The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol

Journal of Virology

Volumn 74, Issue 15, 2000, Pages 7085-7095

  Nakano, M Y ^a   Boucke, K ^a   Suomalainen, M ^a,b   Stidwill, R P ^a   Greber, U F ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; JASPAMIDE; PROTEIN KINASE C;

ACTIN FILAMENT; ADENOVIRUS; ARTICLE; CELL SURFACE; CYTOSOL; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; TARGET CELL; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS SHEDDING;

ACTINS; ADENOVIRUSES, HUMAN; CAPSID; CAPSID PROTEINS; CYTOSOL; ENDOCYTOSIS; HELA CELLS; HUMANS; INTEGRINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; VIRUS ASSEMBLY;

EID: 0033942486     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.15.7085-7095.2000     Document Type: Article

References (63)

1. Bai, M., B. Harfe, and P. Freimuth. 1993. Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton hase protein abolish its cell-rounding activity and delay virus reproduction in flat cells. J. Virol. 67:5198-5205.
2. Baum, S. G., M. S. Horwitz, and J. V. Maizel. 1972. Studies of the mechanism of enhancement of human adenovirus infection in monkey cells by simian virus 40. J. Virol. 10:211-219.
3. Benihoud, K., P. Yeh, and M. Perricaudet. 1999. Adenovirus vectors for gene delivery. Curr. Opin. Biotechnol. 10:440-447.
4. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
5. Blumenthal, R., P. Seth, M. C. Willingham, and I. Pastan. 1986. pH-dependent lysis of liposomes by adenovirus. Biochemistry 25:2231-2237.
6. Bruder, J. T., and I. Kovesdi. 1997. Adenovirus infection stimulates the Raf/MAPK signaling pathway and induces interleukin-8 expression. J. Virol. 71:398-404.
7. Bubb, M. R., I. Spector, B. B. Beyer, and K. M. Fosen. 2000. Effects of jasplakinolide on the kinetics of actin polymerization. An explanation for certain in vivo observations. J. Biol. Chem. 275:5163-5170.
8. Burnett, R. M. 1997. The structure of adenovirus, p. 209-238. In W. Chiu, R. M. Burnett, and R. L. Garcea (ed.), Structural biology of viruses. Oxford University Press, Oxford, United Kingdom.
9. Chardonnet, Y., and S. Dales. 1970. Early events in the interaction of adenoviruses with HeLa cells. I. Penetration of type 5 and intracellular release of the DNA genome. Virology 40:462-477.
10. Colombo, M. I., W. Beron, and P. D. Stahl. 1997. Calmodulin regulates endosome fusion. J. Biol. Chem. 272:7707-7712.
11. Crews, P., L. V. Manes, and M. Boehler. 1986. Jasplakinolide, a cyclodepsipeptide from the marine sponge Jaspis SP. Tetrahedron Lett. 27:2797-2800.
12. Curiel, D. T. 1999. Strategies to adapt adenoviral vectors for targeted delivery. Ann. N. Y. Acad. Sci. 886:158-171.
13. Damke, H., T. Baba, D. E. Warnock, and S. L. Schmid. 1994. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127:915-934.
14. Eichholtz, T., D. B. de Bont, J. de Widt, R. M. Liskamp, and H. L. Ploegh. 1993. A myristoylated pseudosubstrate peptide, a novel protein kinase C inhibitor. J. Biol. Chem. 268:1982-1986.
15. Freimuth, P., K. Springer, C. Berard, J. Hainfeld, M. Bewley, and J. Flanagan, 1999. Coxsackievirus and adenovirus receptor amino-terminal immunoglobulin V-related domain binds adenovirus type 2 and fiber knob from adenovirus type 12. J. Virol. 73:1392-1398.
16. Geli, M. I., and H. Riezman. 1998. Endocytic internalization in yeast and animal cells: similar and different. J. Cell Sci. 111:1031-1037.
17. Greber, U. F. 1998. Delivery of animal virus DNA into the nucleus, p. 89-114. In L. Seymour, A. Kabanov, and P. Felgner (ed.), Self-assembling complexes for gene delivery: from chemistry to clinical trial. John Wiley & Sons, Ltd., Chichester, United Kingdom.
18. Greber, U. F. 1998. Virus assembly and disassembly: the adenovirus cysteine protease as a trigger factor. Rev. Med. Virol. 8:213-222.
