disease progression. Nat Med 1997;3: 1160-1162.
54. Mummidi S, Ahuja SS, Gonzalez E, Anderson SA, Santiago EN, Stephan KT, et al.: Genealogy of the CCR5 locus and chemokine system gene variants associated with altered rates of HIV-1 disease progression. Nat Med 1998;4:786-793.
55. de Roda Husman AM, Blaak H, Brouwer M, and Schuitemaker H: CC chemokine receptor 5 cell-surface expression in relation to CC chemokine receptor 5 genotype and the clinical course of HIV-1 infection. J Immunol 1999;163:4597-4603.
56. Martin MP, Dean M, Smith MW, Winkler C, Gerrard B, Michael NL, et al.: Genetic acceleration of AIDS progression by a promoter variant of CCR5. Science 1998;282:1907-1911.
57. McDermott DH, Zimmerman PA, Guignard F, Kleeberger CA, Leitman SF, and Murphy PM: CCR5 promoter polymorphism and HIV-1 disease progression. Multicenter AIDS Cohort Study (MACS). Lancet 1998;352:866-870.
58. Ostrowski MA, Justement SJ, Catanzaro A, Hallahan CA, Ehler LA, Mizell SB, et al.: Expression of chemokine receptors CXCR4 and CCR5 in HIV-1-infected and uninfected individuals. J Immunol 1998;161:3195-3201.
59. Aramori I, Ferguson S, Bieniasz P, Zhang J, Cullen B, and Cullen M: Molecular mechanism of desensitization of the chemokine receptor CCR-5: Receptor signaling and internalization are dissociable from its role as an HIV-1 co-receptor. EMBO J 1997;16: 4606-4616.
60. Pedroza-Martins L, Gurney K, Torbett B, and Uittenbogaart C: Differential tropism and replication kinetics of human immunodeficiency virus type 1 isolates in thymocytes: Coreceptor expression allows viral entry, but productive infection of distinct subsets is determined at the postentry level. J Virol 1998;72:9441-9452.
61. Kinter A, Catanzaro A, Monaco J, Ruiz M, Justement J, Moir S, et al.: CC-chemokines enhance the replication of T-tropic strains of HIV-1 in CD4(+) T cells: Role of signal transduction. Proc Natl Acad Sci USA 1998;95:11880-11885.
62. Reynes J, Portales P, Segondy M, Baillat V, Andre P, Avinens O, et al.: CD4 T cell surface CCR5 density as a host factor in HIV-1 disease progression. AIDS 2001;15:1627-1634.
63. Berndt C, Mopps B, Angermuller S, Gierschik P, and Krammer PH: CXCR4 and CD4 mediate a rapid CD95-independent cell death in CD4(+) T cells. Proc Natl Acad Sci USA 1998;95:12556-12561.
64. Biard-Piechaczyk M, Robert-Hebmann V, Richard V, Roland J, Hipskind RA, and Devaux C: Caspase-dependent apoptosis of cells expressing the chemokine receptor CXCR4 is induced by cell membrane-associated human immunodeficiency virus type 1 envelope glycoprotein (gp120). Virology 2000;268:329-344.
65. Blanco J, Jacotot E, Cabrera C, Cardona A, Clotet B, De Clercq E, et al.: The implication of the chemokine receptor CXCR4 in HIV-1 envelope protein-induced apoptosis is independent of the G protein-mediated signalling. AIDS 1999;13:909-917.
66. Hesselgesser J, Taub D, Baskar P, Greenberg M, Hoxie J, Kolson DL, et al.: Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1 alpha is mediated by the chemokine receptor CXCR4. Curr Biol 1998;8:595-598.
67. Colamussi ML, Secchiero P, Zella D, Curreli S, Mirandola P, Capitani S, et al.: Stromal derived factor-1 alpha induces apoptosis in activated primary CD4+ T cells. AIDS 2000;14:748-750.
68. Sodroski J, Goh WC, Rosen C, Campbell K, and Haseltine WA: Role of the HTLV-III/LAV envelope in syncytium formation and cytopathicity. Nature 1986;322:470-474.
69. Lifson JD, Feinberg MB, Reyes GR, Rabin L, Banapour B, Chakrabarti S, et al.: Induction of CD4-dependent cell fusion by the HTLV-III/LAV envelope glycoprotein. Nature 1986;323:725-728.
70. Laurent-Crawford AG, Krust B, Riviere Y, Desgranges C, Muller S, Kieny MP, et al.: Membrane expression of HIV envelope glycoproteins triggers apoptosis in CD4 cells. AIDS Res Hum Retroviruses 1993;9:761-773.
71. Cao J, Park IW, Cooper A, and Sodroski J: Molecular determinants of acute single-cell lysis by human immunodeficiency virus type 1. J Virol 1996;70:1340-1354.
72. Kowalski M, Bergeron L, Dorfman T, Haseltine W, and Sodroski J: Attenuation of human immunodeficiency virus type 1 cytopathic effect by a mutation affecting the transmembrane envelope glycoprotein. J Virol 1991;65:281-291.
73. LaBonte JA, Patel T, Hofmann W, and Sodroski J: Importance of membrane fusion mediated by human immunodeficiency virus envelope glycoproteins for lysis of primary CD4-positive T cells. J Virol 2000;74:10690-10698.
74. Estaquier J, Lelièvre JD, Petit F, Brunner T, Moutouh-De Parseval L, Richman DD, et al.: Effects of antiretroviral drugs on human immunodeficiency virus type 1-induced CD4(+) T-cell death. J Virol 2002;76:5966-5973.
75. Petit F, Corbeil J, Lelièvre JD, Moutouh-de Parseval L, Pinon G, Green DR, et al.: Role of CD95-activated caspase-1 processing of IL-1beta in TCR-mediated proliferation of HIV-infected CD4(+) T cells. Eur J Immunol 2001;31:3513-3524.
76. Lelièvre J, Mammano F, Arnoult D, Petit F, Grodet A, Estaquier J, et al.: A novel mechanism for HIV1-mediated bystander CD4+ T-cell death: Neighboring dying cells drive the capacity of HIV1 to kill non-cycling primary CD4+ T cells. Cell Death Differ 2002; 11:1017-1027.
77. Veazey RS, Mansfield KG, Tham IC, Carville AC, Shvetz DE, Forand AE, et al.: Dynamics of CCR5 expression by CD4(+) T cells in lymphoid tissues during simian immunodeficiency virus infection. J Virol 2000;74:11001-11007.
78. Harouse JM, Gettie A, Tan RC, Blanchard J, and Cheng-Mayer C: Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. Science 1999;284:816-819.
79. Edinger AL, Amedee A, Miller K, Doranz BJ, Endres M, Sharron M, et al.: Differential utilization of CCR5 by macrophage and T cell tropic simian immunodeficiency virus strains. Proc Natl Acad Sci USA 1997;94:4005-4010.
80. Valdez H, Purvis S, Lederman M, Fillingame M, and Zimmerman P: Association of the CCR5delta32 mutation with improved response to antiretroviral therapy. JAMA 1999;282:734.
81. O'Brien T, McDermott D, Ioannidis J, Carrington M, Murphy P, Havlir D, et al.: Effect of chemokine receptor gene polymorphisms on the response to potent antiretroviral therapy. AIDS 2000;14: 821-826.