Host cell factors in filovirus entry: Novel players, new insights

Viruses

Volumn 4, Issue 12, 2012, Pages 3336-3362

  Hofmann Winkler, Heike ^a   Kaup, Franziska ^a   Pöhlmann, Stefan ^a  

^a GERMAN PRIMATE CENTER   (Germany)

Author keywords

Axl; Cathepsins; Ebola; Entry; Filovirus; Marburg; NPC1; TIM 1

Indexed keywords

AX1 PROTEIN; CATHEPSIN B; CATHEPSIN L; CELL PROTEIN; HOST CELL FACTOR; KIDNEY INJURY MOLECULE 1; LECTIN; MEMBRANE PROTEIN; NPC1 PROTEIN; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; VIRUS GLYCOPROTEIN;

CELL MEMBRANE; DENDRITIC CELL; EPITHELIUM CELL; FILOVIRUS; HOST CELL; HUMAN; LYSOSOME; MACROPHAGE; MEMBRANE FUSION; MUCOSA; NONHUMAN; PERSISTENT VIRUS INFECTION; PINOCYTOSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REVIEW; T LYMPHOCYTE; VIRAL TROPISM; VIRION; VIRUS ENTRY; VIRUS ENVELOPE;

DENDRITIC CELLS; EPITHELIAL CELLS; FILOVIRIDAE; GLYCOPROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; LECTINS; MACROPHAGES; PROTEIN BINDING; RECEPTORS, VIRUS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

MARBURGVIRUS;

EID: 84871869230     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v4123336     Document Type: Review

References (192)

1. Mahanty, S.; Bray, M. Pathogenesis of filoviral haemorrhagic fevers. Lancet Infect. Dis. 2004, 4, 487-498.
2. Kuhn, J.H.; Becker, S.; Ebihara, H.; Geisbert, T.W.; Jahrling, P.B.; Kawaoka, Y.; Netesov, S.V.; Nichol, S.T.; Peters, C.J.; Volchkov, V.E.; et al. Family Filoviridae. In Virus Taxonomy-Ninth Report of the International Committee on Taxonomy of Viruses; King, A.M.Q., Adams, M.J., Carstens, E.B., Lefkowitz, E.J., Eds.; Elsevier/Academic Press: London, UK, 2001; pp. 665-671.
3. Adams, M.J.; Carstens, E.B. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2012). Arch. Virol. 2012, 157, 1411-1422.
4. Hutchinson, K.L.; Rollin, P.E. Cytokine and chemokine expression in humans infected with Sudan Ebola virus. J. Infect. Dis. 2007, 196, S357-S363.
5. Kuhn, J.H.; Dodd, L.E.; Wahl-Jensen, V.; Radoshitzky, S.R.; Bavari, S.; Jahrling, P.B. Evaluation of perceived threat differences posed by filovirus variants. Biosecur. Bioterror. 2011, 9, 361-371.
6. Barrette, R.W.; Metwally, S.A.; Rowland, J.M.; Xu, L.; Zaki, S.R.; Nichol, S.T.; Rollin, P.E.; Towner, J.S.; Shieh, W.J.; Batten, B.; et al. Discovery of swine as a host for the Reston ebolavirus. Science 2009, 325, 204-206.
7. Miranda, M.E.; Ksiazek, T.G.; Retuya, T.J.; Khan, A.S.; Sanchez, A.; Fulhorst, C.F.; Rollin, P.E.; Calaor, A.B.; Manalo, D.L.; Roces, M.C.; et al. Epidemiology of Ebola (subtype Reston) virus in the Philippines, 1996. J. Infect. Dis. 1999, 179, S115-S119.
8. Rollin, P.E.; Williams, R.J.; Bressler, D.S.; Pearson, S.; Cottingham, M.; Pucak, G.; Sanchez, A.; Trappier, S.G.; Peters, R.L.; Greer, P.W.; et al. Ebola (subtype Reston) virus among quarantined nonhuman primates recently imported from the Philippines to the United States. J. Infect. Dis. 1999, 179, S108-S114.
9. Jahrling, P.B.; Geisbert, T.W.; Jaax, N.K.; Hanes, M.A.; Ksiazek, T.G.; Peters, C.J. Experimental infection of cynomolgus macaques with Ebola-Reston filoviruses from the 1989-1990 U.S. epizootic. Arch. Virol. Suppl. 1996, 11, 115-134.
10. Leroy, E.M.; Kumulungui, B.; Pourrut, X.; Rouquet, P.; Hassanin, A.; Yaba, P.; Delicat, A.; Paweska, J.T.; Gonzalez, J.P.; Swanepoel, R. Fruit bats as reservoirs of Ebola virus. Nature 2005, 438, 575-576.
11. Pourrut, X.; Souris, M.; Towner, J.S.; Rollin, P.E.; Nichol, S.T.; Gonzalez, J.P.; Leroy, E. Large serological survey showing cocirculation of Ebola and Marburg viruses in Gabonese bat populations, and a high seroprevalence of both viruses in Rousettus aegyptiacus. BMC Infect. Dis. 2009, 9, 159.
12. Towner, J.S.; Amman, B.R.; Sealy, T.K.; Carroll, S.A.; Comer, J.A.; Kemp, A.; Swanepoel, R.; Paddock, C.D.; Balinandi, S.; Khristova, M.L.; et al. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog. 2009, 5, e1000536.
13. Kuzmin, I.V.; Niezgoda, M.; Franka, R.; Agwanda, B.; Markotter, W.; Breiman, R.F.; Shieh, W.J.; Zaki, S.R.; Rupprecht, C.E. Marburg virus in fruit bat, Kenya. Emerg. Infect. Dis. 2010, 16, 352-354.
14. Taniguchi, S.; Watanabe, S.; Masangkay, J.S.; Omatsu, T.; Ikegami, T.; Alviola, P.; Ueda, N.; Iha, K.; Fujii, H.; Ishii, Y.; et al. Reston Ebolavirus antibodies in bats, the Philippines. Emerg. Infect. Dis. 2011, 17, 1559-1560.
15. Negredo, A.; Palacios, G.; Vazquez-Moron, S.; Gonzalez, F.; Dopazo, H.; Molero, F.; Juste, J.; Quetglas, J.; Savji, N.; de la Cruz, M.M.; et al. Discovery of an ebolavirus-like filovirus in europe. PLoS Pathog. 2011, 7, e1002304.
