Inhibiting the Arp2/3 complex limits infection of both intracellular mature vaccinia virus and primate lentiviruses

Molecular Biology of the Cell

Volumn 15, Issue 12, 2004, Pages 5197-5207

  Komano, Jun ^a   Miyauchi, Kosuke ^a   Matsuda, Zene ^a   Yamamoto, Naoki ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; BINDING PROTEIN; CORTACTIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VESICULAR STOMATITIS VIRUS G PROTEIN; VIRUS PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ACTIN POLYMERIZATION; ADENOVIRUS; ANIMAL CELL; ARTICLE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRINAE; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RETROVIRUS INFECTION; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; VACCINIA; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS TYPING;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ACTIN-RELATED PROTEIN 2; ACTIN-RELATED PROTEIN 3; ADENOVIRIDAE; ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CRICETINAE; CYTOSKELETAL PROTEINS; HIV-1; HUMANS; INTRACELLULAR SPACE; LENTIVIRUSES, PRIMATE; MEMBRANE FUSION; MEMBRANE GLYCOPROTEINS; MICROFILAMENTS; NERVE TISSUE PROTEINS; PROTEIN BINDING; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINIA VIRUS; VIRAL ENVELOPE PROTEINS; VIRUS REPLICATION; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

ADENOVIRIDAE; ANIMALIA; DNA VIRUSES; HUMAN HERPESVIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRUS; PRIMATES; RNA VIRUSES; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS; UNIDENTIFIED RETROVIRUS; VACCINIA; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 9444244486     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-04-0279     Document Type: Article

References (64)

