Apoptosis of Bystander T Cells Induced by Human Immunodeficiency Virus Type 1 with Increased Envelope/Receptor Affinity and Coreceptor Binding Site Exposure

Journal of Virology

Volumn 78, Issue 9, 2004, Pages 4541-4551

  Holm, Geoffrey H ^a   Zhang, Chengsheng ^a   Gorry, Paul R ^a   Peden, Keith ^b   Schols, Dominique ^c   De Clercq, Erik ^c   Gabuzda, Dana ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^d DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,1' [1,4 PHENYLENEBIS(METHYLENE)]BIS(1,4,8,11 TETRAAZACYCLOTETRADECANE); AMINO ACID; ANTIBODY; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; ENFUVIRTIDE; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; BYSTANDER EFFECT; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOCYTE DEPLETION; MEMBRANE FUSION; MOLECULAR CLONING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BINDING; T LYMPHOCYTE; VIRION; VIRUS CELL INTERACTION; VIRUS STRAIN;

ANIMALS; APOPTOSIS; BYSTANDER EFFECT; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CELL LINE, TRANSFORMED; GENE PRODUCTS, ENV; HERPESVIRUS 2, SAIMIRIINE; HIV-1; HUMANS; RECEPTORS, CCR5; RECEPTORS, CXCR4; VIRION;

EID: 4644277015     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.9.4541-4551.2004     Document Type: Article

References (82)

1. Arthos, J., C. Cicala, S. M. Selig, A. A. A. White, H. M. Ravidranath, D. Van Ryk, T. D. Steenbeke, E. Machado, P. Khazanie, M. S. Hanback, D. B. Hanback, R. L. Rabin, and A. S. Fauci. 2002. The role of the CD4 receptor versus HIV coreceptors in envelope-mediated apoptosis in peripheral blood mononuclear cells. Virology 292:98-106.
2. Arthur, L. O., J. W. Bess, Jr., R. C. Sowder II, R. E. Benveniste, L. E. Henderson, and J. D. Lifson. 1992. Cellular proteins bound to immunodeficiency viruses: implications for pathogenesis and vaccines. Science 258: 1935-1938.
3. + T lymphocytes from HIV-1 infected individuals is mediated by FasL and tumor necrosis factor. J. Exp. Med. 185:55-64.
4. Badley, A. D., D. H. Dockrell, A. Algeciras, S. Ziesmer, A. Landay, M. M. Lederman, E. Connick, H. Kessler, D. Kuritzkes, D. H. Lynch, P. Roche, H. Yagita, and C. V. Paya. 1998. In vivo analysis of Fas/FasL interactions in HIV-1 infected patients. J. Clin. Investig. 102:79-87.
5. Banda, N. K., J. Bernier, D. K. Kurahara, R. Kurrie, N. Haigwood, R. P. Sekaly, and T. H. Finkel. 1992. Crosslinking CD4 by human immunodeficiency virus gpl20 primes T cells for activation-induced apoptosis. J. Exp. Med. 176:1099-1106.
6. Basmaciogullari, S., G. J. Babcock, D. Van Ryk, W. Wojtowicz, and J. Sodroski. 2002. Identification of conserved and variable structures in the human immunodeficiency virus gpl20 glycoprotein of importance for CXCR4 binding. J. Virol. 76:10791-10800.
7. Berger, E. A., P. M. Murphy, and J. M. Farber. 1999. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu. Rev. Immunol. 17:657-700.
8. + T cells. Proc. Natl. Acad. Sci. USA 95:12556-12561.
9. Biard-Piechaczyk, M., V. Robert-Hebmann, V. Richard, J. Roland, R. A. Hipskind, and C. Devaux. 2000. Caspase-dependent apoptosis of cells expressing the chemokine receptor CXCR4 is induced by cell membrane-associated human immunodeficiency virus type 1 envelope glycoprotein (gpl20). Virology 268:329-344.
10. Birsinger, B., I. Muller-Fleckenstein, D. Simmer, G. Lang, S. Wittman, E. Platzer, R. C. Desrosiers, and B. Fleckenstein. 1992. Stable growth transformation of human T lymphocytes by herpesvirus saimiri. Proc. Natl. Acad. Sci. USA 89:3116-3119.
