Endocytosis of adenovirus and adenovirus capsid proteins

Advanced Drug Delivery Reviews

Volumn 55, Issue 11, 2003, Pages 1485-1496

  Medina Kauwe, Lali K ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Adenovirus; Capsid; Endocytosis; Fiber; Penton

Indexed keywords

CELLS; DNA; GENE TRANSFER; PROTEINS; VIRUSES;

CELL BINDING; INTEGRIN SIGNALING;

DRUG INFUSION;

ADENOVIRUS VECTOR; CAPSID PROTEIN; PEPTIDE DERIVATIVE; SERYLARGINYLLEUCYLSERYLASPARAGINYLLEUCYLLEUCYLGLYCINE; UNCLASSIFIED DRUG;

ADENOVIRUS; AMINO ACID SEQUENCE; CELL ACTIVITY; CYTOLYSIS; DRUG SAFETY; ENDOCYTOSIS; ENDOSOME; FIBER; GENE DELIVERY SYSTEM; GENE INTERACTION; GENE TRANSFER; GENE TRANSLOCATION; HUMAN; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN MOTIF; REVIEW;

EID: 0345283128     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.addr.2003.07.010     Document Type: Article

References (99)

1. Ilan Y., Prakash R., Davidson A., Jona V., Droguett G., Horwitz M.S., Chowdhury N.R., Chowdhury J.R. Oral tolerization to adenoviral antigens permits long-term gene expression using recombinant adenoviral vectors. Journal of Clinical Investigation. 99:1997;1098-1106.
2. Yang Y., Ertl H.C., Wilson J.M. MHC class I-restricted cytotoxic T lymphocytes to viral antigens destroy hepatocytes in mice infected with E1-deleted recombinant adenoviruses. Immunity. 1:1994;433-442.
3. Greber U.F., Willetts M., Webster P., Helenius A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell. 75:1993;477-486.
4. Kozarsky K.F., Wilson J.M. Gene therapy: adenovirus vectors. Current Opinion in Genetics and Development. 3:1993;499-503.
5. Michael S.I., Curiel D.T. Strategies to achieve targeted gene delivery via the receptor-mediated endocytosis pathway. Gene Therapy. 1:1994;223-232.
6. Wagner E., Zenke M., Cotten M., Beug H., Birnstiel M.L. Transferrin-polycation conjugates as carriers for DNA uptake into cells. Proceedings of the National Academy of Sciences of the United States of America. 87:1990;3410-3414.
7. Cotten M., Wagner E., Zatloukal K., Phillips S., Curiel D.T., Birnstiel M.L. High-efficiency receptor-mediated delivery of small and large (48 kilobase) gene constructs using the endosome-disruption activity of defective or chemically inactivated adenovirus particles. Proceedings of the National Academy of Sciences of the United States of America. 89:1992;6094-6098.
8. Curiel D.T., Agarwal S., Wagner E., Cotten M. Adenovirus enhancement of transferrin-polylysine-mediated gene delivery. Proceedings of the National Academy of Sciences of the United States of America. 88:1991;8850-8854.
9. Wagner E., Zatloukal K., Cotten M., Kirlappos H., Mechtler K., Curiel D.T., Birnstiel M.L. Coupling of adenovirus to transferrin-polylysine/DNA complexes greatly enhances receptor-mediated gene delivery and expression of transfected genes. Proceedings of the National Academy of Sciences of the United States of America. 89:1992;6099-6103.
10. Burnett R.M., Grutter M.G., White J.L. The structure of the adenovirus capsid: I. An envelope model of hexon at 6 A resolution. Journal of Molecular Biology. 185:1984;105-123.
11. Boudin M.L., Boulanger P. Assembly of adenovirus penton base and fiber. Virology. 116:1982;589-604.
12. Devaux C., Adrian M., Berthet-Colominas C., Cusack S., Jacrot B. Structure of adenovirus fibre: I. Analysis of crystals of fibre from adenovirus serotypes 2 and 5 by electron microscopy and X-ray crystallography. Journal of Molecular Biology. 215:1990;567-588.
13. Novelli A., Boulanger P.A. Deletion analysis of functional domains in baculovirus-expressed adenovirus type 2 fiber. Virology. 185:1991;365-376.
