Virus entry at a glance

Journal of Cell Science

Volumn 126, Issue 6, 2013, Pages 1289-1295

  Yamauchi, Yohei ^a   Helenius, Ari ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; DECAY ACCELERATING FACTOR; GLYCOPROTEIN; PROTEIN KINASE FYN; VIRUS PROTEIN;

CELL ADHESION; CELL COMPARTMENTALIZATION; CELL INTERACTION; CELL MEMBRANE; CELL NUCLEUS; CELL ORGANELLE; CELL SURFACE; CELL TRANSPORT; CELL VACUOLE; CYTOPLASM; CYTOSOL; DNA VIRUS; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; HELA CELL; HOST CELL; HUMAN; NONHUMAN; NOTE; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; RNA VIRUS; SIGNAL TRANSDUCTION; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENOME; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; DNA, VIRAL; ENDOCYTOSIS; ENDOSOMES; HUMANS; RNA, VIRAL; VIRUS ATTACHMENT; VIRUS INTERNALIZATION; VIRUS RELEASE; VIRUS REPLICATION;

EID: 84877898099     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.119685     Document Type: Note

References (146)

1. Alkhatib, G., Combadiere, C., Broder, C. C., Feng, Y., Kennedy, P. E., Murphy, P. M. and Berger, E. A. (1996). CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272, 1955-1958.
2. Amstutz, B., Gastaldelli, M., Kälin, S., Imelli, N., Boucke, K., Wandeler, E., Mercer, J., Hemmi, S. and Greber, U. F. (2008). Subversion of CtBP1-controlled macropinocytosis by human adenovirus serotype 3. EMBO J. 27, 956-969.
3. Arhel, N. J., Souquere-Besse, S., Munier, S., Souque, P., Guadagnini, S., Rutherford, S., Prévost, M. C., Allen, T. D. and Charneau, P. (2007). HIV-1 DNA Flap formation promotes uncoating of the pre-integration complex at the nuclear pore. EMBO J. 26, 3025-3037.
4. Arii, J., Goto, H., Suenaga, T., Oyama, M., Kozuka-Hata, H., Imai, T., Minowa, A., Akashi, H., Arase, H., Kawaoka, Y. et al. (2010). Non-muscle myosin IIA is a functional entry receptor for herpes simplex virus-1. Nature 467, 859-862.
5. Barth, H., Schafer, C., Adah, M. I., Zhang, F., Linhardt, R. J., Toyoda, H., Kinoshita-Toyoda, A., Toida, T., Van Kuppevelt, T. H., Depla, E. et al. (2003). Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem. 278, 41003-41012.
6. Bartlett, A. H. and Park, P. W. (2010). Proteoglycans in host-pathogen interactions: molecular mechanisms and therapeutic implications. Expert Rev. Mol. Med. 12, e5.
7. Bertram, S., Glowacka, I., Müller, M. A., Lavender, H., Gnirss, K., Nehlmeier, I., Niemeyer, D., He, Y., Simmons, G., Drosten, C. et al. (2011). Cleavage and activation of the severe acute respiratory syndrome coronavirus spike protein by human airway trypsin-like protease. J. Virol. 85, 13363-13372.
8. Bose, S. and Banerjee, A. K. (2002). Role of heparan sulfate in human parainfluenza virus type 3 infection. Virology 298, 73-83.
9. Boulo, S., Akarsu, H., Ruigrok, R. W. and Baudin, F. (2007). Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res. 124, 12-21.
10. Bremner, K. H., Scherer, J., Yi, J., Vershinin, M., Gross, S. P. and Vallee, R. B. (2009). Adenovirus transport via direct interaction of cytoplasmic dynein with the viral capsid hexon subunit. Cell Host Microbe 6, 523-535.
11. Brindley, M. A., Hunt, C. L., Kondratowicz, A. S., Bowman, J., Sinn, P. L., McCray, P. B., Jr, Quinn, K., Weller, M. L., Chiorini, J. A. and Maury, W. (2011). Tyrosine kinase receptor Axl enhances entry of Zaire ebolavirus without direct interactions with the viral glycoprotein. Virology 415, 83-94.
