Hepatitis C virus entry into host cells

Cellular and Molecular Life Sciences

Volumn 65, Issue 1, 2008, Pages 100-112

  Helle, F ^a   Dubuisson, J ^a  

^a INSTITUT DE BIOLOGIE DE LILLE   (France)

Author keywords

Entry factor; Envelope glycoprotein; Hepatitis C virus; Viral fusion; Viral receptor; Virus attachment; Virus entry

Indexed keywords

CD81 ANTIGEN; CLATHRIN; CLAUDIN 1; GLYCAN; GLYCOPROTEIN E1; GLYCOPROTEIN E2; GLYCOSAMINOGLYCAN; LOW DENSITY LIPOPROTEIN RECEPTOR; SCAVENGER RECEPTOR B; TETRASPANIN; VIRUS ENVELOPE PROTEIN; VIRUS FUSION PROTEIN; VIRUS GLYCOPROTEIN;

CELL ADHESION; ENDOCYTOSIS; ENDOSOME; GLYCOSYLATION; HEPATITIS C VIRUS; HOST CELL; HUMAN; LIFE CYCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; REVIEW; TIGHT JUNCTION; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS PARTICLE;

ANTIGENS, CD; HEPACIVIRUS; HUMANS; MEMBRANE PROTEINS; RECEPTORS, VIRUS; SCAVENGER RECEPTORS, CLASS B; VIRUS INTERNALIZATION;

HEPATITIS C VIRUS;

EID: 38549086984     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-7291-8     Document Type: Review

References (138)

1. Lemon, S. M., Walker, C., Alter, M. J. and Yi, M. (2007) Hepatitis C virus. In: Fields Virology, pp. 1253-1304 (Knipe, D. M. and Howley, P. M., Eds.). Lippincott Williams & Wilkins, Philadelphia.
2. Deleersnyder, V., Pillez, A., Wychowski, C., Blight, K., Xu, J., Hahn, Y. S., Rice, C. M. and Dubuisson, J. (1997) Formation of native hepatitis C virus glycoprotein complexes. J. Virol. 71, 697-704.
3. Op De Beeck, A., Voisset, C., Bartosch, B., Ciczora, Y., Cocquerel, L., Keck, Z., Foung, S., Cosset, F. L. and Dubuisson, J. (2004) Characterization of functional hepatitis C virus envelope glycoproteins. J. Virol. 78, 2994-3002.
4. Bartosch, B. and Cosset, F. L. (2006) Cell entry of hepatitis C virus. Virology 348, 1-12.
5. Barth, H., Liang, T. J. and Baumert, T. F. (2006) Hepatitis C virus entry: molecular biology and clinical implications. Hepatology 44, 527-535.
6. Cocquerel, L., Voisset, C. and Dubuisson, J. (2006) Hepatitis C virus entry: potential receptors and their biological functions. J. Gen. Virol. 87, 1075-1084.
7. Bartosch, B., Dubuisson, J. and Cosset, F. L. (2003) Infectious hepatitis C pseudo-particles containing functional E1E2 envelope protein complexes. J. Exp. Med. 197, 633-642.
8. Drummer, H. E., Maerz, A. and Poumbourios, P. (2003) Cell surface expression of functional hepatitis C virus E1 and E2 glycoproteins. FEBS Lett. 546, 385-390.
9. Hsu, M., Zhang, J., Flint, M., Logvinoff, C., Cheng-Mayer, C., Rice, C. M. and McKeating, J. A. (2003) Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. USA 100, 7271-7276.
10. Ott, D. E. (1997) Cellular proteins in HIV virions. Rev. Med. Virol. 7, 167-180.
11. Sandrin, V., Boson, B., Salmon, P., Gay, W., Nègre, D., Le, Grand R., Trono, D. and Cosset, F.-L. (2002) Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and non-human primates. Blood 100, 823-832.
12. Negre, D., Duisit, G., Mangeot, P. E., Moullier, P., Darlix, J. L. and Cosset, F. L. (2002) Lentiviral vectors derived from simian immunodeficiency virus. Curr. Top. Microbiol. Immunol. 261, 53-74.