16. Leroy, E.M.; Rouquet, P.; Formenty, P.; Souquiere, S.; Kilbourne, A.; Froment, J.M.; Bermejo, M.; Smit, S.; Karesh, W.; Swanepoel, R.; et al. Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 2004, 303, 387-390.
17. Bermejo, M.; Rodriguez-Teijeiro, J.D.; Illera, G.; Barroso, A.; Vila, C.; Walsh, P.D. Ebola outbreak killed 5000 gorillas. Science 2006, 314, 1564.
18. Sayama, Y.; Demetria, C.; Saito, M.; Azul, R.R.; Taniguchi, S.; Fukushi, S.; Yoshikawa, T.; Iizuka, I.; Mizutani, T.; Kurane, I.; et al. A seroepidemiologic study of Reston ebolavirus in swine in the Philippines. BMC Vet. Res. 2012, 8, 82.
19. Miller, E.H.; Harrison, J.S.; Radoshitzky, S.R.; Higgins, C.D.; Chi, X.; Dong, L.; Kuhn, J.H.; Bavari, S.; Lai, J.R.; Chandran, K. Inhibition of Ebola virus entry by a C-peptide targeted to endosomes. J. Biol. Chem. 2011, 286, 15854-15861.
20. Cote, M.; Misasi, J.; Ren, T.; Bruchez, A.; Lee, K.; Filone, C.M.; Hensley, L.; Li, Q.; Ory, D.; Chandran, K.; et al. Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 2011, 477, 344-348.
21. Saeed, M.F.; Kolokoltsov, A.A.; Freiberg, A.N.; Holbrook, M.R.; Davey, R.A. Phosphoinositide-3 kinase-Akt pathway controls cellular entry of Ebola virus. PLoS Pathog. 2008, 4, e1000141.
22. Barrientos, L.G.; O'Keefe, B.R.; Bray, M.; Sanchez, A.; Gronenborn, A.M.; Boyd, M.R. Cyanovirin-N binds to the viral surface glycoprotein, GP1,2 and inhibits infectivity of Ebola virus. Antivir. Res. 2003, 58, 47-56.
23. Basu, A.; Li, B.; Mills, D.M.; Panchal, R.G.; Cardinale, S.C.; Butler, M.M.; Peet, N.P.; Majgier-Baranowska, H.; Williams, J.D.; Patel, I.; et al. Identification of a small-molecule entry inhibitor for filoviruses. J. Virol. 2011, 85, 3106-3119.
24. Shah, P.P.; Wang, T.; Kaletsky, R.L.; Myers, M.C.; Purvis, J.E.; Jing, H.; Huryn, D.M.; Greenbaum, D.C.; Smith, A.B., III; Bates, P.; et al. A small-molecule oxocarbazate inhibitor of human cathepsin L blocks severe acute respiratory syndrome and ebola pseudotype virus infection into human embryonic kidney 293T cells. Mol. Pharmacol. 2010, 78, 319-324.
25. Groseth, A.; Marzi, A.; Hoenen, T.; Herwig, A.; Gardner, D.; Becker, S.; Ebihara, H.; Feldmann, H. The Ebola virus glycoprotein contributes to but is not sufficient for virulence in vivo. PLoS Pathog. 2012, 8, e1002847.
26. Takada, A.; Robison, C.; Goto, H.; Sanchez, A.; Murti, K.G.; Whitt, M.A.; Kawaoka, Y. A system for functional analysis of Ebola virus glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 14764-14769.
27. Wool-Lewis, R.J.; Bates, P. Characterization of Ebola virus entry by using pseudotyped viruses: Identification of receptor-deficient cell lines. J. Virol. 1998, 72, 3155-3160.
28. Yang, Z.Y.; Duckers, H.J.; Sullivan, N.J.; Sanchez, A.; Nabel, E.G.; Nabel, G.J. Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat. Med. 2000, 6, 886-889.
29. Feldmann, H.; Volchkov, V.E.; Volchkova, V.A.; Klenk, H.D. The glycoproteins of Marburg and Ebola virus and their potential roles in pathogenesis. Arch. Virol. Suppl. 1999, 15, 159-169.
30. Hoenen, T.; Groseth, A.; Falzarano, D.; Feldmann, H. Ebola virus: Unravelling pathogenesis to combat a deadly disease. Trends Mol. Med. 2006, 12, 206-215.
31. Takada, A.; Kawaoka, Y. The pathogenesis of Ebola hemorrhagic fever. Trends Microbiol. 2001, 9, 506-511.
32. Volchkov, V.E.; Feldmann, H.; Volchkova, V.A.; Klenk, H.D. Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 5762-5767.
33. Sanchez, A.; Yang, Z.Y.; Xu, L.; Nabel, G.J.; Crews, T.; Peters, C.J. Biochemical analysis of the secreted and virion glycoproteins of Ebola virus. J. Virol. 1998, 72, 6442-6447.
34. Powlesland, A.S.; Fisch, T.; Taylor, M.E.; Smith, D.F.; Tissot, B.; Dell, A.; Pöhlmann, S.; Drickamer, K. A novel mechanism for LSECtin binding to Ebola virus surface glycoprotein through truncated glycans. J. Biol. Chem. 2008, 283, 593-602.
35. Ritchie, G.; Harvey, D.J.; Stroeher, U.; Feldmann, F.; Feldmann, H.; Wahl-Jensen, V.; Royle, L.; Dwek, R.A.; Rudd, P.M. Identification of N-glycans from Ebola virus glycoproteins by matrix-assisted laser desorption/ionisation time-of-flight and negative ion electrospray tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2010, 24, 571-585.
36. Manicassamy, B.; Wang, J.; Rumschlag, E.; Tymen, S.; Volchkova, V.; Volchkov, V.; Rong, L. Characterization of Marburg virus glycoprotein in viral entry. Virology 2007, 358, 79-88.
37. Lee, J.E.; Fusco, M.L.; Hessell, A.J.; Oswald, W.B.; Burton, D.R.; Saphire, E.O. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 2008, 454, 177-182.
38. Sanchez, A.; Trappier, S.G.; Mahy, B.W.; Peters, C.J.; Nichol, S.T. The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing. Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 3602-3607.
39. Jeffers, S.A.; Sanders, D.A.; Sanchez, A. Covalent modifications of the ebola virus glycoprotein. J. Virol. 2002, 76, 12463-12472.