12. Burckhardt, C. J. and Greber, U. F. (2009). Virus movements on the plasma membrane support infection and transmission between cells. PLoS Pathog. 5, e1000621.
13. Burckhardt, C. J., Suomalainen, M., Schoenenberger, P., Boucke, K., Hemmi, S. and Greber, U. F. (2011). Drifting motions of the adenovirus receptor CAR and immobile integrins initiate virus uncoating and membrane lytic protein exposure. Cell Host Microbe 10, 105-117.
14. Byrnes, A. P. and Griffin, D. E. (1998). Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 72, 7349-7356.
15. Callahan, M. K., Popernack, P. M., Tsutsui, S., Truong, L., Schlegel, R. A. and Henderson, A. J. (2003). Phosphatidylserine on HIV envelope is a cofactor for infection of monocytic cells. J. Immunol. 170, 4840-4845.
16. Cerqueira, C. and Schelhaas, M. (2012). Principles of polyoma- and papillomavirus uncoating. Med. Microbiol. Immunol. (Berl.) 201, 427-436.
17. Chakraborty, S., ValiyaVeettil, M., Sadagopan, S., Paudel, N. and Chandran, B. (2011). c-Cbl-mediated selective virus-receptor translocations into lipid rafts regulate productive Kaposi's sarcoma-associated herpesvirus infection in endothelial cells. J. Virol. 85, 12410-12430.
18. Chen, C. and Zhuang, X. (2008). Epsin 1 is a cargospecific adaptor for the clathrin-mediated endocytosis of the influenza virus. Proc. Natl. Acad. Sci. USA 105, 11790-11795.
19. Chen, Y., Maguire, T., Hileman, R. E., Fromm, J. R., Esko, J. D., Linhardt, R. J. and Marks, R. M. (1997). Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3, 866-871.
20. Choe, H., Farzan, M., Sun, Y., Sullivan, N., Rollins, B., Ponath, P. D., Wu, L., Mackay, C. R., LaRosa, G., Newman, W. et al. (1996). The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85, 1135-1148.
21. Coller, K. E., Berger, K. L., Heaton, N. S., Cooper, J. D., Yoon, R. and Randall, G. (2009). RNA interference and single particle tracking analysis of hepatitis C virus endocytosis. PLoS Pathog. 5, e1000702.
22. Coyne, C. B. and Bergelson, J. M. (2006). Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124, 119-131.
23. Cros, J. F., Garci{dotless}́a-Sastre, A. and Palese, P. (2005). An unconventional NLS is critical for the nuclear import of the influenza A virus nucleoprotein and ribonucleoprotein. Traffic 6, 205-213.
24. Cureton, D. K., Massol, R. H., Saffarian, S., Kirchhausen, T. L. and Whelan, S. P. (2009). Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 5, e1000394.
25. Damm, E. M. and Pelkmans, L. (2006). Systems biology of virus entry in mammalian cells. Cell. Microbiol. 8, 1219-1227.
26. Darshan, M. S., Lucchi, J., Harding, E. and Moroianu, J. (2004). The l2 minor capsid protein of human papillomavirus type 16 interacts with a network of nuclear import receptors. J. Virol. 78, 12179-12188.
27. de Vries, E., Tscherne, D. M., Wienholts, M. J., Cobos-Jiménez, V., Scholte, F., Garci{dotless}́a-Sastre, A., Rottier, P. J. and de Haan, C. A. (2011). Dissection of the influenza A virus endocytic routes reveals macropinocytosis as an alternative entry pathway. PLoS Pathog. 7, e1001329.
28. Deng, H., Liu, R., Ellmeier, W., Choe, S., Unutmaz, D., Burkhart, M., Di Marzio, P., Marmon, S., Sutton, R. E., Hill, C. M. et al. (1996). Identification of a major co-receptor for primary isolates of HIV-1. Nature 381, 661-666.
29. Dodding, M. P. and Way, M. (2011). Coupling viruses to dynein and kinesin-1. EMBO J. 30, 3527-3539.
30. Döhner, K., Wolfstein, A., Prank, U., Echeverri, C., Dujardin, D., Vallee, R. and Sodeik, B. (2002). Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13, 2795-2809.
