Hepatitis C virus entry into hepatocytes: Molecular mechanisms and targets for antiviral therapies

Journal of Hepatology

Volumn 54, Issue 3, 2011, Pages 566-576

  Zeisel, Mirjam B ^a,b   Fofana, Isabel ^a,b   Fafi Kremer, Samira ^a,b,c   Baumert, Thomas F ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITY HOSPITAL OF STRASBOURG   (France)

Author keywords

Antivirals; Entry; Hepatitis C virus

Indexed keywords

ANTIVIRUS AGENT; ARBIDOL; CD81 ANTIGEN; CHLOROQUINE; ENFUVIRTIDE; GLYCOPROTEIN E1; GLYCOPROTEIN E2; IMIDAZOLE; IMMUNOGLOBULIN; ITX 5061; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; SILYMARIN; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ANTIVIRAL THERAPY; CELL INTERACTION; CELL MEMBRANE; CELL SURFACE; DRUG TARGETING; HEPATITIS C; HEPATITIS C VIRUS; HOST CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TARGET CELL; VIRUS ASSEMBLY; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS IMMUNITY; VIRUS REPLICATION; VIRUS STRAIN;

ANTIVIRAL AGENTS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; MODELS, BIOLOGICAL; VIRUS INTERNALIZATION;

EID: 79951669627     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2010.10.014     Document Type: Review

References (150)

1. C. Hezode, N. Forestier, G. Dusheiko, P. Ferenci, S. Pol, and T. Goeser Telaprevir and peginterferon with or without ribavirin for chronic HCV infection N Engl J Med 360 2009 1839 1850
2. A.A. Pereira, and I.M. Jacobson New and experimental therapies for HCV Nat Rev Gastroenterol Hepatol 6 2009 403 411
3. C. Sarrazin, and S. Zeuzem Resistance to direct antiviral agents in patients with hepatitis C virus infection Gastroenterology 138 2010 447 462
4. R.S. Brown Hepatitis C and liver transplantation Nature 436 2005 973 978
5. B. Roche, and D. Samuel Liver transplantation in viral hepatitis: prevention of recurrence Best Pract Res Clin Gastroenterol 22 2008 1153 1169
6. D. Rosa, S. Campagnoli, C. Moretto, E. Guenzi, L. Cousens, and M. Chin A quantitative test to estimate neutralizing antibodies to the hepatitis C virus: cytofluorimetric assessment of envelope glycoprotein 2 binding to target cells Proc Natl Acad Sci USA 93 1996 1759 1763 (Pubitemid 26079830)
7. T.F. Baumert, S. Ito, D.T. Wong, and T.J. Liang Hepatitis C virus structural proteins assemble into virus-like particles in insect cells J Virol 72 1998 3827 3836 (Pubitemid 28188682)
8. B. Bartosch, J. Dubuisson, and F.L. Cosset Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes J Exp Med 197 2003 633 642 (Pubitemid 36314658)
9. M. Hsu, J. Zhang, M. Flint, C. Logvinoff, C. Cheng-Mayer, and C.M. Rice Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles Proc Natl Acad Sci USA 100 2003 7271 7276 (Pubitemid 36706428)
10. T. Wakita, T. Pietschmann, T. Kato, T. Date, M. Miyamoto, and Z. Zhao Production of infectious hepatitis C virus in tissue culture from a cloned viral genome Nat Med 11 2005 791 796 (Pubitemid 41021213)
11. B.D. Lindenbach, M.J. Evans, A.J. Syder, B. Wolk, T.L. Tellinghuisen, and C.C. Liu Complete replication of hepatitis C virus in cell culture Science 309 2005 623 626 (Pubitemid 41033648)
12. J. Zhong, P. Gastaminza, G. Cheng, S. Kapadia, T. Kato, and D.R. Burton Robust hepatitis C virus infection in vitro Proc Natl Acad Sci USA 102 2005 9294 9299 (Pubitemid 40923557)
13. D.F. Mercer, D.E. Schiller, J.F. Elliott, D.N. Douglas, C. Hao, and A. Rinfret Hepatitis C virus replication in mice with chimeric human livers Nat Med 7 2001 927 933 (Pubitemid 32756430)
14. K.D. Bissig, S.F. Wieland, P. Tran, M. Isogawa, T.T. Le, and F.V. Chisari Human liver chimeric mice provide a model for hepatitis B and C virus infection and treatment J Clin Invest 120 2010 924 930
15. H. Barth, E. Robinet, T.J. Liang, and T.F. Baumert Mouse models for the study of HCV infection and virus-host interactions J Hepatol 49 2008 134 142
16. A. Boonstra, L.J. van der Laan, T. Vanwolleghem, and H.L. Janssen Experimental models for hepatitis C viral infection Hepatology 50 2009 1646 1655
