Engagement of the CD4 receptor affects the redistribution of Lck to the immunological synapse in primary T cells: Implications for T-cell activation during human immunodeficiency virus type 1 infection

Journal of Virology

Volumn 83, Issue 3, 2009, Pages 1193-1200

  Nyakeriga, Alice M ^a   Fichtenbaum, Carl J ^b   Goebel, Jens ^a   Nicolaou, Stella A ^b   Conforti, Laura ^b   Chougnet, Claire A ^a,c  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIBODY; CD4 ANTIGEN; F ACTIN; GLYCOPROTEIN GP 120; PROTEIN KINASE LCK;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME INHIBITION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOSTIMULATION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SYNAPSE; T LYMPHOCYTE ACTIVATION;

ACTINS; ANTIGENS, CD4; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CD4-POSITIVE T-LYMPHOCYTES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOLOGICAL SYNAPSES; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK);

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 59749088570     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01023-08     Document Type: Article

References (69)

1. Algeciras, A., D. H. Dockrell, D. H. Lynch, and C. V. Paya. 1998. CD4 regulates susceptibility to Fas ligand- and tumor necrosis factor-mediated apoptosis. J. Exp. Med. 187:711-720.
2. Amadori, A., G. De Silvestro, R. Zamarchi, M. L. Veronese, M. R. Mazza, G. Schiavo, M. Panozzo, A. De Rossi, L. Ometto, J. Mous, et al. 1992. CD4 epitope masking by gp120/anti-gp120 antibody complexes. A potential mechanism for CD4+ cell function down-regulation in AIDS patients. J. Immunol. 148:2709-2716.
3. Babiychuk, E. B., and A. Draeger. 2006. Biochemical characterization of detergent-resistant membranes: a systematic approach. Biochem. J. 397:407-416.
4. Baldari, C. T., E. Milia, M. M. Di Somma, F. Baldoni, S. Valitutti, and J. L. Telford. 1995. Distinct signaling properties identify functionally different CD4 epitopes. Eur. J. Immunol. 25:1843-1850.
5. Banda, N. K., J. Bernier, D. K. Kurahara, R. Kurrle, N. Haigwood, R. P. Sekaly, and T. H. Finkel. 1992. Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J. Exp. Med. 176:1099-1106.
6. Bonnard, M., L. Haughn, and M. Julius. 1999. CD4-mediated inhibiton of IL-2 production in activated T cells. J. Immunol. 162:1252-1260.
7. Bonnard, M., C. R. Maroun, and M. Julius. 1997. Physical association of CD4 and CD45 in primary, resting CD4 T cells. Cell Immunol. 175:1-11.
8. Brenchley, J. M., D. A. Price, and D. C. Douek. 2006. HIV disease: fallout from a mucosal catastrophe? Nat. Immunol. 7:235-239.
9. Cefai, D., P. Debre, M. Kaczorek, T. Idziorek, B. Autran, and G. Bismuth. 1990. Human immunodeficiency virus-1 glycoproteins gp120 and gp160 specifically inhibit the CD3/T cell-antigen receptor phosphoinositide transduction pathway. J. Clin. Investig. 86:2117-2124.
10. Cefai, D., M. Ferrer, N. Serpente, T. Idziorek, A. Dautry-Varsat, P. Debre, and G. Bismuth. 1992. Internalization of HIV glycoprotein gp120 is associated with down-modulation of membrane CD4 and p56lck together with impairment of T cell activation. J. Immunol. 149:285-294.
11. Chirmule, N., T. W. McCloskey, R. Hu, V. S. Kalyanaraman, and S. Pahwa. 1995. HIV gp120 inhibits T cell activation by interfering with expression of costimulatory molecules CD40 ligand and CD80 (B71). J. Immunol. 155:917-924.
12. Cruikshank, W. W., K. Lim, A. C. Theodore, J. Cook, G. Fine, P. F. Weller, and D. M. Center. 1996. IL-16 inhibition of CD3-dependent lymphocyte activation and proliferation. J. Immunol. 157:5240-5248.