13. Sandrin, V., Boulanger, P., Penin, F., Granier, C., Cosset, F. L. and Bartosch, B. (2005) Assembly of functional hepatitis C virus glycoproteins on infectious pseudoparticles occurs intracellularly and requires concomitant incorporation of E1 and E2 glycoproteins. J. Gen. Virol. 86, 3189-3199.
14. Bartosch, B., Bukh, J., Meunier, J. C., Granier, C., Engle, R. E., Blackwelder, W. C., Emerson, S. U., Cosset, F. L. and Purcell, R. H. (2003) In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc. Natl. Acad. Sci. USA 100, 14199-14204.
15. Wakita, T., Pietschmann, T., Kato, T., Date, T., Miyamoto, M., Zhao, Z., Murthy, K., Habermann, A., Krausslich, H. G., Mizokami, M., Bartenschlager, R. and Liang, T. J. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11, 791-796.
16. Lindenbach, B. D., Evans, M. J., Syder, A. J., Wolk, B., Tellinghuisen, T. L., Liu, C. C., Maruyama, T., Hynes, R. O., Burton, D. R., McKeating, J. A. and Rice, C. M. (2005) Complete replication of hepatitis C virus in cell culture. Science 309, 623-626.
17. Zhong, J., Gastaminza, P., Cheng, G., Kapadia, S., Kato, T., Burton, D. R., Wieland S. F., Uprichard, S. L., Wakita, T. and Chisari, F. V. (2005) Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. USA 102, 9294-9299.
18. Yi, M., Villanueva, R. A., Thomas, D. L., Wakita, T. and Lemon, S. M. (2006) Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc. Natl. Acad. Sci. USA 103, 2310-2315.
19. Kato, T., Matsumura, T., Heller, T., Saito, S., Sapp, R. K., Murthy, K., Wakita, T. and Liang, T. J. (2007) Production of infectious hepatitis C virus of various genotypes in cell cultures. J. Virol. 81, 4405-4411.
20. Pietschmann, T., Kaul, A., Koutsoudakis, G., Shavinskaya, A., Kallis, S., Steinmann, E., Abid, K., Negro, F., Dreux, M., Cosset, F. L. and Bartenschlager, R. (2006) Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. USA 103, 7408-7413.
21. Yi, M., Ma, Y., Yates, J. and Lemon, S. M. (2007) Compensatory mutations in, E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J. Virol. 81, 629-638.
22. Koutsoudakis, G., Kaul, A., Steinmann, E., Kallis, S., Lohmann, V., Pietschmann, T. and Bartenschlager, R. (2006) Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J. Virol. 80, 5308-5320.
23. Tscherne, D. M., Jones C. T., Evans, M. J., Lindenbach, B. D., McKeating, J. A. and Rice, C. M. (2006) Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J. Virol. 80, 1734-1741.
24. Santolini, E., Migliaccio, G. and La Monica, N. (1994) Biosynthesis and biochemical properties of the hepatitis C virus core protein. J. Virol. 68, 3631-3641.
25. Cocquerel, L., Op De Beeck, A., Lambot, M., Roussel, J., Delgrange, D., Pillez, A., Wychowski, C., Penin, F. and Dubuisson, J. (2002) Topologic changes in the transmembrane domains of hepatitis C virus envelope glycoproteins. EMBO J. 21, 2893-2902.
26. Cocquerel, L., Meunier, J.-C., Pillez, A., Wychowski, C. and Dubuisson, J. (1998) A retention signal necessary and sufficient for endoplasmic reticulum localization maps to the transmembrane domain of hepatitis C virus glycoprotein E2. J. Virol. 72, 2183-2191.
27. Cocquerel, L., Duvet, S., Meunier, J. C., Pillez, A., Cacan, R., Wychowski, C. and Dubuisson, J. (1999) The transmembrane domain of hepatitis C virus glycoprotein E1 is a signal for static retention in the endoplasmic reticulum. J. Virol. 73, 2641-2649.
28. Flint, M. and McKeating, J. A. (1999) The C-terminal region of the hepatitis C virus E1 glycoprotein confers localization within the endoplasmic reticulum. J. Gen. Virol. 80, 1943-1947.
29. Cocquerel, L., Wychowski, C., Minner, F., Penin, F. and Dubuisson, J. (2000) Charged residues in the transmembrane domains of hepatitis C virus glycoproteins play a key role in the processing, subcellular localization and assembly of these envelope proteins. J. Virol. 74, 3623-3633.
