The infectious synapse formed between mature dendritic cells and CD4+ T cells is independent of the presence of the HIV-1 envelope glycoprotein

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Rodriguez Plata, Maria T ^a   Puigdomènech, Isabel ^a   Izquierdo Useros, Nuria ^a   Puertas, Maria C ^a   Carrillo, Jorge ^a   Erkizia, Itziar ^a   Clotet, Bonaventura ^a   Blanco, Julià ^a   Martinez Picado, Javier ^a,b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

CD4+ T cell; Cell to cell; Dendritic cell; HIV 1; Immunological synapse; Infectious synapse; Trans infection; Transmission; Virological synapse

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN; T LYMPHOCYTE RECEPTOR; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN;

ANTIGEN RECOGNITION; ARTICLE; CD4+ T LYMPHOCYTE; CELL ADHESION; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOLOGICAL SYNAPSE; LYMPHOCYTE PROLIFERATION; NONHUMAN; PATHOGENESIS; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE ACTIVATION; VIRUS CELL INTERACTION; VIRUS TRANSMISSION;

CD4-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELLS, CULTURED; DENDRITIC CELLS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84876082473     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-42     Document Type: Article

References (76)

1. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998, 392:245-252. 10.1038/32588, 9521319.
2. Revy P, Sospedra M, Barbour B, Trautmann A. Functional antigen-independent synapses formed between T cells and dendritic cells. Nat Immunol 2001, 2:925-931.
3. Delon J, Bercovici N, Raposo G, Liblau R, Trautmann A. Antigen-dependent and -independent Ca2+ responses triggered in T cells by dendritic cells compared with B cells. J Exp Med 1998, 188:1473-1484. 10.1084/jem.188.8.1473, 2213410, 9782124.
4. Hauss P, Selz F, Cavazzana-Calvo M, Fischer A. Characteristics of antigen-independent and antigen-dependent interaction of dendritic cells with CD4+ T cells. Eur J Immunol 1995, 25:2285-2294. 10.1002/eji.1830250826, 7545116.
5. Miller MJ, Hejazi AS, Wei SH, Cahalan MD, Parker I. T cell repertoire scanning is promoted by dynamic dendritic cell behavior and random T cell motility in the lymph node. Proc Natl Acad Sci U S A 2004, 101:998-1003. 10.1073/pnas.0306407101, 327133, 14722354.
6. Irvine DJ, Purbhoo MA, Krogsgaard M, Davis MM. Direct observation of ligand recognition by T cells. Nature 2002, 419:845-849. 10.1038/nature01076, 12397360.
7. Lee KH, Holdorf AD, Dustin ML, Chan AC, Allen PM, Shaw AS. T cell receptor signaling precedes immunological synapse formation. Science 2002, 295:1539-1542. 10.1126/science.1067710, 11859198.
8. Friedl P, den Boer AT, Gunzer M. Tuning immune responses: diversity and adaptation of the immunological synapse. Nat Rev Immunol 2005, 5:532-545. 10.1038/nri1647, 15999094.
9. Huppa JB, Davis MM. T-cell-antigen recognition and the immunological synapse. Nat Rev Immunol 2003, 3:973-983. 10.1038/nri1245, 14647479.
10. Doms RW, Moore JP. HIV-1 membrane fusion: targets of opportunity. J Cell Biol 2000, 151:F9-F14. 10.1083/jcb.151.2.F9, 2192632, 11038194.
11. 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, 199:283-293. 10.1084/jem.20030648, 2211771, 14734528.
12. 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, 300:1295-1297. 10.1126/science.1084238, 12730499.
13. Fais S, Capobianchi MR, Abbate I, Castilletti C, Gentile M, Cordiali Fei P, Ameglio F, Dianzani F. Unidirectional budding of HIV-1 at the site of cell-to-cell contact is associated with co-polarization of intercellular adhesion molecules and HIV-1 viral matrix protein. AIDS 1995, 9:329-335.
14. Carr JM, Hocking H, Li P, Burrell CJ. Rapid and efficient cell-to-cell transmission of human immunodeficiency virus infection from monocyte-derived macrophages to peripheral blood lymphocytes. Virology 1999, 265:319-329. 10.1006/viro.1999.0047, 10600603.
