T cell virological synapses and HIV-1 pathogenesis

Immunologic Research

Volumn 54, Issue 1-3, 2012, Pages 133-139

  Chen, Benjamin K ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cell adhesion; Endocytosis; Env; Gag; Human immunodeficiency virus type 1; T lymphocyte; Viral assembly; Viral fusion; Viral maturation; Virological synapse

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADAPTIVE IMMUNITY; CD4+ T LYMPHOCYTE; CELL ADHESION; CELL INTERACTION; DENDRITIC CELL; ENDOCYTOSIS; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; VIRUS REPLICATION;

CD4-POSITIVE T-LYMPHOCYTES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOLOGICAL SYNAPSES; VIRUS REPLICATION;

EID: 84867847173     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-012-8320-8     Document Type: Review

References (76)

1. 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(6510):123-6.
2. 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(5255):1582-6.
3. Simon V, Ho DD. HIV-1 dynamics in vivo: implications for therapy. Nat Rev Microbiol. 2003;1(3):181-90.
4. Wei X, Ghosh SK, Taylor ME, Johnson VA, Emini EA, Deutsch P, et al. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 1995;373(6510):117-22.
5. 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(5102):1749-54.
6. Coombs RW, Collier AC, Allain JP, Nikora B, Leuther M, Gjerset GF, et al. Plasma viremia in human immunodeficiency virus infection. N Engl J Med. 1989;321(24):1626-31.
7. Ho DD, Moudgil T, Alam M. Quantitation of human immunodeficiency virus type 1 in the blood of infected persons. N Engl J Med. 1989;321(24):1621-5.
8. Mohri H, Singh MK, Ching WT, Ho DD. Quantitation of zidovudine-resistant human immunodeficiency virus type 1 in the blood of treated and untreated patients. Proc Natl Acad Sci USA. 1993;90(1):25-9.
9. O'Brien WA, Hartigan PM, Daar ES, Simberkoff MS, Hamilton JD. Changes in plasma HIV RNA levels and CD4+ lymphocyte counts predict both response to antiretroviral therapy and therapeutic failure. VA Cooperative Study Group on AIDS. Ann Intern Med. 1997;126(12):939-45.
10. 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(7):426-31.
11. Katzenstein DA, Hammer SM, Hughes MD, Gundacker H, Jackson JB, Fiscus S, et al. The relation of virologic and immunologic markers to clinical outcomes after nucleoside therapy in HIV-infected adults with 200 to 500 CD4 cells per cubic millimeter. AIDS Clinical Trials Group Study 175 Virology Study Team. N Engl J Med. 1996;335(15):1091-8.
12. Sperling RS, Shapiro DE, Coombs RW, Todd JA, Herman SA, McSherry GD, et al. Maternal viral load, zidovudine treatment, and the risk of transmission of human immunodeficiency virus type 1 from mother to infant. Pediatric AIDS Clinical Trials Group Protocol 076 Study Group. N Engl J Med. 1996;335(22):1621-9.
13. Grossman Z, Feinberg MB, Paul WE. Multiple modes of cellular activation and virus transmission in HIV infection: a role for chronically and latently infected cells in sustaining viral replication. Proc Natl Acad Sci USA. 1998;95(11):6314-9.
14. Layne SP, Merges MJ, Dembo M, Spouge JL, Conley SR, Moore JP, et al. Factors underlying spontaneous inactivation and susceptibility to neutralization of human immunodeficiency virus. Virology. 1992;189(2):695-714.
15. Chertova E, Bess JW Jr, Crise BJ, Sowder IR, Schaden TM, Hilburn JM, et al. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol. 2002;76(11):5315-25.
16. Hart TK, Klinkner AM, Ventre J, Bugelski PJ. Morphometric analysis of envelope glycoprotein gp120 distribution on HIV-1 virions. J Histochem Cytochem. 1993;41(2):265-71.
17. Zhu P, Chertova E, Bess J Jr, Lifson JD, Arthur LO, Liu J, et al. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc Natl Acad Sci USA. 2003;100(26):15812-7.