30. Ciczora, Y., Callens, N., Penin, F., Pecheur, E. I. and Dubuisson, J. (2007) The transmembrane domains of HCV envelope glycoproteins: residues involved in E1E2 heterodimerization and involvement of these domains in virus entry. J. Virol. 81, 2372-2381.
31. Bowen, D. G. and Walker, C. M. (2005) Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 436, 946-952.
32. Gremion, C. and Cerny, A. (2005) Hepatitis C virus and the immune system: a concise review. Rev. Med. Virol. 15, 235-268.
33. Kanto, T. and Hayashi, N. (2006) Immunopathogenesis of hepatitis C virus infection: multifaceted strategies subverting innate and adaptive immunity. Intern. Med. 45, 183-191.
34. Thimme, R., Lohmann, V. and Weber, F. (2006) A target on the move: innate and adaptive immune escape strategies of hepatitis C virus. Antiviral Res. 69, 129-141.
35. von Hahn, T., Yoon, J. C., Alter, H., Rice, C. M., Rehermann, B., Balfe, P. and McKeating, J. A. (2007) Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 132, 667-678.
36. Forns, X., Thimme, R., Govindarajan, S., Emerson, S. U., Purcell, R. H., Chisari, F. V. and Bukh, J. (2000) Hepatitis C virus lacking the hypervariable region 1 of the second envelope protein is infectious and causes acute resolving or persistent infection in chimpanzees. Proc. Natl. Acad. Sci. USA 97, 13318-13323.
37. Penin, F., Combet, C., Germanidis, G., Frainais, P. O., Deléage, G. and Pawlotsky, J. M. (2001) Conservation of the conformation and positive charges of hepatitis C virus E2 envelope glycoprotein hypervariable region 1 points to a role in cell attachment. J. Virol. 75, 5703-5710.
38. Callens, N., Ciczora, Y., Bartosch, B., Vu-Dac, N., Cosset, F. L., Pawlotsky, J. M., Penin, F. and Dubuisson, J. (2005) Basic residues in hypervariable region 1 of hepatitis C virus envelope glycoprotein e2 contribute to virus entry. J. Virol. 79, 15331-15341.
39. Weiner, A. J., Brauer, R., Rosenblatt, J., Richman, K. H., Tung, J., Crarford, K., Bonino, F., Saracco, G., Choo, Q.-L., Houghton, M. and Han, J. H. (1991) 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, 842-848.
40. Roccasecca, R., Ansuini, H., Vitelli, A., Meola, A., Scarselli, E., Acali, S., Pezzanera, M., Ercole, B. B., McKeating, J., Yagnik, A., Lahm, A., Tramontano, A., Cortese, R. and Nicosia, A. (2003) Binding of the hepatitis C virus E2 glycoprotein to CD81 is strain specific and is modulated by a complex interplay between hypervariable regions 1 and 2. J. Virol. 77, 1856-1867.
41. Troesch, M., Meunier, I., Lapierre, P., Lapointe, N., Alvarez, F., Boucher, M. and Soudeyns, H. (2006) Study of a novel hypervariable region in hepatitis C virus (HCV) E2 envelope glycoprotein. Virology 352, 357-367.
42. Goffard, A. and Dubuisson, J. (2003) Glycosylation of hepatitis C virus envelope proteins. Biochimie 85, 295-301.
43. Zhang, M., Gaschen, B., Blay, W., Foley, B., Haigwood, N., Kuiken, C. and Korber, B. (2004) Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14, 1229-1246.
44. Helle, F., Goffard, A., Morel, V., Duverlie, G., McKeating, J., Keck, Z. Y., Foung, S., Penin, F., Dubuisson, J. and Voisset, C. (2007) The neutralizing activity of anti-hepatitis C virus antibodies is modulated by specific glycans on the e2 envelope protein. J. Virol. 81, 8101-8111.
45. Goffard, A., Callens, N., Bartosch, B., Wychowski, C., Cosset, F. L., Montpellier-Pala, C. and Dubuisson, J. (2005) Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins. J. Virol. 79, 8400-8409.
46. Falkowska, E., Kajumo, F., Garcia, E., Reinus, J. and Dragic, T. (2007) Hepatitis C virus envelope glycoprotein E2 glycans modulate entry CD81 binding and neutralization. J. Virol. 81, 8072-8079.