14. van Raaij M.J., Mitraki A., Lavigne G., Cusack S. A triple beta-spiral in the adenovirus fibre shaft reveals a new structural motif for a fibrous protein. Nature. 401:1999;935-938.
15. Henry L.J., Xia D., Wilke M.E., Deisenhofer J., Gerard R.D. Characterization of the knob domain of the adenovirus type 5 fiber protein expressed in Escherichia coli. Journal of Virology. 68:1994;5239-5246.
16. Xia D., Henry L.J., Gerard R.D., Deisenhofer J. Crystal structure of the receptor-binding domain of adenovirus type 5 fiber protein at 1.7 A resolution. Structure. 2:1994;1259-1270.
17. 5 promote adenovirus internalization but not virus attachment. Cell. 73:1993;309-319.
18. Bergelson J.M., Cunningham J.A., Droguett G., Kurt-Jones E.A., Krithivas A., Hong J.S., Horwitz M.S., Crowell R.L., Finberg R.W. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science. 275:1997;1320-1323.
19. Freimuth P., Springer K., Berard C., Hainfeld J., Bewley M., Flanagan J. Coxsackievirus and adenovirus receptor amino-terminal immunoglobulin V-related domain binds adenovirus type 2 and fiber knob from adenovirus type 12. Journal of Virology. 73:1999;1392-1398.
20. Wang X., Bergelson J.M. Coxsackievirus and adenovirus receptor cytoplasmic and transmembrane domains are not essential for coxsackievirus and adenovirus infection. Journal of Virology. 73:1999;2559-2562.
21. Zhang F., Andreassen P., Fender E., Geissler J., Hernandez F., Chroboczek J. A transfecting peptide derived from adenovirus fiber protein. Gene Therapy. 6:1999;171-181.
22. Roelvink P.W., Mi Lee G., Einfeld D.A., Kovesdi I., Wickham T.J. Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science. 286:1999;1568-1571.
23. Bergelson J.M., Krithivas A., Celi L., Droguett G., Horwitz M.S., Wickham T., Crowell R.L., Finberg R.W. The murine CAR homolog is a receptor for coxsackie B viruses and adenoviruses. Journal of Virology. 72:1998;415-419.
24. Noutsias M., Fechner H., de Jonge H., Wang X., Dekkers D., Houtsmuller A.B., Pauschinger M., Bergelson J., Warraich R., Yacoub M., Hetzer R., Lamers J., Schultheiss H.P., Poller W. Human coxsackie-adenovirus receptor is colocalized with integrins alpha(v)beta(3) and alpha(v)beta(5) on the cardiomyocyte sarcolemma and upregulated in dilated cardiomyopathy: implications for cardiotropic viral infections. Circulation. 104:2001;275-280.
25. Ito M., Kodama M., Masuko M., Yamaura M., Fuse K., Uesugi Y., Hirono S., Okura Y., Kato K., Hotta Y., Honda T., Kuwano R., Aizawa Y. Expression of coxsackievirus and adenovirus receptor in hearts of rats with experimental autoimmune myocarditis [comment]. Circulation Research. 86:2000;275-280.
26. Cohen C.J., Shieh J.T.C., Pickles R.J., Okegawa T., Hsieh J.-T., Bergelson J.M. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. PNAS Early Edition. 2001;1-6. http://www.pnas.org/cgi/doi/10.1073/pnas.261452898.
27. Honda T., Saitoh H., Masuko M., Katagiri-Abe T., Tominaga K., Kozakai I., Kobayashi K., Kumanishi T., Watanabe Y.G., Odani S., Kuwano R. The coxsackievirus-adenovirus receptor protein as a cell adhesion molecule in the developing mouse brain. Brain Research: Molecular Brain Research. 77:2000;19-28.
28. Walters R.W., Freimuth P., Moninger T.O., Ganske I., Zabner J., Welsh M.J. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell. 110:2002;789-799.
29. Medina-Kauwe L.K., Leung V., Wu L., Kedes L. Assessing the binding and endocytosis activity of cellular receptors using GFP-ligand fusions. BioTechniques. 29:2000;602-609.
30. Medina-Kauwe L.K., Chen X. Using GFP-ligand fusions to measure receptor-mediated endocytosis in living cells. Litwack G. Vitamins and Hormones. 2002;81-95 Elsevier, San Diego.