11. Bleul, C. C., L. Wu, J. A. Hoxie, T. A. Springer, and C. R. Mackay. 1997. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl. Acad. Sci. USA 94:1925-1930.
12. +-T-cell depletion in human lymphoid tissue, a major site of replication in vivo. J. Virol. 76:1004-1014.
13. Briant, L., V. Robert-Hebmann, V. Sivan, A. Brunet, J. Pouyssegur, and C. Devaux. 1998. Involvement of extracellular signal-regulated kinase module in HIV-mediated CD4 signals controlling activation of nuclear factor-kB and AP-1 transcription factors. J. Immunol. 160:1875-1885.
14. Cantin, R., J. F. Fortin, G. Lamontagne, and M. Tremblay. 1997. The presence of host-derived HLA-DR1 on human immunodeficiency virus type 1 increases viral infectivity. J. Virol. 71:1922-1930.
15. Cao, J., I. L. Park, A. Cooper, and J. Sodroski. 1996. Molecular determinants of acute single-cell lysis by human immunodeficiency virus type 1. J. Virol. 70:1340-1354.
16. Carbonari, M., A. M. Pesce, M. Cibati, A. Modica, L. Dell'Anna, G. D'Offlizi, A. Angelici, S. Uccini, A. Modesti, and M. Fiorilli. 1997. Death of bystander cells by a novel pathway involving early mitochondrial damage in human immunodeficiency virus-related lymphadenopathy. Blood 90:209-216.
17. + cells. AIDS Res. Hum. Retrovir. 11:789-794.
18. + T cells. Proc. Natl. Acad. Sci. USA 97:1178-1183.
19. + cell numbers and clinical staging. J. Clin. Investig. 84:1892-1899.
20. + T-lymphocyte decline and clinical progression in human immunodeficiency virus type 1-infected individuals. J. Virol. 67:1772-1777.
21. + antigen-specific T cells to undergo apoptosis by HIV-infected monocytes. J. Clin. Investig. 99:257-266.
22. Davis, C. B., I. Dikic, D. Unutmaz, C. M. Hill, J. Arthos, M. A. Siani, D. A. Thompson, J. Schlessinger, and D. R. Littman. 1997. Signal transduction due to HIV-1 envelope interactions with chemokine receptors CXCR4 or CCR5. J. Exp. Med. 186:1793-1798.
23. Del Corno, M., Q. Liu, D. Schols, E. De Clercq, S. Gessani, B. D. Freedman, and R. G. Collman. 2001. HIV-1 gpl20 and chemokine activation of Pyk2 and mitogen-activated protein kinases in primary macrophages mediated by calcium-dependent, pertussis toxin-insensitive chemokine receptor signaling. Blood 98:2909-2916.
24. Dimitrov, D. S., R. S. Willey, H. Sato, L. J. Chang, R. Blumenthal, and M. A. Martin. 1993. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 67:2182-2190.
25. Doms, R. W., and D. Trono. 2000. The plasma membrane as a combat zone in the HIV battlefield. Genes Dev. 14:2677-2688.
26. Donzella, G. A., D. Schols, S. W. Lin, J. A. Este, K. A. Nagashima, P. J. Maddon, G. P. Allaway, T. P. Sakmar, G. Henson, E. De Clercq, and J. P. Moore. 1998. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4:72-77.
27. Esser, M. T., D. R. Graham, L. V. Coren, C. M. Trubey, J. W. Bess, Jr., L. O. Arthur, D. E. Ott, and J. D. Lifson. 2001. Differential incorporation of CD45, CD80 (B7-1), CD86 (B7-2), and major histocompatibility complex class I and II molecules into human immunodeficiency virus type 1 virions and microvesicles: implications for viral pathogenesis and immune regulation. J. Virol. 75:6173-6182.
28. + T lymphocytes by conformationally authentic noninfectious human immunodeficiency virus type 1. J. Virol. 75:1152-1164.
29. +-T-cell death. J. Virol. 76:5966-5973.
30. Finkel, T. H., G. Tudor-Williams, N. K. Banda, M. F. Cotton, T. Curiel, C. Monks, T. W. Baba, R. M. Ruprecht, and A. Kupfer. 1995. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat. Med. 1:129-134.
31. Fortin, J.-F., R. Cantin, G. Lamontagne, and M. Tremblay. 1997. Host-derived ICAM-1 glycoproteins incorporated on human immunodeficiency virus type 1 are biologically active and enhance viral infectivity. J. Virol. 71:3588-3596.
