ZAP-70 kinase regulates HIV cell-to-cell spread and virological synapse formation

EMBO Journal

Volumn 26, Issue 2, 2007, Pages 516-526

  Sol Foulon, Nathalie ^a   Sourisseau, Marion ^a   Porrot, Françoise ^a   Thoulouze, Maria Isabel ^a   Trouillet, Céline ^a   Nobile, Cinzia ^b   Blanchet, Fabien ^a   Di Bartolo, Vincenzo ^a   Noraz, Nelly ^c   Taylor, Naomi ^c   Alcover, Andres ^a   Hivroz, Claire ^b   Schwartz, Olivier ^a,d  

^a INSTITUT PASTEUR   (France)

^b INSTITUT CURIE   (France)

^c INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^d CNRS   (France)

Author keywords

HIV; Virological synapse; ZAP 70

Indexed keywords

CD4 ANTIGEN; PROTEIN KINASE ZAP 70;

ARTICLE; CD4+ T LYMPHOCYTE; CELL CONTACT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME DEFICIENCY; ENZYME REGULATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; INFANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; T LYMPHOCYTE ACTIVATION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS LATENCY; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE;

EID: 33846472081     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601509     Document Type: Article

References (62)

1. Abraham RT, Weiss A (2004) Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat Rev Immunol 4: 301-308
2. Arpaia E, Shahar M, Dadi H, Cohen A, Roifman CM (1994) Defective T cell receptor signaling and CD8+ thymic selection in humans lacking zap-70 kinase. Cell 76: 947-958
3. Bacon KB, Szabo MC, Yssel H, Bolen JB, Schall TJ (1996) RANTES induces tyrosine kinase activity of stably complexed p125FAK and ZAP-70 in human T cells. J Exp Med 184: 873-882
4. Barda-Saad M, Braiman A, Titerence R, Bunnell SC, Barr VA, Samelson LE (2005) Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat Immunol 6: 80-89
5. Barnard AL, Igakura T, Tanaka Y, Taylor GP, Bangham CR (2005) Engagement of specific T-cell surface molecules regulates cytoskeletal polarization in HTLV-1-infected lymphocytes. Blood 106: 988-995
6. Blanchard N, Di Bartolo V, Hivroz C (2002) In the immune synapse, ZAP-70 controls T cell polarization and recruitment of signaling proteins but not formation of the synaptic pattern. Immunity 17: 389-399
7. Blot G, Janvier K, Le Panse S, Benarous R, Berlioz-Torrent C (2003) Targeting of the human immunodeficiency virus type 1 envelope to the trans-Golgi network through binding to TIP47 is required for env incorporation into virions and infectivity. J Virol 77: 6931-6945
8. Cemerski S, Shaw A (2006) Immune synapses in T-cell activation. Curr Opin Immunol 18: 298-304
9. Chazal N, Gerlier D (2003) Virus entry, assembly, budding, and membrane rafts. Microbiol Mol Biol Rev 67: 226-237
10. Chiu YL, Soros VB, Kreisberg JF, Stopak K, Yonemoto W, Greene WC (2005) Cellular APOBEC3G restricts HIV-1 infection in resting CD4(+) T cells. Nature 435: 108-114
11. Connor RI, Chen BK, Choe S, Landau NR (1995) Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206: 935-944
12. Das V, Nal B, Dujeancourt A, Thoulouze MI, Galli T, Roux P, Dautry-Varsat A, Alcover A (2004) Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes. Immunity 20: 577-588
13. Davis AJ, Li P, Burrell CJ (1997) Kinetics of viral RNA synthesis following cell-to-cell transmission of human immunodeficiency virus type 1. J Gen Virol 78 (Part 8): 1897-1906
14. Demirov DG, Freed EO (2004) Retrovirus budding. Virus Res 106: 87-102
15. Dimitrov DS, Willey RL, Sato H, Chang LJ, Blumenthal R, Martin MA (1993) Quantitation of human immunodeficiency virus type 1 infection kinetics. J Virol 67: 2182-2190
16. Dustin ML, Tseng SY, Varma R, Campi G (2006) T cell-dendritic cell immunological synapses. Curr Opin Immunol 18: 512-516
17. Elder ME, Lin D, Clever J, Chan AC, Hope TJ, Weiss A, Parslow TG (1994) Human severe combined immunodeficiency due to a defect in ZAP-70, a T cell tyrosine kinase. Science 264: 1596-1599