31. Nakano M.Y., Boucke K., Suomalainen M., Stidwill R.P., Greber U.F. The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. Journal of Virology. 74:2000;7085-7095.
32. Stupack D.G., Li E., Silletti S.A., Kehler J.A., Geahlen R.L., Hahn K., Nemerow G.R., Cheresh D.A. Matrix valency regulates integrin-mediated lymphoid adhesion via Syk kinase. Journal of Cell Biology. 144:1999;777-788.
33. Greber U.F., Webster P., Weber J., Helenius A. The role of the adenovirus protease on virus entry into cells. EMBO Journal. 15:1996;1766-1777.
34. Cotten M., Weber J.M. The adenovirus protease is required for virus entry into host cells. Virology. 213:1995;494-502.
35. Hong S.S., Karayan L., Tournier J., Curiel D.T., Boulanger P.A. Adenovirus type 5 fiber knob binds to MHC class I alpha2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO Journal. 16:1997;2294-2306.
36. Dechecchi M.C., Tamanini A., Bonizzato A., Cabrini G. Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Virology. 268:2000;382-390.
37. Goldman M.J., Wilson J.M. Expression of alpha v beta 5 integrin is necessary for efficient adenovirus-mediated gene transfer in the human airway. Journal of Virology. 69:1995;5951-5958.
38. v integrins for infection. Journal of Virology. 68:1994;6811-6814.
39. Neumann 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.
40. Karayan L., Hong S.S., Gay B., Tournier J., d'Angeac A.D., Boulanger P. Structural and functional determinants in adenovirus type 2 penton base recombinant protein. Journal of Virology. 71:1997;8678-8689.
41. 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.
42. 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 Journal. 16:1997;1189-1198.
43. Schoehn G., Fender P., Chroboczek J., Hewat E.A. Adenovirus 3 penton dodecahedron exhibits structural changes of the base on fibre binding. EMBO Journal. 15:1996;6841-6846.
44. Von Seggern D.J., Chiu C.Y., Fleck S.K., Stewart P.L., Nemerow G.R. A helper-independent adenovirus vector with E1, E3, and fiber deleted: structure and infectivity of fiberless particles. Journal of Virology. 73:1999;1601-1608.
45. Chiu C.Y., Mathias P., Nemerow G.R., Stewart P.L. Structure of adenovirus complexed with its internalization receptor, alphavbeta5 integrin. Journal of Virology. 73:1999;6759-6768.
46. Miyamoto S., Akiyama S.K., Yamada K.M. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science. 267:1995;883-885.
47. Acharya R., Fry E., Stuart D., Fox G., Rowlands D., Brown F. The three-dimensional structure of foot-and-mouth disease virus at 2.9 A resolution. Nature. 337:1989;709-716.
48. Jackson T., Sharma A., Ghazaleh R.A., Blakemore W.E., Ellard F.M., Simmons D.L., Newman J.W., Stuart D.I., King A.M. Arginine-glycine-aspartic acid-specific binding by foot-and-mouth disease viruses to the purified integrin alpha(v)beta3 in vitro. Journal of Virology. 71:1997;8357-8361.
49. Medina-Kauwe L.K., Kasahara N., Kedes L. 3PO, a novel non-viral gene delivery system using engineered Ad5 penton proteins. Gene Therapy. 8:2001;795-803.
50. Li E., Stupack D., Bokoch G.M., Nemerow G.R. Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. Journal of Virology. 72:1998;8806-8812.
51. Heilker R., Spiess M., Crottet P. Recognition of sorting signals by clathrin adaptors. Bioessays. 21:1999;558-567.
52. Kirchhausen T. Adaptors for clathrin-mediated traffic. Annual Review of Cell and Developmental Biology. 15:1999;705-732.
53. De Deyne P.G., O'Neill A., Resneck W.G., Dmytrenko G.M., Pumplin D.W., Bloch R.J. The vitronectin receptor associates with clathrin-coated membrane domains via the cytoplasmic domain of its beta5 subunit. Journal of Cell Science. 111:1998;2729-2740.
54. Mukherjee S., Ghosh R.N., Maxfield F.R. Endocytosis. Physiological Reviews. 77:1997;759-803.
