Adenovirus membrane penetration: Tickling the tail of a sleeping dragon

Virology

Volumn 479-480, Issue , 2015, Pages 591-599

  Wiethoff, Christopher M ^a   Nemerow, Glen R ^b  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Adenovirus; Cell trafficking; Innate immunity; Membrane destruction; Protein VI; Receptors; Virus structure

Indexed keywords

VIRUS PROTEIN;

ADENOVIRIDAE; ANIMAL; CELL MEMBRANE; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY; VIRUS ENTRY;

ADENOVIRIDAE; ANIMALS; CELL MEMBRANE; HOST-PATHOGEN INTERACTIONS; HUMANS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 84939939551     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.03.006     Document Type: Review

References (103)

1. Amstutz B., Gastaldelli M., Kälin S., Imelli N., Boucke K., Wandeler E., Mercer J., Hemmi S., Greber U.F. Subversion of CtBP1-controlled macropinocytosis by human adenovirus serotype 3. EMBO J. 2008, 27:956-969.
2. Arnberg N., Edlund K., Kidd A.H., Wadell G. Adenovirus type 37 uses sialic acid as a cellular receptor. J. Virol. 2000, 74:42-48.
3. Baniecki M.L., McGrath W.J., Mangel W.F. Regulation of a viral proteinase by a peptide and DNA in one-dimensional space: III. atomic resolution structure of the nascent form of the adenovirus proteinase. J. Biol. Chem. 2013, 288:2081-2091.
4. Barlan A.U., Griffin T.M., McGuire K.A., Wiethoff C.M. Adenovirus membrane penetration activates the NLRP3 inflammasome. J. Virol. 2011, 85:146-155.
5. Benevento M., Di Palma S., Snijder J., Moyer C.L., Reddy V.S., Nemerow G.R., Heck A.J. Adenovirus composition, proteolysis, and disassembly studied by in-depth qualitative and quantitative proteomics. J. Biol. Chem. 2014, 289:11421-11430.
6. Berclaz P.Y., Zsengellér Z., Shibata Y., Otake K., Strasbaugh S., Whitsett J.A., Trapnell B.C. Endocytic internalization of adenovirus, nonspecific phagocytosis, and cytoskeletal organization are coordinately regulated in alveolar macrophages by GM-CSF and PU.1. J. Immunol. 2002, 169:6332-6342.
7. 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 1997, 275:1320-1323.
8. Bewley M.C., Springer K., Zhang Y.B., Freimuth P., Flanagan J.M. Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science 1999, 286:1579-1583.
9. Blainey P.C., Graziano V., Pérez-Berná A.J., McGrath W.J., Flint S.J., San Martín C., Xie X.S., Mangel W.F. Regulation of a viral proteinase by a peptide and DNA in one-dimensional space: IV. viral proteinase slides along DNA to locate and process its substrates. J. Biol. Chem. 2013, 288:2092-2102.
10. Boyle K.B., Randow F. The role of 'eat-me' signals and autophagy cargo receptors in innate immunity. Curr. Opin. Microbiol. 2013, 16:339-348.
11. Brabec M., Schober D., Wagner E., Bayer N., Murphy R.F., Blaas D., Fuchs R. Opening of size-selective pores in endosomes during human rhinovirus serotype 2 in vivo uncoating monitored by single-organelle flow analysis. J. Virol. 2005, 79:1008-1016.
12. Burckhardt C.J., Suomalainen M., Schoenenberger P., Boucke K., Hemmi S., Greber U.F. Drifting motions of the adenovirus receptor CAR and immobile integrins initiate virus uncoating and membrane lytic protein exposure. Cell Host Microbe 2011, 10:105-117.
13. Burmeister W.P., Guilligay D., Cusack S., Wadell G., Arnberg N. Crystal structure of species D adenovirus fiber knobs and their sialic acid binding sites. J. Virol. 2004, 78:7727-7736.