18. Moore JP, McKeating JA, Weiss RA, Sattentau QJ. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science. 1990;250(4984):1139-42.
19. Herrera C, Spenlehauer C, Fung MS, Burton DR, Beddows S, Moore JP. Nonneutralizing antibodies to the CD4-binding site on the gp120 subunit of human immunodeficiency virus type 1 do not interfere with the activity of a neutralizing antibody against the same site. J Virol. 2003;77(2):1084-91.
20. Poignard P, Moulard M, Golez E, Vivona V, Franti M, Venturini S, et al. Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies. J Virol. 2003;77(1):353-65.
21. Gratton S, Cheynier R, Dumaurier MJ, Oksenhendler E, Wain-Hobson S. Highly restricted spread of HIV-1 and multiply infected cells within splenic germinal centers. Proc Natl Acad Sci USA. 2000;97(26):14566-71. doi: 10.1073/pnas.97.26.14566.
22. Cheynier R, Henrichwark S, Hadida F, Pelletier E, Oksenhendler E, Autran B, et al. HIV and T cell expansion in splenic white pulps is accompanied by infiltration of HIV-specific cytotoxic T lymphocytes. Cell. 1994;78(3):373-87. doi: 10.1016/0092-8674(94)90417-0.
23. Zhu T, Wang N, Carr A, Nam DS, Moor-Jankowski R, Cooper DA, et al. Genetic characterization of human immunodeficiency virus type 1 in blood and genital secretions: evidence for viral compartmentalization and selection during sexual transmission. J Virol. 1996;70(5):3098-107.
24. Butler DM, Delport W, Kosakovsky Pond SL, Lakdawala MK, Cheng PM, Little SJ, et al. The origins of sexually transmitted HIV among men who have sex with men. Sci Transl Med. 2010;2(18):18re1. doi: 10.1126/scitranslmed.3000447.
25. Heath L, Frenkel LM, Foley BT, Mullins JI. Comment on The origins of sexually transmitted HIV among men who have sex with men. Sci Transl Med. 2(50):50le1; author reply lr1. doi: 10.1126/scitranslmed.3001416.
26. Sodora DL, Gettie A, Miller CJ, Marx PA. Vaginal transmission of SIV: assessing infectivity and hormonal influences in macaques inoculated with cell-free and cell-associated viral stocks. AIDS Res Hum Retrovir. 1998;14(Suppl 1):S119-23.
27. Girard M, Mahoney J, Wei Q, van der Ryst E, Muchmore E, Barre-Sinoussi F, et al. Genital infection of female chimpanzees with human immunodeficiency virus type 1. AIDS Res Hum Retroviruses. 1998;14(15):1357-67.
28. Shedlock DJ, Silvestri G, Weiner DB. Monkeying around with HIV vaccines: using rhesus macaques to define 'gatekeepers' for clinical trials. Nat Rev Immunol. 2009;9(10):717-28. doi: 10.1038/nri2636.
29. Salle B, Brochard P, Bourry O, Mannioui A, Andrieu T, Prevot S, et al. Infection of macaques after vaginal exposure to cell-associated simian immunodeficiency virus. J Infect Dis. 2010;202(3):337-44. doi: 10.1086/653619.
30. Weiler AM, Li Q, Duan L, Kaizu M, Weisgrau KL, Friedrich TC, et al. Genital ulcers facilitate rapid viral entry and dissemination following intravaginal inoculation with cell-associated simian immunodeficiency virus SIVmac239. J Virol. 2008;82(8):4154-8. doi: 10.1128/JVI.01947-07.
31. Dimitrov DS, Willey RL, Sato H, Chang LJ, Blumenthal R, Martin MA. Quantitation of human immunodeficiency virus type 1 infection kinetics. J Virol. 1993;67(4):2182-90.
32. Sato H, Orenstein J, Dimitrov D, Martin M. Cell-to-cell spread of HIV-1 occurs within minutes and may not involve the participation of virus particles. Virology. 1992;186(2):712-24.
33. Zhu T, Mo H, Wang N, Nam DS, Cao Y, Koup RA, et al. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science. 1993;261(5125):1179-81.
34. Weng J, Krementsov DN, Khurana S, Roy NH, Thali M. Formation of syncytia is repressed by tetraspanins in human immunodeficiency virus type 1-producing cells. J Virol. 2009;83(15):7467-74. doi: 10.1128/JVI.00163-09.
