Hepatitis C virus entry: Molecular mechanisms and targets for antiviral therapy

Frontiers in Bioscience

Volumn 14, Issue 9, 2009, Pages 3274-3285

  Zeisel, Mirjam B ^a,b   Barth, Heidi ^c   Schuster, Catherine ^a,b   Baumert, Thomas F ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY HOSPITAL OF STRASBOURG   (France)

Author keywords

Entry inhibitor; Hepatitis C virus; Neutralizing antibodies; Viral entry

Indexed keywords

HEPATITIS C VIRUS;

ANTIVIRUS AGENT;

HEPATITIS C; HEPATITIS C VIRUS; HUMAN; MEMBRANE FUSION; METABOLISM; PHYSIOLOGY; REVIEW;

ANTIVIRAL AGENTS; HEPACIVIRUS; HEPATITIS C; HUMANS; MEMBRANE FUSION;

EID: 63849140326     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2735/3450     Document Type: Article

References (110)

1. Chisari, F. V.: Unscrambling hepatitis C virus-host interactions. Nature, 436, 930-2(2005) (Pubitemid 41191667)
2. De Francesco, R. and G. Migliaccio: Challenges and successes in developing new therapies for hepatitis C. Nature, 436, 953-60(2005) (Pubitemid 41191671)
3. Lindenbach, B. D. and C. M. Rice: Flaviviridae: the viruses and their replication. Fields Virology, 4th ed. D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman and S. E. Straus, Ed. Eds., Lippincott Williams & Wilkins, 991-1041 (2001)
4. Sung, V. M., S. Shimodaira, A. L. Doughty, G. R. Picchio, H. Can, T. S. Yen, K. L. Lindsay, A. M. Levine and M. M. Lai: Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: the apoptotic effects of virus infection. J Virol, 77, 2134-46(2003) (Pubitemid 36110026)
5. Goutagny, N., A. Fatmi, V. de Ledinghen, F. Penin, P. Couzigou, G. Inchauspe and C. Bain: Evidence of viral replication in circulating dendritic cells during hepatitis C virus infection. J Infect Dis, 187, 1951-8(2003) (Pubitemid 36724494)
6. Marsh, M. and A. Helenius: Virus entry: open sesame. Cell, 124, 729-40(2006) (Pubitemid 43261448)
7. Kaito, M., S. Watanabe, K. Tsukiyama-Kohara, K. Yamaguchi, Y. Kobayashi, M. Konishi, M. Yokoi, S. Ishida, S. Suzuki and M. Kohara: Hepatitis C virus particle detected by immunelectron microscopic study. J. Gen. Virol., 75, 1755-1760(1994) (Pubitemid 24211260)
8. Shimizu, Y. K., S. M. Feinstone, M. Kohara, R. Purcell and H. Yoshikura: Hepatitis C virus: detection of intracellular virus particles by electron microscopy. Hepatology, 23, 205-209(1996) (Pubitemid 26045935)
9. Wakita, T., T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H. G. Krausslich, M. Mizokami, R. Bartenschlager and T. J. Liang: Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med, 11, 791-6(2005) (Pubitemid 41021213)
10. Penin, F., J. Dubuisson, F. A. Rey, D. Moradpour and J. M. Pawlotsky: Structural biology of hepatitis C virus. Hepatology, 39, 5-19(2004) (Pubitemid 38461460)
11. Op de Beeck, A., R. Montserret, S. Duvet, L. Cocquerel, R. Cacan, B. Barberot, M. le Maire, F. Penin and J. Dubuisson: The transmembrane domains of hepatitis C virus envelope glycoproteins E1 and E2 play a major role in heterodimerization. J. Biol. Chem., 275, 31428-37. (2000)
12. Barth, H., T. J. Liang and T. F. Baumert: Hepatitis C virus entry: molecular biology and clinical implications. Hepatology, 44, 527-35(2006) (Pubitemid 44433708)