31. Dorr, P., Westby, M., Dobbs, S., Griffin, P., Irvine, B., Macartney, M., Mori, J., Rickett, G., Smith-Burchnell, C., Napier, C. et al. (2005). Maraviroc (UK-427,857), a potent, orally bioavailable, and selective small-molecule inhibitor of chemokine receptor CCR5 with broadspectrum anti-human immunodeficiency virus type 1 activity. Antimicrob. Agents Chemother. 49, 4721-4732.
32. Dragic, T., Litwin, V., Allaway, G. P., Martin, S. R., Huang, Y., Nagashima, K. A., Cayanan, C., Maddon, P. J., Koup, R. A., Moore, J. P. et al. (1996). HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381, 667-673.
33. Drobni, P., Mistry, N., McMillan, N. and Evander, M. (2003). Carboxy-fluorescein diacetate, succinimidyl ester labeled papillomavirus virus-like particles fluoresce after internalization and interact with heparan sulfate for binding and entry. Virology 310, 163-172.
34. Eash, S., Manley, K., Gasparovic, M., Querbes, W. and Atwood, W. J. (2006). The human polyomaviruses. Cell. Mol. Life Sci. 63, 865-876.
35. Ehrlich, M., Boll, W., Van Oijen, A., Hariharan, R., Chandran, K., Nibert, M. L. and Kirchhausen, T. (2004). Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118, 591-605.
36. Eierhoff, T., Hrincius, E. R., Rescher, U., Ludwig, S. and Ehrhardt, C. (2010). The epidermal growth factor receptor (EGFR) promotes uptake of influenza A viruses (IAV) into host cells. PLoS Pathog. 6, e1001099.
37. Eisenberg, R. J., Atanasiu, D., Cairns, T. M., Gallagher, J. R., Krummenacher, C. and Cohen, G. H. (2012). Herpes virus fusion and entry: a story with many characters. Viruses 4, 800-832.
38. Engel, S., Heger, T., Mancini, R., Herzog, F., Kartenbeck, J., Hayer, A. and Helenius, A. (2011). Role of endosomes in simian virus 40 entry and infection. J. Virol. 85, 4198-4211.
39. Engelke, M. F., Burckhardt, C. J., Morf, M. K. and Greber, U. F. (2011). The dynactin complex enhances the speed of microtubule-dependent motions of adenovirus both towards and away from the nucleus. Viruses 3, 233-253.
40. Ewers, H., Romer, W., Smith, A. E., Bacia, K., Dmitrieff, S., Chai, W., Mancini, R., Kartenbeck, J., Chambon, V., Berland, L. et al. (2010). GM1 structure determines SV40-induced membrane invagination and infection. Nat. Cell Biol. 12, 11-18.
41. Farr, G. A., Zhang, L. G. and Tattersall, P. (2005). Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. USA 102, 17148-17153.
42. Feng, Y., Broder, C. C., Kennedy, P. E. and Berger, E. A. (1996). HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272, 872-877.
43. Fuchs, R. and Blaas, D. (2010). Uncoating of human rhinoviruses. Rev. Med. Virol. 20, 281-297.
44. Geiger, R., Andritschke, D., Friebe, S., Herzog, F., Luisoni, S., Heger, T. and Helenius, A. (2011). BAP31 and BiP are essential for dislocation of SV40 from the endoplasmic reticulum to the cytosol. Nat. Cell Biol. 13, 1305-1314.
45. Geijtenbeek, T. B., Kwon, D. S., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Middel, J., Cornelissen, I. L., Nottet, H. S., KewalRamani, V. N., Littman, D. R. et al. (2000). DC-SIGN, a dendritic cellspecific HIV-1-binding protein that enhances transinfection of T cells. Cell 100, 587-597.
46. Geraghty, R. J., Krummenacher, C., Cohen, G. H., Eisenberg, R. J. and Spear, P. G. (1998). Entry of alphaherpesviruses mediated by poliovirus receptorrelated protein 1 and poliovirus receptor. Science 280, 1618-1620.
47. Greber, U. F. (2002). Signalling in viral entry. Cell. Mol. Life Sci. 59, 608-626.
48. Greber, U. F., Willetts, M., Webster, P. and Helenius, A. (1993). Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75, 477-486.
