Human immunodeficiency virus type 1 envelope gp120-induced partial T-cell receptor signaling creates an F-actin-depleted zone in the virological synapse

Journal of Virology

Volumn 83, Issue 21, 2009, Pages 11341-11355

  Vasiliver Shamis, Gaia ^a   Cho, Michael W ^b   Hioe, Catarina E ^a   Dustin, Michael L ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD69 ANTIGEN; F ACTIN; GLYCOPROTEIN GP 120; LAT PROTEIN; PROTEIN KINASE FYN; PROTEIN KINASE LCK; PROTEIN KINASE ZAP 70; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR; VIRUS ENVELOPE PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; PROTEIN INTERACTION; T LYMPHOCYTE ACTIVATION;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIGENS, CD3; CD4-POSITIVE T-LYMPHOCYTES; CELL MEMBRANE; CELLS, CULTURED; ENZYME ACTIVATION; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; INTERCELLULAR JUNCTIONS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MEMBRANE PROTEINS; PHOSPHOLIPASE C GAMMA; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-FYN; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; VIRUS INTERNALIZATION; ZAP-70 PROTEIN-TYROSINE KINASE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 70350317465     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01440-09     Document Type: Article

References (76)

1. Arthos, J., C. Cicala, E. Martinelli, K. Macleod, D. Van Ryk, D. Wei, Z. Xiao, T. D. Veenstra, T. P. Conrad, R. A. Lempicki, S. McLaughlin, M. Pascuccio, R. Gopaul, J. McNally, C. C. Cruz, N. Censoplano, E. Chung, K. N. Reitano, S. Kottilil, D. J. Goode, and A. S. Fauci. 2008. HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat. Immunol. 9:301-309.
2. Barda-Saad, M., A. Braiman, R. Titerence, S. C. Bunnell, V. A. Barr, and L. E. Samelson. 2005. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat. Immunol. 6:80-89.
3. Barrero-Villar, M., J. R. Cabrero, M. Gordon-Alonso, J. Barroso-Gonzalez, S. Alvarez-Losada, M. A. Munoz-Fernandez, F. Sanchez-Madrid, and A. Valenzuela-Fernandez. 2009. Moesin is required for HIV-1-induced CD4-CXCR4 interaction, F-actin redistribution, membrane fusion and viral infection in lymphocytes. J. Cell Sci. 122:103-113.
4. Berg, L. J., L. D. Finkelstein, J. A. Lucas, and P. L. Schwartzberg. 2005. Tec family kinases in T lymphocyte development and function. Annu. Rev. Immunol. 23:549-600.
5. Bhaskar, P. T., and N. Hay. 2007. The two TORCs and Akt. Dev. Cell 12:487-502.
6. 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 (gp120). Virology 268:329-344. (Pubitemid 30159982)
7. Blanco, J., J. Barretina, B. Clotet, and J. A. Este. 2004. R5 HIV gp120-mediated cellular contacts induce the death of single CCR5-expressing CD4 T cells by a gp41-dependent mechanism. J. Leukoc. Biol. 76:804-811.
8. Bosch, B., B. Grigorov, J. Senserrich, B. Clotet, J. L. Darlix, D. Muriaux, and J. A. Este. 2008. A clathrin-dynamin-dependent endocytic pathway for the uptake of HIV-1 by direct T cell-T cell transmission. Antivir. Res. 80:185-193.
9. Bubeck Wardenburg, J., R. Pappu, J. Y. Bu, B. Mayer, J. Chernoff, D. Straus, and A. C. Chan. 1998. Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity 9:607-616. (Pubitemid 28557589)
10. Campi, G., R. Varma, and M. L. Dustin. 2005. Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J. Exp. Med. 202:1031-1036.
11. Cemerski, S., J. Das, E. Giurisato, M. A. Markiewicz, P. M. Allen, A. K. Chakraborty, and A. S. Shaw. 2008. The balance between T cell receptor signaling and degradation at the center of the immunological synapse is determined by antigen quality. Immunity 29:414-422.
12. Chan, T. O., S. E. Rittenhouse, and P. N. Tsichlis. 1999. AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Annu. Rev. Biochem. 68:965-1014.
13. Chen, P., W. Hubner, M. A. Spinelli, and B. K. Chen. 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582-12595. (Pubitemid 350085872)
14. Chirathaworn, C., S. A. Tibbetts, M. A. Chan, and S. H. Benedict. 1995. Cross-linking of ICAM-1 on T cells induces transient tyrosine phosphorylation and inactivation of cdc2 kinase. J. Immunol. 155:5479-5482.
