Cellular uptake and nuclear delivery of recombinant adenovirus penton base

Virology

Volumn 262, Issue 1, 1999, Pages 163-177

  Hong, Saw See ^a,b   Gay, Bernard ^b   Karayan, Lucie ^b   Dabauvalle, Marie Christine ^c   Boulanger, Pierre ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b Laboratoire de Biochimie Genetique   (France)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Adenovirus serotype 2 (Ad2); Endocytosis; Membrane translocation; Nuclear import; Nuclear pore complex; Penton base; Protein trafficking; Vesicular escape

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; INTEGRIN; RECOMBINANT PROTEIN;

ADENOVIRUS 2; ARTICLE; BINDING SITE; CELL ADHESION; CELL STRUCTURE; CONTROLLED STUDY; ENDOCYTOSIS; HELA CELL; HUMAN; HUMAN CELL; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; VIRUS CAPSID;

ADENOVIRIDAE; ANIMALIA; DNA VIRUSES; HUMAN ADENOVIRUS TYPE 2; INSECTA; LACTATE DEHYDROGENASE-ELEVATING VIRUS; MIRIDAE;

EID: 0242652179     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1999.9864     Document Type: Article

References (89)

1. Anderson R. G. H., Kamen B. A., Rothberg K. G., Lacey S. W. Potocytosis: Sequestration and transport of small molecules by caveolae. Science. 255:1992;410-411.
2. Bai M., Harfe B., Freimuth P. Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton base protein abolish its cell-rounding activity and delay virus reproduction in flat cells. J. Virol. 67:1993;5198-5205.
3. Belin M. T., Boulanger P. Cytoskeletal proteins associated with intracytoplasmic human adenovirus at an early stage of infection. Exp. Cell Res. 160:1985;356-370.
4. Belin M. T., Boulanger P. Processing of vimentin occurs during the early stages of adenovirus infection. J. Virol. 61:1987;2559-2566.
5. Belin M. T., Boulanger P. Involvement of cellular adhesion sequences in the attachment of adenovirus to HeLa cell surface. J. Gen. Virol. 74:1993;1485-1497.
6. Bergelson J. M., Cunningham J. A., Droguett G., Kurt-Jones E. A., Krithivas A., Hong J. S., Horwitz M. S., Crowell R. L., Weinberg R. W. Isolation of common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science. 275:1997;1320-1323.
7. Boudin M. L., Boulanger P. Assembly of adenovirus penton base and fiber. Virology. 116:1982;589-604.
8. Boudin M. L., Moncany M., D'Halluin J. C., Boulanger P. Isolation and characterization of adenovirus type 2 vertex capsomer (penton base). Virology. 92:1979;125-138.
9. Boulanger P., Puvion F. Large-scale preparation of soluble adenovirus hexon, penton and fiber antigens in highly purified form. Eur. J. Biochem. 39:1973;37-42.
10. Carriére C., Gay B., Chazal N., Morin N., Boulanger P. Sequence requirements for encapsidation of deletion mutants and chimeras of human immunodeficiency virus type 1 Gag precursor into retrovirus-like particles. J. Virol. 69:1995;2366-2377.
11. Chardonnet Y., Dales S. Early events in the interaction of adenovirus with HeLa cells. I. Penetration of type 5 and intracellular release of the DNA genome. Virology. 40:1970;462-477.
12. Chroboczek J., Ruigrok R. W. H., Cusack S. Adenovirus fiber. The Molecular Repertoire of Adenoviruses, I, Virion Structure and Infection. 1995;Springer-Verlag, Berlin, Heidelberg. p. 165-200.
13. Curiel D. T., Agarwal S., Wagner E., Cotten M. Adenovirus enhancement of transferrin-polylysine-mediated gene delivery. Proc. Natl. Acad. Sci. USA. 88:1991;8850-8854.
14. r 68,000 pore complex glycoprotein interfere with nuclear uptake in Xenopus oocytes. Chromosoma. 97:1988;183-197.
15. Dales S., Chardonnet Y. Early events in the interaction of adenovirus with HeLa cells. IV. Association with microtubules and the nuclear pore complex during vectorial movement of the inoculum. Virology. 56:1973;465-483.
16. Davies D. R., Padlan E. A. Antibody-antigen complexes. Annu. Rev. Biochem. 59:1990;439-473.
17. Davis L. I. The nuclear pore complex. Annu. Rev. Biochem. 64:1995;865-896.
18. Defer C., Belin M. T., Caillet-Boudin M. L., Boulanger P. Human adenovirus-host cell interactions: A comparative study with members of subgroups B and C. J. Virol. 64:1990;3661-3673.