47. Chen, Y., Maguire, T., Hileman, R. E., Fromm, J. R., Esko, J. D., Linhardt, R. J. and Marks, R. M. (1997) Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3, 866-871.
48. Germi, R., Crance, J. M., Garin, D., Guimet, J., Lortat-Jacob, H., Ruigrok, R. W., Zarski, J. P. and Drouet, E. (2002) Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology 292, 162-168.
49. Hilgard, P. and Stockert, R. (2000) Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology 32, 1069-1077.
50. Mandl, C. W., Kroschewski, H., Allison, S. L., Kofler, R., Holzmann, H., Meixner, T. and Heinz, F. X. (2001) Adaptation of tick-borne encephalitis virus to BHK-21 cells results in the formation of multiple heparan sulfate binding sites in the envelope protein and attenuation in vivo. J. Virol. 75, 5627-5637.
51. Germi, R., Crance, J. M., Garin, D., Guimet, J., Lortat-Jacob, H., Ruigrok, R. W., Zarski, J. P. and Drouet, E. (2002) Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J. Med. Virol. 68, 206-215.
52. Barth, H., Schafer, C., Adah, M. I., Zhang, F., Linhardt, R. J., Toyoda, H., Kinoshita-Toyoda, A., Toida, T., Van Kuppevelt, T. H., Depla, E., Von Weizsacker, F., Blum, H. E. and Baumert, T. F. (2003) Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem. 278, 41003-41012.
53. Basu, A., Beyene, A., Meyer, K. and Ray, R. (2004) 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, 4478-4486.
54. Barth, H., Schnober, E. K., Zhang, F., Linhardt, R. J., Depla, E., Boson, B., Cosset, F. L., Patel, A. H., Blum, H. E. and Baumert, T. F. (2006) Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. J. Virol. 80, 10579-10590.
55. Basu, A., Kanda, T., Beyene, A., Saito, K., Meyer, K. and Ray, R. (2007) Sulfated homologues of heparin inhibit hepatitis C virus entry into mammalian cells. J. Virol. 81, 3933-3941.
56. Morikawa, K., Zhao, Z., Date, T., Miyamoto, M., Murayama, A., Akazawa, D., Tanabe, J., Sone, S. and Wakita, T. (2007) The roles of CD81 and glycosaminoglycans in the adsorption and uptake of infectious HCV particles. J. Med. Virol. 79, 714-723.
57. Olenina, L. V., Kuzmina, T. I., Sobolev, B. N., Kuraeva, T. E., Kolesanova, E. F. and Archakov, A. I. (2005) Identification of glycosaminoglycan-binding sites within hepatitis C virus envelope glycoprotein E2. J. Viral Hepat. 12, 584-593.
58. Andreo, U., Maillard, P., Kalinina, O., Walic, M., Meurs, E., Martinot, M., Marcellin, P. and Budkowska, A. (2007) Lipoprotein lipase mediates hepatitis C virus (HCV) cell entry and inhibits HCV infection. Cell. Microbiol. 9, 2445-2456.
59. Thomssen, R., Bonk, S., Propfe, C., Heermann, K. H., Kochel, H. G. and Uy, A. (1992) Association of hepatitis C virus in human sera with beta-lipoprotein. Med. Microbiol. Immunol. 181, 293-300.
60. André, P., Komurian-Pradel, F., Deforges, S., Perret, M., Berland J. L., Sodoyer, M., Pol, S., Brechot, C., Paranhos-Baccala, G. and Lotteau, V. (2002) Characterization of low-and very-low-density hepatitis C virus RNA-containing particles. J. Virol. 76, 6919-6928.
61. Nielsen, S. U., Bassendine, M. F., Burt, A. D., Martin, C., Pumeechockchai, W. and Toms, G. L. (2006) Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients. J. Virol. 80, 2418-2428.
62. Diaz, O., Delers, F., Maynard, M., Demignot, S., Zoulim, F., Chambaz, J., Trepo, C., Lotteau, V. and Andre, P. (2006) Preferential association of hepatitis C virus with apolipoprotein B48-containing lipoproteins. J. Gen. Virol. 87, 2983-2991.
63. Huang, H., Sun, F., Owen, D. M., Li, W., Chen, Y., Gale, M., Jr. and Ye, J. (2007) Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins. Proc. Natl. Acad. Sci. USA 104, 5848-5853.