13. Dalgleish, A. G., P. C. Beverley, P. R. Clapham, D. H. Crawford, M. F. Greaves, and R. A. Weiss. 1984. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312:763-767.
14. 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.
15. Dustin, M. L., and J. A. Cooper. 2000. The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat. Immunol. 1:23-29.
16. Ehrlich, L. I., P. J. Ebert, M. F. Krummel, A. Weiss, and M. M. Davis. 2002. Dynamics of p56lck translocation to the T cell immunological synapse following agonist and antagonist stimulation. Immunity 17:809-822.
17. Fackler, O. T., and H. G. Krausslich. 2006. Interactions of human retroviruses with the host cell cytoskeleton. Curr. Opin. Microbiol. 9:409-415.
18. Fehervari, Z., A. Cooke, S. Brett, and J. Turner. 2002. Perturbation of naive TCR transgenic T cell functional responses and upstream activation events by anti-CD4 monoclonal antibodies. Eur. J. Immunol. 32:333-340.
19. Fernando, K., H. Hu, H. Ni, J. A. Hoxie, and D. Weissman. 2007. Vaccine-delivered HIV envelope inhibits CD4(+) T-cell activation, a mechanism for poor HIV vaccine responses. Blood 109:2538-2544.
20. Filipp, D., B. L. Leung, J. Zhang, A. Veillette, and M. Julius. 2004. Enrichment of lck in lipid rafts regulates colocalized fyn activation and the initiation of proximal signals through TCR alpha beta. J. Immunol. 172:4266-4274.
21. Giurisato, E., D. P. McIntosh, M. Tassi, A. Gamberucci, and A. Benedetti. 2003. T cell receptor can be recruited to a subset of plasma membrane rafts, independently of cell signaling and attendantly to raft clustering. J. Biol. Chem. 278:6771-6778.
22. Glaichenhaus, N., N. Shastri, D. R. Littman, and J. M. Turner. 1991. Requirement for association of p56lck with CD4 in antigen-specific signal transduction in T cells. Cell 64:511-520.
23. Goebel, J., K. Forrest, L. Morford, and T. L. Roszman. 2002. Differential localization of IL-2- and -15 receptor chains in membrane rafts of human T cells. J. Leukoc. Biol. 72:199-206.
24. Goebel, J., B. Logan, K. Forrest, A. Mieczkowski, T. L. Roszman, and M. Wills-Karp. 2005. Atorvastatin affects interleukin-2 signaling by altering the lipid raft enrichment of the interleukin-2 receptor beta chain. J. Investig. Med. 53:322-328.
25. Goldman, F., J. Crabtree, C. Hollenback, and G. Koretzky. 1997. Sequestration of p56(lck) by gp120, a model for TCR desensitization. J. Immunol. 158:2017-2024.
26. Goldman, F., W. A. Jensen, G. L. Johnson, L. Heasley, and J. C. Cambier. 1994. gp120 ligation of CD4 induces p56lck activation and TCR desensitization independent of TCR tyrosine phosphorylation. J. Immunol. 153:2905-2917.
27. Gomez, T. S., M. J. Hamann, S. McCarney, D. N. Savoy, C. M. Lubking, M. P. Heldebrant, C. M. Labno, D. J. McKean, M. A. McNiven, J. K. Burkhardt, and D. D. Billadeau. 2005. Dynamin 2 regulates T cell activation by controlling actin polymerization at the immunological synapse. Nat. Immunol. 6:261-270.
28. Grakoui, A., S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285:221-227.
29. Habeshaw, J. A., A. G. Dalgleish, L. Bountiff, A. L. Newell, D. Wilks, L. C. Walker, and F. Manca. 1990. AIDS pathogenesis: HIV envelope and its interaction with cell proteins. Immunol. Today 11:418-425.
30. Haller, C., S. Rauch, and O. T. Fackler. 2007. HIV-1 Nef employs two distinct mechanisms to modulate Lck subcellular localization and TCR induced actin remodeling. PLoS ONE 2:e1212.