49. Greber, U. F., Suomalainen, M., Stidwill, R. P., Boucke, K., Ebersold, M. W. and Helenius, A. (1997). The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 16, 5998-6007.
50. Grove, J. and Marsh, M. (2011). The cell biology of receptor-mediated virus entry. J. Cell Biol. 195, 1071-1082.
51. Gruenberg, J. (2009). Viruses and endosome membrane dynamics. Curr. Opin. Cell Biol. 21, 582-588.
52. Harrison, S. C. (2005). Mechanism of membrane fusion by viral envelope proteins. Adv. Virus Res. 64, 231-261.
53. Helenius, A. (2007). Virus entry and uncoating. In Fields Virology, pp. 99-118. Philadelphia, PA: Wolters Kluwer/ Lippincott Williams & Wilkins.
54. Helenius, A., Kartenbeck, J., Simons, K. and Fries, E. (1980). On the entry of Semliki forest virus into BHK-21 cells. J. Cell Biol. 84, 404-420.
55. Hummeler, K., Tomassini, N. and Sokol, F. (1970). Morphological aspects of the uptake of simian virus 40 by permissive cells. J. Virol. 6, 87-93.
56. Hunt, C. L., Kolokoltsov, A. A., Davey, R. A. and Maury, W. (2011). The Tyro3 receptor kinase Axl enhances macropinocytosis of Zaire ebolavirus. J. Virol. 85, 334-347.
57. Huotari, J. and Helenius, A. (2011). Endosome maturation. EMBO J. 30, 3481-3500.
58. Huotari, J., Meyer-Schaller, N., Hubner, M., Stauffer, S., Katheder, N., Horvath, P., Mancini, R., Helenius, A. and Peter, M. (2012). Cullin-3 regulates late endosome maturation. Proc. Natl. Acad. Sci. USA 109, 823-828.
59. Inoue, T. and Tsai, B. (2011). A large and intact viral particle penetrates the endoplasmic reticulum membrane to reach the cytosol. PLoS Pathog. 7, e1002037.
60. Johannsdottir, H. K., Mancini, R., Kartenbeck, J., Amato, L. and Helenius, A. (2009). Host cell factors and functions involved in vesicular stomatitis virus entry. J. Virol. 83, 440-453.
61. Jovasevic, V., Liang, L. and Roizman, B. (2008). Proteolytic cleavage of VP1-2 is required for release of herpes simplex virus 1 DNA into the nucleus. J. Virol. 82, 3311-3319.
62. Kälin, S., Amstutz, B., Gastaldelli, M., Wolfrum, N., Boucke, K., Havenga, M., DiGennaro, F., Liska, N., Hemmi, S. and Greber, U. F. (2010). Macropinocytotic uptake and infection of human epithelial cells with species B2 adenovirus type 35. J. Virol. 84, 5336-5350.
63. Kann, M., Sodeik, B., Vlachou, A., Gerlich, W. H. and Helenius, A. (1999). Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex. J. Cell Biol. 145, 45-55.
64. Kartenbeck, J., Stukenbrok, H. and Helenius, A. (1989). Endocytosis of simian virus 40 into the endoplasmic reticulum. J. Cell Biol. 109, 2721-2729.
65. Kemler, I., Whittaker, G. and Helenius, A. (1994). Nuclear import of microinjected influenza virus ribonucleoproteins. Virology 202, 1028-1033.
66. Kilby, J. M., Hopkins, S., Venetta, T. M., DiMassimo, B., Cloud, G. A., Lee, J. Y., Alldredge, L., Hunter, E., Lambert, D., Bolognesi, D. et al. (1998). Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry. Nat. Med. 4, 1302-1307.
67. Kirchhausen, T. (2000). Clathrin. Annu. Rev. Biochem. 69, 699-727.
68. Klasse, P. J. (2012). The molecular basis of HIV entry. Cell. Microbiol. 14, 1183-1192.
69. Klatzmann, D., Champagne, E., Chamaret, S., Gruest, J., Guetard, D., Hercend, T., Gluckman, J. C. and Montagnier, L. (1984). T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 312, 767-768.
70. Klimstra, W. B., Nangle, E. M., Smith, M. S., Yurochko, A. D. and Ryman, K. D. (2003). DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J. Virol. 77, 12022-12032.