15. Johnson DC, Huber MT. Directed egress of animal viruses promotes cell-to-cell spread. J Virol 2002, 76:1-8. 10.1128/JVI.76.1.1-8.2002, 135733, 11739666.
16. Jolly C, Sattentau QJ. Retroviral spread by induction of virological synapses. Traffic 2004, 5:643-650. 10.1111/j.1600-0854.2004.00209.x, 15296489.
17. Dimitrov DS, Willey RL, Sato H, Chang LJ, Blumenthal R, Martin MA. Quantitation of human immunodeficiency virus type 1 infection kinetics. J Virol 1993, 67:2182-2190. 240333, 8445728.
18. Dixit NM, Perelson AS. Multiplicity of human immunodeficiency virus infections in lymphoid tissue. J Virol 2004, 78:8942-8945. 10.1128/JVI.78.16.8942-8945.2004, 479058, 15280505.
19. Jolly C, Sattentau QJ. Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity. J Virol 2005, 79:12088-12094. 10.1128/JVI.79.18.12088-12094.2005, 1212596, 16140785.
20. Puigdomenech I, Massanella M, Izquierdo-Useros N, Ruiz-Hernandez R, Curriu M, Bofill M, Martinez-Picado J, Juan M, Clotet B, Blanco J. HIV transfer between CD4 T cells does not require LFA-1 binding to ICAM-1 and is governed by the interaction of HIV envelope glycoprotein with CD4. Retrovirology 2008, 5:32. 10.1186/1742-4690-5-32, 2359761, 18377648.
21. Turville SG, Santos JJ, Frank I, Cameron PU, Wilkinson J, Miranda-Saksena M, Dable J, Stossel H, Romani N, Piatak M. Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 2004, 103:2170-2179. 10.1182/blood-2003-09-3129, 14630806.
22. 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, 81:12582-12595. 10.1128/JVI.00381-07, 2169007, 17728240.
23. Ganesh L, Leung K, Lore K, Levin R, Panet A, Schwartz O, Koup RA, Nabel GJ. Infection of specific dendritic cells by CCR5-tropic human immunodeficiency virus type 1 promotes cell-mediated transmission of virus resistant to broadly neutralizing antibodies. J Virol 2004, 78:11980-11987. 10.1128/JVI.78.21.11980-11987.2004, 523246, 15479838.
24. Su B, Xu K, Lederle A, Peressin M, Biedma ME, Laumond G, Schmidt S, Decoville T, Proust A, Lambotin M. Neutralizing antibodies inhibit HIV-1 transfer from primary dendritic cells to autologous CD4 T-lymphocytes. Blood 2012, 120:3708-3717. 10.1182/blood-2012-03-418913, 22955927.
25. Turville SG, Aravantinou M, Stossel H, Romani N, Robbiani M. Resolution of de novo HIV production and trafficking in immature dendritic cells. Nat Methods 2008, 5:75-85. 10.1038/nmeth1137, 18059278.
26. Groot F, Welsch S, Sattentau QJ. Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses. Blood 2008, 111:4660-4663. 10.1182/blood-2007-12-130070, 18296630.
27. Izquierdo-Useros N, Esteban O, Rodriguez-Plata MT, Erkizia I, Prado JG, Blanco J, Garcia-Parajo MF, Martinez-Picado J. Dynamic imaging of cell-free and cell-associated viral capture in mature dendritic cells. Traffic 2011, 12:1702-1713. 10.1111/j.1600-0854.2011.01281.x, 21917091.
28. Jolly C, Mitar I, Sattentau QJ. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J Virol 2007, 81:13916-13921. 10.1128/JVI.01585-07, 2168851, 17913807.
29. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000, 100:587-597. 10.1016/S0092-8674(00)80694-7, 10721995.
30. Granelli-Piperno A, Delgado E, Finkel V, Paxton W, Steinman RM. Immature dendritic cells selectively replicate macrophagetropic (M-tropic) human immunodeficiency virus type 1, while mature cells efficiently transmit both M- and T-tropic virus to T cells. J Virol 1998, 72:2733-2737. 109716, 9525591.