17. G. Vieyres, X. Thomas, V. Descamps, G. Duverlie, A.H. Patel, and J. Dubuisson Characterization of the envelope glycoproteins associated with infectious hepatitis C virus J Virol 84 2010 10159 10168
18. Y. Ciczora, N. Callens, F. Penin, E.I. Pecheur, and J. Dubuisson Transmembrane domains of hepatitis C virus envelope glycoproteins: residues involved in E1E2 heterodimerization and involvement of these domains in virus entry J Virol 81 2007 2372 2381
19. A. Goffard, N. Callens, B. Bartosch, C. Wychowski, F.L. Cosset, and C. Montpellier Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins J Virol 79 2005 8400 8409 (Pubitemid 40853542)
20. F. Helle, A. Goffard, V. Morel, G. Duverlie, J. McKeating, and Z.Y. Keck The neutralizing activity of anti-hepatitis C virus antibodies is modulated by specific glycans on the E2 envelope protein J Virol 81 2007 8101 8111 (Pubitemid 47101496)
21. V. Agnello, G. Abel, M. Elfahal, G.B. Knight, and Q.X. Zhang Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor Proc Natl Acad Sci USA 96 1999 12766 12771 (Pubitemid 29513577)
22. M. Hijikata, Y.K. Shimizu, H. Kato, A. Iwamoto, J.W. Shih, and H.J. Alter Equilibrium centrifugation studies of hepatitis C virus: evidence for circulating immune complexes J Virol 67 1993 1953 1958 (Pubitemid 23088368)
23. R. Thomssen, S. Bonk, C. Propfe, K.-H. Heermann, H.G. Koechel, and A. Uy Association of hepatitis C virus in human sera with beta-lipoprotein Med Microbiol Immunol 181 1992 293 300
24. S.U. Nielsen, M.F. Bassendine, A.D. Burt, C. Martin, W. Pumeechockchai, and G.L. Toms Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients J Virol 80 2006 2418 2428 (Pubitemid 43271547)
25. M. Kobayashi, M.C. Bennett, T. Bercot, and I.R. Singh Functional analysis of hepatitis C virus envelope proteins, using a cell-cell fusion assay J Virol 80 2006 1817 1825 (Pubitemid 43228722)
26. D. Lavillette, E.I. Pecheur, P. Donot, J. Fresquet, J. Molle, and R. Corbau Characterization of fusion determinants points to the involvement of three discrete regions of both E1 and E2 glycoproteins in the membrane fusion process of hepatitis C virus J Virol 81 2007 8752 8765 (Pubitemid 47242848)
27. B. Bartosch, A. Vitelli, C. Granier, C. Goujon, J. Dubuisson, and S. Pascale Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor J Biol Chem 278 2003 41624 41630 (Pubitemid 37310418)
28. D. Bankwitz, E. Steinmann, J. Bitzegeio, S. Ciesek, M. Friesland, and E. Herrmann Hepatitis C virus hypervariable region 1 modulates receptor interactions, conceals the CD81 binding site, and protects conserved neutralizing epitopes J Virol 84 2010 5751 5763
29. Z.Y. Keck, K. Machida, M.M. Lai, J.K. Ball, A.H. Patel, and S.K. Foung Therapeutic control of hepatitis C virus: the role of neutralizing monoclonal antibodies Curr Top Microbiol Immunol 317 2008 1 38
30. Z.Y. Keck, T.K. Li, J. Xia, M. Gal-Tanamy, O. Olson, and S.H. Li Definition of a conserved immunodominant domain on hepatitis C virus E2 glycoprotein by neutralizing human monoclonal antibodies J Virol 82 2008 6061 6066 (Pubitemid 351822282)
31. M. Law, T. Maruyama, J. Lewis, E. Giang, A.W. Tarr, and Z. Stamataki Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge Nat Med 14 2008 25 27
32. R.F. Clayton, A. Owsianka, J. Aitken, S. Graham, D. Bhella, and A.H. Patel Analysis of antigenicity and topology of E2 glycoprotein present on recombinant hepatitis C virus-like particles J Virol 76 2002 7672 7682 (Pubitemid 34760991)
33. A. Owsianka, R.F. Clayton, L.D. Loomis-Price, J.A. McKeating, and A.H. Patel Functional analysis of hepatitis C virus E2 glycoproteins and virus-like particles reveals structural dissimilarities between different forms of E2 J Gen Virol 82 2001 1877 1883 (Pubitemid 32707551)
34. H. Barth, E.K. Schnober, F. Zhang, R.J. Linhardt, E. Depla, and B. Boson Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction J Virol 80 2006 10579 10590 (Pubitemid 44628904)
