HIV-1 Tat Enters T Cells Using Coated Pits before Translocating from Acidified Endosomes and Eliciting Biological Responses

Molecular Biology of the Cell

Volumn 15, Issue 5, 2004, Pages 2347-2360

  Vendeville, Agnès ^a   Rayne, Fabienne ^a   Bonhoure, Anne ^a   Bettache, Nadir ^a   Montcourrier, Philippe ^a   Beaumelle, Bruno ^a  

^a UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPROMAZINE; CLATHRIN; CYTOKINE; DIPHTHERIA TOXIN; DYNAMIN; EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 15; HEAT SHOCK PROTEIN 90; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERSECTIN; RAB PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR AP 2;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; APOPTOSIS; ARTICLE; CELL MEMBRANE; COATED PIT; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOSOL; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPATHOLOGY; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VIRUS CELL INTERACTION;

CLATHRIN; COATED PITS, CELL-MEMBRANE; CYTOSOL; DNA-BINDING PROTEINS; ENDOCYTOSIS; ENDOSOMES; GENE PRODUCTS, TAT; HIV-1; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; I-KAPPA B PROTEINS; INTERLEUKIN-2; INTERLEUKIN-8; JURKAT CELLS; NUCLEAR PROTEINS; PROTEIN TRANSPORT; RAB5 GTP-BINDING PROTEINS; T-LYMPHOCYTES; TRANS-ACTIVATION (GENETICS); TRANSFERRIN;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

EID: 2342507144     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-12-0921     Document Type: Article

References (68)