19. De Mey J. The preparation of immunoglobulin gold conjugates (IGS reagents) and their use as markers for light and electronmicroscopic immunocytochemistry. Cuello A. C. Immunohistochemistry. 1983;347-372 Wiley, Chichester.
20. Derossi D., Calvet S., Trembleau A., Brunissen A., Chassaing G., Prochiantz A. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biol. Chem. 271:1996;18188-18193.
21. Derossi D., Joliot A., Chassaing A., Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269:1994;10444-10450.
22. D'Souza S. E., Haas T. A., Piotrowicz R. S., Byers-Ward V., McGrath D. E., Soule H. R., Cierniewski C., Plow E. F., Smith J. W. Ligand and cation binding are dual functions of a discrete segment of the integrin b3 subunit: Cation displacement is involved in ligand binding. Cell. 79:1994;659-667.
23. Elliott G., O'Hare P. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell. 88:1997;223-233.
24. Endo Y., Tsurugi K. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J. Biol. Chem. 262:1987;8128-8130.
25. Fender P., Ruigrok R. W. H., Gout E., Buffet S., Chroboczek J. Adenovirus dodecahedron, a new vector for human gene therapy. Nat. Biotechnol. 15:1997;52-56.
26. FitzGerald D. J. P., Padmanabhan R., Pastan I., Willigham M. C. Adenovirus-induced release of epidermal growth factor and Pseudomonas toxin into the cytosol of KB cells during receptor-mediated endocytosis. Cell. 32:1983a;607-617.
27. FitzGerald D. J. P., Trowbridge I. S., Pastan I., Willigham M. C. Enhancement of toxicity of antitransferrin receptor antibody-Pseudomonas exotoxin conjugates by adenovirus. Proc. Natl. Acad. Sci. USA. 80:1983b;4134-4138.
28. Görlich D., Mattaj I. W. Nucleocytoplasmic transport. Science. 271:1996;1513-1518.
29. Greber U. F., Kasamatsu H. Nuclear targeting of SV40 and adenovirus. Trends Cell Biol. 6:1996;189-195.
30. Greber U. F., Willetts M., Webster P., Helenius A. Stepwise dismantling of adenovirus 2 entry into cells. Cell. 75:1993;477-486.
31. Hong S. S., Boulanger P. Protein ligands of the human adenovirus type 2 outer capsid identified by biopanning of a phage-displayed peptide library on separate domains of wild-type and mutant penton capsomers. EMBO J. 14:1995;4714-4727.
32. Hong S. S., Karayan L., Tournier J., Curiel D. T., Boulanger P. Adenovirus type 5 fiber knob binds to the MHC class I alpha-2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO J. 16:1997;2294-2306.
33. Huang S., Kamata T., Takada Y., Ruggeri Z. M., Nemerow G. R. Adenovirus interaction with distinct integrins mediates separate events in cell entry and gene delivery to hematopoietic cells. J. Virol. 70:1996;4502-4508.
34. Huvent I., Hong S. S., Fournier C., Gay B., Tournier J., Carriére C., Courcoul M., Vigne R., Spire B., Boulanger P. Interaction and co-encapsidation of human immunodeficiency virus type 1 Gag and Vif recombinant proteins. J. Gen. Virol. 79:1998;1069-1081.
35. Hynes R. O. Integrins: Versatility, modulation and signaling in cell adhesion. Cell. 69:1992;11-25.
36. Karayan L., Gay B., Gerfaux J., Boulanger P. Oligomerization of recombinant penton base of adenovirus type 2 and its assembly with fiber in baculovirus-infected cells. Virology. 202:1994;782-796.
37. Karayan L., Hong S. S., Gay B., Tournier J., Dupuy d'Angeac A., Boulanger P. Structural and functional determinants in adenovirus type 2 penton base recombinant protein. J. Virol. 71:1997;8678-8689.
38. Krasnykh V. N., Mikheeva G. V., Douglas J. T., Curiel D. T. Generation of recombinant adenovirus vectors with modified fibers for altering viral tropism. J. Virol. 70:1996;6839-6846.
39. Krohne G., Dabauvalle M.-C., Franke W. W. Cell type specific differences in protein composition of nuclear pore complex-lamina structures in oocytes of Xenopus laevis. J. Mol. Biol. 151:1981;121-141.
40. Lemay P., Boulanger P. Physicochemical characteristics of structural and nonstructural proteins of human adenovirus type 2. Ann. Virol. 131:1980;259-275.
41. Louis N., Fender P., Barge A., Kitts P., Chroboczek J. Cell-binding domain of adenovirus serotype 2 fiber. J. Virol. 68:1994;4104-4106.