71. Klucevsek, K., Daley, J., Darshan, M. S., Bordeaux, J. and Moroianu, J. (2006). Nuclear import strategies of high-risk HPV18 L2 minor capsid protein. Virology 352, 200-208.
72. Kroschewski, H., Allison, S. L., Heinz, F. X. and Mandl, C. W. (2003). Role of heparan sulfate for attachment and entry of tick-borne encephalitis virus. Virology 308, 92-100.
73. Lehmann, M. J., Sherer, N. M., Marks, C. B., Pypaert, M. and Mothes, W. (2005). Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 170, 317-325.
74. Leopold, P. L., Kreitzer, G., Miyazawa, N., Rempel, S., Pfister, K. K., Rodriguez-Boulan, E. and Crystal, R. G. (2000). Dynein- and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis. Hum. Gene Ther. 11, 151-165.
75. Lozach, P. Y., Lortat-Jacob, H., de Lacroix de Lavalette, A., Staropoli, I., Foung, S., Amara, A., Houles, C., Fieschi, F., Schwartz, O., Virelizier, J. L. et al. (2003). DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. J. Biol. Chem. 278, 20358-20366.
76. Lozach, P. Y., Huotari, J. and Helenius, A. (2011a). Late-penetrating viruses. Curr. Opin. Virol. 1, 35-43.
77. Lozach, P. Y., Kühbacher, A., Meier, R., Mancini, R., Bitto, D., Bouloy, M. and Helenius, A. (2011b). DCSIGN as a receptor for phleboviruses. Cell Host Microbe 10, 75-88.
78. Marsh, M. and Helenius, A. (2006). Virus entry: open sesame. Cell 124, 729-740.
79. Matlin, K. S., Reggio, H., Helenius, A. and Simons, K. (1981). Infectious entry pathway of influenza virus in a canine kidney cell line. J. Cell Biol. 91, 601-613.
80. Matthews, T., Salgo, M., Greenberg, M., Chung, J., DeMasi, R. and Bolognesi, D. (2004). Enfuvirtide: the first therapy to inhibit the entry of HIV-1 into host CD4 lymphocytes. Nat. Rev. Drug Discov. 3, 215-225.
81. Mayer, D., Molawi, K., Marti{dotless}́nez-Sobrido, L., Ghanem, A., Thomas, S., Baginsky, S., Grossmann, J., Garci{dotless}́a-Sastre, A. and Schwemmle, M. (2007). Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J. Proteome Res. 6, 672-682.
82. Meertens, L., Carnec, X., Lecoin, M. P., Ramdasi, R., Guivel-Benhassine, F., Lew, E., Lemke, G., Schwartz, O. and Amara, A. (2012). The TIM and TAM families of phosphatidylserine receptors mediate dengue virus entry. Cell Host Microbe 12, 544-557.
83. Meier, O., Boucke, K., Hammer, S. V., Keller, S., Stidwill, R. P., Hemmi, S. and Greber, U. F. (2002). Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 158, 1119-1131.
84. Mercer, J. and Helenius, A. (2008). Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320, 531-535.
85. Mercer, J. and Helenius, A. (2009). Virus entry by macropinocytosis. Nat. Cell Biol. 11, 510-520.
86. Mercer, J. and Helenius, A. (2012). Gulping rather than sipping: macropinocytosis as a way of virus entry. Curr. Opin. Microbiol. 15, 490-499.
87. Mercer, J., Schelhaas, M. and Helenius, A. (2010). Virus entry by endocytosis. Annu. Rev. Biochem. 79, 803-833.
88. Montgomery, R. I., Warner, M. S., Lum, B. J. and Spear, P. G. (1996). Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87, 427-436.
89. Morizono, K., Xie, Y., Olafsen, T., Lee, B., Dasgupta, A., Wu, A. M. and Chen, I. S. (2011). The soluble serum protein Gas6 bridges virion envelope phosphatidylserine to the TAM receptor tyrosine kinase Axl to mediate viral entry. Cell Host Microbe 9, 286-298.
90. Nakanishi, A., Clever, J., Yamada, M., Li, P. P. and Kasamatsu, H. (1996). Association with capsid proteins promotes nuclear targeting of simian virus 40 DNA. Proc. Natl. Acad. Sci. USA 93, 96-100.