35. Wyss S, Dimitrov AS, Baribaud F, Edwards TG, Blumenthal R, Hoxie JA. Regulation of human immunodeficiency virus type 1 envelope glycoprotein fusion by a membrane-interactive domain in the gp41 cytoplasmic tail. J Virol. 2005;79(19):12231-41.
36. Piguet V, Sattentau Q. Dangerous liaisons at the virological synapse. J Clin Invest. 2004;114(5):605-10.
37. Cameron PU, Freudenthal PS, Barker JM, Gezelter S, Inaba K, Steinman RM. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science. 1992;257(5068):383-7.
38. McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D, Hope TJ. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science. 2003;300(5623):1295-7.
39. Piguet V, Steinman RM. The interaction of HIV with dendritic cells: outcomes and pathways. Trends Immunol. 2007;28(11):503-10. doi: 10.1016/j.it.2007.07.010.
40. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J Exp Med. 2004;199(2):283-93.
41. Chen P, Hubner W, Spinelli MA, Chen BK. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol. 2007;81(22):12582-95.
42. Hubner W, McNerney GP, Chen P, Dale BM, Gordon RE, Chuang FY, et al. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science. 2009;323(5922):1743-7. doi: 10.1126/science.1167525.
43. Jolly C, Mitar I, Sattentau QJ. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J Virol. 2007;81(11):5547-60.
44. Blanco J, Bosch B, Fernandez-Figueras MT, Barretina J, Clotet B, Este JA. High level of coreceptor-independent HIV transfer induced by contacts between primary CD4 T cells. J Biol Chem. 2004;279(49):51305-14.
45. Martin N, Welsch S, Jolly C, Briggs JA, Vaux D, Sattentau QJ. Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J Virol. 2010;84(7):3516-27. doi: 10.1128/JVI.02651-09.
46. Dejucq N, Simmons G, Clapham PR. T-cell line adaptation of human immunodeficiency virus type 1 strain SF162: effects on envelope, vpu and macrophage-tropism. J Gen Virol. 2000;81(Pt 12):2899-904.
47. Pais-Correia AM, Sachse M, Guadagnini S, Robbiati V, Lasserre R, Gessain A, et al. Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat Med. 2010;16(1):83-9. doi: 10.1038/nm.2065.
48. Vasiliver-Shamis G, Cho MW, Hioe CE, Dustin ML. Human immunodeficiency virus type 1 envelope gp120-induced partial T-cell receptor signaling creates an F-actin-depleted zone in the virological synapse. J Virol. 2009;83(21):11341- 55. doi: 10.1128/JVI.01440-09.
49. Jolly C, Sattentau QJ. Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity. J Virol. 2005;79(18):12088-94.
50. Jolly C, Sattentau QJ. Human immunodeficiency virus type 1 assembly, budding, and cell-cell spread in T cells take place in tetraspanin-enriched plasma membrane domains. J Virol. 2007;81(15):7873-84.
51. Gordon-Alonso M, Yanez-Mo M, Barreiro O, Alvarez S, Munoz-Fernandez MA, Valenzuela-Fernandez A, et al. Tetraspanins CD9 and CD81 modulate HIV-1-induced membrane fusion. J Immunol. 2006;177(8):5129-37. doi: 10.1016/S0092-8674(88) 91241-X.
52. Marsh M, Helenius A. Virus entry: open sesame. Cell. 2006;124(4):729-40.
53. Sieczkarski SB, Whittaker GR. Dissecting virus entry via endocytosis. J Gen Virol. 2002;83(Pt 7):1535-45.
54. Maddon PJ, McDougal JS, Clapham PR, Dalgleish AG, Jamal S, Weiss RA, et al. HIV infection does not require endocytosis of its receptor, CD4. Cell. 1988;54(6):865-74.
55. Marchant D, Neil SJ, Aubin K, Schmitz C, McKnight A. An envelope-determined, pH-independent endocytic route of viral entry determines the susceptibility of human immunodeficiency virus type 1 (HIV-1) and HIV-2 to Lv2 restriction. J Virol. 2005;79(15):9410-8.
56. Daecke J, Fackler OT, Dittmar MT, Krausslich HG. Involvement of clathrin-mediated endocytosis in human immunodeficiency virus type 1 entry. J Virol. 2005;79(3):1581-94.