14. Carey B., Staudt D., Bonaminio D., van der Loo J.C., Trapnell B.C. PU.1 redirects adenovirus to lysosomes in alveolar macrophages, uncoupling internalization from infection. J. Immunol. 2007, 178:2440-2447.
15. Chintakuntlawar A.V., Zhou X., Rajaiya J., Chodosh J. Viral capsid is a pathogen-associated molecular pattern in adenovirus keratitis. PLoS Pathog. 2010, 6:e1000841.
16. Cotten M., Weber J.M. The adenovirus protease is required for virus entry into host cells. Virology 1995, 213:494-502.
17. Cupelli K., Müller S., Persson B.D., Jost M., Arnberg N., Stehle T. Structure of adenovirus type 21 knob in complex with CD46 reveals key differences in receptor contacts among species B adenoviruses. J. Virol. 2010, 84:3189-3200.
18. Di Paolo N.C., Miao E.A., Iwakura Y., Murali-Krishna K., Aderem A., Flavell R.A., Papayannopoulou T., Shayakhmetov D.M. Virus binding to a plasma membrane receptor triggers interleukin-1[alpha]-mediated proinflammatory macrophage response in vivo. Immunity 2009, 31:110-121.
19. Domanov Y.A., Kinnunen P.K. Antimicrobial peptides temporins B and L induce formation of tubular lipid protrusions from supported phospholipid bilayers. Biophys. J. 2006, 91:4427-4439.
20. Dupont N., Lacas-Gervais S., Bertout J., Paz I., Freche B., Van Nhieu G.T., van der Goot F.G., Sansonetti P.J., Lafont F. Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 2009, 6:137-149.
21. Epand R.M., Epand R.F. Modulation of membrane curvature by peptides. Biopolymers 2000, 55:358-363.
22. Excoffon K.J., Gansemer N.D., Mobily M.E., Karp P.H., Parekh K.R., Zabner J. Isoform-specific regulation and localization of the coxsackie and adenovirus receptor in human airway epithelia. PLoS One 2010, 5:e9909.
23. Fabry C.M., Rosa-Calatrava M., Conway J.F., Zubieta C., Cusack S., Ruigrok R.W., Schoehn G. A quasi-atomic model of human adenovirus type 5 capsid. EMBO J. 2005, 24:1645-1654.
24. Farr G.A., Zhang L.G., Tattersall P. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. USA 2005, 102:17148-17153.
25. Fejer G., Drechsel L., Liese J., Schleicher U., Ruzsics Z., Imelli N., Greber U.F., Keck S., Hildenbrand B., Krug A., Bogdan C., Freudenberg M.A. Key role of splenic myeloid DCs in the IFN-alphabeta response to adenoviruses in vivo. PLoS Pathog. 2008, 4:e1000208.
26. FitzGerald D.J., Padmanabhan R., Pastan I., Willingham M.C. Adenovirus-induced release of epidermal growth factor and pseudomonas toxin into the cytosol of KB cells during receptor-mediated endocytosis. Cell 1983, 32:607-617.
27. Franklin R.M., Pettersson U., Akervall K., Strandberg B., Philipson L. Structural proteins of adenovirus. V. Size and structure of the adenovirus type 2 hexon. J. Mol. Biol. 1971, 57:383-395.
28. Gaggar A., Shayakhmetov D.M., Lieber A. CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 2003, 9:1408-1412.
29. Greber U.F., Willetts M., Webster P., Helenius A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 1993, 75:477-486.
30. Greber U.F., Webster P., Weber J., Helenius A. The role of the adenovirus protease on virus entry into cells. EMBO J. 1996, 15:1766-1777.
31. Gurcel L., Abrami L., Girardin S., Tschopp J., van der Goot F.G. Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 2006, 126:1135-1145.
32. Hannan C., Raptis L.H., Déry C.V., Weber J. Biological and structural studies with an adenovirus type 2 temperature-sensitive mutant defective for uncoating. Intervirology 1983, 19:213-223.