64. Monazahian, M., Bohme, I., Bonk, S., Koch, A., Scholz, C., Grethe, S. and Thomssen, R. (1999) Low density lipoprotein receptor as a candidate receptor for hepatitis C virus. J. Med. Virol. 57, 223-229.
65. Agnello, V., Abel, G., Elfahal, M., Knight, G. B. and Zhang, Q.-X. (1999) Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc. Natl. Acad. Sci. USA 96, 12766-12771.
66. Wunschmann, S., Medh, J. D., Klinzmann, D., Schmidt, W. N. and Stapleton, J. T. (2000) Characterization of hepatitis C virus (HCV) and HCV E2 interactions with CD81 and the low-density lipoprotein receptor. J. Virol. 74, 10055-10062.
67. Molina, S., Castet, V., Fournier-Wirth, C., Pichard-Garcia, L., Avner, R., Harats, D., Roitelman, J., Barbaras, R., Graber, P., Ghersa, P., Smolarsky, M., Funaro, A., Malavasi, F., Larrey, D., Coste, J., Fabre, J. M., Sa-Cunha, A. and Maurel, P. (2007) The low-density lipoprotein receptor plays a role in the infection of primary human hepatocytes by hepatitis C virus. J. Hepatol. 46, 411-419.
68. Pileri, P., Uematsu, Y., Campagnoli, S., Galli, G., Falugi, F., Petracca, R., Weiner, A. J., Houghton, M., Rosa, D., Grandi, G. and Abrignani, S. (1998) Binding of hepatitis C virus to CD81. Science 282, 938-941.
69. Levy, S. and Shoham, T. (2005) The tetraspanin web modulates immune-signalling complexes. Nat. Rev. Immunol. 5, 136-148.
70. Seigneuret, M. (2006) Complete predicted three-dimensional structure of the facilitator transmembrane protein and hepatitis C virus receptor CD81: conserved and variable structural domains in the tetraspanin superfamily. Biophys. J. 90, 212-227.
71. Cormier, E. G., Tsamis, F., Kajumo, F., Durso, R. J., Gardner, J. P. and Dragic, T. (2004) CD81 is an entry coreceptor for hepatitis C virus. Proc. Natl. Acad. Sci. USA 101, 7270-7274.
72. Zhang, J., Randall, G., Higginbottom, A., Monk, P., Rice, C. M. and McKeating, J. A. (2004) CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J. Virol. 78, 1448-1455.
73. Lavillette, D., Tarr, A. W., Voisset, C., Donot, P., Bartosch, B., Bain, C., Patel, A. H., Dubuisson, J., Ball, J. K. and Cosset, F. L. (2005) Characterization of host-range and cell entry properties of hepatitis C virus of major genotypes and subtypes. Hepatology 41, 265-274.
74. Kapadia, S. B., Barth, H., Baumert, T., McKeating, J. A. and Chisari, F. V. (2007) Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I. J. Virol. 81, 374-383.
75. Akazawa, D., Date, T., Morikawa, K., Murayama, A., Miyamoto, M., Kaga, M., Barth, H., Baumert, T. F., Dubuisson, J. and Wakita, T. (2007) CD81 expression is important for the permissiveness of huh7 cell clones for heterogeneous hepatitis C virus infection. J. Virol. 81, 5036-5045.
76. Bartosch, B., Vitelli, A., Granier, C., Goujon, C., Dubuisson, J., Pascale, S., Scarselli, E., Cortese, R., Nicosia, A. and Cosset, F. L. (2003) 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, 41624-41630.
77. Koutsoudakis, G., Herrmann, E., Kallis, S., Bartenschlager, R. and Pietschmann, T. (2007) The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. J. Virol. 81, 588-598.
78. Higginbottom, A., Quinn, E. R., Kuo, C. C., Flint, M., Wilson, L. H., Bianchi, E., Nicosia, A., Monk, P. N., McKeating, J. A. and Levy, S. (2000) Identification of amino acid residues in CD81 critical for interaction with hepatitis C virus envelope glycoprotein E2. J. Virol. 74, 3642-3649.
79. Drummer, H. E., Wilson, K. A. and Poumbourios, P. (2002) Identification of the hepatitis C virus E2 glycoprotein binding site on the large extracellular loop of CD81. J. Virol. 76, 11143-11147.