40. Simmons, G.; Wool-Lewis, R.J.; Baribaud, F.; Netter, R.C.; Bates, P. Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence. J. Virol. 2002, 76, 2518-2528.
41. Takada, A.; Fujioka, K.; Tsuiji, M.; Morikawa, A.; Higashi, N.; Ebihara, H.; Kobasa, D.; Feldmann, H.; Irimura, T.; Kawaoka, Y. Human macrophage C-type lectin specific for galactose and N-acetylgalactosamine promotes filovirus entry. J. Virol. 2004, 78, 2943-2947.
42. Malashkevich, V.N.; Schneider, B.J.; McNally, M.L.; Milhollen, M.A.; Pang, J.X.; Kim, P.S. Core structure of the envelope glycoprotein GP2 from Ebola virus at 1.9-A resolution. Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 2662-2667.
43. Weissenhorn, W.; Carfi, A.; Lee, K.H.; Skehel, J.J.; Wiley, D.C. Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol. Cell 1998, 2, 605-616.
44. Kielian, M.; Rey, F.A. Virus membrane-fusion proteins: More than one way to make a hairpin. Nat. Rev. Microbiol. 2006, 4, 67-76.
45. Kuhn, J.H.; Radoshitzky, S.R.; Guth, A.C.; Warfield, K.L.; Li, W.; Vincent, M.J.; Towner, J.S.; Nichol, S.T.; Bavari, S.; Choe, H.; et al. Conserved receptor-binding domains of Lake Victoria marburgvirus and Zaire ebolavirus bind a common receptor. J. Biol. Chem. 2006, 281, 15951-15958.
46. Neumann, G.; Geisbert, T.W.; Ebihara, H.; Geisbert, J.B.; Daddario-DiCaprio, K.M.; Feldmann, H.; Kawaoka, Y. Proteolytic processing of the Ebola virus glycoprotein is not critical for Ebola virus replication in nonhuman primates. J. Virol. 2007, 81, 2995-2998.
47. Neumann, G.; Feldmann, H.; Watanabe, S.; Lukashevich, I.; Kawaoka, Y. Reverse genetics demonstrates that proteolytic processing of the Ebola virus glycoprotein is not essential for replication in cell culture. J. Virol. 2002, 76, 406-410.
48. Jaskierny, A.J.; Panahi, A.; Feig, M. Effect of flanking residues on the conformational sampling of the internal fusion peptide from Ebola virus. Proteins 2011, 79, 1109-1117.
49. Watanabe, S.; Takada, A.; Watanabe, T.; Ito, H.; Kida, H.; Kawaoka, Y. Functional importance of the coiled-coil of the Ebola virus glycoprotein. J. Virol. 2000, 74, 10194-10201.
50. Usami, K.; Matsuno, K.; Igarashi, M.; Denda-Nagai, K.; Takada, A.; Irimura, T. Involvement of viral envelope GP2 in Ebola virus entry into cells expressing the macrophage galactose-type C-type lectin. Biochem. Biophys. Res. Commun. 2011, 407, 74-78.
51. Adam, B.; Lins, L.; Stroobant, V.; Thomas, A.; Brasseur, R. Distribution of hydrophobic residues is crucial for the fusogenic properties of the Ebola virus GP2 fusion peptide. J. Virol. 2004, 78, 2131-2136.
52. Ito, H.; Watanabe, S.; Sanchez, A.; Whitt, M.A.; Kawaoka, Y. Mutational analysis of the putative fusion domain of Ebola virus glycoprotein. J. Virol. 1999, 73, 8907-8912.
53. Ruiz-Arguello, M.B.; Goni, F.M.; Pereira, F.B.; Nieva, J.L. Phosphatidylinositol-dependent membrane fusion induced by a putative fusogenic sequence of Ebola virus. J. Virol. 1998, 72, 1775-1781.
54. Hofmann, H.; Pöhlmann, S. Cellular entry of the SARS coronavirus. Trends Microbiol. 2004, 12, 466-472.
55. Manicassamy, B.; Wang, J.; Jiang, H.; Rong, L. Comprehensive analysis of ebola virus GP1 in viral entry. J. Virol. 2005, 79, 4793-4805.
56. Schornberg, K.; Matsuyama, S.; Kabsch, K.; Delos, S.; Bouton, A.; White, J. Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J. Virol. 2006, 80, 4174-4178.
57. Chandran, K.; Sullivan, N.J.; Felbor, U.; Whelan, S.P.; Cunningham, J.M. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 2005, 308, 1643-1645.
58. Dias, J.M.; Kuehne, A.I.; Abelson, D.M.; Bale, S.; Wong, A.C.; Halfmann, P.; Muhammad, M.A.; Fusco, M.L.; Zak, S.E.; Kang, E.; et al. A shared structural solution for neutralizing ebolaviruses. Nat. Struct. Mol. Biol. 2011, 18, 1424-1427.
59. Gregory, S.M.; Harada, E.; Liang, B.; Delos, S.E.; White, J.M.; Tamm, L.K. Structure and function of the complete internal fusion loop from Ebolavirus glycoprotein 2. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 11211-11216.
60. Stroher, U.; West, E.; Bugany, H.; Klenk, H.D.; Schnittler, H.J.; Feldmann, H. Infection and activation of monocytes by Marburg and Ebola viruses. J. Virol. 2001, 75, 11025-11033.
61. Gupta, M.; Mahanty, S.; Ahmed, R.; Rollin, P.E. Monocyte-derived human macrophages and peripheral blood mononuclear cells infected with ebola virus secrete MIP-1alpha and TNF-alpha and inhibit poly-IC-induced IFN-alpha in vitro. Virology 2001, 284, 20-25.
62. Bosio, C.M.; Aman, M.J.; Grogan, C.; Hogan, R.; Ruthel, G.; Negley, D.; Mohamadzadeh, M.; Bavari, S.; Schmaljohn, A. Ebola and Marburg viruses replicate in monocyte-derived dendritic cells without inducing the production of cytokines and full maturation. J. Infect. Dis. 2003, 188, 1630-1638.
63. Geisbert, T.W.; Jahrling, P.B.; Hanes, M.A.; Zack, P.M. Association of Ebola-related Reston virus particles and antigen with tissue lesions of monkeys imported to the United States. J. Comp. Pathol. 1992, 106, 137-152.