35. Z.Y. Keck, S.H. Li, J. Xia, T. von Hahn, P. Balfe, and J.A. McKeating Mutations in HCV E2 located outside the CD81 binding sites lead to escape from broadly neutralizing antibodies but compromise virus infectivity J Virol 83 2009 6149 6160
36. J.M. Pestka, M.B. Zeisel, E. Blaser, P. Schurmann, B. Bartosch, and F.L. Cosset Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C Proc Natl Acad Sci USA 104 2007 6025 6030 (Pubitemid 47175652)
37. K.A. Dowd, D.M. Netski, X.H. Wang, A.L. Cox, and S.C. Ray Selection pressure from neutralizing antibodies drives sequence evolution during acute infection with hepatitis C virus Gastroenterology 136 2009 2377 2386
38. D. Lavillette, Y. Morice, G. Germanidis, P. Donot, A. Soulier, and E. Pagkalos Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral replication kinetics at the acute phase of hepatitis C virus infection J Virol 79 2005 6023 6034 (Pubitemid 40617208)
39. W.O. Osburn, B.E. Fisher, K.A. Dowd, G. Urban, L. Liu, and S.C. Ray Spontaneous control of primary hepatitis C virus infection and immunity against persistent reinfection Gastroenterology 138 2010 315 324
40. L. Liu, B.E. Fisher, K.A. Dowd, J. Astemborski, A.L. Cox, and S.C. Ray Acceleration of hepatitis C virus envelope evolution in humans is consistent with progressive humoral immune selection during the transition from acute to chronic infection J Virol 84 2010 5067 5077
41. M.B. Zeisel, F.L. Cosset, and T.F. Baumert Host neutralizing responses and pathogenesis of hepatitis C virus infection Hepatology 48 2008 299 307 (Pubitemid 351975554)
42. L. Uebelhoer, J.H. Han, B. Callendret, G. Mateu, N.H. Shoukry, and H.L. Hanson Stable cytotoxic T cell escape mutation in hepatitis C virus is linked to maintenance of viral fitness PLoS Pathog 4 2008 e1000143
43. S. Fafi-Kremer, I. Fofana, E. Soulier, P. Carolla, P. Meuleman, and G. Leroux-Roels Viral entry and escape from antibody-mediated neutralization influence hepatitis C virus reinfection in liver transplantation J Exp Med 207 2010 2019 2031
44. P. Pileri, Y. Uematsu, S. Campagnoli, G. Galli, F. Falugi, and R. Petracca Binding of hepatitis C virus to CD81 Science 282 1998 938 941 (Pubitemid 28507525)
45. H. Barth, C. Schäfer, M.I. Adah, F. Zhang, R.J. Linhardt, and H. Toyoda Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate J Biol Chem 278 2003 41003 41012 (Pubitemid 37280923)
46. E. Scarselli, H. Ansuini, R. Cerino, R.M. Roccasecca, S. Acali, and G. Filocamo The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus EMBO J 21 2002 5017 5025
47. S. Pohlmann, J. Zhang, F. Baribaud, Z. Chen, G.J. Leslie, and G. Lin Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR J Virol 77 2003 4070 4080 (Pubitemid 36350947)
48. P.Y. Lozach, A. Amara, B. Bartosch, J.L. Virelizier, F. Arenzana-Seisdedos, and F.L. Cosset C-type lectins L-SIGN and DC-SIGN capture and transmit infectious hepatitis C virus pseudotype particles J Biol Chem 279 2004 32035 32045 (Pubitemid 39014648)
49. M.J. Evans, T. von Hahn, D.M. Tscherne, A.J. Syder, M. Panis, and B. Wolk Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry Nature 446 2007 801 805 (Pubitemid 46582027)
50. A. Ploss, M.J. Evans, V.A. Gaysinskaya, M. Panis, H. You, and Y.P. de Jong Human occludin is a hepatitis C virus entry factor required for infection of mouse cells Nature 457 2009 882 886
51. S. Liu, W. Yang, L. Shen, J.R. Turner, C.B. Coyne, and T. Wang Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection J Virol 83 2009 2011 2014
52. W. Yang, C. Qiu, N. Biswas, J. Jin, S.C. Watkins, and R.C. Montelaro Correlation of the tight junction-like distribution of Claudin-1 to the cellular tropism of hepatitis C virus J Biol Chem 283 2008 8643 8653
53. Y. van Kooyk, and T.B. Geijtenbeek DC-SIGN: escape mechanism for pathogens Nat Rev Immunol 3 2003 697 709 (Pubitemid 41070811)
54. J.P. Gardner, R.J. Durso, R.R. Arrigale, G.P. Donovan, P.J. Maddon, and T. Dragic L-SIGN (CD 209L) is a liver-specific capture receptor for hepatitis C virus Proc Natl Acad Sci USA 100 2003 4498 4503 (Pubitemid 36457759)