1. Aoki, Y., Aizaki, H., Shimoike, T., Tani, H., Ishii, K., Saito, I., Matsuura, Y., and Miyamura, T. (1998). A human liver cell line exhibits efficient translation of HCV RNAs produced by a recombinant adenovirus expressing T7 RNA polymerase. Virology 250, 140-150.
2. Bukrinskaya, A., Brichacek, B., Mann, A., and Stevenson, M. (1998). Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J. Exp. Med. 188, 2113-2125.
3. Cantarelli, V.V., Takahashi, A., Akeda, Y., Nagayama, K., and Honda, T. (2000). Interaction of enteropathogenic or enterohemorrhagic Escherichia coli with HeLa cells results in translocation of cortactin to the bacterial adherence site. Infect. Immun. 68, 382-386.
4. Castellano, F., Le Clainche, C., Patin, D., Carlier, M.F., and Chavrier, P. (2001). A WASp-VASP complex regulates actin polymerization at the plasma membrane. EMBO J. 20, 5603-5614.
5. Cudmore, S., Reckmann, I., and Way, M. (1997). Viral manipulations of the actin cytoskeleton. Trends Microbiol. 5, 142-148.
6. Dean, H.J., Terhune, S.S., Shieh, M.T., Susmarski, N., and Spear, P.G. (1994). Single amino acid substitutions in gD of herpes simplex virus 1 confer resistance to gD-mediated interference and cause cell-type-dependent alterations in infectivity. Virology 199, 67-80.
7. Dehio, C., Prevost, M.C., and Sansonetti, P.J. (1995). Invasion of epithelial cells by Shigella flexneri induces tyrosine phosphorylation of cortactin by a pp60c-src-mediated signalling pathway. EMBO J. 14, 2471-2482.
8. Fawaz, F.S., van Ooij, C., Homola, E., Mutka, S.C., and Engel, J.N. (1997). Infection with Chlamydia trachomatis alters the tyrosine phosphorylation and/or localization of several host cell proteins including cortactin. Infect. Immun. 65, 5301-5308.
9. Flanagan, L.A., Chou, J., Falet, H., Neujahr, R., Hartwig, J.H., and Stossel, T.P. (2001). Filamin A, the Arp2/3 complex, and the morphology and function of cortical actin filaments in human melanoma cells. J. Cell Biol. 155, 511-517.
10. Frischknecht, F., Moreau, V., Rottger, S., Gonfloni, S., Reckmann, I., Superti-Furga, G., and Way, M. (1999). Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401, 926-929.
11. Fuerst, T.R., Niles, E.G., Studier, F.W., and Moss, B. (1986). Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83, 8122-8126.
12. Fuller, A.O., and Spear, P.G. (1987). Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface. Proc. Natl. Acad. Sci. USA 84, 5454-5458.
13. Gournier, H., Goley, E.D., Niederstrasser, H., Trinh, T., and Welch, M.D. (2001). Reconstitution of human Arp2/3 complex reveals critical roles of individual subunits in complex structure and activity. Mol. Cell 8, 1041-1052.
14. Gruenheid, S., and Finlay, B.B. (2003). Microbial pathogenesis and cytoskeletal function. Nature 422, 775-781.
15. Gundlach, B.R. et al. (1997). Construction, replication, and immunogenic properties of a simian immunodeficiency virus expressing interleukin-2. J. Virol. 71, 2225-2232.
16. Harlander, R.S., Way, M., Ren, Q., Howe, D., Grieshaber, S.S., and Heinzen, R.A. (2003). Effects of ectopically expressed neuronal Wiskott-Aldrich syndrome protein domains on Rickettsia rickettsii actin-based motility. Infect. Immun. 71, 1551-1556.
17. Higgs, H.N., Blanchoin, L., and Pollard, T.D. (1999). Influence of the C terminus of Wiskott-Aldrich syndrome protein (WASp) and the Arp2/3 complex on actin polymerization. Biochemistry 38, 15212-15222.
18. Higgs, H.N., and Pollard, T.D. (2001). Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70, 649-676.
19. Ichihashi, Y., and Oie, M. (1996). Neutralizing epitope on penetration protein of vaccinia virus. Virology 220, 491-494.
20. Iyengar, S., Hildreth, J.E., and Schwartz, D.H. (1998). Actin-dependent receptor colocalization required for human immunodeficiency virus entry into host cells. J. Virol. 72, 5251-5255.
21. Kizhatil, K., and Albritton, L.M. (1997). Requirements for different components of the host cell cytoskeleton distinguish ecotropic murine leukemia virus entry via endocytosis from entry via surface fusion. J. Virol. 71, 7145-7156.
22. Krause, M., Sechi, A.S., Konradt, M., Monner, D., Gertler, F.B., and Wehland, J. (2000). Fyn-binding protein (Fyb)/SLP-76-associated protein (SLAP), Ena/ vasodilator-stimulated phosphoprotein (VASP) proteins and the Arp2/3 complex link T cell receptor (TCR) signaling to the actin cytoskeleton. J. Cell Biol. 149, 181-194.
23. Li, E., Stupack, D., Bokoch, G.M., and Nemerow, G.R. (1998). Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J. Virol. 72, 8806-8812.
24. Locker, J.K., Kuehn, A., Schleich, S., Rutter, G., Hohenberg, H., Wepf, R., and Griffiths, G. (2000). Entry of the two infectious forms of vaccinia virus at the plasma membrane is signaling-dependent for the IMV but not the EEV. Mol. Biol. Cell 11, 2497-2511.
25. Machesky, L.M., and Insall, R.H. (1998). Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8, 1347-1356.
26. Machesky, L.M., Mullins, R.D., Higgs, H.N., Kaiser, D.A., Blanchoin, L., May, R.C., Hall, M.E., and Pollard, T.D. (1999). Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. USA 96, 3739-3744.
27. Maddon, P.J., McDougal, J.S., Clapham, P.R., Dalgleish, A.G., Jamal, S., Weiss, R.A., and Axel, R. (1988). HIV infection does not require endocytosis of its receptor, CD4. Cell 54, 865-874.
28. Marchand, J.B., Kaiser, D.A., Pollard, T.D., and Higgs, H.N. (2001). Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat. Cell Biol. 3, 76-82.
29. May, R.C., Caron, E., Hall, A., and Machesky, L.M. (2000). Involvement of the Arp2/3 complex in phagocytosis mediated by FcgammaR or CR3. Nat. Cell Biol. 2, 246-248.
30. McClure, M.O., Sommerfelt, M.A., Marsh, M., and Weiss, R.A. (1990). The pH independence of mammalian retrovirus infection. J. Gen. Virol. 71, 767-773.
31. McDonald, D., Vodicka, M.A., Lucero, G., Svitkina, T.M., Borisy, G.G., Emerman, M., and Hope, T.J. (2002). Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159, 441-452.