64. Geisbert, T.W.; Hensley, L.E.; Larsen, T.; Young, H.A.; Reed, D.S.; Geisbert, J.B.; Scott, D.P.; Kagan, E.; Jahrling, P.B.; Davis, K.J. Pathogenesis of Ebola hemorrhagic fever in cynomolgus macaques: Evidence that dendritic cells are early and sustained targets of infection. Am. J. Pathol. 2003, 163, 2347-2370.
65. Geisbert, T.W.; Hensley, L.E.; Gibb, T.R.; Steele, K.E.; Jaax, N.K.; Jahrling, P.B. Apoptosis induced in vitro and in vivo during infection by Ebola and Marburg viruses. Lab. Invest. 2000, 80, 171-186.
66. Feldmann, H.; Geisbert, T.W. Ebola haemorrhagic fever. Lancet 2011, 377, 849-862.
67. Ryabchikova, E.I.; Kolesnikova, L.V.; Luchko, S.V. An analysis of features of pathogenesis in two animal models of Ebola virus infection. J. Infect. Dis. 1999, 179, S199-S202.
68. Zaki, S.R.; Goldsmith, C.S. Pathologic features of filovirus infections in humans. Curr. Top. Microbiol. Immunol. 1999, 235, 97-116.
69. Mahanty, S.; Hutchinson, K.; Agarwal, S.; McRae, M.; Rollin, P.E.; Pulendran, B. Cutting edge: Impairment of dendritic cells and adaptive immunity by Ebola and Lassa viruses. J. Immunol. 2003, 170, 2797-2801.
70. Hartman, A.L.; Towner, J.S.; Nichol, S.T. Ebola and marburg hemorrhagic fever. Clin. Lab. Med. 2010, 30, 161-177.
71. Feldmann, H.; Bugany, H.; Mahner, F.; Klenk, H.D.; Drenckhahn, D.; Schnittler, H.J. Filovirus-induced endothelial leakage triggered by infected monocytes/macrophages. J. Virol. 1996, 70, 2208-2214.
72. Bray, M.; Geisbert, T.W. Ebola virus: The role of macrophages and dendritic cells in the pathogenesis of Ebola hemorrhagic fever. Int. J. Biochem. Cell Biol. 2005, 37, 1560-1566.
73. Schnittler, H.J.; Mahner, F.; Drenckhahn, D.; Klenk, H.D.; Feldmann, H. Replication of Marburg virus in human endothelial cells. A possible mechanism for the development of viral hemorrhagic disease. J. Clin. Invest 1993, 91, 1301-1309.
74. Johnson, E.; Jaax, N.; White, J.; Jahrling, P. Lethal experimental infections of rhesus monkeys by aerosolized Ebola virus. Int. J. Exp. Pathol. 1995, 76, 227-236.
75. Ryabchikova, E.; Strelets, L.; Kolesnikova, L.; Pyankov, O.; Sergeev, A. Respiratory Marburg virus infection in guinea pigs. Arch. Virol. 1996, 141, 2177-2190.
76. Ryabchikova, E.; Kolesnikova, L.; Smolina, M.; Tkachev, V.; Pereboeva, L.; Baranova, S.; Grazhdantseva, A.; Rassadkin, Y. Ebola virus infection in guinea pigs: Presumable role of granulomatous inflammation in pathogenesis. Arch. Virol. 1996, 141, 909-921.
77. Jaax, N.K.; Davis, K.J.; Geisbert, T.J.; Vogel, P.; Jaax, G.P.; Topper, M.; Jahrling, P.B. Lethal experimental infection of rhesus monkeys with Ebola-Zaire (Mayinga) virus by the oral and conjunctival route of exposure. Arch. Pathol. Lab. Med. 1996, 120, 140-155.
78. Davis, K.J.; Anderson, A.O.; Geisbert, T.W.; Steele, K.E.; Geisbert, J.B.; Vogel, P.; Connolly, B.M.; Huggins, J.W.; Jahrling, P.B.; Jaax, N.K. Pathology of experimental Ebola virus infection in African green monkeys. Involvement of fibroblastic reticular cells. Arch. Pathol. Lab. Med. 1997, 121, 805-819.
79. Chan, S.Y.; Speck, R.F.; Ma, M.C.; Goldsmith, M.A. Distinct mechanisms of entry by envelope glycoproteins of Marburg and Ebola (Zaire) viruses. J. Virol. 2000, 74, 4933-4937.
80. Ito, H.; Watanabe, S.; Takada, A.; Kawaoka, Y. Ebola virus glycoprotein: Proteolytic processing, acylation, cell tropism, and detection of neutralizing antibodies. J. Virol. 2001, 75, 1576-1580.
81. Simmons, G.; Rennekamp, A.J.; Chai, N.; Vandenberghe, L.H.; Riley, J.L.; Bates, P. Folate receptor alpha and caveolae are not required for Ebola virus glycoprotein-mediated viral infection. J. Virol. 2003, 77, 13433-13438.
82. Peters, C.J.; Jahrling, P.B.; Ksiazek, T.G.; Johnson, E.D.; Lupton, H.W. Filovirus contamination of cell cultures. Dev. Biol. Stand. 1992, 76, 267-274.
83. Van der Groen, G. Ebola Virus Hemorraghic Fever; Amsterdam Elsevier/North Holland Biomedical Press: Amsterdam, The Netherlands, 1978.
84. Yang, Z.; Delgado, R.; Xu, L.; Todd, R.F.; Nabel, E.G.; Sanchez, A.; Nabel, G.J. Distinct cellular interactions of secreted and transmembrane Ebola virus glycoproteins. Science 1998, 279, 1034-1037.
85. Alvarez, C.P.; Lasala, F.; Carrillo, J.; Muniz, O.; Corbi, A.L.; Delgado, R. C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J. Virol. 2002, 76, 6841-6844.
86. Becker, S.; Spiess, M.; Klenk, H.D. The asialoglycoprotein receptor is a potential liver-specific receptor for Marburg virus. J. Gen. Virol. 1995, 76, 393-399.
87. Gramberg, T.; Hofmann, H.; Moller, P.; Lalor, P.F.; Marzi, A.; Geier, M.; Krumbiegel, M.; Winkler, T.; Kirchhoff, F.; Adams, D.H.; et al. LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus. Virology 2005, 340, 224-236.
88. Marzi, A.; Gramberg, T.; Simmons, G.; Moller, P.; Rennekamp, A.J.; Krumbiegel, M.; Geier, M.; Eisemann, J.; Turza, N.; Saunier, B.; et al. DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus. J. Virol. 2004, 78, 12090-12095.