33. Hara H., Kawamura I., Nomura T., Tominaga T., Tsuchiya K., Mitsuyama M. Cytolysin-dependent escape of the bacterium from the phagosome is required but not sufficient for induction of the Th1 immune response against Listeria monocytogenes infection: distinct role of Listeriolysin O determined by cytolysin gene replacement. Infect. Immun. 2007, 75:3791-3801.
34. Higginbotham J.N., Seth P., Blaese R.M., Ramsey W.J. The release of inflammatory cytokines from human peripheral blood mononuclear cells in vitro following exposure to adenovirus variants and capsid. Hum. Gene Ther. 2002, 13:129-141.
35. Kalyuzhniy O., Di Paolo N.C., Silvestry M., Hofherr S.E., Barry M.A., Stewart P.L., Shayakhmetov D.M. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc. Natl. Acad. Sci. USA 2008, 105:5483-5488.
36. King A.M.Q., Adams M.J., Carstens E.B. Virus Taxonomy: Classification and Nomenclature of Viruses 2012, Elsevier: Academic press, Amsterdam.
37. Li E., Stupack D., Klemke R., Cheresh D.A., Nemerow G.R. Adenovirus endocytosis via alpha(v) integrins requires phosphoinositide-3-OH kinase. J. Virol. 1998, 72:2055-2061.
38. Lindert S., Silvestry M., Mullen T.-M., Nemerow G.R., Stewart P.L. Cryo-electron microscopy structure of an adenovirus-integrin complex indicates conformational changes in both penton base and integrin. J. Virol. 2009, 83:11491-11501.
39. Lion T. Adenovirus infections in immunocompetent and immunocompromised patients. Clin. Microbiol. Rev. 2014, 27:441-462.
40. Liu E.B., Wadford D.A., Seto J., Vu M., Hudson N.R., Thrasher L., Torres S., Dyer D.W., Chodosh J., Seto D., Jones M.S. Computational and serologic analysis of novel and known viruses in species human adenovirus D in which serology and genomics do not correlate. PLoS One 2012, 7:e33212.
41. Liu H., Jin L., Koh S., Atanasov I., Schein S., Wu L., Zhou Z. Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science (New York, NY) 2010, 329:1038-1043.
42. Maier O., Wiethoff C.M. N-terminal α-helix-independent membrane interactions facilitate adenovirus protein VI induction of membrane tubule formation. Virology 2010, 408:31-38.
43. Maier O., Galan D.L., Wodrich H., Wiethoff C.M. An N-terminal domain of adenovirus protein VI fragments membranes by inducing positive membrane curvature. Virology 2010, 402:11-19.
44. Maier O., Marvin S.A., Wodrich H., Campbell E.M., Wiethoff C.M. Spatiotemporal dynamics of adenovirus membrane rupture and endosomal escape. J. Virol. 2012, 86:10821-10828.
45. Martinez R., Schellenberger P., Vasishtan D., Aknin C., Austin S., Dacheux D., Rayne F., Siebert A., Ruzsics Z., Gruenewald K., Wodrich H. THE amphipathic helix of adenovirus capsid protein vi contributes to penton release and post entry sorting. J. Virol. 2014.
46. McGuire K.A., Barlan A.U., Griffin T.M., Wiethoff C.M. Adenovirus type 5 rupture of lysosomes leads to cathepsin B-dependent mitochondrial stress and production of reactive oxygen species. J. Virol. 2011, 85:10806-10813.
47. Miles B.D., Luftig R.B., Weatherbee J.A., Weihing R.R., Weber J. Quantitation of the interaction between adenovirus types 2 and 5 and microtubules inside infected cells. Virology 1980, 105:265-269.
48. 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. J. Virol. 1999, 73:6056-6065.
49. Morgan C., Rosenkranz H.S., Mednis B. Structure and development of viruses as observed in the electron microscope. V. Entry and uncoating of adenovirus. J. Virol. 1969, 4:777-796.