80. Bertaux, C. and Dragic, T. (2006) Different domains of CD81 mediate distinct stages of hepatitis C virus pseudoparticle entry. J. Virol. 80, 4940-4948.
81. Drummer, H. E., Boo, I., Maerz, A. L. and Poumbourios, P. (2006) A conserved Gly436-Trp-Leu-Ala-Gly-Leu-Phe-Tyr motif in hepatitis C virus glycoprotein E2 is a determinant of CD81 binding and viral entry. J. Virol. 80, 7844-7853.
82. Owsianka, A. M., Timms, J. M., Tarr, A. W., Brown, R. J., Hickling, T. P., Szwejk, A., Bienkowska-Szewczyk, K., Thomson, B. J., Patel, A. H. and Ball, J. K. (2006) Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding. J. Virol. 80, 8695-8704.
83. Cocquerel, L., Kuo, C.-C., Dubuisson, J. and Levy, S. (2003) CD81-dependent binding of hepatitis C virus E1E2 heterodimers. J. Virol. 77, 10677-10683.
84. Evans, M. J., von Hahn, T., Tscherne, D. M., Syder, A. J., Panis, M., Wolk, B., Hatziioannou, T., McKeating, J. A., Bieniasz, P. D. and Rice, C. M. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446, 801-805.
85. Boucheix, C. and Rubinstein, E. (2001) Tetraspanins. Cell. Mol. Life Sci. 58, 1189-1205.
86. Charrin, S., Le, Naour, F., Labas, V., Billard, M., LeCaer, J. P., Emile, J. F., Petit, M. A., Boucheix, C. and Rubinstein, E. (2003) EWI-2 is a new component of the tetraspanin web in hepatocytes and lymphoid cells. Biochem. J. 373, 409-421.
87. Stipp, C. S., Orlicky, D. and Hemler, M. E. (2001) FPRP, a major, highly stoichiometric, highly specific CD81- and CD9-associated protein. J. Biol. Chem. 276, 4853-4862.
88. Scarselli, E., Ansuini, H., Cerino, R., Roccasecca, R. M., Acali, S., Filocamo, G., Traboni, C., Nicosia, A., Cortese, R. and Vitelli, A. (2002) The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 21, 5017-5025.
89. Calvo, D. and Vega, M. A. (1993) Identification, primary structure, and distribution of CLA-1, a novel member of the CD36/LIMPII gene family. J. Biol. Chem. 268, 18929-18935.
90. Acton, S. L., Scherer, P. E., Lodish, H. F. and Krieger, M. (1994) Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J. Biol. Chem. 269, 21003-21009.
91. Rhainds, D. and Brissette, L. (2004) The role of scavenger receptor class B type I (SR-BI) in lipid trafficking. defining the rules for lipid traders. Int. J. Biochem. Cell. Biol. 36, 39-77.
92. Barth, H., Cerino, R., Arcuri, M., Hoffmann, M., Schurmann, P., Adah, M. I., Gissler, B., Zhao, X., Ghisetti, V., Lavezzo, B., Blum, H. E., von Weizsacker, F., Vitelli, A., Scarselli, E. and Baumert, T. F. (2005) Scavenger receptor class B type I and hepatitis C virus infection of primary tupaia hepatocytes. J. Virol. 79, 5774-5785.
93. Lavillette, D., Morice, Y., Germanidis, G., Donot, P., Soulier, A., Pagkalos, E., Sakellariou, G., Intrator, L., Bartosch, B., Pawlotsky, J. M. and Cosset, F. L. (2005) Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral rplication kinetics at the acute phase of hepatitis C virus infection. J. Virol. 79, 6023-6034.
94. Voisset, C., Callens, N., Blanchard, E., Op De Beeck, A., Dubuisson, J. and Vu-Dac, N. (2005) High density lipoproteins facilitate hepatitis C virus entry through the scavenger receptor class B type I. J. Biol. Chem. 280, 7793-7799.
95. Grove, J., Huby, T., Stamataki, Z., Vanwolleghem, T., Meuleman, P., Farquhar, M., Schwarz, A., Moreau, M., Owen, J. S., Leroux-Roels, G., Balfe, P. and McKeating, J. A. (2007) Scavenger receptor BI and BII expression levels modulate hepatitis C virus infectivity. J. Virol. 81, 3162-3169.