89. 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. DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 2003, 305, 115-123.
90. Marzi, A.; Moller, P.; Hanna, S.L.; Harrer, T.; Eisemann, J.; Steinkasserer, A.; Becker, S.; Baribaud, F.; Pöhlmann, S. Analysis of the interaction of Ebola virus glycoprotein with DC-SIGN (dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin) and its homologue DC-SIGNR. J. Infect. Dis. 2007, 196, S237-S246.
91. Matsuno, K.; Nakayama, E.; Noyori, O.; Marzi, A.; Ebihara, H.; Irimura, T.; Feldmann, H.; Takada, A. C-type lectins do not act as functional receptors for filovirus entry into cells. Biochem. Biophys. Res. Commun. 2010, 403, 144-148.
92. Marzi, A.; Wegele, A.; Pöhlmann, S. Modulation of virion incorporation of Ebolavirus glycoprotein: Effects on attachment, cellular entry and neutralization. Virology 2006, 352, 345-356.
93. Matsuno, K.; Kishida, N.; Usami, K.; Igarashi, M.; Yoshida, R.; Nakayama, E.; Shimojima, M.; Feldmann, H.; Irimura, T.; Kawaoka, Y.; et al. Different potential of C-type lectin-mediated entry between Marburg virus strains. J. Virol. 2010, 84, 5140-5147.
94. Geijtenbeek, T.B.; Torensma, R.; van Vliet, S.J.; van Duijnhoven, G.C.; Adema, G.J.; van, K.Y.; Figdor, C.G. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 2000, 100, 575-585.
95. Higashi, N.; Fujioka, K.; Denda-Nagai, K.; Hashimoto, S.; Nagai, S.; Sato, T.; Fujita, Y.; Morikawa, A.; Tsuiji, M.; Miyata-Takeuchi, M.; et al. The macrophage C-type lectin specific for galactose/N-acetylgalactosamine is an endocytic receptor expressed on monocyte-derived immature dendritic cells. J. Biol. Chem. 2002, 277, 20686-20693.
96. Spiess, M. The asialoglycoprotein receptor: A model for endocytic transport receptors. Biochemistry 1990, 29, 10009-10018.
97. Bashirova, A.A.; Geijtenbeek, T.B.; van Duijnhoven, G.C.; van Vliet, S.J.; Eilering, J.B.; Martin, M.P.; Wu, L.; Martin, T.D.; Viebig, N.; Knolle, P.A.; et al. A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J. Exp. Med. 2001, 193, 671-678.
98. Pöhlmann, S.; Soilleux, E.J.; Baribaud, F.; Leslie, G.J.; Morris, L.S.; Trowsdale, J.; Lee, B.; Coleman, N.; Doms, R.W. DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans. Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 2670-2675.
99. Gringhuis, S.I.; van der Vlist, M.; van den Berg, L.M.; den, D.J.; Litjens, M.; Geijtenbeek, T.B. HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 2010, 11, 419-426.
100. Michelow, I.C.; Lear, C.; Scully, C.; Prugar, L.I.; Longley, C.B.; Yantosca, L.M.; Ji, X.; Karpel, M.; Brudner, M.; Takahashi, K.; et al. High-dose mannose-binding lectin therapy for Ebola virus infection. J. Infect. Dis. 2011, 203, 175-179.
101. Baribaud, F.; Doms, R.W.; Pöhlmann, S. The role of DC-SIGN and DC-SIGNR in HIV and Ebola virus infection: Can potential therapeutics block virus transmission and dissemination? Expert. Opin. Ther. Targets. 2002, 6, 423-431.
102. Gramberg, T.; Soilleux, E.; Fisch, T.; Lalor, P.F.; Hofmann, H.; Wheeldon, S.; Cotterill, A.; Wegele, A.; Winkler, T.; Adams, D.H.; et al. Interactions of LSECtin and DC-SIGN/DC-SIGNR with viral ligands: Differential pH dependence, internalization and virion binding. Virology 2008, 373, 189-201.
103. Lin, G.; Simmons, G.; Pöhlmann, S.; Baribaud, F.; Ni, H.; Leslie, G.J.; Haggarty, B.S.; Bates, P.; Weissman, D.; Hoxie, J.A.; et al. Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR. J. Virol. 2003, 77, 1337-1346.
104. Kaplan, G.; Totsuka, A.; Thompson, P.; Akatsuka, T.; Moritsugu, Y.; Feinstone, S.M. Identification of a surface glycoprotein on African green monkey kidney cells as a receptor for hepatitis A virus. EMBO J. 1996, 15, 4282-4296.
105. Kondratowicz, A.S.; Lennemann, N.J.; Sinn, P.L.; Davey, R.A.; Hunt, C.L.; Moller-Tank, S.; Meyerholz, D.K.; Rennert, P.; Mullins, R.F.; Brindley, M.; et al. T-cell immunoglobulin and mucin domain 1 (TIM-1) is a receptor for Zaire Ebolavirus and Lake Victoria Marburgvirus. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 8426-8431.
106. McIntire, J.J.; Umetsu, S.E.; Akbari, O.; Potter, M.; Kuchroo, V.K.; Barsh, G.S.; Freeman, G.J.; Umetsu, D.T.; DeKruyff, R.H. Identification of Tapr (an airway hyperreactivity regulatory locus) and the linked Tim gene family. Nat. Immunol. 2001, 2, 1109-1116.
107. Kobayashi, N.; Karisola, P.; Pena-Cruz, V.; Dorfman, D.M.; Jinushi, M.; Umetsu, S.E.; Butte, M.J.; Nagumo, H.; Chernova, I.; Zhu, B.; et al. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 2007, 27, 927-940.
108. Miyanishi, M.; Tada, K.; Koike, M.; Uchiyama, Y.; Kitamura, T.; Nagata, S. Identification of Tim4 as a phosphatidylserine receptor. Nature 2007, 450, 435-439.
109. Umetsu, S.E.; Lee, W.L.; McIntire, J.J.; Downey, L.; Sanjanwala, B.; Akbari, O.; Berry, G.J.; Nagumo, H.; Freeman, G.J.; Umetsu, D.T.; et al. TIM-1 induces T cell activation and inhibits the development of peripheral tolerance. Nat. Immunol. 2005, 6, 447-454.