15. Cho, M. W., Y. B. Kim, M. K. Lee, K. C. Gupta, W. Ross, R. Plishka, A. Buckler-White, T. Igarashi, T. Theodore, R. Byrum, C. Kemp, D. C. Montefiori, and M. A. Martin. 2001. Polyvalent envelope glycoprotein vaccine elicits a broader neutralizing antibody response but is unable to provide sterilizing protection against heterologous simian/human immunodeficiency virus infection in pigtailed macaques. J. Virol. 75:2224-2234.
16. + T-cells. Virology 345:105-114.
17. Cicala, C., J. Arthos, E. Martinelli, N. Censoplano, C. C. Cruz, E. Chung, S. M. Selig, D. Van Ryk, J. Yang, S. Jagannatha, T. W. Chun, P. Ren, R. A. Lempicki, and A. S. Fauci. 2006. R5 and X4 HIV envelopes induce distinct gene expression profiles in primary peripheral blood mononuclear cells. Proc. Natl. Acad. Sci. USA 103:3746-3751.
18. + T cells. Proc. Natl. Acad. Sci. USA 97:1178-1183.
19. + T cells by macrophage-tropic HIV envelope. J. Immunol. 163:420-426.
20. Cicala, C., J. Arthos, S. M. Selig, G. Dennis, Jr., D. A. Hosack, D. Van Ryk, M. L. Spangler, T. D. Steenbeke, P. Khazanie, N. Gupta, J. Yang, M. Daucher, R. A. Lempicki, and A. S. Fauci. 2002. HIV envelope induces a cascade of cell signals in non-proliferating target cells that favor virus replication. Proc. Natl. Acad. Sci. USA 99:9380-9385.
21. 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.
22. Del Corno, M., Q. H. Liu, D. Schols, E. de Clercq, S. Gessani, B. D. Freedman, and R. G. Collman. 2001. HIV-1 gp120 and chemokine activation of Pyk2 and mitogen-activated protein kinases in primary macrophages me- diated by calcium-dependent, pertussis toxin-insensitive chemokine receptor signaling. Blood 98:2909-2916.
23. Dimitrov, D. S., R. L. 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. (Pubitemid 23088394)
24. Dustin, M. L. 2008. T-cell activation through immunological synapses and kinapses. Immunol. Rev. 221:77-89.
25. Dustin, M. L., and T. A. Springer. 1988. Lymphocyte function-associated antigen-1 (LFA-1) interaction with intercellular adhesion molecule-1 (ICAM-1) is one of at least three mechanisms for lymphocyte adhesion to cultured endothelial cells. J. Cell Biol. 107:321-331.
26. Edinger, A. L., J. E. Clements, and R. W. Doms. 1999. Chemokine and orphan receptors in HIV-2 and SIV tropism and pathogenesis. Virology 260:211-221.
27. + T lymphocytes and macrophages. J. Virol. 77:2539-2549.
28. Freiberg, B. A., H. Kupfer, W. Maslanik, J. Delli, J. Kappler, D. M. Zaller, and A. Kupfer. 2002. Staging and resetting T cell activation in SMACs. Nat. Immunol. 3:911-917.
29. Geiger, B., D. Rosen, and G. Berke. 1982. Spatial relationships of microtubule-organizing centers and the contact area of cytotoxic T lymphocytes and target cells. J. Cell Biol. 95:137-143. (Pubitemid 13197083)
30. Giguère, J. F., S. Bounou, J. S. Paquette, J. Madrenas, and M. J. Tremblay. 2004. Insertion of host-derived costimulatory molecules CD80 (B7.1) and CD86 (B7.2) into human immunodeficiency virus type 1 affects the virus life cycle. J. Virol. 78:6222-6232.
31. Giguere, J. F., J. Diou, J. Madrenas, and M. J. Tremblay. 2005. Virus attachment and replication are promoted after acquisition of host CD28 and CD152 by HIV-1. J. Infect. Dis. 192:1265-1268.
32. Goldberg, D. R., T. Butz, M. G. Cardozo, R. J. Eckner, A. Hammach, J. Huang, S. Jakes, S. Kapadia, M. Kashem, S. Lukas, T. M. Morwick, M. Panzenbeck, U. Patel, S. Pav, G. W. Peet, J. D. Peterson, A. S. Prokopowicz III, R. J. Snow, R. Sellati, H. Takahashi, J. Tan, M. A. Tschantz, X. J. Wang, Y. Wang, J. Wolak, P. Xiong, and N. Moss. 2003. Optimization of 2-phenylaminoimidazo[4,5-h] isoquinolin-9-ones: orally active inhibitors of lck kinase. J. Med. Chem. 46:1337-1349.
33. Gomez, T. S., and D. D. Billadeau. 2008. T cell activation and the cytoskeleton: you can't have one without the other. Adv. Immunol. 97:1-64.
34. Hermida-Matsumoto, L., and M. D. Resh. 2000. Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J. Virol. 74:8670-8679. (Pubitemid 30666717)
35. Holdorf, A. D., K. H. Lee, W. R. Burack, P. M. Allen, and A. S. Shaw. 2002. Regulation of Lck activity by CD4 and CD28 in the immunological synapse. Nat. Immunol. 3:259-264.