32. McGee, K., Zettl, M., Way, M., and Fallman, M. (2001). A role for N-WASP in invasin-promoted internalisation. FEBS Lett. 509, 59-65.
33. Miki, H., Miura, K., and Takenawa, T. (1996). N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J. 15, 5326-5335.
34. Miki, H., and Takenawa, T. (1998). Direct binding of the verprolin-homology domain in N-WASP to actin is essential for cytoskeletal reorganization. Biochem. Biophys. Res. Commun. 243, 73-78.
35. Moreau, V., Frischknecht, F., Reckmann, I., Vincentelli, R., Rabut, G., Stewart, D., and Way, M. (2000). A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nat. Cell Biol. 2, 441-448.
36. Nussbaum, O., Broder, C.C., and Berger, E.A. (1994). Fusogenic mechanisms of enveloped-virus glycoproteins analyzed by a novel recombinant vaccinia virus-based assay quantitating cell fusion-dependent reporter gene activation. J. Virol. 68, 5411-5422.
37. Nussbaum, O., Roop, A., and Anderson, W.F. (1993). Sequences determining the pH dependence of viral entry are distinct from the host range-determining region of the murine ecotropic and amphotropic retrovirus envelope proteins. J. Virol. 67, 7402-7405.
38. Panchal, S.C., Kaiser, D.A., Torres, E., Pollard, T.D., and Rosen, M.K. (2003). A conserved amphipathic helix in WASP/Scar proteins is essential for activation of Arp2/3 complex. Nat. Struct. Biol. 10, 591-598.
39. Pantaloni, D., Le Clainche, C., and Carlier, M.F. (2001). Mechanism of actin-based motility. Science 292, 1502-1506.
40. Ragheb, J.A., and Anderson, W.F. (1994). pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: implications for the role of the R peptide and p12E TM in viral entry. J. Virol. 68, 3220-3231.
41. Rietdorf, J., Ploubidou, A., Reckmann, I., Holmstrom, A., Frischknecht, F., Zettl, M., Zimmermann, T., and Way, M. (2001). Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nat. Cell Biol. 3, 992-1000.
42. Robinson, R.C., Turbedsky, K., Kaiser, D.A., Marchand, J.B., Higgs, H.N., Choe, S., and Pollard, T.D. (2001). Crystal structure of Arp2/3 complex. Science 294, 1679-1684.
43. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T., and Kirschner, M.W. (1999). The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231.
44. Rosenthal, K.S., Perez, R., and Hodnichak, C. (1985). Inhibition of herpes simplex virus type 1 penetration by cytochalasins B and D. J. Gen. Virol. 66, 1601-1605.
45. Rozelle, A.L. et al. (2000). Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10, 311-320.
46. Sakamoto, T., Ushijima, H., Okitsu, S., Suzuki, E., Sakai, K., Morikawa, S., and Muller, W.E. (2003). Establishment of an HIV cell-cell fusion assay by using two genetically modified HeLa cell lines and reporter gene. J. Virol. Methods 114, 159-166.
47. Sakisaka, T. et al. (2001). Requirement of interaction of nectin-1alpha/HveC with afadin for efficient cell-cell spread of herpes simplex virus type 1. J. Virol. 75, 4734-4743.
48. Scaplehorn, N., Holmstrom, A., Moreau, V., Frischknecht, F., Reckmann, I., and Way, M. (2002). Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus. Curr. Biol. 12, 740-745.
49. Smith, G.L., Vanderplasschen, A., and Law, M. (2002). The formation and function of extracellular enveloped vaccina virus. J. Gen. Virol. 83, 2915-2931.
50. Stein, B.S., Gowda, S.D., Lifson, J.D., Penhallow, R.C., Bensch, K.G., and Engleman, E.G. (1987). pH-independent HIV entry into CD4-positive T cells via virus envelope fusion to the plasma membrane. Cell 49, 659-668.
51. Takase-Yoden, S., and Watanabe, R. (1999). Contribution of virus-receptor interaction to distinct viral proliferation of neuropathogenic and nonneuropathogenic murine leukemia viruses in rat glial cells. J. Virol. 73, 4461-4464.
52. Takenawa, T., and Miki, H. (2001). WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114, 1801-1809.
53. Uruno, T., Liu, J., Zhang, P., Fan, Y., Egile, C., Li, R., Mueller, S.C., and Zhan, X. (2001). Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat. Cell Biol. 3, 259-266.
54. Vanderplasschen, A., Hollinshead, M., and Smith, G.L. (1998). Intracellular and extracellular vaccinia virions enter cells by different mechanisms. J. Gen. Virol. 79, 877-887.
55. Wang, K., Huang, S., Kapoor-Munshi, A., and Nemerow, G. (1998). Adenovirus internalization and infection require dynamin. J. Virol. 72, 3455-3458.
56. Weaver, A.M., Karginov, A.V., Kinley, A.W., Weed, S.A., Li, Y., Parsons, J.T., and Cooper, J.A. (2001). Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr. Biol. 11, 370-374.
57. Weaver, A.M., Young, M.E., Lee, W.L., and Cooper, J.A. (2003). Integration of signals to the Arp2/3 complex. Curr. Opin. Cell Biol. 15, 23-30.
58. Weed, S.A., Karginov, A.V., Schafer, D.A., Weaver, A.M., Kinley, A.W., Cooper, J.A., and Parsons, J.T. (2000). Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J. Cell Biol. 151, 29-40.
59. Weed, S.A., and Parsons, J.T. (2001). Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20, 6418-6434.
60. Welch, M.D., Rosenblatt, J., Skoble, J., Portnoy, D.A., and Mitchison, T.J. (1998). Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281, 105-108.
61. Wittels, M., and Spear, P.G. (1991). Penetration of cells by herpes simplex virus does not require a low pH-dependent endocytic pathway. Virus Res. 18, 271-290.
62. Zalevsky, J., Grigorova, I., and Mullins, R.D. (2001). Activation of the Arp2/3 complex by the Listeria acta protein. Acta binds two actin monomers and three subunits of the Arp2/3 complex. J. Biol. Chem. 276, 3468-3475.
63. Zhang, J. et al. (1999). Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J. Exp. Med. 190, 1329-1342.
64. Zhang, J., Shi, F., Badour, K., Deng, Y., McGavin, M.K., and Siminovitch, K.A. (2002). WASp verprolin homology, cofilin homology, and acidic region domain-mediated actin polymerization is required for T cell development. Proc. Natl. Acad. Sci. USA 99, 2240-2245.