110. Ichimura, T.; Asseldonk, E.J.; Humphreys, B.D.; Gunaratnam, L.; Duffield, J.S.; Bonventre, J.V. Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J. Clin. Invest. 2008, 118, 1657-1668.
111. Kuhn, J.H. Filoviruses. A compendium of 40 years of epidemiological, clinical, and laboratory studies. Arch. Virol. Suppl. 2008, 20, 13-360.
112. de Souza, A.J.; Oak, J.S.; Jordanhazy, R.; DeKruyff, R.H.; Fruman, D.A.; Kane, L.P. T cell Ig and mucin domain-1-mediated T cell activation requires recruitment and activation of phosphoinositide 3-kinase. J. Immunol. 2008, 180, 6518-6526.
113. de Souza, A.J.; Oriss, T.B.; O'malley, K.J.; Ray, A.; Kane, L.P. T cell Ig and mucin 1 (TIM-1) is expressed on in vivo-activated T cells and provides a costimulatory signal for T cell activation. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 17113-17118.
114. 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.; Maury, W. Tyrosine kinase receptor Axl enhances entry of Zaire ebolavirus without direct interactions with the viral glycoprotein. Virology 2011, 415, 83-94.
115. Hunt, C.L.; Kolokoltsov, A.A.; Davey, R.A.; Maury, W. The Tyro3 receptor kinase Axl enhances macropinocytosis of Zaire ebolavirus. J. Virol. 2011, 85, 334-347.
116. Shimojima, M.; Ikeda, Y.; Kawaoka, Y. The mechanism of Axl-mediated Ebola virus infection. J. Infect. Dis. 2007, 196, S259-S263.
117. Shimojima, M.; Takada, A.; Ebihara, H.; Neumann, G.; Fujioka, K.; Irimura, T.; Jones, S.; Feldmann, H.; Kawaoka, Y. Tyro3 family-mediated cell entry of Ebola and Marburg viruses. J. Virol. 2006, 80, 10109-10116.
118. Crosier, K.E.; Crosier, P.S. New insights into the control of cell growth; the role of the AxI family. Pathology 1997, 29, 131-135.
119. Linger, R.M.; Keating, A.K.; Earp, H.S.; Graham, D.K. TAM receptor tyrosine kinases: Biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv. Cancer Res. 2008, 100, 35-83.
120. Rothlin, C.V.; Ghosh, S.; Zuniga, E.I.; Oldstone, M.B.; Lemke, G. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 2007, 131, 1124-1136.
121. Berman, A.E.; Kozlova, N.I. Integrins: Structure and functions. Membr. Cell Biol. 2000, 13, 207-244.
122. Hynes, R.O. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 1992, 69, 11-25.
123. Schornberg, K.L.; Shoemaker, C.J.; Dube, D.; Abshire, M.Y.; Delos, S.E.; Bouton, A.H.; White, J.M. Alpha5beta1-integrin controls ebolavirus entry by regulating endosomal cathepsins. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 8003-8008.
124. Takada, A.; Watanabe, S.; Ito, H.; Okazaki, K.; Kida, H.; Kawaoka, Y. Downregulation of beta1 integrins by Ebola virus glycoprotein: Implication for virus entry. Virology 2000, 278, 20-26.
125. Misasi, J.; Chandran, K.; Yang, J.Y.; Considine, B.; Filone, C.M.; Cote, M.; Sullivan, N.; Fabozzi, G.; Hensley, L.; Cunningham, J. Filoviruses require endosomal cysteine proteases for entry but exhibit distinct protease preferences. J. Virol. 2012, 86, 3284-3292.
126. Kaletsky, R.L.; Simmons, G.; Bates, P. Proteolysis of the Ebola virus glycoproteins enhances virus binding and infectivity. J. Virol. 2007, 81, 13378-13384.
127. Sanchez, A. Analysis of filovirus entry into vero e6 cells, using inhibitors of endocytosis, endosomal acidification, structural integrity, and cathepsin (B and L) activity. J. Infect. Dis. 2007, 196, S251-S258.
128. Martinez, O.; Johnson, J.; Manicassamy, B.; Rong, L.; Olinger, G.G.; Hensley, L.E.; Basler, C.F. Zaire Ebola virus entry into human dendritic cells is insensitive to cathepsin L inhibition. Cell Microbiol. 2010, 12, 148-157.
129. Carette, J.E.; Raaben, M.; Wong, A.C.; Herbert, A.S.; Obernosterer, G.; Mulherkar, N.; Kuehne, A.I.; Kranzusch, P.J.; Griffin, A.M.; Ruthel, G.; et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 2011, 477, 340-343.
130. Miller, E.H.; Obernosterer, G.; Raaben, M.; Herbert, A.S.; Deffieu, M.S.; Krishnan, A.; Ndungo, E.; Sandesara, R.G.; Carette, J.E.; Kuehne, A.I.; et al. Ebola virus entry requires the host-programmed recognition of an intracellular receptor. EMBO J. 2012, 31, 1947-1960.
131. Lemke, G.; Rothlin, C.V. Immunobiology of the TAM receptors. Nat. Rev. Immunol. 2008, 8, 327-336.
132. Stitt, T.N.; Conn, G.; Gore, M.; Lai, C.; Bruno, J.; Radziejewski, C.; Mattsson, K.; Fisher, J.; Gies, D.R.; Jones, P.F.; et al. The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell 1995, 80, 661-670.
133. Godowski, P.J.; Mark, M.R.; Chen, J.; Sadick, M.D.; Raab, H.; Hammonds, R.G. Reevaluation of the roles of protein S and Gas6 as ligands for the receptor tyrosine kinase Rse/Tyro 3. Cell 1995, 82, 355-358.
134. Scott, R.S.; McMahon, E.J.; Pop, S.M.; Reap, E.A.; Caricchio, R.; Cohen, P.L.; Earp, H.S.; Matsushima, G.K. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 2001, 411, 207-211.
135. Hafizi, S.; Dahlback, B. Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J. 2006, 273, 5231-5244.
136. Nanbo, A.; Imai, M.; Watanabe, S.; Noda, T.; Takahashi, K.; Neumann, G.; Halfmann, P.; Kawaoka, Y. Ebolavirus is internalized into host cells via macropinocytosis in a viral glycoprotein-dependent manner. PLoS Pathog. 2010, 6, e1001121.