31. Izquierdo-Useros N, Blanco J, Erkizia I, Fernandez-Figueras MT, Borras FE, Naranjo-Gomez M, Bofill M, Ruiz L, Clotet B, Martinez-Picado J. Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission. J Virol 2007, 81:7559-7570. 10.1128/JVI.02572-06, 1933337, 17475656.
32. Yu HJ, Reuter MA, McDonald D. HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells. PLoS Pathog 2008, 4:e1000134. 10.1371/journal.ppat.1000134, 2515344, 18725936.
33. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-1371.
34. Sanders RW, de Jong EC, Baldwin CE, Schuitemaker JH, Kapsenberg ML, Berkhout B. Differential transmission of human immunodeficiency virus type 1 by distinct subsets of effector dendritic cells. J Virol 2002, 76:7812-7821. 10.1128/JVI.76.15.7812-7821.2002, 136398, 12097593.
35. Wu L, KewalRamani VN. Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 2006, 6:859-868. 10.1038/nri1960, 1796806, 17063186.
36. Rodriguez-Plata MT, Urrutia A, Cardinaud S, Buzon MJ, Izquierdo-Useros N, Prado JG, Puertas MC, Erkizia I, Coulon PG, Cedeno S. HIV-1 capture and antigen presentation by dendritic cells: enhanced viral capture does not correlate with better T cell activation. J Immunol 2012, 188:6036-6045. 10.4049/jimmunol.1200267, 22581857.
37. Wang JH, Kwas C, Wu L. Intercellular adhesion molecule 1 (ICAM-1), but not ICAM-2 and -3, is important for dendritic cell-mediated human immunodeficiency virus type 1 transmission. J Virol 2009, 83:4195-4204. 10.1128/JVI.00006-09, 2668448, 19211748.
38. Arrighi JF, Pion M, Garcia E, Escola JM, van Kooyk Y, Geijtenbeek TB, Piguet V. DC-SIGN-mediated infectious synapse formation enhances X4 HIV-1 transmission from dendritic cells to T cells. J Exp Med 2004, 200:1279-1288. 10.1084/jem.20041356, 2211914, 15545354.
39. Groot F, Kuijpers TW, Berkhout B, de Jong EC. Dendritic cell-mediated HIV-1 transmission to T cells of LAD-1 patients is impaired due to the defect in LFA-1. Retrovirology 2006, 3:75. 10.1186/1742-4690-3-75, 1635562, 17078873.
40. Tsunetsugu-Yokota Y, Yasuda S, Sugimoto A, Yagi T, Azuma M, Yagita H, Akagawa K, Takemori T. Efficient virus transmission from dendritic cells to CD4+ T cells in response to antigen depends on close contact through adhesion molecules. Virology 1997, 239:259-268. 10.1006/viro.1997.8895, 9434717.
41. Hu J, Gardner MB, Miller CJ. Simian immunodeficiency virus rapidly penetrates the cervicovaginal mucosa after intravaginal inoculation and infects intraepithelial dendritic cells. J Virol 2000, 74:6087-6095. 10.1128/JVI.74.13.6087-6095.2000, 112107, 10846092.
42. Spira AI, Marx PA, Patterson BK, Mahoney J, Koup RA, Wolinsky SM, Ho DD. Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J Exp Med 1996, 183:215-225. 10.1084/jem.183.1.215, 2192425, 8551225.
43. Hladik F, Sakchalathorn P, Ballweber L, Lentz G, Fialkow M, Eschenbach D, McElrath MJ. Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 2007, 26:257-270. 10.1016/j.immuni.2007.01.007, 1885958, 17306567.
44. Morrow G, Vachot L, Vagenas P, Robbiani M. Current concepts of HIV transmission. Curr HIV/AIDS Rep 2007, 4:29-35. 10.1007/s11904-007-0005-x, 17338858.
45. Wu L. Biology of HIV mucosal transmission. Curr Opin HIV AIDS 2008, 3:534-540. 10.1097/COH.0b013e32830634c6, 2542876, 18802490.