19. Greber, U. F., M. Suomalainen, R. P. Stidwill, K. Boucke, M. Ebersold, and A. Helenius. 1997. The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 16:5998-6007.
20. Greber, U. F., P. Webster, J. Weber, and A. Helenius. 1996. The role of the adenovirus protease in virus entry into cells. EMBO J. 15:1766-1777.
21. Greber, U. F., M. Willetts, P. Webster, and A. Helenius. 1993. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75:477-486.
22. Gruenberg, J., and F. R. Maxheld. 1995. Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7:552-563.
23. Hong, S. S., L. Karayan, J. Tournier, D. T. Curiel, and P. A. Boulanger. 1997. Adenovirus type 5 fiber knob binds to MHC class I alpha2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO J. 16:2294-2306.
24. Horwitz, M. S. 1990. Adenoviruses, p. 1723-1740. In B. N. Fields and D. M. Knipe (ed.), Virology, 2nd ed., vol. I. Raven Press, New York, N.Y.
25. Ishida, A., I. Kameshita, S. Okuno, T. Kitani, and H. Fujisawa. 1995. A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem. Biophys. Res. Commun. 212:806-812.
26. Jörnvall, H., and L. Philipson. 1980. Limited proteolysis and a reactive cysteine residue define accessible regions in the native conformation of the adenovirus hexon protein. Eur. J. Biochem. 104:237-247.
27. Lawson, M. A., and F. R. Maxfield. 1995. Ca(2+)- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 377:75-79.
28. Li, E., D. Stupack, G. M. Bokoch, and G. R. Nemerow. 1998. Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J. Virol. 72:8806-8812.
29. Li, E., D. Stupack, R. Klemke, D. A. Cheresh, and G. R. Nemerow. 1998 Adenovirus endocytosis via α(V) integrins requires phosphoinositide-3-OH kinase. J. Virol. 72:2055-2061.
30. Marsh, M., E. Bolzau, and A. Helenius. 1983. Penetration of Semliki Forest virus from acidic prelysosomal vacuoles. Cell 32:931-940.
31. Marsh, M., and R Bron. 1997. SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface. J. Cell Sci. 110:95-103.
32. Mathias, P., M. Galleno, and G. R. Nemerow. 1998. Interactions of soluble recombinant integrin αv β5 with human adenoviruses. J. Virol. 72:8669-8675.
33. Miles, B. D., R. B. Luftig, J. A. Weatherbee, R. R. Weihing, and J. Weber. 1980. Quantitation of the interaction between adenovirus types 2 and 5 and microtubules inside infected cells. Virology 195:265-269.
34. Miyazawa, N., P. L. Leopold, N. R. Hackett, B. Ferris, S. Worgall, E. Falck-Pedersen, and R. G. Crystal. 1999. Fiber swap between adenovirus subgroups B and C alters intracellular trafficking of adenovirus gene transfer vectors. J. Virol. 73:6056-6065.
35. Muallem, S., K. Kwiatkowska, X. Xu, and H. L. Yin. 1995. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J. Cell Biol. 128:589-598.
36. Murphy, C., R. Saffrich, M. Grummt, H. Gournier, V. Rybin, M. Rubino, P. Auvinen, A. Lutcke, R. G. Parton, and M. Zerial. 1996. Endosome dynamics regulated by a Rho protein. Nature 384:427-432.
37. Nakano, M. Y., and U. F. Greber. 2000. Quantitative microscopy of fluorescent adenovirus entry. J. Struct. Biol. 129:57-68.
38. Ng, T., D. Shima, A. Squire, P. I. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker. 1999. PKCalpha regulates betal integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18:3909-3923.
39. Panetti, T. S., and P. J. McKeown-Longo. 1993. The alpha v beta 5 integrin receptor regulates receptor-mediated endocytosis of vitronectin. J. Biol. Chem. 268:11492-11495.
40. Panetti, T. S., S. A. Wilcox, C. Horzempa, and P. J. McKeown-Longo. 1995. Alpha v beta 5 integrin receptor-mediated endocytosis of vitronectin is protein kinase C-dependent. J. Biol. Chem. 270:18593-18597.
41. Pastan, I., P. Seth, D. FitzGerald, and M. Willingham. 1986. Adenovirus entry into cells: some new observations on an old problem. Springer-Verlag, New York, N.Y.