13. Pileri, P., Y. Uematsu, S. Campagnoli, G. Galli, F. Falugi, R. Petracca, A. J. Weiner, M. Houghton, D. Rosa, G. Grandi and S. Abrignani: Binding of hepatitis C virus to CD81. Science, 282, 938-41(1998) (Pubitemid 28507525)
14. Baumert, T. F., S. Ito, D. T. Wong and T. J. Liang: Hepatitis C virus structural proteins assemble into viruslike particles in insect cells. J. Virol., 72, 3827-36(1998) (Pubitemid 28188682)
15. Barth, H., R. Cerino, M. Arcuri, M. Hoffmann, P. Schurmann, M. I. Adah, B. Gissler, X. Zhao, V. Ghisetti, B. Lavezzo, H. E. Blum, F. von Weizsacker, A. Vitelli, E. Scarselli and T. F. Baumert: Scavenger receptor class B type I and hepatitis C virus infection of primary tupaia hepatocytes. J Virol, 79, 5774-85. (2005) (Pubitemid 40548246)
16. Wellnitz, S., B. Klumpp, H. Barth, S. Ito, E. Depla, J. Dubuisson, H. E. Blum and T. F. Baumert: Binding of hepatitis C virus-like particles derived from infectious clone H77C to defined human cell lines. J. Virol., 76, 1181-93. (2002) (Pubitemid 34066422)
17. Bartosch, B., J. Dubuisson and F. L. Cosset: Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med., 197, 633-42(2003) (Pubitemid 36314658)
18. Hsu, M., J. Zhang, M. Flint, C. Logvinoff, C. Cheng-Mayer, C. M. Rice and J. A. McKeating: Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. U S A, 100, 7271-7276. (2003) (Pubitemid 36706428)
19. Lindenbach, B. D., M. J. Evans, A. J. Syder, B. Wolk, T. L. Tellinghuisen, C. C. Liu, T. Maruyama, R. O. Hynes, D. R. Burton, J. A. McKeating and C. M. Rice: Complete replication of hepatitis C virus in cell culture. Science, 309, 623-6(2005) (Pubitemid 41033648)
20. Zhong, J., P. Gastaminza, G. Cheng, S. Kapadia, T. Kato, D. R. Burton, S. F. Wieland, S. L. Uprichard, T. Wakita and F. V. Chisari: Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A, 102, 9294-9(2005) (Pubitemid 40923557)
21. Weiner, A. J., M. J. Brauer, J. Rosenblatt, K. H. Richman, J. Tung, K. Crawford, F. Bonino, G. Saracco, Q. L. Choo, M. Houghton and et al.: Variable and hypervariable domains are found in the regions of HCV corresponding to the flavivirus envelope and NS1 proteins and the pestivirus envelope glycoproteins. Virology, 180, 842-8(1991)
22. Bartosch, B., A. Vitelli, C. Granier, C. Goujon, J. Dubuisson, S. Pascale, E. Scarselli, R. Cortese, A. Nicosia and F. L. Cosset: 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, 41624-30(2003) (Pubitemid 37310418)
23. Callens, N., Y. Ciczora, B. Bartosch, N. Vu-Dac, F. L. Cosset, J. M. Pawlotsky, F. Penin and J. Dubuisson: Basic residues in hypervariable region 1 of hepatitis C virus envelope glycoprotein e2 contribute to virus entry. J Virol, 79, 15331-41(2005) (Pubitemid 43032315)
24. Scarselli, E., H. Ansuini, R. Cerino, R. M. Roccasecca, S. Acali, G. Filocamo, C. Traboni, A. Nicosia, R. Cortese and A. Vitelli: The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J, 21, 5017-5025. (2002)
25. Rosa, D., S. Campagnoli, C. Moretto, E. Guenzi, L. Cousens, M. Chin, C. Dong, A. Weiner, J. Y. N. Lau, Q.-L. Choo, D. Chien, P. Pileri, M. Houghton and S. Abrignani: 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, 1759-1763(1996) (Pubitemid 26079830)