42. Mathias P., Wickham T., Moore M., Nemerow G. Multiple adenovirus serotypes use αV integrins for infection. J. Virol. 68:1994;6811-6814.
43. Matunis M. J., Coutavas E., Blobel G. A novel ubiquitin-like modification modulates the positioning of the Ran-GTPas-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135:1996;1457-1470.
44. Morgan C., Rosenkranz H. S., Mednis B. Structure and development of viruses as observed in the electron microscope. X. Entry and uncoating of adenovirus. J. Virol. 4:1969;777-796.
45. Neer E. J., Schimdt C. J., Nambudripad R., Smith T. F. The ancient regulatory-protein family of WD-repeat proteins. Nature. 371:1994;297-300.
46. Nemerow G. R., Cheresh D. A., Wickham T. J. Adenovirus entry into host cells: A role for αv integrins. Trends Cell Biol. 4:1994;52-55.
47. Nermut M. V. The architecture of adenoviruses. Ginsberg H. S. The Adenoviruses. 1984;5-34 Plenum, New York.
48. Neuman R., Chroboczek J., Jacrot B. Determination of the nucleotide sequence for the penton-base gene of human adenovirus type 5. Gene. 69:1988;153-157.
49. Nigg E. A. Nucleocytoplasmic transport: Signals, mechanisms and regulation. Nature. 386:1997;779-787.
50. Olsnes S., Phil A. Cohen P., van Heyningen. Molecular Action of Toxins and Viruses. 1982;51-105 Elsevier, Amsterdam.
51. Otero N. J., Carrasco L. Proteins are co-internalized with virion particles during early infection. Virology. 160:1987;75-80.
52. Parton R. G. Caveolae and caveolins. Curr. Opin. Cell Biol. 8:1996;542-546.
53. Richardson W. D., Mills A. D., Dilworth S. M., Laskey R. A., Dingwall C. Nuclear protein migration involves two steps: Rapid binding at the nuclear envelope, followed by slower translocation through nuclear pores. Cell. 52:1988;655-664.
54. Roelvink P. W., Lizonova A., Lee J. G. M., Li Y., Bergelson J. M., Finberg R. W., Brough D. E., Kovesdi I., Wickham T. J. The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J. Virol. 72:1998;7909-7915.
55. Ruoslahti E. Fibronectin and its receptors. Ann. Rev. Biochem. 57:1988;375-413.
56. Ruigrok R. W. H., Barge A., Albiges-Rizo C., Dayan S. Structure of adenovirus fibre. II. Morphology of single fibres. J. Mol. Biol. 215:1990;589-596.
57. Santis G., Legrand V., Hong S. S., Davison E., Kirby I., Imler J. L., Finberg R. W., Bergelson J. M., Mehtali M., Boulanger P. Molecular determinants of adenovirus serotype 5 fibre binding to its cellular receptor CAR. J. Gen. Virol. 80:1999;1519-1527.
58. Saphire, A. C. S, Nemerow, G. R, and, Gerace, L. 1995, Adenovirus Docking at the Nuclear Pore Complex by an NLS-Mediated Pathway, American Society for Cell Biology, Annual Meeting Report, p, 1822.
59. Schoen G., Fender P., Chroboczek J., Hewat E. A. Adenovirus 3 penton dodecahedron exhibits structural changes of the base on fibre binding. EMBO J. 15:1996;6841-6846.
60. Seth P. Adenovirus-dependent release of choline from plasma membrane vesicles at an acidic pH is mediated by the penton base protein. J. Virol. 68:1994a;1204-1206.
61. Seth P. Mechanism of adenovirus-mediated endosome lysis: Role of intact adenovirus capsid structure. Biochem. Biophys. Res. Commun. 205:1994b;1318-1324.
62. Seth P., FitzGerald D., Ginsberg H. S., Willingham M., Pastan I. Evidence that the penton base of adenovirus is involved in potentiation of toxicity of Pseudomonas exotoxin conjugated to epidermal growth factor. Mol. Cell. Biol. 4:1984;1528-1533.
63. Seth P., FitzGerald D., Willingham M., Pastan I. Pathway of adenovirus entry into cells. Crowell R. L., Lonberg-Holm K. Virus Attachment and Entry into Cells. 1986;191-195 Am. Soc. Microbiol. Washington.
64. Seth P., Pastan I., Willingham M. C. Adenovirus-dependent increase in cell membrane permeability. J. Biol. Chem. 260:1985;9598-9602.
65. Seth P., Rosenfeld M., Higginbotham J., Crystal R. G. Mechanism of enhancement of DNA expression consequent to cointernalization of a replication-deficient adenovirus and unmodified plasmid DNA. J. Virol. 68:1994;933-940.
66. Starr C. M., D'Onofrio M., Park M. K., Hanover J. A. Primary sequence and heterologous expression of nuclear pore glycoprotein p62. J. Cell Biol. 110:1990;1861-1871.