55. Hinshaw J.E., Schmid S.L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding [comment]. Nature. 374:1995;190-192.
56. Takei K., McPherson P.S., Schmid S.L., De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals [comment]. Nature. 374:1995;186-190.
57. Wang K., Huang S., Kapoor-Munshi A., Nemerow G. Adenovirus internalization and infection require dynamin. Journal of Virology. 72:1998;3455-3458.
58. Lamaze C., Fujimoto L.M., Yin H.L., Schmid S.L. The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. Journal of Biological Chemistry. 272:1997;20332-20335.
59. Suomalainen M., Nakano M.Y., Keller S., Boucke K., Stidwill R.P., Greber U.F. Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. Journal of Cell Biology. 144:1999;657-672.
60. Seth P. Adenovirus-dependent release of choline from plasma membrane vesicles at an acidic pH is mediated by the penton base protein. Journal of Virology. 68:1994;1204-1206.
61. Seth P., Willingham M.C., Pastan I. Binding of adenovirus and its external proteins to Triton X-114. Dependence on pH. Journal of Biological Chemistry. 260:1985;14431-14434.
62. Seth P., Fitzgerald D., Ginsberg H., 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. Molecular and Cellular Biology. 4:1984;1528-1533.
63. Bal H.P., Chroboczek J., Schoehn G., Ruigrok R.W., Dewhurst S. Adenovirus type 7 penton purification of soluble pentamers from Escherichia coli and development of an integrin-dependent gene delivery system. European Journal of Biochemistry. 267:2000;6074-6081.
64. Fender P., Ruigrok R.W., Gout E., Buffet S., Chroboczek J. Adenovirus dodecahedron, a new vector for human gene transfer [see comments]. Nature Biotechnology. 15:1997;52-56.
65. Medina-Kauwe L.K., Maguire M., Kasahara N., Kedes L. Non-viral gene delivery to human breast cancer cells by targeted Ad5 penton proteins. Gene Therapy. 8:2001;1753-1761.
66. Wang K., Guan T., Cheresh D.A., Nemerow G.R. Regulation of adenovirus membrane penetration by the cytoplasmic tail of integrin beta5. Journal of Virology. 74:2000;2731-2739.
67. Wickham T.J., Filardo E.J., Cheresh D.A., Nemerow G.R. Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization. Journal of Cell Biology. 127:1994;257-264.
68. Rodriguez E., Everitt E. Adenovirus uncoating and nuclear establishment are not affected by weak base amines. Journal of Virology. 70:1996;3470-3477.
69. Meier O., Boucke K., Hammer S.V., Keller S., Stidwill R.P., Hemmi S., Greber U.F. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. Journal of Cell Biology. 158:2002;1119-1131.
70. Miyazawa N., Leopold P.L., Hackett N.R., Ferris B., Worgall S., Falck-Pedersen E., Crystal R.G. Fiber swap between adenovirus subgroups B and C alters intracellular trafficking of adenovirus gene transfer vectors. Journal of Virology. 73:1999;6056-6065.
71. Miyazawa N., Crystal R.G., Leopold P.L. Adenovirus serotype 7 retention in a late endosomal compartment prior to cytosol escape is modulated by fiber protein. Journal of Virology. 75:2001;1387-1400.
72. Greber U.F. Virus assembly and disassembly: the adenovirus cysteine protease as a trigger factor. Reviews in Medical Virology. 8:1998;213-222.
73. Anderson C.W. The proteinase polypeptide of adenovirus serotype 2 virions. Virology. 177:1990;259-272.
74. Weber J. Genetic analysis of adenovirus type 2: III. Temperature sensitivity of processing viral proteins. Journal of Virology. 17:1976;462-471.
75. Yeh-Kai L., Akusjarvi G., Alestrom P., Pettersson U., Tremblay M., Weber J. Genetic identification of an endoproteinase encoded by the adenovirus genome. Journal of Molecular Biology. 167:1983;217-222.