26. Steinmann, D., H. Barth, B. Gissler, P. Schürmann, M. I. Adah, J. T. Gerlach, G. R. Pape, E. Depla, D. Jacobs, G. Maertens, A. H. Patel, G. Inchauspé, T. J. Liang, H. E. Blum and T. F. Baumert: Inhibition of hepatitis C virus-like particle binding to target cells by antiviral antibodies in acute and chronic hepatitis C. J Virol, 78, 9030-9040(2004) (Pubitemid 39096514)
27. Bartosch, B., J. Bukh, J. C. Meunier, C. Granier, R. E. Engle, W. C. Blackwelder, S. U. Emerson, F. L. Cosset and R. H. Purcell: In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci U S A, 100, 14199-204. Epub 2003 Nov. 14. (2003) (Pubitemid 37499214)
28. Triyatni, M., B. Saunier, P. Maruvada, A. R. Davis, L. Ulianich, T. Heller, A. Patel, L. D. Kohn and T. J. Liang: Interaction of hepatitis C virus-like particles and cells: a model system for studying viral binding and entry. J. Virol., 76, 9335-9344. (2002) (Pubitemid 34919891)
29. Keck, Z. Y., V. M. Sung, S. Perkins, J. Rowe, S. Paul, T. J. Liang, M. M. Lai and S. K. Foung: Human monoclonal antibody to hepatitis C virus E1 glycoprotein that blocks virus attachment and viral infectivity. J Virol, 78, 7257-63(2004) (Pubitemid 38781563)
30. Takikawa, S., K. Ishii, H. Aizaki, T. Suzuki, H. Asakura, Y. Matsuura and T. Miyamura: Cell fusion activity of hepatitis C virus envelope proteins. J. Virol., 74, 5066-74(2000) (Pubitemid 30313845)
31. Agnello, V., 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. U S A, 96, 12766-71. (1999) (Pubitemid 29513577)
32. Barth, H., C. Schäfer, M. I. Adah, F. Zhang, R. J. Linhardt, H. Toyoda, A. Kinoshita-Toyoda, T. Toida, T. H. Van Kuppevelt, E. Depla, F. v. Weizsäcker, H. E. Blum and T. F. Baumert: Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem., 278, 41003-12(2003) (Pubitemid 37280923)
33. Pohlmann, S., J. Zhang, F. Baribaud, Z. Chen, G. J. Leslie, G. Lin, A. Granelli-Piperno, R. W. Doms, C. M. Rice and J. A. McKeating: Hepatitis C Virus Glycoproteins Interact with DC-SIGN and DC-SIGNR. J. Virol., 77, 4070-4080. (2003) (Pubitemid 36350947)
34. Lozach, P. Y., A. Amara, B. Bartosch, J. L. Virelizier, F. Arenzana-Seisdedos, F. L. Cosset and R. Altmeyer: C-type lectins L-SIGN and DC-SIGN capture and transmit infectious hepatitis C virus pseudotype particles. J Biol Chem, 279, 32035-45(2004) (Pubitemid 39014648)
35. Koutsoudakis, G., A. Kaul, E. Steinmann, S. Kallis, V. Lohmann, T. Pietschmann and R. Bartenschlager: Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol, 80, 5308-20(2006)
36. Grove, J., T. Huby, Z. Stamataki, T. Vanwolleghem, P. Meuleman, M. Farquhar, A. Schwarz, M. Moreau, J. S. Owen, G. Leroux-Roels, P. Balfe and J. A. McKeating: Scavenger receptor BI and BII expression levels modulate Hepatitis C virus infectivity. J Virol, 81, 3162-9(2007) (Pubitemid 46456625)
37. Kapadia, S. B., H. Barth, T. Baumert, J. A. McKeating and F. V. Chisari: Initiation of Hepatitis C Virus Infection Is Dependent on Cholesterol and Cooperativity between CD81 and Scavenger Receptor B Type I. J Virol, 81, 374-83(2007) (Pubitemid 44975176)