50. Moyer C.L., Nemerow G.R. Viral weapons of membrane destruction: variable modes of membrane penetration by non-enveloped viruses. Curr. Opin. Virol. 2011, 1:44-449.
51. Moyer C.L., Wiethoff C.M., Maier O., Smith J.G., Nemerow G.R. Functional genetic and biophysical analyses of membrane disruption by human adenovirus. J. Virol. 2011, 85:2631-2641.
52. Muruve D.A., Petrilli V., Zaiss A.K., White L.R., Clark S.A., Ross P.J., Parks R.J., Tschopp J. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 2008, 452:103-107.
53. Nguyen E.K., Nemerow G.R., Smith J.G. Direct evidence from single-cell analysis that human {alpha}-defensins block adenovirus uncoating to neutralize infection. J. Virol. 2010, 84:4041-4049.
54. Nilsson E.C., Storm R.J., Bauer J., Johansson S.M., Lookene A., Ångström J., Hedenström M., Eriksson T.L., Frängsmyr L., Rinaldi S., Willison H.J., Pedrosa Domellöf F., Stehle T., Arnberg N. The GD1a glycan is a cellular receptor for adenoviruses causing epidemic keratoconjunctivitis. Nat. Med. 2011, 17:105-109.
55. Nociari M., Ocheretina O., Murphy M., Falck-Pedersen E. Adenovirus induction of IRF3 occurs through a binary trigger targeting Jun N-terminal kinase and TBK1 kinase cascades and type I interferon autocrine signaling. J. Virol. 2009, 83:4081-4091.
56. Ortega-Esteban A., Pérez-Berná A.J., Menéndez-Conejero R., Flint S.J., San Martín C., de Pablo P.J. Monitoring dynamics of human adenovirus disassembly induced by mechanical fatigue. Sci. Rep. 2013, 3(1434).
57. Pache L., Venkataraman S., Reddy V.S., Nemerow G.R. Structural variations in species B adenovirus fibers impact CD46 association. J. Virol. 2008, 82:7923-7931.
58. Paglino J.C., Andres W., van den Pol A.N. Autonomous parvoviruses neither stimulate nor are inhibited by the type I interferon response in human normal or cancer cells. J. Virol. 2014, 88:4932-4942.
59. Paz I., Sachse M., Dupont N., Mounier J., Cederfur C., Enninga J., Leffler H., Poirier F., Prevost M.C., Lafont F., Sansonetti P. Galectin-3, a marker for vacuole lysis by invasive pathogens. Cell. Microbiol. 2010, 12:530-544.
60. Pérez L., Carrasco L. Involvement of the vacuolar H(+)-ATPase in animal virus entry. J. Gen. Virol. 1994, 75(Pt 10):2595-2606.
61. Persson B.D., Reiter D.M., Marttila M., Mei Y.-F., Casasnovas J.M., Arnberg N., Stehle T. Adenovirus type 11 binding alters the conformation of its receptor CD46. Nat. Struct. Mol. Biol. 2007, 14:164-166.
62. Prchla E., Plank C., Wagner E., Blaas D., Fuchs R. Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2. J. Cell Biol. 1995, 131:111-123.
63. 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 1999, 401:935-938.
64. Raper S.E., Chirmule N., Lee F.S., Wivel N.A., Bagg A., Gao G.-p., Wilson J.M., Batshaw M.L. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol. Gen. Metab. 2003, 80:148-158.
65. Reddy V.S., Nemerow G.R. Structures and organization of adenovirus cement proteins provide insights into the role of capsid maturation in virus entry and infection. Proc. Natl. Acad. Sci. USA 2014, 111:11715-11720.
66. Reddy V.S., Natchiar S.K., Stewart P.L., Nemerow G.R. Crystal structure of human adenovirus at 3.5A resolution. Science 2010, 329:1071-1075.
67. Roberts M.M., White J.L., Grütter M.G., Burnett R.M. Three-dimensional structure of the adenovirus major coat protein hexon. Science 1986, 232:1148-1151.