76. Greber U.F. Signalling in viral entry. Cellular and Molecular Life Sciences. 59:2002;608-626.
77. Reese E.L., Haimo L.T. Dynein, dynactin, and kinesin II's interaction with microtubules is regulated during bidirectional organelle transport. Journal of Cell Biology. 151:2000;155-166.
78. Reilein A.R., Tint I.S., Peunova N.I., Enikolopov G.N., Gelfand V.I. Regulation of organelle movement in melanophores by protein kinase A (PKA), protein kinase C (PKC), and protein phosphatase 2A (PP2A). Journal of Cell Biology. 142:1998;803-813.
79. Leopold P.L., Ferris B., Grinberg I., Worgall S., Hackett N.R., Crystal R.G. Fluorescent virions: dynamic tracking of the pathway of adenoviral gene transfer vectors in living cells. Human Gene Therapy. 9:1998;367-378.
80. Mitchison T., Kirschner M. Dynamic instability of microtubule growth. Nature. 312:1984;237-242.
81. Mitchison T., Kirschner M. Microtubule assembly nucleated by isolated centrosomes. Nature. 312:1984;232-237.
82. Salmon E.D., Leslie R.J., Saxton W.M., Karow M.L., McIntosh J.R. Spindle microtubule dynamics in sea urchin embryos: analysis using a fluorescein-labeled tubulin and measurements of fluorescence redistribution after laser photobleaching. Journal of Cell Biology. 99:1984;2165-2174.
83. Echeverri C.J., Paschal B.M., Vaughan K.T., Vallee R.B. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. Journal of Cell Biology. 132:1996;617-633.
84. Dillman J.F., Pfister K.K. III Differential phosphorylation in vivo of cytoplasmic dynein associated with anterogradely moving organelles. Journal of Cell Biology. 127:1994;1671-1681.
85. Leopold P.L., Kreitzer G., Miyazawa N., Rempel S., Pfister K.K., Rodriguez-Boulan E., Crystal R.G. Dynein- and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis. Human Gene Therapy. 11:2000;151-165.
86. Mandelkow E., Mandelkow E.M. Microtubules and microtubule-associated proteins. Current Opinion in Cell Biology. 7:1995;72-81.
87. Aniento F., Emans N., Griffiths G., Gruenberg J. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. Journal of Cell Biology. 123:1993;1373-1387. (erratum appears in Journal of Cell Biology 124 (3) (1994) 397).
88. Thaler C.D., Haimo L.T. Microtubules and microtubule motors: mechanisms of regulation. International Review of Cytology. 164:1996;269-327.
89. Vallee R.B., Sheetz M.P. Targeting of motor proteins. Science. 271:1996;1539-1544.
90. Hamm-Alvarez S.F., Wang Y., Medina-Kauwe L.K. Modulation of secretory functions in epithelia by adenovirus capsid proteins. Journal of Controlled Release. 2003;. (in press).
91. 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 Journal. 14:1995;4714-4727.
92. Greber U.F., Suomalainen M., Stidwill R.P., Boucke K., Ebersold M.W., Helenius A. The role of the nuclear pore complex in adenovirus DNA entry. EMBO Journal. 16:1997;5998-6007.
93. Pante N., Aebi U. Sequential binding of import ligands to distinct nucleopore regions during their nuclear import. Science. 273:1996;1729-1732.
94. Finlay D.R., Newmeyer D.D., Price T.M., Forbes D.J. Inhibition of in vitro nuclear transport by a lectin that binds to nuclear pores. Journal of Cell Biology. 104:1987;189-200.
95. Martin K., Helenius A. Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell. 67:1991;117-130.
96. Pollard V.W., Michael W.M., Nakielny S., Siomi M.C., Wang F., Dreyfuss G. A novel receptor-mediated nuclear protein import pathway. Cell. 86:1996;985-994.
97. Greber U.F., Gerace L. Depletion of calcium from the lumen of endoplasmic reticulum reversibly inhibits passive diffusion and signal-mediated transport into the nucleus. Journal of Cell Biology. 128:1995;5-14.
98. 2+ store. Science. 270:1995;1835-1838.
99. 2+ stores. Science. 273:1996;1875-1877.