38. Zeisel, M. B, Koutsoudakis, G, Schnober, E. K., Haberstroh, A, Blum, H. E., Cosset, F-L, Wakita, T, Jaeck, D, Doffoel, M, Royer, C, Soulier, E, Schvoerer, E, Schuster, C, Stoll-Keller, F, Bartenschlager, R, Pietschmann, T, Barth, H, Baumert, T. F.: Scavenger receptor BI is a key host factor for Hepatitis C virus infection required for an entry step closely linked to CD81. Hepatology, 46, 1722-31(2007)
39. Evans, M. J., T. von Hahn, D. M. Tscherne, A. J. Syder, M. Panis, B. Wolk, T. Hatziioannou, J. A. McKeating, P. D. Bieniasz and C. M. Rice: Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature, 446, 801-5(2007) (Pubitemid 46582027)
40. Germi, R., J. M. Crance, D. Garin, J. Guimet, H. Lortat-Jacob, R. W. Ruigrok, J. P. Zarski and E. Drouet: Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J Med Virol, 68, 206-15(2002)
41. Basu, A., A. Beyene, K. Meyer and R. Ray: The hypervariable region 1 of the E2 glycoprotein of hepatitis C virus binds to glycosaminoglycans, but this binding does not lead to infection in a pseudotype system. J Virol, 78, 4478-86(2004) (Pubitemid 38501067)
42. van Kooyk, Y. and T. B. Geijtenbeek: DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol, 3, 697-709(2003) (Pubitemid 41070811)
43. Koppel, E. A., K. P. van Gisbergen, T. B. Geijtenbeek and Y. van Kooyk: Distinct functions of DC-SIGN and its homologues L-SIGN (DC-SIGNR) and mSIGNR1 in pathogen recognition and immune regulation. Cell Microbiol, 7, 157-65(2005) (Pubitemid 40259732)
44. Gardner, J. P., R. J. Durso, R. R. Arrigale, G. P. Donovan, P. J. Maddon, T. Dragic and W. C. Olson: L-SIGN (CD 209L) is a liver-specific capture receptor for hepatitis C virus. Proc. Natl. Acad. Sci. U S A, 100, 4498-4503. (2003) (Pubitemid 36457759)
45. Cormier, E. G., R. J. Durso, F. Tsamis, L. Boussemart, C. Manix, W. C. Olson, J. P. Gardner and T. Dragic: L-SIGN (CD209L) and DC-SIGN (CD209) mediate transinfection of liver cells by hepatitis C virus. Proc Natl Acad Sci U S A, 101, 14067-72(2004) (Pubitemid 39305031)
46. Hemler, M. E.: Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol, 6, 801-11(2005) (Pubitemid 41726118)
47. Zhang, J., 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, 1448-55. (2004) (Pubitemid 38095855)
48. McKeating, J. A., L. Q. Zhang, C. Logvinoff, M. Flint, J. Zhang, J. Yu, D. Butera, D. D. Ho, L. B. Dustin, C. M. Rice and P. Balfe: Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner. J Virol, 78, 8496-505(2004) (Pubitemid 39025115)
49. Akazawa, D., T. Date, K. Morikawa, A. Murayama, M. Miyamoto, M. Kaga, H. Barth, T. F. Baumert, J. Dubuisson and T. Wakita: Cd81 Expression Is Important For Heterogeneous Hcv Permissiveness Of Huh7 Cell Clones. J Virol, 81, 5036-45(2007) (Pubitemid 46744415)
50. Koutsoudakis, G., E. Herrmann, S. Kallis, R. Bartenschlager and T. Pietschmann: The level of CD81 cell surface expression is a key determinant for productive entry of Hepatitis C Virus into host cells. J Virol, 81, 588-98(2007) (Pubitemid 46067886)
51. Meola, A., A. Sbardellati, B. Bruni Ercole, M. Cerretani, M. Pezzanera, A. Ceccacci, A. Vitelli, S. Levy, A. Nicosia, C. Traboni, J. McKeating and E. Scarselli: Binding of hepatitis C virus E2 glycoprotein to CD81 does not correlate with species permissiveness to infection. J. Virol., 74, 5933-8(2000) (Pubitemid 30412962)