32. Fujita, K., J. Silver, and K. Peden. 1992. Changes in both gp120 and gp41 can account for increased growth potential and expanded host range of human immunodeficiency virus type 1. J. Virol. 66: 4445-4451.
33. Geleziunas, R., W. Xu, K. Takeda, H. Ichijo, and W. C. Greene. 2001. HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infected host cell. Nature 410:834-838.
34. Ghosh, S. K., P. N. Fultz, E. Keddie, M. S. Saag, P. M. Sharp, B. H. Hahn, and G. M. Shaw. 1993. A molecular clone of HIV-1 tropic and cytopathic for human and chimpanzee lymphocytes. Virology 194:858-864.
35. Glushakova, S., B. Baibakov, L. B. Margolis, and J. Zimmerberg. 1995. Infection of human tonsil histocultures: a model for HIV pathogenesis. Nat. Med. 1:1320-1322.
36. Glushakova, S., J. C. Grivel, W. Fitzgerald, A. Sylwester, J. Zimmerberg, and L. B. Margolis. 1998. Evidence for the HIV-1 phenotype switch as a causal factor in acquired immunodeficiency. Nat. Med. 4:346-349.
37. Glushakova, S., Y. Yi, J. C. Grivel, A. Singh, D. Schols, E. De Clercq, R. G. Collman, and L. Margolis. 1999. Preferential coreceptor utilization and cytopathicity by dual-tropic HIV-1 in human lymphoid tissue ex vivo. J. Clin. Investig. 104:R7-R11.
38. Gorry, P. R., J. Taylor, G. Holm, A. Mehle, T. Morgan, M. Cayabyab, M. Farzan, H. Wang, J. E. Bell, K. Kunstman, J. P. Moore, S. M. Wolinsky, and D. Gabuzda. 2002. Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J. Virol. 76:6277-6292.
39. Grivel, J. C., and L. B. Margolis. 1999. CCR5- and CXCR4-tropic HIV-1 are equally cytopathic for their T-cell targets in human lymphoid tissue. Nat. Med. 5:592-593.
40. + T cells in ex vivo-infected human lymphoid tissue. J. Virol. 74:8077-8084.
41. Herbein, G., C. Van Lint, J. L. Lovett, and E. Verdin. 1998. Distinct mechanisms trigger apoptosis in human immunodeficiency virus type 1-infected and in uninfected bystander T lymphocytes. J. Virol. 72:660-670.
42. + T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 395:189-194.
43. Hoffman, T. L., C. C. LaBranche, W. Zhang, G. Canziani, J. Robinson, I. Chaiken, J. A. Hoxie, and R. W. Doms. 1999. Stable exposure of the coreceptor-binding site in a CD4-independent HIV-1 envelope protein. Proc. Natl. Acad. Sci. USA 96:6359-6364.
44. Jekle, A., O. T. Keppler, E. De Clercq, D. Schols, M. Weinstein, and M. A. Goldsmith. 2003. In vivo evolution of human immunodeficiency virus type 1 toward increased pathogenicity through CXCR4-mediated killing of uninfected CD4 T cells. J. Virol. 77:5846-5854.
45. Katsikis, P. D., E. S. Wunderlich, C. A. Smith, L. A. Herzenberg, and L. A. Herzenberg. 1995. Fas antigen stimulation induces marked apoptosis of T lymphocytes in human immunodeficiency virus-infected individuals. J. Exp. Med. 181:2029-2036.
46. + cell depletion and progression to AIDS. Ann. Intern. Med. 118:681-688.
47. Kozak, S. L., E. J. Platt, N. Madani, F. E. Ferro, Jr., K. Peden, and D. Kabat. 1997. CD4, CXCR-4, and CCR-5 dependencies for infections by primary patient and laboratory-adapted isolates of human immunodeficiency virus type 1. J. Virol. 71:873-882.
48. Kraft, M. S., G. Henning, H. Fickenscher, D. Lengenfelder, J. Tschopp, B. Fleckenstein, and E. Meinl. 1998. Herpesvirus saimiri transforms human T-cell clones to stable growth without inducing resistance to apoptosis. J. Virol. 72:3138-3145.