1. Alami, M., Taupiac, M.P., Reggio, H., Bienvenue, A., and Beaumelle, B. (1998). Involvement of ATP-dependent Pseudomonas exotoxin translocation from a late recycling compartment in lymphocyte intoxication procedure. Mol. Biol. Cell 9, 387-402.
2. Aragane, Y., Kulms, D., Metze, D., Wilkes, G., Poppelmann, B., Luger, T.A., and Schwarz, T. (1998). Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L. J. Cell Biol. 140, 171-182.
3. Barth, H., Blocker, D., Behlke, J., Bergsma-Schutter, W., Brisson, A., Benz, R., and Aktories, K. (2000). Cellular uptake of Clostridium botulinum C2 toxin requires oligomerization and acidification. J. Biol. Chem. 275, 18704-18711.
4. Beaumelle, B., Bensammar, L., and Bienvenue, A. (1992). Selective translocation of the A chain of diphtheria toxin across the membrane of purified endosomes. J. Biol. Chem. 267, 11525-11531.
5. Beaumelle, B., Gibson, A., and Hopkins, C.R. (1990). Isolation and preliminary characterization of the major membrane boundaries of the endocytic pathway in lymphocytes. J. Cell Biol. 111, 1811-1823.
6. Beaumelle, B., and Hopkins, C.R. (1989). High-yield isolation of functionally competent endosomes from mouse lymphocytes. Biochem J. 264, 137-149.
7. Benmerah, A., Bayrou, M., Cerf-Bensussan, N., and Dautry-Varsat, A. (1999). Inhibition of dathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112, 1303-1311.
8. Bonifaci, N., Sitia, R., and Rubartelli, A. (1995). Nuclear translocation of an exogenous fusion protein containing HIV Tat requires unfolding. AIDS 9, 995-1000.
9. Ceresa, B.P., Lotscher, M., and Schmid, S.L. (2001). Receptor and membrane recycling can occur with unaltered efficiency despite dramatic Rab5(q791)-induced changes in endosome geometry. J. Biol. Chem. 276, 9649-9654.
10. Chang, H.C., Samaniego, F., Nair, B.C., Buonaguro, L., and Ensoli, B. (1997). HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. AIDS 11, 1421-1431.
11. Chen, D., Wang, M., Zhou, S., and Zhou, Q. (2002). HIV-1 Tat targets microtubules to induce apoptosis, a process promoted by the pro-apoptotic Bcl-2 relative Bim. EMBO J. 21, 6801-6810.
12. Clague, M.J., Urbe, S., Aniento, F., and Gruenberg, J. (1994). Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 269, 21-24.
13. Contamin, S., Galmiche, A., Doye, A., Flatau, G., Benmerah, A., and Boquet, P. (2000). The p21 Rho-activating toxin cytotoxic necrotizing factor 1 is endocytosed by a clathrin-independent mechanism and enters the cytosol by an acidic-dependent membrane translocation step. Mol. Biol. Cell 11, 1775-1787.
14. Falnes, P.O., and Sandvig, K. (2000). Penetration of protein toxins into cells. Curr. Opin. Cell Biol. 12, 407-413.
15. Fawell, S., Seery, J., Daikh, Y., Moore, C., Chen, L.L., Pepinsky, B., and Barsoum, J. (1994). Tat-mediated delivery of heterologous proteins into cells. Proc. Natl. Acad. Sci. USA 91, 664-668.
16. Fittipaldi, A., Ferrari, A., Zoppe, M., Arcangeli, C., Pellegrini, V., Beltram, F., and Giacca, M. (2003). Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 tat fusion proteins. J. Biol. Chem. 36, 34141-34149.
17. Foti, M., Mangasarian, A., Piguet, V., Lew, D.P., Krause, K.H., Trono, D., and Carpentier, J.L. (1997). Nef-mediated clathrin-coated pit formation. J. Cell Biol. 139, 37-47.
18. Fra, A.M., Williamson, E., Simons, K., and Parton, R.G. (1994). Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269, 30745-30748.
19. Frankel, A.D., Bredt, D.S., and Pabo, C.O. (1988). Tat protein from human immunodeficiency virus forms a metal-linked dimer. Science 240, 70-73.
20. Frankel, A.D., and Pabo, C.O. (1988). Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 55, 1189-1193.
21. Green, I., Christison, R., Voyce, C.J., Bundell, K.R., and Lindsay, M.A. (2003). Protein transduction domains: are they delivering? Trends Pharmacol. Sci. 24, 213-215.
22. Gruenberg, J. (2001). The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell. Biol. 2, 721-730.
23. Gutheil, W.G., Subramanyam, M., Flentke, G.R., Sanford, D.G., Munoz, E., Huber, B.T., and Bachovchin, W.W. (1994). Human immunodeficiency virus 1 Tat binds to dipeptidyl aminopeptidase IV (CD26): a possible mechanism for Tat's immunosuppressive activity. Proc. Natl. Acad. Sci. USA 91, 6594-6598.