52. Flint, M., T. von Hahn, J. Zhang, M. Farquhar, C. T. Jones, P. Balfe, C. M. Rice and J. A. McKeating: Diverse CD81 proteins support hepatitis C virus infection. J Virol, 80, 11331-42(2006) (Pubitemid 44706573)
53. Cormier, E. G., 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 U S A, 101, 7270-4(2004) (Pubitemid 38638022)
54. Furuse, M., 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, 1539-50(1998) (Pubitemid 28309169)
55. Krieger, M.: Scavenger receptor class B type I is a multiligand HDL receptor that influences diverse physiologic systems. J. Clin. Invest., 108, 793-7. (2001) (Pubitemid 32880286)
56. Yamada, E., M. Montoya, C. G. Schuettler, T. P. Hickling, A. W. Tarr, A. Vitelli, J. Dubuisson, A. H. Patel, J. K. Ball and P. Borrow: Analysis of the binding of hepatitis C virus genotype 1a and 1b E2 glycoproteins to peripheral blood mononuclear cell subsets. J Gen Virol, 86, 2507-12(2005) (Pubitemid 41167599)
57. Philips, J. A., E. J. Rubin and N. Perrimon: Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science, 309, 1251-3(2005) (Pubitemid 41170920)
58. Vishnyakova, T. G., R. Kurlander, A. V. Bocharov, I. N. Baranova, Z. Chen, M. S. Abu-Asab, M. Tsokos, D. Malide, F. Basso, A. Remaley, G. Csako, T. L. Eggerman and A. P. Patterson: CLA-1 and its splicing variant CLA-2 mediate bacterial adhesion and cytosolic bacterial invasion in mammalian cells. Proc Natl Acad Sci U S A, 103, 16888-93(2006) (Pubitemid 44737348)
59. Lavillette, D., A. W. Tarr, C. Voisset, P. Donot, B. Bartosch, C. Bain, A. H. Patel, J. Dubuisson, J. K. Ball and F. L. Cosset: Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus. Hepatology, 41, 265-74(2005) (Pubitemid 40173981)
60. Lavillette, D., Y. Morice, G. Germanidis, P. Donot, A. Soulier, E. Pagkalos, G. Sakellariou, L. Intrator, B. Bartosch, J. M. Pawlotsky and F. L. Cosset: 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, 6023-34(2005) (Pubitemid 40617208)
61. Bartosch, B., G. Verney, M. Dreux, P. Donot, Y. Morice, F. Penin, J. M. Pawlotsky, D. Lavillette and F. L. Cosset: 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, 8217-29(2005) (Pubitemid 40853525)
62. Voisset, C., 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, 7793-9(2005) (Pubitemid 40349673)
63. von Hahn, T., B. D. Lindenbach, A. Boullier, O. Quehenberger, M. Paulson, C. M. Rice and J. A. McKeating: Oxidized low-density lipoprotein inhibits hepatitis C virus cell entry in human hepatoma cells. Hepatology, 43, 932-42(2006) (Pubitemid 43724618)
64. Molina, S., V. Castet, C. Fournier-Wirth, L. Pichard-Garcia, R. Avner, D. Harats, J. Roitelman, R. Barbaras, P. Graber, P. Ghersa, M. Smolarsky, A. Funaro, F. Malavasi, D. Larrey, J. Coste, J. M. Fabre, A. Sa-Cunha and P. Maurel: The low-density lipoprotein receptor plays a role in the infection of primary human hepatocytes by hepatitis C virus. J Hepatol, 46, 411-9(2007) (Pubitemid 46201721)
65. Beglova, N. and S. C. Blacklow: The LDL receptor: how acid pulls the trigger. Trends Biochem Sci, 30, 309-17(2005) (Pubitemid 40799049)
66. Thomssen, R., 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, 293-300(1992)