137. Saeed, M.F.; Kolokoltsov, A.A.; Albrecht, T.; Davey, R.A. Cellular entry of ebola virus involves uptake by a macropinocytosis-like mechanism and subsequent trafficking through early and late endosomes. PLoS Pathog. 2010, 6, e1001110.
138. Morizono, K.; Xie, Y.; Olafsen, T.; Lee, B.; Dasgupta, A.; Wu, A.M.; Chen, I.S. The soluble serum protein Gas6 bridges virion envelope phosphatidylserine to the TAM receptor tyrosine kinase Axl to mediate viral entry. Cell Host Microbe 2011, 9, 286-298.
139. Hynes, R.O. Cell adhesion: Old and new questions. Trends Cell Biol. 1999, 9, M33-M37.
140. Cary, L.A.; Han, D.C.; Guan, J.L. Integrin-mediated signal transduction pathways. Histol. Histopathol. 1999, 14, 1001-1009.
141. Akula, S.M.; Pramod, N.P.; Wang, F.Z.; Chandran, B. Integrin alpha3beta1 (CD 49c/29) is a cellular receptor for Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 2002, 108, 407-419.
142. Tugizov, S.M.; Berline, J.W.; Palefsky, J.M. Epstein-Barr virus infection of polarized tongue and nasopharyngeal epithelial cells. Nat. Med. 2003, 9, 307-314.
143. Feire, A.L.; Koss, H.; Compton, T. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 15470-15475.
144. Mathias, P.; Wickham, T.; Moore, M.; Nemerow, G. Multiple adenovirus serotypes use alpha v integrins for infection. J. Virol. 1994, 68, 6811-6814.
145. 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.
146. Gavrilovskaya, I.N.; Brown, E.J.; Ginsberg, M.H.; Mackow, E.R. Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J. Virol. 1999, 73, 3951-3959.
147. Gavrilovskaya, I.N.; Shepley, M.; Shaw, R.; Ginsberg, M.H.; Mackow, E.R. beta3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 7074-7079.
148. Raymond, T.; Gorbunova, E.; Gavrilovskaya, I.N.; Mackow, E.R. Pathogenic hantaviruses bind plexin-semaphorin-integrin domains present at the apex of inactive, bent alphavbeta3 integrin conformers. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 1163-1168.
149. Berinstein, A.; Roivainen, M.; Hovi, T.; Mason, P.W.; Baxt, B. Antibodies to the vitronectin receptor (integrin alpha V beta 3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. J. Virol. 1995, 69, 2664-2666.
150. Bergelson, J.M.; Shepley, M.P.; Chan, B.M.; Hemler, M.E.; Finberg, R.W. Identification of the integrin VLA-2 as a receptor for echovirus 1. Science 1992, 255, 1718-1720.
151. Xing, L.; Huhtala, M.; Pietiainen, V.; Kapyla, J.; Vuorinen, K.; Marjomaki, V.; Heino, J.; Johnson, M.S.; Hyypia, T.; Cheng, R.H. Structural and functional analysis of integrin alpha2I domain interaction with echovirus 1. J. Biol. Chem. 2004, 279, 11632-11638.
152. Whitton, J.L.; Cornell, C.T.; Feuer, R. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 2005, 3, 765-776.
153. Graham, K.L.; Fleming, F.E.; Halasz, P.; Hewish, M.J.; Nagesha, H.S.; Holmes, I.H.; Takada, Y.; Coulson, B.S. Rotaviruses interact with alpha4beta7 and alpha4beta1 integrins by binding the same integrin domains as natural ligands. J. Gen. Virol. 2005, 86, 3397-3408.
154. Maginnis, M.S.; Forrest, J.C.; Kopecky-Bromberg, S.A.; Dickeson, S.K.; Santoro, S.A.; Zutter, M.M.; Nemerow, G.R.; Bergelson, J.M.; Dermody, T.S. Beta1 integrin mediates internalization of mammalian reovirus. J. Virol. 2006, 80, 2760-2770.
155. Stewart, P.L.; Nemerow, G.R. Cell integrins: Commonly used receptors for diverse viral pathogens. Trends Microbiol. 2007, 15, 500-507.
156. Nemerow, G.R.; Cheresh, D.A. Herpesvirus hijacks an integrin. Nat. Cell Biol. 2002, 4, E69-E71.
157. Francica, J.R.; Varela-Rohena, A.; Medvec, A.; Plesa, G.; Riley, J.L.; Bates, P. Steric shielding of surface epitopes and impaired immune recognition induced by the ebola virus glycoprotein. PLoS Pathog. 2010, 6, e1001098.
158. Harrison, S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 2008, 15, 690-698.
159. Diederich, S.; Sauerhering, L.; Weis, M.; Altmeppen, H.; Schaschke, N.; Reinheckel, T.; Erbar, S.; Maisner, A. Activation of the Nipah virus fusion protein in MDCK cells is mediated by cathepsin B within the endosome-recycling compartment. J. Virol. 2012, 86, 3736-3745.
160. Popa, A.; Carter, J.R.; Smith, S.E.; Hellman, L.; Fried, M.G.; Dutch, R.E. Residues in the hendra virus fusion protein transmembrane domain are critical for endocytic recycling. J. Virol. 2012, 86, 3014-3026.
161. White, J.; Kartenbeck, J.; Helenius, A. Membrane fusion activity of influenza virus. EMBO J. 1982, 1, 217-222.
162. Van der Schaar, H.M.; Rust, M.J.; Chen, C.; Ende-Metselaar, H.; Wilschut, J.; Zhuang, X.; Smit, J.M. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 2008, 4, e1000244.
163. Lozach, P.Y.; Huotari, J.; Helenius, A. Late-penetrating viruses. Curr. Opin. Virol. 2011, 1, 35-43.
164. Mothes, W.; Boerger, A.L.; Narayan, S.; Cunningham, J.M.; Young, J.A. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 2000, 103, 679-689.
165. Raymond, T.; Gorbunova, E.; Gavrilovskaya, I.N.; Mackow, E.R. Pathogenic hantaviruses bind plexin-semaphorin-integrin domains present at the apex of inactive, bent alphavbeta3 integrin conformers. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 1163-1168.
166. Berinstein, A.; Roivainen, M.; Hovi, T.; Mason, P.W.; Baxt, B. Antibodies to the vitronectin receptor (integrin alpha V beta 3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. J. Virol. 1995, 69, 2664-2666.