91. Nakanishi, A., Shum, D., Morioka, H., Otsuka, E. and Kasamatsu, H. (2002). Interaction of the Vp3 nuclear localization signal with the importin alpha 2/beta heterodimer directs nuclear entry of infecting simian virus 40. J. Virol. 76, 9368-9377.
92. Nanbo, A., Imai, M., Watanabe, S., Noda, T., Takahashi, K., Neumann, G., Halfmann, P. and Kawaoka, Y. (2010). Ebolavirus is internalized into host cells via macropinocytosis in a viral glycoproteindependent manner. PLoS Pathog. 6, e1001121.
93. Nemerow, G. R. (2000). Cell receptors involved in adenovirus entry. Virology 274, 1-4.
94. Ojala, P. M., Sodeik, B., Ebersold, M. W., Kutay, U. and Helenius, A. (2000). Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol. Cell. Biol. 20, 4922-4931.
95. Pasdeloup, D., Blondel, D., Isidro, A. L. and Rixon, F. J. (2009). Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J. Virol. 83, 6610-6623.
96. Pearse, B. M. (1976). Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc. Natl. Acad. Sci. USA 73, 1255-1259.
97. Pelkmans, L., Fava, E., Grabner, H., Hannus, M., Habermann, B., Krausz, E. and Zerial, M. (2005). Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436, 78-86.
98. Pérez-Berná, A. J., Ortega-Esteban, A., Menéndez-Conejero, R., Winkler, D. C., Menéndez, M., Steven, A. C., Flint, S. J., de Pablo, P. J. and San Marti{dotless}́n, C. (2012). The role of capsid maturation on adenovirus priming for sequential uncoating. J. Biol. Chem. 287, 31582-31595.
99. Pöhlmann, S., Baribaud, F. and Doms, R. W. (2001). DC-SIGN and DC-SIGNR: helping hands for HIV. Trends Immunol. 22, 643-646.
100. Prchla, E., Plank, C., Wagner, E., Blaas, D. and Fuchs, R. (1995). Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2. J. Cell Biol. 131, 111-123.
101. Preston, V. G., Murray, J., Preston, C. M., McDougall, I. M. and Stow, N. D. (2008). The UL25 gene product of herpes simplex virus type 1 is involved in uncoating of the viral genome. J. Virol. 82, 6654-6666.
102. Puntener, D. and Greber, U. F. (2009). DNA-tumor virus entry-from plasma membrane to the nucleus. Semin. Cell Dev. Biol. 20, 631-642.
103. Qu, Q., Sawa, H., Suzuki, T., Semba, S., Henmi, C., Okada, Y., Tsuda, M., Tanaka, S., Atwood, W. J. and Nagashima, K. (2004). Nuclear entry mechanism of the human polyomavirus JC virus-like particle: role of importins and the nuclear pore complex. J. Biol. Chem. 279, 27735-27742.
104. Rabe, B., Vlachou, A., Panté, N., Helenius, A. and Kann, M. (2003). Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc. Natl. Acad. Sci. USA 100, 9849-9854.
105. Rabe, B., Delaleau, M., Bischof, A., Foss, M., Sominskaya, I., Pumpens, P., Cazenave, C., Castroviejo, M. and Kann, M. (2009). Nuclear entry of hepatitis B virus capsids involves disintegration to protein dimers followed by nuclear reassociation to capsids. PLoS Pathog. 5, e1000563.
106. Radtke, K., Kieneke, D., Wolfstein, A., Michael, K., Steffen, W., Scholz, T., Karger, A. and Sodeik, B. (2010). Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog. 6, e1000991.
107. Raghu, H., Sharma-Walia, N., Veettil, M. V., Sadagopan, S. and Chandran, B. (2009). Kaposi's sarcoma-associated herpesvirus utilizes an actin polymerization-dependent macropinocytic pathway to enter human dermal microvascular endothelial and human umbilical vein endothelial cells. J. Virol. 83, 4895-4911.
108. Rust, M. J., Lakadamyali, M., Zhang, F. and Zhuang, X. (2004). Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat. Struct. Mol. Biol. 11, 567-573.