67. Andre, P., F. Komurian-Pradel, S. Deforges, M. Perret, J. L. Berland, M. Sodoyer, S. Pol, C. Brechot, G. Paranhos-Baccala and V. Lotteau: Characterization of low-and verylow-density hepatitis C virus RNA-containing particles. J Virol, 76, 6919-28. (2002) (Pubitemid 41246207)
68. Wunschmann, S., 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 lowdensity lipoprotein receptor. J. Virol., 74, 10055-62(2000)
69. Heinz, F. X. and S. L. Allison: Flavivirus structure and membrane fusion. Adv Virus Res, 59, 63-97(2003) (Pubitemid 137639364)
70. Smith, A. E. and A. Helenius: How viruses enter animal cells. Science, 304, 237-42. (2004) (Pubitemid 38452168)
71. Bressanelli, S., K. Stiasny, S. L. Allison, E. A. Stura, S. Duquerroy, J. Lescar, F. X. Heinz and F. A. Rey: Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. Embo J, 23, 728-38(2004) (Pubitemid 38425440)
72. Blanchard, E., S. Belouzard, L. Goueslain, T. Wakita, J. Dubuisson, C. Wychowski and Y. Rouille: Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol, 80, 6964-72(2006) (Pubitemid 44025195)
73. Meertens, L., 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, 11571-8(2006) (Pubitemid 44788871)
74. Codran, A., C. Royer, D. Jaeck, M. Bastien-Valle, T. F. Baumert, M. P. Kieny, C. A. Pereira and J. P. Martin: Entry of hepatitis C virus pseudotypes into primary human hepatocytes by clathrin-dependent endocytosis. J Gen Virol, 87, 2583-93(2006)
75. Yagnik, A. T., A. Lahm, A. Meola, R. M. Roccasecca, B. B. Ercole, A. Nicosia and A. Tramontano: A model for the hepatitis C virus envelope glycoprotein E2. Proteins, 40, 355-66. (2000) (Pubitemid 30624444)
76. Heinz, F. X., K. Stiasny and S. L. Allison: The entry machinery of flaviviruses. Arch Virol Suppl, 133-7 (2004)
77. Voisset, C. and J. Dubuisson: Functional hepatitis C virus envelope glycoproteins. Biol Cell, 96, 413-20(2004) (Pubitemid 39157945)
78. Lavillette, D., B. Bartosch, D. Nourrisson, G. Verney, F. L. Cosset, F. Penin and E. I. Pecheur: Hepatitis C virus glycoproteins mediate low pH-dependent membrane fusion with liposomes. J Biol Chem, 281, 3909-17(2006) (Pubitemid 43847814)
79. Tscherne, D. M., 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, 1734-41(2006) (Pubitemid 43228714)
80. Walker, M. A.: Hepatitis C virus: an overview of current approaches and progress. Drug Discov Today, 4, 518-529(1999) (Pubitemid 29497855)
81. Farci, P., H. J. Alter, D. C. Wong, R. H. Miller, S. Govindarajan, R. Engle, M. Shapiro and R. H. Purcell: Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc Natl Acad Sci U S A, 91, 7792-6(1994)
82. Farci, P., A. Shimoda, D. Wong, T. Cabezon, D. de Gioannis, A. Strazzera, Y. Shimizu, M. Shapiro, H. J. Alter and R. H. Purcell: Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc. Natl. Acad. Sci. U S A, 93, 15394-9(1996) (Pubitemid 27009611)
83. Zibert, A., P. Dudziak, E. Schreier and M. Roggendorf: Characterization of antibody response to hepatitis C virus protein E2 and significance of hypervariable region 1-specific antibodies in viral neutralization. Arch Virol, 142, 523-34(1997) (Pubitemid 27161772)
84. Christie, J. M., C. J. Healey, J. Watson, V. S. Wong, M. Duddridge, N. Snowden, W. M. Rosenberg, K. A. Fleming, H. Chapel and R. W. Chapman: Clinical outcome of hypogammaglobulinaemic patients following outbreak of acute hepatitis C: 2 year follow up. Clin Exp Immunol, 110, 4-8(1997) (Pubitemid 27428507)