46. Dong C, Janas AM, Wang JH, Olson WJ, Wu L. Characterization of human immunodeficiency virus type 1 replication in immature and mature dendritic cells reveals dissociable cis- and trans-infection. J Virol 2007, 81:11352-11362. 10.1128/JVI.01081-07, 2045571, 17686876.
47. Wang JH, Janas AM, Olson WJ, Wu L. Functionally distinct transmission of human immunodeficiency virus type 1 mediated by immature and mature dendritic cells. J Virol 2007, 81:8933-8943. 10.1128/JVI.00878-07, 1951429, 17567699.
48. Garcia E, Pion M, Pelchen-Matthews A, Collinson L, Arrighi JF, Blot G, Leuba F, Escola JM, Demaurex N, Marsh M, Piguet V. HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 2005, 6:488-501. 10.1111/j.1600-0854.2005.00293.x, 15882445.
49. Whitelegg A, Barber LD. The structural basis of T-cell allorecognition. Tissue Antigens 2004, 63:101-108. 10.1111/j.1399-0039.2004.00188.x, 14705981.
50. Lindahl KF, Wilson DB. Histocompatibility antigen-activated cytotoxic T lymphocytes. II. Estimates of the frequency and specificity of precursors. J Exp Med 1977, 145:508-522. 10.1084/jem.145.3.508, 2180715, 233899.
51. Suchin EJ, Langmuir PB, Palmer E, Sayegh MH, Wells AD, Turka LA. Quantifying the frequency of alloreactive T cells in vivo: new answers to an old question. J Immunol 2001, 166:973-981.
52. Felix NJ, Allen PM. Specificity of T-cell alloreactivity. Nat Rev Immunol 2007, 7:942-953. 10.1038/nri2200, 18007679.
53. Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J Virol 2007, 81:1000-1012. 10.1128/JVI.01629-06, 1797449, 17079292.
54. Fooksman DR, Vardhana S, Vasiliver-Shamis G, Liese J, Blair DA, Waite J, Sacristan C, Victora GD, Zanin-Zhorov A, Dustin ML. Functional anatomy of T cell activation and synapse formation. Annu Rev Immunol 2010, 28:79-105. 10.1146/annurev-immunol-030409-101308, 2885351, 19968559.
55. Dustin ML, Springer TA. Role of lymphocyte adhesion receptors in transient interactions and cell locomotion. Annu Rev Immunol 1991, 9:27-66. 10.1146/annurev.iy.09.040191.000331, 1716919.
56. 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, 81:5547-5560. 10.1128/JVI.01469-06, 1900271, 17360745.
57. Blanchard N, Decraene M, Yang K, Miro-Mur F, Amigorena S, Hivroz C. Strong and durable TCR clustering at the T/dendritic cell immune synapse is not required for NFAT activation and IFN-gamma production in human CD4+ T cells. J Immunol 2004, 173:3062-3072.
58. Dellabona P, Peccoud J, Kappler J, Marrack P, Benoist C, Mathis D. Superantigens interact with MHC class II molecules outside of the antigen groove. Cell 1990, 62:1115-1121. 10.1016/0092-8674(90)90388-U, 2401011.
59. Kappler J, Kotzin B, Herron L, Gelfand EW, Bigler RD, Boylston A, Carrel S, Posnett DN, Choi Y, Marrack P. V beta-specific stimulation of human T cells by staphylococcal toxins. Science 1989, 244:811-813. 10.1126/science.2524876, 2524876.
60. Grossman Z, Meier-Schellersheim M, Paul WE, Picker LJ. Pathogenesis of HIV infection: what the virus spares is as important as what it destroys. Nat Med 2006, 12:289-295. 10.1038/nm1380, 16520776.
61. Stevenson M, Stanwick TL, Dempsey MP, Lamonica CA. HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J 1990, 9:1551-1560. 551849, 2184033.
62. St Gelais C, Coleman CM, Wang JH, Wu L. HIV-1 Nef enhances dendritic cell-mediated viral transmission to CD4+ T cells and promotes T-cell activation. PLoS One 2012, 7:e34521. 10.1371/journal.pone.0034521, 3316695, 22479639.