55. G. Koutsoudakis, A. Kaul, E. Steinmann, S. Kallis, V. Lohmann, and T. Pietschmann Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses J Virol 80 2006 5308 5320
56. J.A. McKeating, L.Q. Zhang, C. Logvinoff, M. Flint, J. Zhang, and J. Yu Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner J Virol 78 2004 8496 8505 (Pubitemid 39025115)
57. D. Lavillette, A.W. Tarr, C. Voisset, P. Donot, B. Bartosch, and C. Bain Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus Hepatology 41 2005 265 274 (Pubitemid 40173981)
58. J. Zhang, G. Randall, A. Higginbottom, P. Monk, C.M. Rice, and J.A. McKeating CD81 is required for hepatitis C virus glycoprotein-mediated viral infection J Virol 78 2004 1448 1455 (Pubitemid 38095855)
59. M. Flint, C.M. Maidens, L.D. Loomis-Price, C. Shotton, J. Dubuisson, and P. Monk Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor CD81 J Virol 73 1999 6235 6244 (Pubitemid 29327798)
60. A.H. Patel, J. Wood, F. Penin, J. Dubuisson, and J.A. McKeating Construction and characterization of chimeric hepatitis C virus E2 glycoproteins: analysis of regions critical for glycoprotein aggregation and CD81 binding J Gen Virol 81 2000 2873 2883 (Pubitemid 32000634)
61. C. Bertaux, and T. Dragic Different domains of CD81 mediate distinct stages of hepatitis C virus pseudoparticle entry J Virol 80 2006 4940 4948
62. A.M. Owsianka, J.M. Timms, A.W. Tarr, R.J. Brown, T.P. Hickling, and A. Szwejk Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding J Virol 80 2006 8695 8704 (Pubitemid 44384879)
63. S. Dhillon, J. Witteveldt, D. Gatherer, A.M. Owsianka, M.B. Zeisel, and M.N. Zahid Mutations within a conserved region of the hepatitis C virus E2 glycoprotein that influence virus-receptor interactions and sensitivity to neutralizing antibodies J Virol 84 2010 5494 5507
64. M. Krieger Scavenger receptor class B type I is a multiligand HDL receptor that influences diverse physiologic systems J Clin Invest 108 2001 793 797 (Pubitemid 32880286)
65. M.T. Catanese, H. Ansuini, R. Graziani, T. Huby, M. Moreau, and J.K. Ball Role of scavenger receptor class B type I in hepatitis C virus entry: kinetics and molecular determinants J Virol 84 2010 34 43
66. M.B. Zeisel, G. Koutsoudakis, E.K. Schnober, A. Haberstroh, H.E. Blum, and F.-L. Cosset Scavenger receptor BI is a key host factor for hepatitis C virus infection required for an entry step closely linked to CD81 Hepatology 46 2007 1722 1731
67. B. Bartosch, G. Verney, M. Dreux, P. Donot, Y. Morice, and F. Penin An interplay between hypervariable region 1 of the hepatitis C virus E2 glycoprotein, the scavenger receptor BI, and high-density lipoprotein promotes both enhancement of infection and protection against neutralizing antibodies J Virol 79 2005 8217 8229 (Pubitemid 40853525)
68. C. Voisset, N. Callens, E. Blanchard, A. Op De Beeck, J. Dubuisson, and N. Vu-Dac High density lipoproteins facilitate hepatitis C virus entry through the scavenger receptor class B type I J Biol Chem 280 2005 7793 7799 (Pubitemid 40349673)
69. T. von Hahn, B.D. Lindenbach, A. Boullier, O. Quehenberger, M. Paulson, and C.M. Rice Oxidized low-density lipoprotein inhibits hepatitis C virus cell entry in human hepatoma cells Hepatology 43 2006 932 942 (Pubitemid 43724618)
70. S. Molina, V. Castet, C. Fournier-Wirth, L. Pichard-Garcia, R. Avner, and D. Harats The low-density lipoprotein receptor plays a role in the infection of primary human hepatocytes by hepatitis C virus J Hepatol 46 2007 411 419 (Pubitemid 46201721)
71. P. Maillard, T. Huby, U. Andreo, M. Moreau, J. Chapman, and A. Budkowska The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/Cla1 is mediated by ApoB-containing lipoproteins FASEB J 20 2006 735 737 (Pubitemid 46671198)