96. Catanese, M. T., Graziani, R., von Hahn, T., Moreau, M., Huby, T., Paonessa, G., Santini, C., Luzzago, A., Rice, C. M., Cortese, R., Vitelli, A. and Nicosia, A. (2007) High-avidity monoclonal atibodies 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, 8063-8071.
97. Zeisel, M. B., Koutsoudakis, G., Schnober, E. K., Haberstroh, A., Blum, E., Cosset, F. L., Wakita, T., Jaeck, D., Doffoel, M., Royer, C., Joulier, E., Schvoerer, E., Schuster, C., Stoll-Keller, F., Bartenschlager, R., Pietschmann, T., Barth, H. and Baumert, T. F. (in press) Scavenger receptor BI is a key host factor for hepatitis C virus infection required for an entry step closely linked to CD81. Hepatology.
98. Acton, S., Rigotti, A., Landschulz, K. T., Xu, S., Hobbs, H. H. and Krieger, M. (1996) Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271, 518-520.
99. Landschulz, K. T., Pathak, R. K., Rigotti, A., Krieger, M. and Hobbs, H. H. (1996) Regulation of scavenger receptor, class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of the rat. J. Clin. Invest. 98, 984-995.
100. Cao, G., Garcia, C. K., Wyne, K. L., Schultz, R. A., Parker, K. L. and Hobbs, H. H. (1997) Structure and localization of the human gene encoding SR-BI/CLA-1: evidence for transcriptional control by steroidogenic factor 1. J. Biol. Chem. 272, 33068-33076.
101. Yamada, E., Montoya, M., Schuettler, C. G., Hickling, T. P., Tarr, A. W., Vitelli, A., Dubuisson, J., Patel, A. H., Ball, J. K. and Borrow, P. (2005) Analysis of the binding of hepatitis C virus genotype 1a and 1b E2 glycoproteins to peripheral blood mononuclear cell subsets. J. Gen. Virol. 86, 2507-2512.
102. von Hahn, T., Lindenbach, B. D., Boullier, A., Quehenberger, O., Paulson, M., Rice, C. M. and McKeating, J. A. (2006) Oxidized low-density lipoprotein inhibits hepatitis C virus cell entry in human hepatoma cells. Hepatology 43, 932-942.
103. Dreux, M., Pietschmann, T., Granier, C., Voisset, C., Ricard-Blum, S., Mangeot, P. E., Keck, Z., Foung, S., Vu-Dac, N., Dubuisson, J., Bartenschlager, R., Lavillette, D. and Cosset, F. L. (2006) High density lipoprotein inhibits hepatitis C virus neutralizing antibodies by stimulating cell entry via activation of the scavenger receptor BI. J. Biol. Chem. 281, 18285-18295.
104. Bartosch, B., Verney, G., Dreux, M., Donot, P., Morice, Y., Penin, F., Pawlotsky, J. M., Lavillette, D. and Cosset, F. L. (2005) An interplay between the hyper-variable region 1 of the HCV E2 glycoprotein, the scavenger receptor BI and HDLpromotes both enhancement of infection and protection against neutralizing antibodies. J. Virol. 79, 8217-8229.
105. Meunier, J. C., Engle, R. E., Faulk, K., Zhao, M., Bartosch, B., Alter, H., Emerson, S. U., Cosset, F. L., Purcell, R. H. and Bukh, J. (2005) Evidence for cross-genotype neutralization of hepatitis C virus pseudo-particles and enhancement of infectivity by apolipoprotein C1. Proc. Natl. Acad. Sci. USA 102, 4560-4565.
106. Baranova, I. N., Vishnyakova, T. G., Bocharov, A. V., Kurlander, R., Chen, Z., Kimelman, M. L., Remaley, A. T., Csako, G., Thomas, F., Eggerman, T. L. and Patterson, A. P. (2005) 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, 8031-8040.
107. Cai, L., de Beer, M. C., de Beer, F. C. and van der Westhuyzen, D. R. (2005) 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, 2954-2961.
108. Uhlar, C. M. and Whitehead, A. S. (1999) Serum amyloid A the major vertebrate acute-phase reactant. Eur. J. Biochem. 265, 501-523.