42. Patterson, S., and W. C. Russell. 1983. Ultrastructural and immunofluorescence studies of early events in adenovirus-HeLa cell interactions. J. Gen. Virol. 64:1091-1099.
43. Rauma, T., J. Tuukkanen, J. M. Bergelson, G. Denning, and T. Hautala. 1999. rab5 GTPase regulates adenovirus endocytosis. J. Virol. 73:9664-9668.
44. Ren, X. D., W. B. Kiosses, and M. A. Schwartz. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18:578-585.
45. Ringerike, T., E. Stang, L. E. Johannessen, D. Sandnes, F. O. Levy, and I. H. Madshus. 1998. High-affinity binding of epidermal growth factor (EGF) to EGF receptor is disrupted by overexpression of mutant dynamin (K44A). J. Biol. Chem. 273:16639-16642.
46. Rodriguez, E., and E. Everitt. 1996. Adenovirus uncoating and nuclear establishment are not affected by weak base amines. J. Virol. 70:3470-3477.
47. Sampath, P., and T. D. Pollard. 1991. Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 30:1973-1980.
48. Schmid, S. L., M. A. McNiven, and P. De Camilli. 1998. Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10:504-512.
49. Shenk, T. 1996. Adenoviridae, p. 979-1016. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fundamental virology, 3rd ed. Lippincott-Raven, New York, N.Y.
50. Shurety, W., N. L. Stewart, and J. L. Stow. 1998. Fluid-phase markers in the basolateral endocytic pathway accumulate in response to the actin assembly-promoting drug Jasplakinolide. Mol. Biol. Cell 9:957-975.
51. Siddhanta, U., J. McIlroy, A. Shah, Y. Zhang, and J. M. Backer. 1998. Distinct roles for the p110alpha and hVPS34 phosphatidylinositol 3′-kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J. Cell Biol. 143:1647-1659.
52. Song, J. C., B. J. Hrnjez, O. C. Farokhzad, and J. B. Matthews. 1999. PKC-epsilon regulates basolateral endocytosis in human T84 intestinal epithelia: role of F-actin and MARCKS. Am. J. Physiol. 277:C1239-C1249.
53. Stauffer, T. P., D. Guerini, and E. Carafoli. 1995. Tissue distribution of the four gene products of the plasma membrane Ca2+ pump. A study using specific antibodies. J. Biol. Chem. 270:12184-12190.
54. Suomalainen, M., M. Y. Nakano, K. Boucke, S. Keller, R. P. Stidwill, and U. F. Greber. 1999. Microtubule-dependent minus and plus end-directed motilities are competing processes for nuclear targeting of adenovirus. J. Cell Biol. 144:657-672.
55. Sussenbach, J. S. 1967. Early events in the infection of adenovirus type 5 in HeLa cells. Virology 33:567-574.
56. Tomko, R. P., R. Xu, and L. Philipson. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 94:3352-3356.
57. Von Seggern, D. J., C. Y. Chiu, S. K. Fleck, P. L. Stewart, and G. R. Nemerow. 1999. A helper-independent adenovirus vector with E1, E3, and fiber deleted: structure and infectivity of fiberless particles. J. Virol. 73:1601-1608.
58. Wang, K. N., S. Huang, A. Kapoormunshi, and G. Nemerow. 1998. Adenovirus internalization and infection require dynamin. J. Virol. 72:3455-3458.
59. Wang, X. H., and J. M. Bergelson. 1999. Coxsackievirus and adenovirus receptor cytoplasmic and transmembrane domains are not essential for coxsackievirus and adenovirus infection. J. Virol. 73:2559-2562.
60. Weber, J. 1976. Genetic analysis of adenovirus type 2. III. Temperature sensitivity of processing of viral proteins. J. Virol. 17:462-471.
61. Wickham, T. J., E. J. Filardo, D. A. Cheresh, and G. R. Nemerow. 1994. Integrin αvβ5 selectively promotes adenovirus mediated cell membrane permeabilization. J. Cell Biol. 127:257-264.
62. Wickham, T. J., P. Mathias, D. A. Cheresh, and G. R. Nemerow. 1993. Integrin-alpha-v-beta-3 and integrin-alpha-v-beta-5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
63. Zen, K., J. Biwersi, N. Periasamy, and A. S. Verkman. 1992. Second messengers regulate endosomal acidification in Swiss 3T3 fibroblasts. J. Cell Biol. 119:99-110.