72. M. Dreux, V.L. Dao Thi, J. Fresquet, M. Guerin, Z. Julia, and G. Verney Receptor complementation and mutagenesis reveal SR-BI as an essential HCV entry factor and functionally imply its intra- and extra-cellular domains PLoS Pathog 5 2009 e1000310
73. A. Zheng, F. Yuan, Y. Li, F. Zhu, P. Hou, and J. Li Claudin-6 and claudin-9 function as additional coreceptors for hepatitis C virus J Virol 81 2007 12465 12471
74. L. Meertens, C. Bertaux, L. Cukierman, E. Cormier, D. Lavillette, and F.L. Cosset The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus J Virol 82 2008 3555 3560 (Pubitemid 351429931)
75. M. Furuse, K. Fujita, T. Hiiragi, K. Fujimoto, and S. Tsukita Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin J Cell Biol 141 1998 1539 1550 (Pubitemid 28309169)
76. G.M. Reynolds, H.J. Harris, A. Jennings, K. Hu, J. Grove, and P.F. Lalor Hepatitis C virus receptor expression in normal and diseased liver tissue Hepatology 47 2008 418 427 (Pubitemid 351280709)
77. L. Cukierman, L. Meertens, C. Bertaux, F. Kajumo, and T. Dragic Residues in a highly conserved claudin-1 motif are required for hepatitis C virus entry and mediate the formation of cell-cell contacts J Virol 83 2009 5477 5484
78. S.E. Krieger, M.B. Zeisel, C. Davis, C. Thumann, H.J. Harris, and E.K. Schnober Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations Hepatology 51 2010 1144 1157
79. H.J. Harris, M.J. Farquhar, C.J. Mee, C. Davis, G.M. Reynolds, and A. Jennings CD81 and claudin 1 coreceptor association: role in hepatitis C virus entry J Virol 82 2008 5007 5020 (Pubitemid 351657061)
80. H.J. Harris, C. Davis, J.G. Mullins, K. Hu, M. Goodall, and M.J. Farquhar Claudin association with CD81 defines hepatitis C virus entry J Biol Chem 285 2010 21092 21102
81. I. Benedicto, F. Molina-Jimenez, B. Bartosch, F.L. Cosset, D. Lavillette, and J. Prieto The tight junction-associated protein occludin is required for a postbinding step in hepatitis C virus entry and infection J Virol 83 2009 8012 8020
82. S. Ciesek, E. Steinmann, M. Iken, M. Ott, F.A. Helfritz, and I. Wappler Glucocorticosteroids increase cell entry by hepatitis C virus Gastroenterology 138 2010 1875 1884
83. S. Wunschmann, J.D. Medh, D. Klinzmann, W.N. Schmidt, and J.T. Stapleton Characterization of hepatitis C virus (HCV) and HCV E2 interactions with CD81 and the low-density lipoprotein receptor J Virol 74 2000 10055 10062
84. H. Barth, E.K. Schnober, C. Neumann-Haefelin, C. Thumann, M.B. Zeisel, and H.M. Diepolder Scavenger receptor class B is required for hepatitis C virus uptake and cross-presentation by human dendritic cells J Virol 82 2008 3466 3479 (Pubitemid 351429922)
85. A.K. Schwarz, J. Grove, K. Hu, C.J. Mee, P. Balfe, and J.A. McKeating Hepatoma cell density promotes claudin-1 and scavenger receptor BI expression and hepatitis C virus internalization J Virol 83 2009 12407 12414
86. E. Blanchard, S. Belouzard, L. Goueslain, T. Wakita, J. Dubuisson, and C. Wychowski Hepatitis C virus entry depends on clathrin-mediated endocytosis J Virol 80 2006 6964 6972 (Pubitemid 44025195)
87. L. Meertens, C. Bertaux, and T. Dragic Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles J Virol 80 2006 11571 11578 (Pubitemid 44788871)
88. A. Codran, C. Royer, D. Jaeck, M. Bastien-Valle, T.F. Baumert, and M.P. Kieny Entry of hepatitis C virus pseudotypes into primary human hepatocytes by clathrin-dependent endocytosis J Gen Virol 87 2006 2583 2593
89. M. Trotard, C. Lepere-Douard, M. Regeard, C. Piquet-Pellorce, D. Lavillette, and F.L. Cosset Kinases required in hepatitis C virus entry and replication highlighted by small interference RNA screening FASEB J 23 2009 3780 3789
90. K.E. Coller, K.L. Berger, N.S. Heaton, J.D. Cooper, R. Yoon, and G. Randall RNA interference and single particle tracking analysis of hepatitis C virus endocytosis PLoS Pathog 5 2009 e1000702
91. M.J. Farquhar, H.J. Harris, M. Diskar, S. Jones, C.J. Mee, and S.U. Nielsen Protein kinase A-dependent step(s) in hepatitis C virus entry and infectivity J Virol 82 2008 8797 8811