109. Saeed, M. F., Kolokoltsov, A. A., Albrecht, T. and Davey, R. A. (2010). Cellular entry of ebola virus involves uptake by a macropinocytosis-like mechanism and subsequent trafficking through early and late endosomes. PLoS Pathog. 6, e1001110.
110. Satoh, T., Arii, J., Suenaga, T., Wang, J., Kogure, A., Uehori, J., Arase, N., Shiratori, I., Tanaka, S., Kawaguchi, Y. et al. (2008). PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132, 935-944.
111. Sayah, D. M., Sokolskaja, E., Berthoux, L. and Luban, J. (2004). Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430, 569-573.
112. Schelhaas, M. (2010). Come in and take your coat off -how host cells provide endocytosis for virus entry. Cell. Microbiol. 12, 1378-1388.
113. Schelhaas, M., Malmström, J., Pelkmans, L., Haugstetter, J., Ellgaard, L., Grünewald, K. and Helenius, A. (2007). Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131, 516-529.
114. Schelhaas, M., Ewers, H., Rajamäki, M. L., Day, P. M., Schiller, J. T. and Helenius, A. (2008). Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog. 4, e1000148.
115. Schmidt, F. I., Bleck, C. K., Helenius, A. and Mercer, J. (2011). Vaccinia extracellular virions enter cells by macropinocytosis and acid-activated membrane rupture. EMBO J. 30, 3647-3661.
116. Schmitz, A., Schwarz, A., Foss, M., Zhou, L., Rabe, B., Hoellenriegel, J., Stoeber, M., Panté, N. and Kann, M. (2010). Nucleoporin 153 arrests the nuclear import of hepatitis B virus capsids in the nuclear basket. PLoS Pathog. 6, e1000741.
117. Schober, D., Kronenberger, P., Prchla, E., Blaas, D. and Fuchs, R. (1998). Major and minor receptor group human rhinoviruses penetrate from endosomes by different mechanisms. J. Virol. 72, 1354-1364.
118. Shah, V. B., Shi, J., Hout, D. R., Oztop, I., Krishnan, L., Ahn, J., Shotwell, M. S., Engelman, A. and Aiken, C. (2013). The host proteins transportin SR2/TNPO3 and cyclophilin A exert opposing effects on HIV-1 uncoating. J. Virol. 87, 422-432.
119. Shimojima, M., Takada, A., Ebihara, H., Neumann, G., Fujioka, K., Irimura, T., Jones, S., Feldmann, H. and Kawaoka, Y. (2006). Tyro3 family-mediated cell entry of Ebola and Marburg viruses. J. Virol. 80, 10109-10116.
120. Shukla, D., Rowe, C. L., Dong, Y., Racaniello, V. R. and Spear, P. G. (1999). The murine homolog (Mph) of human herpesvirus entry protein B (HveB) mediates entry of pseudorabies virus but not herpes simplex virus types 1 and 2. J. Virol. 73, 4493-4497.
121. Sieczkarski, S. B. and Whittaker, G. R. (2002). Dissecting virus entry via endocytosis. J. Gen. Virol. 83, 1535-1545.
122. Simmons, G., Reeves, J. D., Grogan, C. C., Vandenberghe, L. H., Baribaud, F., Whitbeck, J. C., Burke, E., Buchmeier, M. J., Soilleux, E. J., Riley, J. L. et al. (2003). DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 305, 115-123.
123. Simmons, G., Gosalia, D. N., Rennekamp, A. J., Reeves, J. D., Diamond, S. L. and Bates, P. (2005). Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad. Sci. USA 102, 11876-11881.
124. Simmons, G., Bertram, S., Glowacka, I., Steffen, I., Chaipan, C., Agudelo, J., Lu, K., Rennekamp, A. J., Hofmann, H., Bates, P. et al. (2011). Different host cell proteases activate the SARS-coronavirus spike-protein for cell-cell and virus-cell fusion. Virology 413, 265-274.
125. Skehel, J. J. and Wiley, D. C. (2000). Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69, 531-569.
126. Sodeik, B., Ebersold, M. W. and Helenius, A. (1997). Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136, 1007-1021.
127. Spear, P. G., Eisenberg, R. J. and Cohen, G. H. (2000). Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275, 1-8.