18. Garcia E, Pion M, Pelchen-Matthews A, Collinson L, Arrighi JF, Blot G, Leuba F, Escola JM, Demaurex N, Marsh M, Piguet V (2005) HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 6: 488-501
19. Goda S, Quale AC, Woods ML, Felthauser A, Shimizu Y (2004) Control of TCR-mediated activation of beta 1 integrins by the ZAP-70 tyrosine kinase interdomain B region and the linker for activation of T cells adapter protein. J Immunol 172: 5379-5387
20. Gomez TS, McCarney SD, Carrizosa E, Labno CM, Comiskey EO, Nolz JC, Zhu P, Freedman BD, Clark MR, Rawlings DJ, Billadeau DD, Burkhardt JK (2006) HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse. Immunity 24: 741-752
21. Griffith CE, Zhang W, Wange RL (1998) ZAP-70-dependent and -independent activation of Erk in Jurkat T cells. Differences in signaling induced by H2o2 and Cd3 cross-linking. J Biol Chem 273: 10771-10776
22. Grigorov B, Arcanger F, Roingeard P, Darlix JL, Muriaux D (2006) Assembly of infectious HIV-1 in human epithelial and T-lymphoblastic cell lines. J Mol Biol 359: 848-862
23. Haase AT (2005) Perils at mucosal front lines for HIV and SIV and their hosts. Nat Rev Immunol 5: 783-792
24. Hioe CE, Chien Jr PC, Lu C, Springer TA, Wang XH, Bandres J, Tuen M (2001) LFA-1 expression on target cells promotes human immunodeficiency virus type 1 infection and transmission. J Virol 75: 1077-1082
25. Hivroz C, Fischer A (1994) Immunodeficiency diseases. Multiple roles for ZAP-70. Curr Biol 4: 731-733
26. Igakura T, Stinchcombe JC, Goon PK, Taylor GP, Weber JN, Griffiths GM, Tanaka Y, Osame M, Bangham CR (2003) Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299: 1713-1716
27. Johnson DC, Huber MT (2002) Directed egress of animal viruses promotes cell-to-cell spread. J Virol 76: 1-8
28. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ (2004) HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J Exp Med 199: 283-293
29. Jolly C, Sattentau QJ (2005) Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity. J Virol 79: 12088-12094
30. Kok T, Li P, Burrell C (1993) Cell-to-cell transmission of human immunodeficiency virus infection induces two distinct phases of viral RNA expression under separate regulatory control. J Gen Virol 74 (Part 1): 33-38
31. Krogsgaard M, Huppa JB, Purbhoo MA, Davis MM (2003) Linking molecular and cellular events in T-cell activation and synapse formation. Semin Immunol 15: 307-315
32. Li Q, Duan L, Estes JD, Ma ZM, Rourke T, Wang Y, Reilly C, Carlis J, Miller CJ, Haase AT (2005) Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434: 1148-1152
33. Maréchal V, Clavel F, Heard JM, Schwartz O (1998) Cytosolic Gag p24 as an index of productive entry of human immunodeficiency virus type 1. J Virol 72: 2208-2212
34. Marsh M, Helenius A (2006) Virus entry: open sesame. Cell 124: 729-740
35. Meinl E, Lengenfelder D, Blank N, Pirzer R, Barata L, Hivroz C (2000) Differential requirement of ZAP-70 for CD2-mediated activation pathways of mature human T cells. J Immunol 165: 3578-3583
36. Miranda LR, Schaefer BC, Kupfer A, Hu Z, Franzusoff A (2002) Cell surface expression of the HIV-1 envelope glycoproteins is directed from intracellular CTLA-4-containing regulated secretory granules. Proc Natl Acad Sci USA 99: 8031-8036
37. Morita E, Sundquist WI (2004) Retrovirus budding. Annu Rev Cell Dev Biol 20: 395-425
38. Nejmeddine M, Barnard AL, Tanaka Y, Taylor GP, Bangham CR (2005) Human T-lymphotropic virus, type 1, tax protein triggers microtubule reorientation in the virological synapse. J Biol Chem 280: 29653-29660
39. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, Mammano F, Schwartz O (2005) Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J Virol 79: 5386-5399
40. Noraz N, Schwarz K, Steinberg M, Dardalhon V, Rebouissou C, Hipskind R, Friedrich W, Yssel H, Bacon K, Taylor N (2000) Alternative antigen receptor (TCR) signaling in T cells derived from ZAP-70-deficient patients expressing high levels of Syk. J Biol Chem 275: 15832-15838