92. C.J. Mee, H.J. Harris, M.J. Farquhar, G. Wilson, G. Reynolds, and C. Davis Polarization restricts hepatitis C virus entry into HepG2 hepatoma cells J Virol 83 2009 6211 6221
93. M. Marsh, and A. Helenius Virus entry: open sesame Cell 124 2006 729 740 (Pubitemid 43261448)
94. A.E. Smith, and A. Helenius How viruses enter animal cells Science 304 2004 237 242 (Pubitemid 38452168)
95. F. Penin, J. Dubuisson, F.A. Rey, D. Moradpour, and J.M. Pawlotsky Structural biology of hepatitis C virus Hepatology 39 2004 5 19 (Pubitemid 38461460)
96. A.T. Yagnik, A. Lahm, A. Meola, R.M. Roccasecca, B.B. Ercole, and A. Nicosia A model for the hepatitis C virus envelope glycoprotein E2 Proteins 40 2000 355 366 (Pubitemid 30624444)
97. F.X. Heinz, K. Stiasny, and S.L. Allison The entry machinery of flaviviruses Arch Virol Suppl 2004 133 137
98. C. Voisset, and J. Dubuisson Functional hepatitis C virus envelope glycoproteins Biol Cell 96 2004 413 420 (Pubitemid 39157945)
99. D. Lavillette, B. Bartosch, D. Nourrisson, G. Verney, F.L. Cosset, and F. Penin Hepatitis C virus glycoproteins mediate low pH-dependent membrane fusion with liposomes J Biol Chem 281 2006 3909 3917 (Pubitemid 43847814)
100. D.M. Tscherne, C.T. Jones, M.J. Evans, B.D. Lindenbach, J.A. McKeating, and C.M. Rice Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry J Virol 80 2006 1734 1741 (Pubitemid 43228714)
101. A. Haberstroh, E.K. Schnober, M.B. Zeisel, P. Carolla, H. Barth, and H.E. Blum Neutralizing host responses in hepatitis C virus infection target viral entry at postbinding steps and membrane fusion Gastroenterology 135 2008 1719 1728 e1711
102. S. Haid, T. Pietschmann, and E.I. Pecheur Low pH-dependent hepatitis C virus membrane fusion depends on E2 integrity, target lipid composition, and density of virus particles J Biol Chem 284 2009 17657 17667
103. J.M. Timpe, Z. Stamataki, A. Jennings, K. Hu, M.J. Farquhar, and H.J. Harris Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies Hepatology 47 2008 17 24 (Pubitemid 351171037)
104. J. Witteveldt, M.J. Evans, J. Bitzegeio, G. Koutsoudakis, A.M. Owsianka, and A.G. Angus CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells J Gen Virol 90 2009 48 58
105. M. Gao, R.E. Nettles, M. Belema, L.B. Snyder, V.N. Nguyen, and R.A. Fridell Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect Nature 465 2010 96 100
106. M.B. Zeisel, H. Barth, C. Schuster, and T.F. Baumert Hepatitis C virus entry: molecular mechanisms and targets for antiviral therapy Front Biosci 14 2009 3274 3285
107. S. Khaliq, S.A. Khaliq, M. Zahur, B. Ijaz, S. Jahan, and M. Ansar RNAi as a new therapeutic strategy against HCV Biotechnol Adv 28 2010 27 34
108. J. Balzarini Carbohydrate-binding agents: a potential future cornerstone for the chemotherapy of enveloped viruses? Antivir Chem Chemother 18 2007 1 11 (Pubitemid 46426933)
109. M.R. Boyd, K.R. Gustafson, J.B. McMahon, R.H. Shoemaker, B.R. O'Keefe, and T. Mori Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development Antimicrob Agents Chemother 41 1997 1521 1530 (Pubitemid 27289680)
110. B.R. O'Keefe, D.F. Smee, J.A. Turpin, C.J. Saucedo, K.R. Gustafson, and T. Mori Potent anti-influenza activity of cyanovirin-N and interactions with viral hemagglutinin Antimicrob Agents Chemother 47 2003 2518 2525 (Pubitemid 36919454)
111. S.R. Shenoy, B.R. O'Keefe, A.J. Bolmstedt, L.K. Cartner, and M.R. Boyd Selective interactions of the human immunodeficiency virus-inactivating protein cyanovirin-N with high-mannose oligosaccharides on gp120 and other glycoproteins J Pharmacol Exp Ther 297 2001 704 710 (Pubitemid 32378003)
112. F. Helle, C. Wychowski, N. Vu-Dac, K.R. Gustafson, C. Voisset, and J. Dubuisson Cyanovirin-N inhibits hepatitis C virus entry by binding to envelope protein glycans J Biol Chem 281 2006 25177 25183 (Pubitemid 44401904)
113. X. Wei, J.M. Decker, S. Wang, H. Hui, J.C. Kappes, and X. Wu Antibody neutralization and escape by HIV-1 Nature 422 2003 307 312 (Pubitemid 36378357)