167. Bergelson, J.M.; Shepley, M.P.; Chan, B.M.; Hemler, M.E.; Finberg, R.W. Identification of the integrin VLA-2 as a receptor for echovirus 1. Science 1992, 255, 1718-1720.
168. Xing, L.; Huhtala, M.; Pietiainen, V.; Kapyla, J.; Vuorinen, K.; Marjomaki, V.; Heino, J.; Johnson, M.S.; Hyypia, T.; Cheng, R.H. Structural and functional analysis of integrin alpha2I domain interaction with echovirus 1. J. Biol. Chem. 2004, 279, 11632-11638.
169. Whitton, J.L.; Cornell, C.T.; Feuer, R. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 2005, 3, 765-776.
170. Graham, K.L.; Fleming, F.E.; Halasz, P.; Hewish, M.J.; Nagesha, H.S.; Holmes, I.H.; Takada, Y.; Coulson, B.S. Rotaviruses interact with alpha4beta7 and alpha4beta1 integrins by binding the same integrin domains as natural ligands. J. Gen. Virol. 2005, 86, 3397-3408.
171. Maginnis, M.S.; Forrest, J.C.; Kopecky-Bromberg, S.A.; Dickeson, S.K.; Santoro, S.A.; Zutter, M.M.; Nemerow, G.R.; Bergelson, J.M.; Dermody, T.S. Beta1 integrin mediates internalization of mammalian reovirus. J. Virol. 2006, 80, 2760-2770.
172. Stewart, P.L.; Nemerow, G.R. Cell integrins: Commonly used receptors for diverse viral pathogens. Trends Microbiol. 2007, 15, 500-507.
173. Nemerow, G.R.; Cheresh, D.A. Herpesvirus hijacks an integrin. Nat. Cell Biol. 2002, 4, E69-E71.
174. Francica, J.R.; Varela-Rohena, A.; Medvec, A.; Plesa, G.; Riley, J.L.; Bates, P. Steric shielding of surface epitopes and impaired immune recognition induced by the ebola virus glycoprotein. PLoS Pathog. 2010, 6, e1001098.
175. Harrison, S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 2008, 15, 690-698.
176. Diederich, S.; Sauerhering, L.; Weis, M.; Altmeppen, H.; Schaschke, N.; Reinheckel, T.; Erbar, S.; Maisner, A. Activation of the Nipah virus fusion protein in MDCK cells is mediated by cathepsin B within the endosome-recycling compartment. J. Virol. 2012, 86, 3736-3745.
177. Popa, A.; Carter, J.R.; Smith, S.E.; Hellman, L.; Fried, M.G.; Dutch, R.E. Residues in the hendra virus fusion protein transmembrane domain are critical for endocytic recycling. J. Virol. 2012, 86, 3014-3026.
178. White, J.; Kartenbeck, J.; Helenius, A. Membrane fusion activity of influenza virus. EMBO J. 1982, 1, 217-222.
179. Van der Schaar, H.M.; Rust, M.J.; Chen, C.; Ende-Metselaar, H.; Wilschut, J.; Zhuang, X.; Smit, J.M. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 2008, 4, e1000244.
180. Lozach, P.Y.; Huotari, J.; Helenius, A. Late-penetrating viruses. Curr. Opin. Virol. 2011, 1, 35-43.
181. Mothes, W.; Boerger, A.L.; Narayan, S.; Cunningham, J.M.; Young, J.A. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 2000, 103, 679-689.
182. Guicciardi, M.E.; Deussing, J.; Miyoshi, H.; Bronk, S.F.; Svingen, P.A.; Peters, C.; Kaufmann, S.H.; Gores, G.J. Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J. Clin. Invest. 2000, 106, 1127-1137.
183. Wong, A.C.; Sandesara, R.G.; Mulherkar, N.; Whelan, S.P.; Chandran, K. A forward genetic strategy reveals destabilizing mutations in the Ebolavirus glycoprotein that alter its protease dependence during cell entry. J. Virol. 2010, 84, 163-175.
184. Haines, K.M.; Vande Burgt, N.H.; Francica, J.R.; Kaletsky, R.L.; Bates, P. Chinese hamster ovary cell lines selected for resistance to ebolavirus glycoprotein mediated infection are defective for NPC1 expression. Virology 2012, 432, 20-28.
185. Loftus, S.K.; Morris, J.A.; Carstea, E.D.; Gu, J.Z.; Cummings, C.; Brown, A.; Ellison, J.; Ohno, K.; Rosenfeld, M.A.; Tagle, D.A.; et al. Murine model of Niemann-Pick C disease: Mutation in a cholesterol homeostasis gene. Science 1997, 277, 232-235.
186. Garver, W.S.; Xie, C.; Repa, J.J.; Turley, S.D.; Dietschy, J.M. Niemann-Pick C1 expression is not regulated by the amount of cholesterol flowing through cells in the mouse. J. Lipid. Res. 2005, 46, 1745-1754.
187. Carstea, E.D.; Morris, J.A.; Coleman, K.G.; Loftus, S.K.; Zhang, D.; Cummings, C.; Gu, J.; Rosenfeld, M.A.; Pavan, W.J.; Krizman, D.B.; et al. Niemann-Pick C1 disease gene: Homology to mediators of cholesterol homeostasis. Science 1997, 277, 228-231.
188. Karten, B.; Peake, K.B.; Vance, J.E. Mechanisms and consequences of impaired lipid trafficking in Niemann-Pick type C1-deficient mammalian cells. Biochim. Biophys. Acta 2009, 1791, 659-670.
189. Rosenbaum, A.I.; Maxfield, F.R. Niemann-Pick type C disease: Molecular mechanisms and potential therapeutic approaches. J. Neurochem. 2011, 116, 789-795.
190. Lai, C.K.; Jeng, K.S.; Machida, K.; Lai, M.M. Hepatitis C virus egress and release depend on endosomal trafficking of core protein. J. Virol. 2010, 84, 11590-11598.
191. Poh, M.K.; Shui, G.; Xie, X.; Shi, P.Y.; Wenk, M.R.; Gu, F. U18666A, an intra-cellular cholesterol transport inhibitor, inhibits dengue virus entry and replication. Antivir. Res. 2012, 93, 191-198.
192. Sainz, B., Jr.; Barretto, N.; Martin, D.N.; Hiraga, N.; Imamura, M.; Hussain, S.; Marsh, K.A.; Yu, X.; Chayama, K.; Alrefai, W.A.; et al. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat. Med. 2012, 18, 281-285.