31. Hazenberg, M. D., S. A. Otto, B. H. van Benthem, M. T. Roos, R. A. Coutinho, J. M. Lange, D. Hamann, M. Prins, and F. Miedema. 2003. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 17:1881-1888.
32. 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.
33. Hu, H., K. Fernando, H. Ni, and D. Weissman. 2008. HIV envelope suppresses CD4+ T cell activation independent of T regulatory cells. J. Immunol. 180:5593-5600.
34. Huang, Y., and J. K. Burkhardt. 2007. T-cell-receptor-dependent actin regulatory mechanisms. J. Cell Sci. 120:723-730.
35. Igakura, T., J. C. Stinchcombe, P. K. Goon, G. P. Taylor, J. N. Weber, G. M. Griffiths, Y. Tanaka, M. Osame, and C. R. Bangham. 2003. Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299:1713-1716.
36. 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.
37. 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.
38. 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.
39. Jolly, C., and Q. J. Sattentau. 2005. Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity. J. Virol. 79:12088-12094.
40. Jolly, C., and Q. J. Sattentau. 2004. Retroviral spread by induction of virological synapses. Traffic 5:643-650.
41. Jones, M. V., J. E. Bell, and A. Nath. 2000. Immunolocalization of HIV envelope gp120 in HIV encephalitis with dementia. AIDS 14:2709-2713.
42. Kanner, S. B., and O. K. Haffar. 1995. HIV-1 down-regulates CD4 costimulation of TCR/CD3-directed tyrosine phosphorylation through CD4/p56lck dissociation. J. Immunol. 154:2996-3005.
43. Kusumi, A., H. Ike, C. Nakada, K. Murase, and T. Fujiwara. 2005. Single-molecule tracking of membrane molecules: plasma membrane compartmentalization and dynamic assembly of raft-philic signaling molecules. Semin. Immunol. 17:3-21.
44. Levy, J. A. 1993. Pathogenesis of human immunodeficiency virus infection. Microbiol. Rev. 57:183-289.
45. Lu, T. C., J. C. He, Z. H. Wang, X. Feng, T. Fukumi-Tominaga, N. Chen, J. Xu, R. Iyengar, and P. E. Klotman. 2008. HIV-1 Nef disrupts the podocyte actin cytoskeleton by interacting with diaphanous interacting protein. J. Biol. Chem. 283:8173-8182.
46. Manca, F., J. A. Habeshaw, and A. G. Dalgleish. 1990. HIV envelope glycoprotein, antigen specific T-cell responses, and soluble CD4. Lancet 335:811-815.
47. Mittler, R. S., and M. K. Hoffmann. 1989. Synergism between HIV gp120 and gp120-specific antibody in blocking human T cell activation. Science 245:1380-1382.
48. Moanna, A., R. Dunham, M. Paiardini, and G. Silvestri. 2005. CD4+ T-cell depletion in HIV infection: killed by friendly fire? Curr. HIV/AIDS Rep. 2:16-23.
49. Mukherjee, A., L. Arnaud, and J. A. Cooper. 2003. Lipid-dependent recruitment of neuronal Src to lipid rafts in the brain. J. Biol. Chem. 278:40806-40814.
50. Nicolaou, S. A., P. Szigligeti, L. Neumeier, S. M. Lee, H. J. Duncan, S. K. Kant, A. B. Mongey, A. H. Filipovich, and L. Conforti. 2007. Altered dynamics of Kv1.3 channel compartmentalization in the immunological synapse in systemic lupus erythematosus. J. Immunol. 179:346-356.
51. Oh, S. K., W. W. Cruikshank, J. Raina, G. C. Blanchard, W. H. Adler, J. Walker, and H. Kornfeld. 1992. Identification of HIV-1 envelope glycoprotein in the serum of AIDS and ARC patients. J. Acquir. Immune Defic. Syndr. 5:251-256.
52. Paiardini, M., I. Frank, I. Pandrea, C. Apetrei, and G. Silvestri. 2008. Mucosal immune dysfunction in AIDS pathogenesis. AIDS Rev. 10:36-46.