67. Stevenson S. C., Rollence M., White B., Weaver L., McClelland A. Human adenovirus serotypes 3 and 5 bind to two different cellular receptors via the fiber head domain. J. Virol. 69:1995;2850-2857.
68. Stewart P. L., Burnett R. M., Cyrklaff M., Fuller S. D. Image reconstruction reveals the complex molecular organization of adenovirus. Cell. 67:1991;145-154.
69. Stewart P. L., Chiu C. Y., Huang S., Muir T., Zhao Y., Chait B., Mathias P., Nemerow G. R. Cryo-EM visualization of an exposed RGD epitope on adenovirus that escapes antibody neutralization. EMBO J. 16:1997;1189-1198.
70. Stewart P. L., Fuller S. D., Burnett R. M. Difference imaging of adenovirus: Bridging the resolution gap between X-ray crystallography and electron microscopy. EMBO J. 12:1993;2589-2599.
71. Stouten P. F. W., Sader C., Ruigrok R. W. H., Cusack S. New triple-helical model for the shaft of the adenovirus fibre. J. Mol. Biol. 226:1992;1073-1084.
72. Svensson U. Role of vesicles during of adenovirus 2 internalization into HeLa cells. J. Virol. 55:1985;442-449.
73. Théodore L., Derossi D., Chassaing G., Llirbat B., Kurbes M., Jordan P., Chneiweiss H., Godement P., Prochiantz A. Intraneuronal delivery of protein kinase C pseudosubstrate leads to growth cone collapse. J. Neurosci. 15:1995;7158-7167.
74. Tomko R. P., Xu R., Philipson L. HCAR and MCAR: The human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA. 94:1997;3352-3356.
75. Varga M. J., Weibull C., Everitt E. Infectious entry pathway of adenovirus type 2. J. Virol. 65:1991;6061-6070.
76. Wang K., Huang S., Kapoor-Munshi A., Nemerow G. Adenovirus internalization and infection requires dynamin. J. Virol. 72:1998;3455-3458.
77. Weatherbee J. A., Luftig R. B., Weihing R. R. Binding of adenovirus to microtubules. II. Depletion of high-molecular-weight microtubule-associated protein content reduces specificity of in vitro binding. J. Virol. 21:1977;732-742.
78. White J. M. Integrins as virus receptors. Curr. Biol. 3:1993;596-599.
79. Whittaker G. R., Helenius A. Nuclear import and export of viruses and virus genomes. Virology. 246:1998;1-23.
80. Wickham T. J., Filardo E. J., Cheresh D. A., Nemerow G. R. Integrin αvβ5 selectively promotes adenovirus-mediated cell membrane permeabilization. J. Cell Biol. 127:1994;257-264.
81. Wickham T. J., Mathias P., Cheresh D. A., Nemerow G. R. Integrins αvβ3 and αvβ5 promote adenovirus internalization but not virus attachment. Cell. 73:1993;309-320.
82. Wickham T. J., Carrion M. E., Kovesdi I. Targeting of adenovirus penton base to new receptors through replacement of its RGD motif with other receptor-specific peptide motifs. Gene Ther. 2:1995;750-758.
83. Wickham T. J., Segal D. M., Roelvink P. W., Carrion M. E., Lizonova A., Lee G. M., Kovesdi I. Targeted adenovirus gene transfer to endothelial and smooth muscle cells by using bispecific antibodies. J. Virol. 70:1996;6831-6838.
84. Wilken N., Kossner U., Sénécal J.-L., Scheer U., Dabauvalle M. C. Nup180, a novel nuclear pore complex protein localizing to the cytoplasmic ring and associated fibrils. J. Cell Biol. 123:1993;1345-1354.
85. Xia D., Henry L., Gerard R. D., Deisenhofer J. Structure of the receptor binding domain of adenovirus type 5 fiber protein. Doerfler W., Böhm P. The Molecular Repertoire of Adenoviruses, I, Virion Structure and Infection. 1995;39-46 Springer-Verlag, Berlin, Heidelberg.
86. Yoshimura A. Adenovirus-induced leakage of co-endocytosed macromolecules into the cytosol. Cell Struct. Funct. 10:1985;391-404.
87. Yoshimura K., Rosenfeld M. A., Seth P., Crystal R. Adenovirus-mediated augmentation of cell transformation with unmodified plasmid vectors. J. Biol. Chem. 268:1993;2300-2303.
88. Zhai Z., Wang X., Qian X. Nuclear-matrix-intermediate filament system and its alteration in adenovirus infected HeLa cells. Cell Biol. Int. Rep. 12:1988;99-108.
89. Zhang Y., Schneider R. J. Adenovirus inhibition of cell translation facilitates release of virus particles and enhances degradation of the cytokeratin network. J. Virol. 68:1994;2544-2555.