68. Rodríguez E., Everitt E. Adenovirus uncoating and nuclear establishment are not affected by weak base amines. J. Virol. 1996, 70:3470-3477.
69. Saban S.D., Silvestry M., Nemerow G.R., Stewart P.L. Visualization of alpha-helices in a 6-angstrom resolution cryoelectron microscopy structure of adenovirus allows refinement of capsid protein assignments. J. Virol. 2006, 80:12049-12059.
70. Salinas S., Bilsland L.G., Henaff D., Weston A.E., Keriel A., Schiavo G., Kremer E.J. CAR-associated vesicular transport of an adenovirus in motor neuron axons. PLoS Pathog. 2009, 5:e1000442.
71. Salinas S., Zussy C., Loustalot F., Henaff D., Menendez G., Morton P.E., Parsons M., Schiavo G., Kremer E.J. Disruption of the coxsackievirus and adenovirus receptor-homodimeric interaction triggers lipid microdomain- and dynamin-dependent endocytosis and lysosomal targeting. J. Biol. Chem. 2014, 289:680-695.
72. Schagen F.H.E., Wensveen F.M., Carette J.E., Dermody T.S., Gerritsen W.R., van Beusechem V.W. Genetic targeting of adenovirus vectors using a reovirus [sigma]1-Based attachment protein. Mol. Ther. 2006, 13:997-1005.
73. Schmid D., Pypaert M., Münz C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 2007, 26:79-92.
74. Seiradake E., Lortat-Jacob H., Billet O., Kremer E.J., Cusack S. Structural and mutational analysis of human Ad37 and canine adenovirus 2 fiber heads in complex with the D1 domain of coxsackie and adenovirus receptor. J. Biol. Chem. 2006, 281:33704-33716.
75. Seth P. Adenovirus-dependent release of choline from plasma membrane vesicles at an acidic pH is mediated by the penton base protein. J. Virol. 1994, 68:1204-1206.
76. Seth P., Willingham M.C., Pastan I. Adenovirus-dependent release of 51Cr from KB cells at an acidic pH. J. Biol. Chem. 1984, 259:14350-14353.
77. Seth P., Fitzgerald D.J., Willingham M.C., Pastan I. Role of a low-pH environment in adenovirus enhancement of the toxicity of a Pseudomonas exotoxin-epidermal growth factor conjugate. J. Virol. 1984, 51:650-655.
78. Seth P., Pastan I., Willingham M.C. Adenovirus-dependent increase in cell membrane permeability. J. Biol. Chem. 1985, 260:9598-9602.
79. Shayakhmetov D.M., Li Z.Y., Ternovoi V., Gaggar A., Gharwan H., Lieber A. The interaction between the fiber knob domain and the cellular attachment receptor determines the intracellular trafficking route of adenoviruses. J. Virol. 2003, 77:3712-3723.
80. Silvestry M., Lindert S., Smith J.G., Maier O., Wiethoff C.M., Nemerow G.R., Stewart P.L. Cryo-electron microscopy structure of adenovirus type 2 temperature-sensitive mutant 1 reveals insight into the cell entry defect. J. Virol. 2009, 83:7375-7383.
81. Smith J.G., Silvestry M., Lindert S., Lu W., Nemerow G.R., Stewart P.L. Insight into the mechanisms of adenovirus capsid disassembly from studies of defensin neutralization. PLoS Pathog. 2010, 6:e1000959.
82. Smith J.S., Xu Z., Tian J., Palmer D.J., Ng P., Byrnes A.P. The role of endosomal escape and mitogen-activated protein kinases in adenoviral activation of the innate immune response. PLoS One 2011, 6:e26755.
83. Smith T.A. Adenovirus serotype 5 fiber shaft influences in vivo gene transfer in mice. Hum. Gene Ther. 2003, 14:777-787.
84. Snijder J., Reddy V.S., May E.R., Roos W.H., Nemerow G.R., Wuite G.J. Integrin and defensin modulate the mechanical properties of adenovirus. J. Virol. 2013, 87:2756-2766.