53. Pantaleo, G., C. Graziosi, J. F. Demarest, L. Butini, M. Montroni, C. H. Fox, J. M. Orenstein, D. P. Kotler, and A. S. Fauci. 1993. HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature 362:355-358.
54. 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.
55. Picker, L. J. 2006. Immunopathogenesis of acute AIDS virus infection. Curr. Opin. Immunol. 18:399-405.
56. Rossio, J. L., M. T. Esser, K. Suryanarayana, D. K. Schneider, J. W. Bess, Jr., G. M. Vasquez, T. A. Wiltrout, E. Chertova, M. K. Grimes, Q. Sattentau, L. O. Arthur, L. E. Henderson, and J. D. Lifson. 1998. Inactivation of human immunodeficiency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins. J. Virol. 72:7992-8001.
57. Ruegg, C. L., and E. G. Engleman. 1990. Impaired immunity in AIDS. The mechanisms responsible and their potential reversal by antiviral therapy. Ann. N. Y. Acad. Sci. 616:307-317.
58. Ruegg, C. L., C. R. Monell, and M. Strand. 1989. Inhibition of lymphoproliferation by a synthetic peptide with sequence identity to gp41 of human immunodeficiency virus type 1. J. Virol. 63:3257-3260.
59. Shearer, G. M., D. C. Bernstein, K. S. Tung, C. S. Via, R. Redfield, S. Z. Salahuddin, and R. C. Gallo. 1986. A model for the selective loss of major histocompatibility complex self-restricted T cell immune responses during the development of acquired immune deficiency syndrome (AIDS). J. Immunol. 137:2514-2521.
60. Tavano, R., G. Gri, B. Molon, B. Marinari, C. E. Rudd, L. Tuosto, and A. Viola. 2004. CD28 and lipid rafts coordinate recruitment of Lck to the immunological synapse of human T lymphocytes. J. Immunol. 173:5392-5397.
61. Thoulouze, M. I., N. Sol-Foulon, F. Blanchet, A. Dautry-Varsat, O. Schwartz, and A. Alcover. 2006. Human immunodeficiency virus type-1 infection impairs the formation of the immunological synapse. Immunity 24:547-561.
62. Turner, J. M., M. H. Brodsky, B. A. Irving, S. D. Levin, R. M. Perlmutter, and D. R. Littman. 1990. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell 60:755-765.
63. Van Drenth, C., A. Jenkins, L. Ledwich, T. C. Ryan, M. V. Mashikian, W. Brazer, D. M. Center, and W. W. Cruikshank. 2000. Desensitization of CXC chemokine receptor 4, mediated by IL-16/CD4, is independent of p56lck enzymatic activity. J. Immunol. 165:6356-6363.
64. Wang, M. W., S. Wei, R. Faccio, S. Takeshita, P. Tebas, W. G. Powderly, S. L. Teitelbaum, and F. P. Ross. 2004. The HIV protease inhibitor ritonavir blocks osteoclastogenesis and function by impairing RANKL-induced signaling. J. Clin. Investig. 114:206-213.
65. Weinhold, K. J., H. K. Lyerly, S. D. Stanley, A. A. Austin, T. J. Matthews, and D. P. Bolognesi. 1989. HIV-1 GP120-mediated immune suppression and lymphocyte destruction in the absence of viral infection. J. Immunol. 142:3091-3097.
66. Wulfing, C., and M. M. Davis. 1998. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282:2266-2269.
67. Zamoyska, R., A. Basson, A. Filby, G. Legname, M. Lovatt, and B. Seddon. 2003. The influence of the src-family kinases, Lck and Fyn, on T cell differentiation, survival and activation. Immunol. Rev. 191:107-118.
68. + cells and overexpression of CTLA-4 are linked to loss of antigen-specific CD4 T cells during primary human immunodeficiency virus type 1 infection. J. Virol. 80:10162-10172.
69. Zhang, R., C. J. Fichtenbaum, D. A. Hildeman, J. D. Lifson, and C. Chougnet. 2004. CD40 ligand dysregulation in HIV infection: HIV glycoprotein 120 inhibits signaling cascades upstream of CD40 ligand transcription. J. Immunol. 172:2678-2686.