85. Chapel, H. M., J. M. Christie, V. Peach and R. W. Chapman: Five-year follow-up of patients with primary antibody deficiencies following an outbreak of acute hepatitis C. Clin Immunol, 99, 320-4(2001)
86. Logvinoff, C., M. E. Major, D. Oldach, S. Heyward, A. Talal, P. Balfe, S. M. Feinstone, H. Alter, C. M. Rice and J. A. McKeating: Neutralizing antibody response during acute and chronic hepatitis C virus infection. Proc Natl Acad Sci U S A, 101, 10149-54(2004) (Pubitemid 38891210)
87. Meunier, J. C., R. E. Engle, K. Faulk, M. Zhao, B. Bartosch, H. Alter, S. U. Emerson, F. L. Cosset, R. H. Purcell and J. Bukh: Evidence for cross-genotype neutralization of hepatitis C virus pseudo-particles and enhancement of infectivity by apolipoprotein C1. Proc Natl Acad Sci U S A, 102, 4560-5. Epub 2005 Mar. 14. (2005) (Pubitemid 40397151)
88. Hadlock, K. G., R. Gish, J. Rowe, S. S. Rajyaguru, M. Newsom, A. Warford and S. K. Foung: Cross-reactivity and clinical impact of the antibody response to hepatitis C virus second envelope glycoprotein (E2) J Med Virol, 65, 23-9(2001)
89. Netski, D. M., T. Mosbruger, E. Depla, G. Maertens, S. C. Ray, R. G. Hamilton, S. Roundtree, D. L. Thomas, J. McKeating and A. Cox: Humoral immune response in acute hepatitis C virus infection. Clin Infect Dis, 41, 667-75(2005) (Pubitemid 41170355)
90. Pestka, J. M., M. B. Zeisel, E. Blaser, P. Schurmann, B. Bartosch, F. L. Cosset, A. H. Patel, H. Meisel, J. Baumert, S. Viazov, K. Rispeter, H. E. Blum, M. Roggendorf and T. F. Baumert: Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc Natl Acad Sci U S A, 104, 6025-30(2007) (Pubitemid 47175652)
91. Dreux, M., T. Pietschmann, C. Granier, C. Voisset, S. Ricard-Blum, P. E. Mangeot, Z. Keck, S. Foung, N. Vu-Dac, J. Dubuisson, R. Bartenschlager, D. Lavillette and F. L. Cosset: High density lipoprotein inhibits hepatitis C virus-neutralizing antibodies by stimulating cell entry via activation of the scavenger receptor BI. J Biol Chem, 281, 18285-95(2006) (Pubitemid 44035485)
92. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong and G. M. Shaw: Antibody neutralization and escape by HIV-1. Nature, 422, 307-12(2003) (Pubitemid 36378357)
93. Kwong, P. D., M. L. Doyle, D. J. Casper, C. Cicala, S. A. Leavitt, S. Majeed, T. D. Steenbeke, M. Venturi, I. Chaiken, M. Fung, H. Katinger, P. W. Parren, J. Robinson, D. Van Ryk, L. Wang, D. R. Burton, E. Freire, R. Wyatt, J. Sodroski, W. A. Hendrickson and J. Arthos: HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature, 420, 678-82(2002) (Pubitemid 36764500)
94. Owsianka, A., A. W. Tarr, V. S. Juttla, D. Lavillette, B. Bartosch, F. L. Cosset, J. K. Ball and A. H. Patel: Monoclonal antibody AP33 defines a broadly neutralizing epitope on the hepatitis C virus E2 envelope glycoprotein. J Virol, 79, 11095-104(2005) (Pubitemid 41170650)
95. Schofield, D. J., B. Bartosch, Y. K. Shimizu, T. Allander, H. J. Alter, S. U. Emerson, F. L. Cosset and R. H. Purcell: Human monoclonal antibodies that react with the E2 glycoprotein of hepatitis C virus and possess neutralizing activity. Hepatology, 42, 1055-62(2005) (Pubitemid 43112672)