85. Snijder J., Benevento M., Moyer C.L., Reddy V., Nemerow G.R., Heck A.J. The cleaved N-terminus of pVI binds peripentonal hexons in mature adenovirus. J. Mol. Biol. 2014, 426:1971-1979.
86. 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. 1997, 16:1189-1198.
87. Tam C., Idone V., Devlin C., Fernandes M.C., Flannery A., He X., Schuchman E., Tabas I., Andrews N.W. Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. J. Cell Biol. 2010, 189:1027-1038.
88. Teigler J.E., Kagan J.C., Barouch D.H. Late endosomal trafficking of alternative serotype adenovirus vaccine vectors augments antiviral innate immunity. J. Virol. 2014, 88:10354-10363.
89. Thurston T.L., Wandel M.P., von Muhlinen N., Foeglein A., Randow F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 2012, 482:414-418.
90. Waddington S.N., McVey J.H., Bhella D., Parker A.L., Barker K., Atoda H., Pink R., Buckley S.M., Greig J.A., Denby L., Custers J., Morita T., Francischetti I.M., Monteiro R.Q., Barouch D.H., van Rooijen N., Napoli C., Havenga M.J., Nicklin S.A., Baker A.H. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 2008, 132:397-409.
91. Walters R.W., Grunst T., Bergelson J.M., Finberg R.W., Welsh M.J., Zabner J. Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J. Biol Chem. 1999, 274:10219-10226.
92. 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 2002, 110:789-799.
93. Wang H., Li Z.Y., Liu Y., Persson J., Beyer I., Möller T., Koyuncu D., Drescher M.R., Strauss R., Zhang X.B., Wahl J.K., Urban N., Drescher C., Hemminki A., Fender P., Lieber A. Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nat. Med. 2011, 17:96-104.
94. Wang K., Huang S., Kapoor-Munshi A., Nemerow G. Adenovirus internalization and infection require dynamin. J. Virol. 1998, 72:3455-3458.
95. Wickham T.J., Mathias P., Cheresh D.A., Nemerow G.R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993, 73:309-319.
96. Wickham T.J., Filardo E.J., Cheresh D.A., Nemerow G.R. Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization. J. Cell Biol. 1994, 127:257-264.
97. Wiethoff C.M., Wodrich H., Gerace L., Nemerow G.R. Adenovirus protein VI mediates membrane disruption following capsid disassembly. J. Virol. 2005, 79:1992-2000.
98. Wu E., Trauger S.A., Pache L., Mullen T.-M., von Seggern D.J., Siuzdak G., Nemerow G.R. Membrane cofactor protein is a receptor for adenoviruses associated with epidemic keratoconjunctivitis. J. Virol. 2004, 78:3897-3905.
99. Xu Z., Qiu Q., Tian J., Smith J.S., Conenello G.M., Morita T., Byrnes A.P. Coagulation factor X shields adenovirus type 5 from attack by natural antibodies and complement. Nat. Med. 2013, 19:452-457.
100. Yamaguchi T., Kawabata K., Kouyama E., Ishii K.J., Katayama K., Suzuki T., Kurachi S., Sakurai F., Akira S., Mizuguchi H. Induction of type I interferon by adenovirus-encoded small RNAs. Proc. Natl. Acad. Sci. USA 2010, 107:17286-17291.
101. Zabner J., Freimuth P., Puga A., Fabrega A., Welsh M.J. Lack of high affinity fiber receptor activity explains the resistance of ciliated airway epithelia to adenovirus infection. J. Clin. Invest. 1997, 100:1144-1149.
102. Zeng X., Carlin C.R. Host cell autophagy modulates early stages of adenovirus infections in airway epithelial cells. J. Virol. 2013, 87:2307-2319.
103. Zubieta C., Schoehn G., Chroboczek J., Cusack S. The structure of the human adenovirus 2 penton. Mol. Cell 2005, 17:121-135.