24. Haug, G., Leemhuis, J., Tiemann, D., Meyer, D.K., Aktories, K., and Barth, H. (2003). The host cell chaperone Hsp90 is essential for translocation of the binary Clostridium botulinum C2 toxin into the cytosol. J. Biol. Chem. 278, 32266-32274.
25. Hirst, J., Futter, C.E., and Hopkins, C.R. (1998). The kinetics of mannose 6-phosphate receptor trafficking in the endocytic pathway in HEp-2 cells: the receptor enters and rapidly leaves multivesicular endosomes without accumulating in a prelysosomal compartment. Mol. Biol. Cell 9, 809-816.
26. Jiang, M.C., Lin, J.K., and Chen, S.S.L. (1996). Inhibition of HIV-1 Tat-mediated transactivation by quinacrine and chloroquine. Biochem. Biophys. Res. Commun. 226, 1-7.
27. Johannes, L., and Lamaze, C. (2002). Clathrin-dependent or not: is it still the question? Traffic 3, 443-451.
28. Kobayashi, T., Stang, E., Fang, K.S., de Moerloose, P., Parton, R.G., and Gruenberg, J. (1998). A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197.
29. Lamaze, C., Dujeancourt, A., Baba, T., Lo, C.G., Benmerah, A., and Dautry-Varsat, A. (2001). Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7, 661-71.
30. Latz, E., Visintin, A., Lien, E., Fitzgerald, K.A., Monks, B.G., Kurt-Jones, E.A., Golenbock, D.T., and Espevik, T. (2002). Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J. Biol. Chem. 277, 47834-47843.
31. Lemichez, E., Bomsel, M., Devilliers, G., vanderSpek, J., Murphy, J.R., Lukianov, E.V., Olsnes, S., and Boquet, P. (1997). Membrane translocation of diphtheria toxin fragment A exploits early to late endosome trafficking machinery. Mol. Microbiol. 23, 445-457.
32. Li, C., Friedman, D., Wang, C., Metelev, V., and Pardee, A. (1995). Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science 268, 429-439.
33. Liu, Y., Jones, M., Hingtgen, C.M., Bu, G., Laribee, N., Tanzi, R.E., Moir, R.D., Nath, A., and He, J.J. (2000). Uptake of HIV-1 Tat protein mediated by low-density lipoprotein receptor-related protein disrupts the neuronal metabolic balance of the receptor ligands. Nat. Med. 6, 1380-1387.
34. Mallard, F., Antony, C., Tenza, D., Salamero, J., Goud, B., and Johannes, L. (1998). Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. J. Cell Biol. 143, 973-90.
35. Mann, D.A., and Frankel, A.D. (1991). Endocytosis and targeting of exogenous HIV-1 Tat protein. EMBO J. 10, 1733-1739.
36. Manna, S.K., and Aggarwal, B.B. (2000). Differential requirement for p561ck in HIV-tat versus TNF-induced cellular responses: effects on NF-kappa B, activator protein-1, c-Jun N-terminal kinase, and apoptosis. J. Immunol. 164, 5156-5166.
37. McNiven, M.A., Cao, H., Pitts, K.R., and Yoon, Y. (2000). The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem. Sci. 25, 115-120.
38. Morlon-Guyot, J., Helmy, M., Lombard-Frasca, S., Pignol, D., Pieroni, G., and Beaumelle, B. (2003). Identification of the ricin lipase site and implication in cytotoxicity. J. Biol. Chem. 278, 17006-17011.
39. Mukhopadhyay, A., Barbieri, A.M., Funato, K., Roberts, R., and Stahl, P.D. (1997). Sequential actions of Rab5 and Rab7 regulate endocytosis in the Xenopus oocyte. J. Cell Biol. 136, 1227-1237.
40. Nabi, I.R., and Le, P.U. (2003). Caveolae/raft-dependent endocytosis. J. Cell Biol. 161, 673-677.
41. Nguyen, D.H., and Taub, D. (2002). CXCR4 function requires membrane cholesterol: implications for HIV infection. J. Immunol. 168, 4121-4126.
42. Noonan, D., and Albini, A. (2000). From the outside in: extracellular activities of HIV Tat. Adv. Pharmacol. 48, 229-250.
43. Orlandi, P.A., and Fishman, P.H. (1998). Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141, 905-915.
44. Ory, S., Munari-Silem, Y., Fort, P., and Jurdic, P. (2000). Rho and Rac exert antagonistic functions on spreading of macrophage-derived multinucleated cells and are not required for actin fiber formation. J. Cell Sci. 113, 1177-1188.
45. Ott, M., Emiliani, S., Van Lint, C., Herbein, G., Lovett, J., Chirmule, N., McCloskey, T., Pahwa, S., and Verdin, E. (1997). Immune hyperactivation of HIV-1-infected T cells mediated by Tat and the CD28 pathway. Science 275, 1481-1485.