41. Nydegger S, Khurana S, Krementsov DN, Foti M, Thali M (2006) Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1. J Cell Biol 173: 795-807
42. Pearce-Pratt R, Malamud D, Phillips DM (1994) Role of the cytoskeleton in cell-to-cell transmission of human immunodeficiency virus. J Virol 68: 2898-2905
43. Pelchen-Matthews A, Kramer B, Marsh M (2003) Infectious HIV-1 assembles in late endosomes in primary macrophages. J Cell Biol 162: 443-455
44. Pelkmans L (2005) Viruses as probes for systems analysis of cellular signalling, cytoskeleton reorganization and endocytosis. Curr Opin Microbiol 8: 331-337
45. Perlman M, Resh MD (2006) Identification of an intracellular trafficking and assembly pathway for HIV-1 gag. Traffic 7: 731-745
46. Petit C, Buseyne F, Boccaccio C, Abastado JP, Heard JM, Schwartz O (2001) Nef is required for efficient HIV-1 replication in cocultures of dendritic cells and lymphocytes. Virology 286: 225-236
47. Phillips DM (1994) The role of cell-to-cell transmission in HIV infection. Aids 8: 719-731
48. Piguet V, Sattentau Q (2004) Dangerous liaisons at the virological synapse. J Clin Invest 114: 605-610
49. Roumier A, Olivo-Marin JC, Arpin M, Michel F, Martin M, Mangeat P, Acuto O, Dautry-Varsat A, Alcover A (2001) The membrane-microfilament linker ezrin is involved in the formation of the immunological synapse and in T cell activation. Immunity 15: 715-728
50. Sasahara Y, Rachid R, Byrne MJ, de la Fuente MA, Abraham RT, Ramesh N, Geha RS (2002) Mechanism of recruitment of WASP to the immunological synapse and of its activation following TCR ligation. Mol Cell 10: 1269-1281
51. Sato H, Orenstein J, Dimitrov D, Martin M (1992) Cell-to-cell spread of HIV-1 occurs within minutes and may not involve the participation of virus particles. Virology 186: 712-724
52. Schwartz O, Maréchal V, Danos O, Heard JM (1995) Human immunodeficiency virus type 1 Nef increases the efficiency of reverse transcription in the infected cell. J Virol 69: 4053-4059
53. Simmons A, Aluvihare V, McMichael A (2001) Nef triggers a transcriptional program in T cells imitating single-signal T cell activation and inducing HIV virulence mediators. Immunity 14: 763-777
54. Soede RD, Driessens MH, Ruuls-Van Stalle L, Van Hulten PE, Brink A, Roos E (1999) LFA-1 to LFA-1 signals involve zeta-associated protein-70 (ZAP-70) tyrosine kinase: relevance for invasion and migration of a T cell hybridoma. J Immunol 163: 4253-4261
55. Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O (2007) Inefficient HIV replication in mobile lymphocytes. J Virol (in press)
56. Stevenson M (2003) HIV-1 pathogenesis. Nat Med 9: 853-860
57. Stevenson M, Stanwick TL, Dempsey MP, Lamonica CA (1990) HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J 9: 1551-1560
58. Tardif MR, Tremblay MJ (2005) LFA-1 is a key determinant for preferential infection of memory CD4+ T cells by human immunodeficiency virus type 1. J Virol 79: 13714-13724
59. Thoulouze MI, Sol-Foulon N, Blanchet F, Dautry-Varsat A, Schwartz O, Alcover A (2006) Human immunodeficiency virus type-1 infection impairs the formation of the immunological synapse. Immunity 24: 547-561
60. Ticchioni M, Charvet C, Noraz N, Lamy L, Steinberg M, Bernard A, Deckert M (2002) Signaling through ZAP-70 is required for CXCL12-mediated T-cell transendothelial migration. Blood 99: 3111-3118
61. Williams BL, Schreiber KL, Zhang W, Wange RL, Samelson LE, Leibson PJ, Abraham RT (1998) Genetic evidence for differential coupling of Syk family kinases to the T-cell receptor: reconstitution studies in a ZAP-70-deficient Jurkat T-cell line. Mol Cell Biol 18: 1388-1399
62. Zack JA, Arrigo SJ, Weitsman SR, Go AS, Haislip A, Chen ISY (1990) HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61: 213-222