114. E.G. Cormier, F. Tsamis, F. Kajumo, R.J. Durso, J.P. Gardner, and T. Dragic CD81 is an entry coreceptor for hepatitis C virus Proc Natl Acad Sci USA 101 2004 7270 7274 (Pubitemid 38638022)
115. E. Lee, M. Pavy, N. Young, C. Freeman, and M. Lobigs Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses Antiviral Res 69 2006 31 38 (Pubitemid 41790479)
116. H. Huang, F. Sun, D.M. Owen, W. Li, Y. Chen, and M. Gale Jr. Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins Proc Natl Acad Sci USA 104 2007 5848 5853 (Pubitemid 47175622)
117. P. Gastaminza, G. Cheng, S. Wieland, J. Zhong, W. Liao, and F.V. Chisari Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion J Virol 82 2008 2120 2129 (Pubitemid 351293514)
118. K.S. Chang, J. Jiang, Z. Cai, and G. Luo Human apolipoprotein e is required for infectivity and production of hepatitis C virus in cell culture J Virol 81 2007 13783 13793 (Pubitemid 350247871)
119. W.J. Benga, S.E. Krieger, M. Dimitrova, M.B. Zeisel, M. Parnot, and J. Lupberger Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles Hepatology 51 2010 43 53
120. M.B. Zeisel, S. Fafi-Kremer, I. Fofana, H. Barth, F. Stoll-Keller, and M. Doffoel Neutralizing antibodies in hepatitis C virus infection World J Gastroenterol 13 2007 4824 4830 (Pubitemid 47496747)
121. A. Zibert, E. Schreier, and M. Roggendorf Antibodies in human sera specific to hypervariable region 1 of hepatitis C virus can block viral attachment Virology 208 1995 653 661
122. T. Vanwolleghem, J. Bukh, P. Meuleman, I. Desombere, J.C. Meunier, and H. Alter Polyclonal immunoglobulins from a chronic hepatitis C virus patient protect human liver-chimeric mice from infection with a homologous hepatitis C virus strain Hepatology 47 2008 1846 1855 (Pubitemid 351945552)
123. M. Perotti, N. Mancini, R.A. Diotti, A.W. Tarr, J.K. Ball, and A. Owsianka Identification of a broadly cross-reacting and neutralizing human monoclonal antibody directed against the hepatitis C virus E2 protein J Virol 82 2008 1047 1052
124. D.X. Johansson, C. Voisset, A.W. Tarr, M. Aung, J.K. Ball, and J. Dubuisson Human combinatorial libraries yield rare antibodies that broadly neutralize hepatitis C virus Proc Natl Acad Sci USA 104 2007 16269 16274 (Pubitemid 350099395)
125. J.C. Meunier, R.S. Russell, V. Goossens, S. Priem, H. Walter, and E. Depla Isolation and characterization of broadly neutralizing human monoclonal antibodies to the e1 glycoprotein of hepatitis C virus J Virol 82 2008 966 973
126. S.E. VanCompernolle, A.V. Wiznycia, J.R. Rush, M. Dhanasekaran, P.W. Baures, and S.C. Todd Small molecule inhibition of hepatitis C virus E2 binding to CD81 Virology 314 2003 371 380 (Pubitemid 37158015)
127. P. Meuleman, J. Hesselgesser, M. Paulson, T. Vanwolleghem, I. Desombere, and H. Reiser Anti-CD81 antibodies can prevent a hepatitis C virus infection in vivo Hepatology 48 2008 1761 1768
128. I.N. Baranova, T.G. Vishnyakova, A.V. Bocharov, R. Kurlander, Z. Chen, and M.L. Kimelman Serum amyloid A binding to CLA-1 (CD36 and LIMPII analogous-1) mediates serum amyloid A protein-induced activation of ERK1/2 and p38 mitogen-activated protein kinases J Biol Chem 280 2005 8031 8040 (Pubitemid 40349701)
129. L. Cai, M.C. de Beer, F.C. de Beer, and D.R. van der Westhuyzen Serum amyloid A is a ligand for scavenger receptor class B type I and inhibits high density lipoprotein binding and selective lipid uptake J Biol Chem 280 2005 2954 2961 (Pubitemid 40189405)
130. M. Lavie, C. Voisset, N. Vu-Dac, V. Zurawski, G. Duverlie, and C. Wychowski Serum amyloid A has antiviral activity against hepatitis C virus by inhibiting virus entry in a cell culture system Hepatology 44 2006 1626 1634 (Pubitemid 44953668)
131. M.T. Catanese, R. Graziani, T. von Hahn, M. Moreau, T. Huby, and G. Paonessa High-avidity monoclonal antibodies against the human scavenger class B type I receptor efficiently block hepatitis C virus infection in the presence of high-density lipoprotein J Virol 81 2007 8063 8071 (Pubitemid 47101492)