57. Fredericksen BL, Wei BL, Yao J, Luo T, Van Ryk D. Inhibition of endosomal/lysosomal degradation increases the infectivity of human immunodeficiency virus. J Virol. 2002;76(22):11440-6.
58. Schaeffer E, Soros VB, Greene WC. Compensatory link between fusion and endocytosis of human immunodeficiency virus type 1 in human CD4 T lymphocytes. J Virol. 2004;78(3):1375-83.
59. Fackler OT, Peterlin BM. Endocytic entry of HIV-1. Curr Biol. 2000;10(16):1005-8.
60. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell. 2009;137(3):433-44. doi: 10.1016/j.cell.2009.02.046.
61. Mercer J, Schelhaas M, Helenius A. Virus entry by endocytosis. Annu Rev Biochem. 2010;79:803-33. doi: 10.1146/annurev-biochem-060208-104626.
62. Bosch B, Grigorov B, Senserrich J, Clotet B, Darlix JL, Muriaux D, et al. A clathrin-dynamin-dependent endocytic pathway for the uptake of HIV-1 by direct T cell-T cell transmission. Antiviral Res. 2008;80(2):185-93. doi: 10.1016/j.antiviral.2008.06.004.
63. Dale BM, McNerney GP, Thompson DL, Hubner W. de Los Reyes K, Chuang FY et al. Cell-to-Cell Transfer of HIV-1 via Virological Synapses Leads to Endosomal Virion Maturation that Activates Viral Membrane Fusion. Cell Host Microbe. 2011;10(6):551-62. doi: 10.1016/j.chom.2011.10.015.
64. Zhou W, Resh MD. Differential membrane binding of the human immunodeficiency virus type 1 matrix protein. J Virol. 1996;70(12):8540-8.
65. Wyma DJ, Jiang J, Shi J, Zhou J, Lineberger JE, Miller MD, et al. Coupling of human immunodeficiency virus type 1 fusion to virion maturation: a novel role of the gp41 cytoplasmic tail. J Virol. 2004;78(7):3429-35.
66. Wyma DJ, Kotov A, Aiken C. Evidence for a stable interaction of gp41 with Pr55(Gag) in immature human immunodeficiency virus type 1 particles. J Virol. 2000;74(20):9381-7.
67. Murakami T, Ablan S, Freed EO, Tanaka Y. Regulation of human immunodeficiency virus type 1 Env-mediated membrane fusion by viral protease activity. J Virol. 2004;78(2):1026-31.
68. Jiang J, Aiken C. Maturation-dependent human immunodeficiency virus type 1 particle fusion requires a carboxyl-terminal region of the gp41 cytoplasmic tail. J Virol. 2007;81(18):9999-10008. doi: 10.1128/JVI.00592-07.
69. Massanella M, Puigdomenech I, Cabrera C, Fernandez-Figueras MT, Aucher A, Gaibelet G, et al. Antigp41 antibodies fail to block early events of virological synapses but inhibit HIV spread between T cells. Aids. 2009;23(2):183-8. doi: 10.1097/QAD.0b013e32831ef1a300002030-200901140-00004.
70. Durham ND, Yewdall AW, Chen P, Lee R, Zony C, Robinson JE et al. Neutralization resistance of HIV-1 virological synapse-mediated infection is regulated by the gp41 cytoplasmic tail in preparation. 2012.
71. Jung A, Maier R, Vartanian JP, Bocharov G, Jung V, Fischer U, et al. Multiply infected spleen cells in HIV patients. Nature. 2002;418(6894):144.
72. Dixit NM, Perelson AS. Multiplicity of human immunodeficiency virus infections in lymphoid tissue. J Virol. 2004;78(16):8942-5.
73. Dixit NM, Perelson AS. HIV dynamics with multiple infections of target cells. Proc Natl Acad Sci USA. 2005;102(23):8198-203.
74. Del Portillo A, Tripodi J, Najfeld V, Wodarz D, Levy DN, Chen BK. Multiploid inheritance of HIV-1 during cell-to-cell infection. J Virol. 2011;85(14):7169-76. doi: 10.1128/JVI.00231-11.
75. Sigal A, Kim JT, Balazs AB, Dekel E, Mayo A, Milo R, et al. Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy. Nature. 2011;477(7362):95-8. doi: 10.1038/nature10347.
76. Josefsson L, King MS, Makitalo B, Brannstrom J, Shao W, Maldarelli F, et al. Majority of CD4+ T cells from peripheral blood of HIV-1-infected individuals contain only one HIV DNA molecule. Proc Natl Acad Sci USA. 2011;108(27):11199- 204. doi: 10.1073/pnas.1107729108.