96. Keck, Z. Y., A. Op de Beeck, K. G. Hadlock, J. Xia, T. K. Li, J. Dubuisson and S. K. Foung: Hepatitis C virus E2 has three immunogenic domains containing conformational epitopes with distinct properties and biological functions. J Virol, 78, 9224-32(2004) (Pubitemid 39096532)
97. Tarr, A. W., A. M. Owsianka, J. M. Timms, C. P. McClure, R. J. Brown, T. P. Hickling, T. Pietschmann, R. Bartenschlager, A. H. Patel and J. K. Ball: Characterization of the hepatitis C virus E2 epitope defined by the broadly neutralizing monoclonal antibody AP33. Hepatology, 43, 592-601(2006)
98. Boyd, M. R., K. R. Gustafson, J. B. McMahon, R. H. Shoemaker, B. R. O'Keefe, T. Mori, R. J. Gulakowski, L. Wu, M. I. Rivera, C. M. Laurencot, M. J. Currens, J. H. Cardellina, 2nd, R. W. Buckheit, Jr., P. L. Nara, L. K. Pannell, R. C. Sowder, 2nd and L. E. Henderson: 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, 1521-30(1997) (Pubitemid 27289680)
99. O'Keefe, B. R., D. F. Smee, J. A. Turpin, C. J. Saucedo, K. R. Gustafson, T. Mori, D. Blakeslee, R. Buckheit and M. R. Boyd: Potent anti-influenza activity of cyanovirin-N and interactions with viral hemagglutinin. Antimicrob Agents Chemother, 47, 2518-25(2003) (Pubitemid 36919454)
100. Shenoy, S. R., 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, 704-10(2001) (Pubitemid 32378003)
101. Helle, F., 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, 25177-83(2006) (Pubitemid 44401904)
102. Balzarini, J.: Carbohydrate-binding agents: a potential future cornerstone for the chemotherapy of enveloped viruses? Antivir Chem Chemother, 18, 1-11(2007) (Pubitemid 46426933)
103. Barth, H., E. K. Schnober, F. Zhang, R. J. Linhardt, E. Depla, B. Boson, F. L. Cosset, A. H. Patel, H. E. Blum and T. F. Baumert: Viral and Cellular Determinants of Hepatitis C Virus Envelope-Heparan Sulfate Interaction. J Virol, 80, 10579-90(2006) (Pubitemid 44628904)
104. Lee, E., 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, 31-8(2006) (Pubitemid 41790479)
105. Vaillant, A., J. M. Juteau, H. Lu, S. Liu, C. Lackman-Smith, R. Ptak and S. Jiang: Phosphorothioate oligonucleotides inhibit human immunodeficiency virus type 1 fusion by blocking gp41 core formation. Antimicrob Agents Chemother, 50, 1393-401(2006)
106. VanCompernolle, S. E., 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, 371-80(2003) (Pubitemid 37158015)
107. Baranova, I. N., T. G. Vishnyakova, A. V. Bocharov, R. Kurlander, Z. Chen, M. L. Kimelman, A. T. Remaley, G. Csako, F. Thomas, T. L. Eggerman and A. P. Patterson: 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, 8031-40(2005) (Pubitemid 40349701)
108. Cai, L., 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, 2954-61(2005) (Pubitemid 40189405)
109. Lavie, M., C. Voisset, N. Vu-Dac, V. Zurawski, G. Duverlie, C. Wychowski and J. Dubuisson: Serum amyloid A has antiviral activity against hepatitis C virus by inhibiting virus entry in a cell culture system. Hepatology, 44, 1626-34(2006) (Pubitemid 44953668)
110. Poveda, E., V. Briz and V. Soriano: Enfuvirtide, the first fusion inhibitor to treat HIV infection. AIDS Rev, 7, 139-47(2005) (Pubitemid 41671913)