132. A.J. Syder, L. Haekyung, M.B. Zeisel, J. Grove, E. Soulier, and J. MacDonald Small molecule scavenger receptor bi antagonists are potent HCV entry inhibitors J Hepatol 54 2011 48 55
133. I. Fofana, S.E. Krieger, F. Grunert, S. Glauben, F. Xiao, and S. Fafi-Kremer Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes Gastroenterology 39 2010 953 964
134. A. Vaillant, J.M. Juteau, H. Lu, S. Liu, C. Lackman-Smith, and R. Ptak Phosphorothioate oligonucleotides inhibit human immunodeficiency virus type 1 fusion by blocking gp41 core formation Antimicrob Agents Chemother 50 2006 1393 1401
135. T. Matsumura, Z. Hu, T. Kato, M. Dreux, Y.Y. Zhang, and M. Imamura Amphipathic DNA polymers inhibit hepatitis C virus infection by blocking viral entry Gastroenterology 137 2009 673 681
136. E. Poveda, V. Briz, and V. Soriano Enfuvirtide, the first fusion inhibitor to treat HIV infection AIDS Rev 7 2005 139 147 (Pubitemid 41671913)
137. Y.S. Boriskin, I.A. Leneva, E.I. Pecheur, and S.J. Polyak Arbidol: a broad-spectrum antiviral compound that blocks viral fusion Curr Med Chem 15 2008 997 1005 (Pubitemid 351736402)
138. Y.S. Boriskin, E.I. Pecheur, and S.J. Polyak Arbidol: a broad-spectrum antiviral that inhibits acute and chronic HCV infection Virol J 3 2006 56
139. S.J. Polyak, C. Morishima, M.C. Shuhart, C.C. Wang, Y. Liu, and D.Y. Lee Inhibition of T-cell inflammatory cytokines, hepatocyte NF-κB signaling, and HCV infection by standardized silymarin Gastroenterology 132 2007 1925 1936 (Pubitemid 46677939)
140. J. Wagoner, A. Negash, O.J. Kane, L.E. Martinez, Y. Nahmias, and N. Bourne Multiple effects of silymarin on the hepatitis C virus lifecycle Hepatology 51 2010 1912 1921
141. M.B. Zeisel, M. Turek, and T.F. Baumert Tight junctions and viral entry Future Virol 5 2010 263 271
142. G.L. Davis, D.R. Nelson, N. Terrault, T.L. Pruett, T.D. Schiano, and C.V. Fletcher A randomized, open-label study to evaluate the safety and pharmacokinetics of human hepatitis C immune globulin (Civacir) in liver transplant recipients Liver transpl 11 2005 941 949 (Pubitemid 41122452)
143. G. Borgia HepeX-C (XTL Biopharmaceuticals) Curr Opin Investig Drugs 5 2004 892 897
144. T.D. Schiano, M. Charlton, Z. Younossi, E. Galun, T. Pruett, and R. Tur-Kaspa Monoclonal antibody HCV-AbXTL68 in patients undergoing liver transplantation for HCV: results of a phase 2 randomized study Liver transpl 12 2006 1381 1389 (Pubitemid 44405128)
145. R. Eren, D. Landstein, D. Terkieltaub, O. Nussbaum, A. Zauberman, and J. Ben-Porath Preclinical evaluation of two neutralizing human monoclonal antibodies against hepatitis C virus (HCV): a potential treatment to prevent HCV reinfection in liver transplant patients J Virol 80 2006 2654 2664 (Pubitemid 43346361)
146. Z.Y. Keck, T.K. Li, J. Xia, B. Bartosch, F.L. Cosset, and J. Dubuisson Analysis of a highly flexible conformational immunogenic domain a in hepatitis C virus E2 J Virol 79 2005 13199 13208 (Pubitemid 41508135)
147. A. Owsianka, A.W. Tarr, V.S. Juttla, D. Lavillette, B. Bartosch, and F.L. Cosset Monoclonal antibody AP33 defines a broadly neutralizing epitope on the hepatitis C virus E2 envelope glycoprotein J Virol 79 2005 11095 11104 (Pubitemid 41170650)
148. J. Grove, S. Nielsen, J. Zhong, M.F. Bassendine, H.E. Drummer, and P. Balfe Identification of a residue in hepatitis C virus E2 glycoprotein that determines scavenger receptor BI and CD81 receptor dependency and sensitivity to neutralizing antibodies J Virol 82 2008 12020 12029
149. T.J. Broering, K.A. Garrity, N.K. Boatright, S.E. Sloan, F. Sandor, and W.D. Thomas Jr. Identification and characterization of broadly neutralizing human monoclonal antibodies directed against the E2 envelope glycoprotein of hepatitis C virus J Virol 83 2009 12473 12482
150. M. Biermer, and T. Berg Rapid suppression of hepatitis C viremia induced by intravenous silibinin plus ribavirin Gastroenterology 137 2009 390 391