63. Douek DC, Brenchley JM, Betts MR, Ambrozak DR, Hill BJ, Okamoto Y, Casazza JP, Kuruppu J, Kunstman K, Wolinsky S. HIV preferentially infects HIV-specific CD4+ T cells. Nature 2002, 417:95-98. 10.1038/417095a, 11986671.
64. Lore K, Smed-Sorensen A, Vasudevan J, Mascola JR, Koup RA. Myeloid and plasmacytoid dendritic cells transfer HIV-1 preferentially to antigen-specific CD4+ T cells. J Exp Med 2005, 201:2023-2033. 10.1084/jem.20042413, 2212038, 15967828.
65. McNeil AC, Shupert WL, Iyasere CA, Hallahan CW, Mican JA, Davey RT, Connors M. High-level HIV-1 viremia suppresses viral antigen-specific CD4(+) T cell proliferation. Proc Natl Acad Sci U S A 2001, 98:13878-13883. 10.1073/pnas.251539598, 61135, 11717444.
66. Montoya MC, Sancho D, Bonello G, Collette Y, Langlet C, He HT, Aparicio P, Alcover A, Olive D, Sanchez-Madrid F. Role of ICAM-3 in the initial interaction of T lymphocytes and APCs. Nat Immunol 2002, 3:159-168.
67. Wang JH, Wells C, Wu L. Macropinocytosis and cytoskeleton contribute to dendritic cell-mediated HIV-1 transmission to CD4+ T cells. Virology 2008, 381:143-154. 10.1016/j.virol.2008.08.028, 2575140, 18804253.
68. Bachmann MF, McKall-Faienza K, Schmits R, Bouchard D, Beach J, Speiser DE, Mak TW, Ohashi PS. Distinct roles for LFA-1 and CD28 during activation of naive T cells: adhesion versus costimulation. Immunity 1997, 7:549-557. 10.1016/S1074-7613(00)80376-3, 9354475.
69. Groot F, van Capel TM, Schuitemaker J, Berkhout B, de Jong EC. Differential susceptibility of naive, central memory and effector memory T cells to dendritic cell-mediated HIV-1 transmission. Retrovirology 2006, 3:52. 10.1186/1742-4690-3-52, 1562438, 16916447.
70. Baba M, Miyake H, Okamoto M, Iizawa Y, Okonogi K. Establishment of a CCR5-expressing T-lymphoblastoid cell line highly susceptible to R5 HIV type 1. AIDS Res Hum Retroviruses 2000, 16:935-941. 10.1089/08892220050058344, 10890354.
71. 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, 279:51305-51314. 10.1074/jbc.M408547200, 15371410.
72. Blanco J, Barretina J, Clotet B, Este JA. R5 HIV gp120-mediated cellular contacts induce the death of single CCR5-expressing CD4 T cells by a gp41-dependent mechanism. J Leukoc Biol 2004, 76:804-811. 10.1189/jlb.0204100, 15258189.
73. Lampe M, Briggs JA, Endress T, Glass B, Riegelsberger S, Krausslich HG, Lamb DC, Brauchle C, Muller B. Double-labelled HIV-1 particles for study of virus-cell interaction. Virology 2007, 360:92-104. 10.1016/j.virol.2006.10.005, 17097708.
74. O'Brien WA, Koyanagi Y, Namazie A, Zhao JQ, Diagne A, Idler K, Zack JA, Chen IS. HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature 1990, 348:69-73. 10.1038/348069a0, 2172833.
75. Garcia-Perez J, Sanchez-Palomino S, Perez-Olmeda M, Fernandez B, Alcami J. A new strategy based on recombinant viruses as a tool for assessing drug susceptibility of human immunodeficiency virus type 1. J Med Virol 2007, 79:127-137. 10.1002/jmv.20770, 17177310.
76. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, Koutsoukos M, Voss G, Goepfert P, Gilbert P, Greene KM. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol 2005, 79:10108-10125. 10.1128/JVI.79.16.10108-10125.2005, 1182643, 16051804.