36. Hubner, W., G. P. McNerney, P. Chen, B. M. Dale, R. E. Gordon, F. Y. Chuang, X. D. Li, D. M. Asmuth, T. Huser, and B. K. Chen. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743-1747.
37. Huppa, J. B., and M. M. Davis. 2003. T-cell-antigen recognition and the immunological synapse. Nat. Rev. Immunol. 3:973-983.
38. Izzard, C. S., and L. R. Lochner. 1976. Cell-to-substrate contacts in living fibroblasts: an interference reflexion study with an evaluation of the technique. J. Cell Sci. 21:129-159.
39. Ji, W. T., and H. J. Liu. 2008. PI3K-Akt signaling and viral infection. Recent Patents Biotechnol. 2:218-226.
40. Jimenez-Baranda, S., C. Gomez-Mouton, A. Rojas, L. Martinez-Prats, E. Mira, R. Ana Lacalle, A. Valencia, D. S. Dimitrov, A. Viola, R. Delgado, A. C. Martinez, and S. Manes. 2007. Filamin-A regulates actin-dependent clustering of HIV receptors. Nat. Cell Biol. 9:838-846.
41. Jolly, C., K. Kashefi, M. Hollinshead, and Q. J. Sattentau. 2004. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 199:283-293.
42. Jolly, C., I. Mitar, and Q. J. Sattentau. 2007. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J. Virol. 81:5547-5560. (Pubitemid 46846995)
43. Kaizuka, Y., A. D. Douglass, R. Varma, M. L. Dustin, and R. D. Vale. 2007. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. Proc. Natl. Acad. Sci. USA 104:20296-20301.
44. Krogsgaard, M., Q. J. Li, C. Sumen, J. B. Huppa, M. Huse, and M. M. Davis. 2005. Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 434:238-243. (Pubitemid 40388057)
45. Kumar, A., T. D. Humphreys, K. N. Kremer, P. S. Bramati, L. Bradfield, C. E. Edgar, and K. E. Hedin. 2006. CXCR4 physically associates with the T cell receptor to signal in T cells. Immunity 25:213-224. (Pubitemid 44224150)
46. Kupfer, A., G. Dennert, and S. J. Singer. 1983. Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc. Natl. Acad. Sci. USA 80:7224-7228.
47. Lee, C., Q. H. Liu, B. Tomkowicz, Y. Yi, B. D. Freedman, and R. G. Collman. 2003. Macrophage activation through CCR5- and CXCR4-mediated gp120-elicited signaling pathways. J. Leukoc. Biol. 74:676-682.
48. Lee, C., B. Tomkowicz, B. D. Freedman, and R. G. Collman. 2005. HIV-1 gp120-induced TNF-α production by primary human macrophages is mediated by phosphatidylinositol-3 (PI-3) kinase and mitogen-activated protein (MAP) kinase pathways. J. Leukoc. Biol. 78:1016-1023.
49. Lee, K. H., A. D. Holdorf, M. L. Dustin, A. C. Chan, P. M. Allen, and A. S. Shaw. 2002. T cell receptor signaling precedes immunological synapse formation. Science 295:1539-1542.
50. Liu, D., Y. T. Bryceson, T. Meckel, G. Vasiliver-Shamis, M. L. Dustin, and E. O. Long. 2009. Integrin-dependent organization and bidirectional vesicular traffic at cytotoxic immune synapses. Immunity 31:99-109.
51. Liu, Y., N. V. Belkina, and S. Shaw. 2009. HIV infection of T cells: actin-in and actin-out. Sci. Signal. 2:pe23.
52. McDonald, D., L. Wu, S. M. Bohks, V. N. KewalRamani, D. Unutmaz, and T. J. Hope. 2003. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300:1295-1297. (Pubitemid 36618241)
53. Melar, M., D. E. Ott, and T. J. Hope. 2007. Physiological levels of virion-associated human immunodeficiency virus type 1 envelope induce coreceptor-dependent calcium flux. J. Virol. 81:1773-1785. (Pubitemid 46214451)
54. Mittler, R. S., S. J. Goldman, G. L. Spitalny, and S. J. Burakoff. 1989. T-cell receptor-CD4 physical association in a murine T-cell hybridoma: induction by antigen receptor ligation. Proc. Natl. Acad. Sci. USA 86:8531-8535.
55. Miyauchi, K., Y. Kim, O. Latinovic, V. Morozov, and G. B. Melikyan. 2009. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137:433-444.