46. Ott, M., Lovett, J.L., Mueller, L., and Verdin, E. (1998). Superinduction of IL-8 in T cells by HIV-1 Tat protein is mediated through NF-kappaB factors. J. Immunol. 160, 2872-2880.
47. Peters, P.J. et al. (2003). Trafficking of prion proteins through a caveolae-mediated endosomal pathway. J. Cell Biol. 162, 703-717.
48. Picard, D. (2002). Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol. Life Sci. 59, 1640-1648.
49. Pitas, R.E., Innerarity, T.L., Weinstein, J.N., and Mahley, R.W. (1981). Aceto-acetylated lipoproteins used to distinguish fibroblasts from macrophages in vitro by fluorescence microscopy. Arteriosclerosis 1, 177-185.
50. Ratts, R., Zeng, H., Berg, E.A., Blue, C., McComb, M.E., Costello, C.E., vanderSpek, J.C., and Murphy, J.R. (2003). The cytosolic entry of diphtheria toxin catalytic domain requires a host cell cytosolic translocation factor complex. J. Cell Biol. 160, 1139-1150.
51. Richard, J.P., Melikov, K., Vives, E., Ramos, C., Verbeure, B., Gait, M.J., Chernomordik, L.V., and Lebleu, B. (2003). Cell-penetrating peptides. A re-evaluation of the mechanism of cellular uptake. J. Biol. Chem. 278, 585-590.
52. Roumier, A., Olivo-Marin, J.C., Arpin, M., Michel, F., Martin, M., Mangeat, P., Acuto, O., Dautry-Varsat A., and 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.
53. Rubartelli, A., Poggi, A., Sitia, R., and Zocchi, M.R. (1998). HIV-I Tat: a polypeptide for all seasons. Immunol. Today 19, 543-545.
54. Salgado, F.J., Lojo, J., Alonso-Lebrero, J.L., Lluis, C., Franco, R., Cordero, O.J., and Nogueira, M. (2003). A role for interleukin-12 in the regulation of T cell plasma membrane compartmentation. J. Biol. Chem. 278, 24849-24857.
55. Secchiero, P., Zella, D., Curreli, S., Mirandola, P., Capitani, S., Gallo, R.C., and Zauli, G. (2000). Pivotal role of cyclic nucleoside phosphodiesterase 4 in Tat-mediated CD4+ T cell hyperactivation and HIV type 1 replication. Proc. Natl. Acad. Sci. USA 97, 14620-14625.
56. Signoret, N. et al. (1997). Phorbol esters and SDF-1 induce rapid endocytosis and down modulation of the chemokine receptor CXCR4. J. Cell Biol. 139, 651-664.
57. Simpson, F., Hussain, N.K., Qualmann, B., Kelly, R.B., Kay, B.K., McPherson, P.S., and Schmid, S.L. (1999). SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nat. Cell Biol. 1, 119-124.
58. Singh, R.D., Puri, V., Valiyaveettil, J.T., Marks, D.L., Bittman, R., and Pagano, R.E. (2003). Selective caveolin-1-dependent endocytosis of glycosphingolipids. Mol. Biol. Cell 14, 3254-3265.
59. Stenmark, H., Valencia, A., Martinez, O., Ullrich, O., Goud, B., and Zerial, M. (1994). Distinct structural elements of Rab5 define its functional specificity. EMBO J. 13, 575-583.
60. Subtil, A., Hemar, A., and Dautry-varsat, A. (1994). rapid endocytosis of interleukin 2 receptor when clathrin-coated pit endocytosis is inhibited. J. Cell Sci. 107, 3461-3468.
61. Traub, L.M. (2003). Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 163, 203-208.
62. Tyagi, M., Rusnati, M., Presta, M., and Giacca, M. (2001). Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 276, 3254-3261.
63. van Weert, A.W.M., Dunn, K.W., Geuze, H.J., Maxfield, F.R., and Stoorvogel, W. (1995). Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol. 130, 821-834.
64. Vitelli, R., Santillo, M., Lattero, D., Chiariello, M., Bifulco, M., Bruni, C.B., and Bucci, C. (1997). Role of the small GTPase Rab7 in the late endocytic pathway. J. Biol. Chem. 272, 4391-4397.
65. Voss, G., Manson, K., Montefiori, D., Watkins, D.I., Heeney, J., Wyand, M., Cohen, J., and Bruck, C. (2003). Prevention of disease induced by a partially heterologous AIDS virus in rhesus monkeys by using an adjuvanted multi-component protein vaccine. J Virol. 77, 1049-1058.
66. Watson, K., and Edwards, R.J. (1999). HIV-1-trans-activating (Tat) protein: both a target and a tool in therapeutic approaches. Biochem. Pharmacol. 58, 1521-1528.
67. Wei, P., Garber, M.E., Fang, S.M., Fischer, W.H., and Jones, K.A. (1998). A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92, 451-462.
68. Xiao, H., Neuveut, C., Tiffany, H.L., Benkirane, M., Rich, E.A., Murphy, P.M., and Jeang, K.T. (2000). Selective CXCR4 antagonism by tat: implications for in vivo expansion of coreceptor use by HIV-1. Proc. Natl. Acad. Sci. USA 97, 11466-11471.