49. Kreisberg, J. F., D. Kwa, B. Schramm, V. Trautner, R. Connor, H. Schuitemaker, J. I. Mullins, A. B. van't Wout, and M. A. Goldsmith. 2001. Cytopathicity of human immunodeficiency virus type 1 primary isolates depends on coreceptor usage and not patient disease status. J. Virol. 75:8842-8847.
50. Kuhmann, S. E., P. Pugach, K. J. Kunstman, J. Taylor, R. L. Stanfield, A. Snyder, J. M. Strizki, J. Riley, B. M. Baroudy, I. A. Wilson, B. T. Korber, S. M. Wolinsky, and J. P. Moore. 2003. Genetic and phenotypic analyses of human immunodeficiency virus type 1 escape from a small-molecule CCR5 inhibitor. J. Virol. 78:2790-2807.
51. + T-cell subsets are determined only by coreceptor expression. J. Virol. 75: 10455-10459.
52. LaBonte, J. A., N. Madani, and J. Sodroski. 2003. Cytolysis by CCR5-using human immunodeficiency virus type 1 envelope glycoproteins is dependent on membrane fusion and can be inhibited by high levels of CD4 expression. J. Virol. 77:6645-6659.
53. LaBonte, J. A., T. Patel, W. Hofmann, and J. Sodroski. 2000. Importance of membrane fusion mediated by human immunodeficiency virus envelope glycoproteins for lysis of primary CD4-positive T cells. J. Virol. 74:10690-10698.
54. LaBranche, C. C., T. L. Hoffman, J. Romano, B. S. Haggarty, T. G. Edwards, T. J. Matthews, R. W. Doms, and J. A. Hoxie. 1999. Determinants of CD4 independence for a human immunodeficiency virus type 1 variant map outside regions required for coreceptor specificity. J. Virol. 73:10310-10319.
55. Laurent-Crawford, A. G., B. Krust, Y. Riviere, C. Desgranges, S. Muller, M. Paule Kieny, C. Dauguet, and A. G. Hovanessian. 1993. Membrane expression of HIV envelope glycoproteins triggers apoptosis in CD4 cells. AIDS Res. Hum. Retrovir. 9:761-773.
56. Lawless, M. K., S. Barney, K. I. Guthrie, T. B. Bucy, S. R. Petteway, Jr., and G. Merutka. 1996. HIV-1 membrane fusion mechanism: structural studies of the interactions between biologically-active peptides from gp41. Biochemistry 35:13697-13708.
57. + T lymphocytes by human immunodeficiency virus type 1 appears necrotic rather than apoptotic and does not require env. J. Virol. 76:5082-5093.
58. Li, C. J., D. J. Friedman, C. Wang, V. Metelev, and A. B. Pardee. 1995. Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science 268: 429-431.
59. + cells expressing gp160 of human immunodeficiency virus type 1. J. Virol. 68:390-399.
60. + T lymphocytes is mediated by macrophages: role for Nef and immune activation in viral persistence. J. Immunol. 165:6437-6446.
61. + T-cell depletion in HIV disease. Nature 410:974-979.
62. Meyaard, L., S. A. Otto, R. R. Jonker, M. J. Mijnster, R. P. Keet, and F. Miedema. 1992. Programmed death of T cells in HIV-1 infection. Science 257:217-219.
63. Misse, D., M. Cerutti, N. Noraz, P. Jourdan, J. Favero, G. Devauchelle, H. Yssel, N. Taylor, and F. Veas. 1999. A CD4-independent interaction of human immunodeficiency virus-1 gp120 with CXCR4 induces their cointernalization, cell signaling, and T-cell chemotaxis. Blood 93:2454-2462.
64. Muro-Cacho, C. A., G. Pantaleo, and A. S. Fauci. 1995. Analysis of apoptosis in lymph nodes of HIV-infected persons. J. Immunol. 154:5555-5566.
65. Ohagen, A., S. Ghosh, J. He, K. Huang, Y. Chen, M. Yuan, R. Osathanondh, S. Gartner, G. Shaw, and D. Gabuzda. 1999. Apoptosis induced by infection of primary brain cultures with diverse human immunodeficiency virus type 1 isolates: evidence for a role of the envelope. J. Virol. 73:897-906.
66. + T cells apoptosis. J. Immunol. 158:2456-2463.