56. Molina, L., M. Grimaldi, V. Robert-Hebmann, L. Espert, M. Varbanov, C. Devaux, C. Granier, and M. Biard-Piechaczyk. 2007. Proteomic analysis of the cellular responses induced in uninfected immune cells by cell-expressed X4 HIV-1 envelope. Proteomics 7:3116-3130. (Pubitemid 47477955)
57. Monks, C. R., B. A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395:82-86.
58. O'Shea, J. J., J. A. Johnston, J. Kehrl, G. Koretzky, and L. E. Samelson. 2001. Key molecules involved in receptor-mediated lymphocyte activation. In Current protocols in immunology. Chapter 11, unit 119A. Wiley Interscience, Hoboken, NJ.
59. Pearce-Pratt, R., D. Malamud, and D. M. Phillips. 1994. Role of the cytoskeleton in cell-to-cell transmission of human immunodeficiency virus. J. Virol. 68:2898-2905. (Pubitemid 24129737)
60. Porter, M., T. Schindler, J. Kuriyan, and W. T. Miller. 2000. Reciprocal regulation of Hck activity by phosphorylation of Tyr(527) and Tyr(416). Effect of introducing a high affinity intramolecular SH2 ligand. J. Biol. Chem. 275:2721-2726.
61. Rudnicka, D., J. Feldmann, F. Porrot, S. Wietgrefe, S. Guadagnini, M. C. Prevost, J. Estaquier, A. Haase, N. Sol-Foulon, and O. Schwartz. 2009. Simultaneous human immunodeficiency virus cell-to-cell transmission to multiple targets through polysynapses. J. Virol. 83:6234-6246.
62. Schmoranzer, J., M. Goulian, D. Axelrod, and S. M. Simon. 2000. Imaging constitutive exocytosis with total internal reflection fluorescence microscopy. J. Cell Biol. 149:23-32. (Pubitemid 30196696)
63. Sedwick, C. E., M. M. Morgan, L. Jusino, J. L. Cannon, J. Miller, and J. K. Burkhardt. 1999. TCR, LFA-1, and CD28 play unique and complementary roles in signaling T cell cytoskeletal reorganization. J. Immunol. 162:1367-1375.
64. Sims, T. N., T. J. Soos, H. S. Xenias, B. Dubin-Thaler, J. M. Hofman, J. C. Waite, T. O. Cameron, V. K. Thomas, R. Varma, C. H. Wiggins, M. P. Sheetz, D. R. Littman, and M. L. Dustin. 2007. Opposing effects of PKCtheta and WASp on symmetry breaking and relocation of the immunological synapse. Cell 129:773-785.
65. Sourisseau, M., N. Sol-Foulon, F. Porrot, F. Blanchet, and O. Schwartz. 2007. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J. Virol. 81:1000-1012. (Pubitemid 46067924)
66. Sowinski, S., C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Kohler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis. 2008. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10:211-219.
67. Stevenson, M. 2003. HIV-1 pathogenesis. Nat. Med. 9:853-860.
68. Stinchcombe, J. C., E. Majorovits, G. Bossi, S. Fuller, and G. M. Griffiths. 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443:462-465.
69. Unutmaz, D., V. N. KewalRamani, S. Marmon, and D. R. Littman. 1999. Cytokine signals are sufficient for HIV-1 infection of resting human T lymphocytes. J. Exp. Med. 189:1735-1746.
70. Varbanov, M., L. Espert, and M. Biard-Piechaczyk. 2006. Mechanisms of CD4 T-cell depletion triggered by HIV-1 viral proteins. AIDS Rev. 8:221-236. (Pubitemid 46138920)
71. Varma, R., G. Campi, T. Yokosuka, T. Saito, and M. L. Dustin. 2006. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25:117-127. (Pubitemid 44066825)
72. + T cells. J. Virol. 82:9445-9457.
73. Weissman, D., R. L. Rabin, J. Arthos, A. Rubbert, M. Dybul, R. Swofford, S. Venkatesan, J. M. Farber, and A. S. Fauci. 1997. Macrophage-tropic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor. Nature 389:981-985. (Pubitemid 27485691)
74. Yoder, A., D. Yu, L. Dong, S. R. Iyer, X. Xu, J. Kelly, J. Liu, W. Wang, P. J. Vorster, L. Agulto, D. A. Stephany, J. N. Cooper, J. W. Marsh, and Y. Wu. 2008. HIV envelope-CXCR4 signaling activates cofilin to overcome cortical actin restriction in resting CD4 T cells. Cell 134:782-792.
75. Yokosuka, T., K. Sakata-Sogawa, W. Kobayashi, M. Hiroshima, A. Hashimoto-Tane, M. Tokunaga, M. L. Dustin, and T. Saito. 2005. Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 6:1253-1262.
76. Zhu, P., J. Liu, J. Bess, Jr., E. Chertova, J. D. Lifson, H. Grise, G. A. Ofek, K. A. Taylor, and K. H. Roux. 2006. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441:847-852. (Pubitemid 43910414)