128. Stremlau, M., Owens, C. M., Perron, M. J., Kiessling, M., Autissier, P. and Sodroski, J. (2004). The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427, 848-853.
129. Stremlau, M., Perron, M., Lee, M., Li, Y., Song, B., Javanbakht, H., Diaz-Griffero, F., Anderson, D. J., Sundquist, W. I. and Sodroski, J. (2006). Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc. Natl. Acad. Sci. USA 103, 5514-5519.
130. Strunze, S., Engelke, M. F., Wang, I. H., Puntener, D., Boucke, K., Schleich, S., Way, M., Schoenenberger, P., Burckhardt, C. J. and Greber, U. F. (2011). Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 10, 210-223.
131. Suenaga, T., Satoh, T., Somboonthum, P., Kawaguchi, Y., Mori, Y. and Arase, H. (2010). Myelin-associated glycoprotein mediates membrane fusion and entry of neurotropic herpesviruses. Proc. Natl. Acad. Sci. USA 107, 866-871.
132. Summerford, C. and Samulski, R. J. (1998). Membraneassociated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72, 1438-1445.
133. Suomalainen, M. and Greber, U. F. (2013). Uncoating of non-enveloped viruses. Curr. Opin. Virol. 3, 27-33.
134. Suomalainen, M., Nakano, M. Y., Keller, S., Boucke, K., Stidwill, R. P. and Greber, U. F. (1999). Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J. Cell Biol. 144, 657-672.
135. Svajger, U., Anderluh, M., Jeras, M. and Obermajer, N. (2010). C-type lectin DC-SIGN: an adhesion, signalling and antigen-uptake molecule that guides dendritic cells in immunity. Cell. Signal. 22, 1397-1405.
136. Tassaneetrithep, B., Burgess, T. H., Granelli-Piperno, A., Trumpfheller, C., Finke, J., Sun, W., Eller, M. A., Pattanapanyasat, K., Sarasombath, S., Birx, D. L. et al. (2003). DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197, 823-829.
137. Valiya Veettil, M., Sadagopan, S., Kerur, N., Chakraborty, S. and Chandran, B. (2010). Interaction of c-Cbl with myosin IIA regulates Bleb associated macropinocytosis of Kaposi's sarcoma-associated herpesvirus. PLoS Pathog. 6, e1001238.
138. van der Schaar, H. M., Rust, M. J., Chen, C., van der Ende-Metselaar, H., Wilschut, J., Zhuang, X. and Smit, J. M. (2008). Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 4, e1000244.
139. Wahlberg, J. M. and Garoff, H. (1992). Membrane fusion process of Semliki Forest virus. I: Low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells. J. Cell Biol. 116, 339-348.
140. West, M. A., Bretscher, M. S. and Watts, C. (1989). Distinct endocytotic pathways in epidermal growth factorstimulated human carcinoma A431 cells. J. Cell Biol. 109, 2731-2739.
141. Wodrich, H., Cassany, A., D'Angelo, M. A., Guan, T., Nemerow, G. and Gerace, L. (2006). Adenovirus core protein pVII is translocated into the nucleus by multiple import receptor pathways. J. Virol. 80, 9608-9618.
142. Wolfrum, N. and Greber, U. F. (2013). Adenovirus signalling in entry. Cell. Microbiol. 15, 53-62.
143. Wu, W. W., Sun, Y. H. and Panté, N. (2007). Nuclear import of influenza A viral ribonucleoprotein complexes is mediated by two nuclear localization sequences on viral nucleoprotein. Virol. J. 4, 49.
144. Yamauchi, Y., Kiriyama, K., Kubota, N., Kimura, H., Usukura, J. and Nishiyama, Y. (2008). The UL14 tegument protein of herpes simplex virus type 1 is required for efficient nuclear transport of the alpha transinducing factor VP16 and viral capsids. J. Virol. 82, 1094-1106.
145. Yamauchi, Y., Boukari, H., Banerjee, I., Sbalzarini, I. F., Horvath, P. and Helenius, A. (2011). Histone deacetylase 8 is required for centrosome cohesion and influenza A virus entry. PLoS Pathog. 7, e1002316.
146. Zaitseva, E., Yang, S. T., Melikov, K., Pourmal, S. and Chernomordik, L. V. (2010). Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog. 6, e1001131.