67. Peden, K., M. Emerman, and L. Montagnier. 1991. Changes in growth properties on passage in tissue culture of viruses derived from infectious molecular clones of HIV-1LAI, HIV-1MAL, and HIV-1ELI Virology 185: 661-672.
68. Piatak, M., Jr., M. S. Saag, L. C. Yang, S. J. Clark, J. C. Kappes, K.C. Luk, B. H. Hahn, G. M. Shaw, and J. D. Lifson. 1993. High levels of HIV-1 in plasma during all stages of infection determined by competitive PCR. Science 259:1749-1754.
69. Popik, W., J. E. Hesselgesser, and P. M. Pitha. 1998. Binding of human immunodeficiency virus type 1 to CD4 and CXCR4 receptors differentially regulates expression of inflammatory genes and activates the MEK/ERK signaling pathway. J. Virol. 72:6406-6413.
70. Rho, H., B. Poiesz, F. Ruscetti, and R. C. Gallo. 1981. Characterization of the reverse transcriptase from a new retrovirus (HTLV) produced by a human cutaneous T-cell lymphoma cell line. Virology 112:355-360.
71. + cells during human immunodeficiency virus type 1 infection - correlation with clinical progression, viral load, and loss of humoral immunity. Virology 238:180-188.
72. Schols, D., S. Struyf, J. Van Damme, J. A. Este, G. Henson, and E. De Clercq. 1997. Inhibition of T-tropic HIV strains by selective antagonization of the chemokine receptor CXCR4. J. Exp. Med. 186:1383-1388.
73. Shi, B., U. De Girolami, J. He, S. Wang, A. Lorenzo, J. Busciglio, and D. Gabuzda. 1996. Apoptosis induced by HIV-1 infection of the central nervous system. J. Clin. Investig. 98:1979-1990.
74. Stewart, S. A., B. Poon, J. Y. Song, and I. S. Y. Chen. 2000. Human immunodeficiency virus type 1 Vpr induces apoptosis through caspase activation. J. Virol. 74:3105-3111.
75. Su, L., H. Kaneshima, M. Bonyhadi, S. Salimi, D. Kraft, L. Rabin, and J. M. McCune. 1995. HIV-1-induced thymocyte depletion is associated with indirect cytopathogenicity and infection of progenitor cells in vivo. Immunity 2:25-36.
76. Tateyama, M., N. Oyaizu, T. W. McCloskey, S. Than, and S. Pahwa. 2000. CD4 T lymphocytes are primed to express Fas ligand by CD4 cross-linking and to contribute to CD8 T-cell apoptosis via Fas/FasL death signaling pathway. Blood 96:195-202.
77. Trkola, A., S. E. Kuhmann, J. M. Strizki, E. Maxwell, T. Ketas, T. Morgan, P. Pugach, S. Xu, L. Wojcik, J. Tagat, A. Palani, S. Shapiro, J. W. Clader, S. McCombie, G. R. Reyes, B. M. Baroudy, and J. P. Moore. 2002. HIV-1 escape from a small molecule, CCR5-specific entry inhibitor does not involve CXCR4 use. Proc. Natl. Acad. Sci. USA 99: 395-400.
78. Vlahakis, S. R., A. Algeciras-Schimnich, G. Bou, C. J. Heppelmann, A. Villasis-Keever, R. G. Collman, and C. V. Paya. 2001. Chemokine-receptor activation by env determines the mechanism of death in HIV-infected and uninfected T lymphocytes. J. Clin. Investig. 107:207-215.
79. Vlahakis, S. R., A. Villasis-Keever, T. Gomez, M. Vanegas, N. Vlahakis, C. V. Paya. 2002. G protein-coupled chemokine receptors induce both survival and apoptotic signaling pathways. J. Immunol. 169:5546-5554.
80. Westendorp, M. O., R. Frank, C. Ochsenbauer, K. Stricker, J. Dhein, H. Walczak, K. M. Debatin, and P. H. Krammer. 1995. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375:497-500.
81. Willey, R. L, M. A. Martin, and K. W. Peden. 1994. Increase in soluble CD4 binding to and CD4-induced dissociation of gp120 from virions correlates with infectivity of human immunodeficiency virus type 1. J. Virol. 68:1029-1039.
82. Yao, Q., R. W. Compans, and C. Chen. 2001. HIV envelope proteins differentially utilize CXCR4 and CCR5 coreceptors for induction of apoptosis. Virology 285:128-137.