109. Lavie, M., Voisset, C., Vu-Dac, N., Zurawski, V., Duverlie, G., Wychowski, C. and Dubuisson, J. (2006) Serum amyloid A has antiviral activity against hepatitis C virus by inhibiting virus entry in a cell culture system. Hepatology 44, 1626-1634.
110. Cai, Z., Cai, L., Jiang, J., Chang, K. S., van der Westhuyzen, D. R. and Luo, G. (2007) Human serum amyloid A protein inhibits hepatitis C virus entry into cells. J. Virol. 81, 6128-6133.
111. Maillard, P., Huby, T., Andreo, U., Moreau, M., Chapman, J. and Budkowska, A. (2006)The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/Cla1 is mediated by ApoB-containing lipoproteins. FASEB J. 20, 735-737.
112. Rigotti, A., Edelman, E. R., Seifert, P., Iqbal, S. N., DeMattos, R. B., Temel, R. E., Krieger, M. and Williams, D. L. (1996) Regulation by adrenocorticotropic hormone of the in vivo expression of scavenger receptor class B type I (SR-BI), a high density lipoprotein receptor in steroidogenic cells of the murine adrenal gland. J. Biol. Chem. 271, 33545-33549.
113. Reaven, E., Nomoto, A., Leers-Sucheta, S., Temel, R., Williams, D. L. and Azhar, S. (1998) Expression and microvillar localization of scavenger receptor, class B, type I (a high density lipoprotein receptor) in luteinized and hormone-desensitized rat ovarian models. Endocrinology 139, 2847-2856.
114. Kellner-Weibel, G., de La Llera-Moya, M., Connelly, M. A., Stoudt, G., Christian, A. E., Haynes, M. P., Williams, D. L. and Rothblat, G. H. (2000) Expression of scavenger receptor BI in COS-7 cells alters cholesterol content and distribution. Biochemistry 39, 221-229.
115. Reaven, E., Zhan, L., Nomoto, A., Leers-Sucheta, S. and Azhar, S. (2000) Expression and microvillar localization of scavenger receptor class B, type I (SR-BI) and selective cholesteryl ester uptake in Leydig cells from rat testis. J. Lipid Res. 41, 343-356.
116. Reaven, E., Leers-Sucheta, S., Nomoto, A. and Azhar, S. (2001) Expression of scavenger receptor class B type 1 (SRBI) promotes microvillar channel formation and selective cholesteryl ester transport in a heterologous reconstituted system. Proc. Natl. Acad. Sci. USA 98, 1613-1618.
117. Williams, D. L., Wong, J. S. and Hamilton, R. L. (2002) SR-BI is required for microvillar channel formation and the localization of HDL particles to the surface of adrenocortical cells in vivo. J. Lipid Res. 43, 544-549.
118. Huang, Z. H., Gu, D., Lange, Y. and Mazzone, T. (2003) Expression of scavenger receptor BI facilitates sterol movement between the plasma membrane and the endoplasmic reticulum in macrophages. Biochemistry 42, 3949-3955.
119. Peng, Y., Akmentin, W., Connelly, M. A., Lund-Katz, S., Phillips, M. C. and Williams, D. L. (2004) Scavenger receptor BI (SR-BI) clustered on microvillar extensions suggests that this plasmamembrane domain is a way station for cholesterol trafficking between cells and high-density lipoprotein. Mol. Biol. Cell 15, 384-396.
120. Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K. and Tsukita, S. (1998) Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141, 1539-1550.
121. Van, Itallie, C. M. and Anderson, J. M. (2006) Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 68, 403-429.
122. Meertens, L., Bertaux, C. and Dragic, T. (2006) Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. J. Virol. 80, 11571-11578.
123. Blanchard, E., Belouzard, S., Goueslain, L., Wakita, T., Dubuisson, J., Wychowski, C. and Rouille, Y. (2006) Hepatitis C virus entry depends on clathrin-mediated endocytosis. J. Virol. 80, 6964-6972.
124. Kielian, M. and Rey, F. A. (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4, 67-76.
125. Lavillette, D., Bartosch, B., Nourrisson, D., Verney, G., Cosset, F. L., Penin, F. and Pecheur, E. I. (2006) Hepatitis C virus glycoproteins mediate low pH-dependent membrane fusion with liposomes. J. Biol. Chem. 281, 3909-3917.
126. Penin, F., Dubuisson, J., Rey, F. A., Moradpour, D. and Pawlotsky, J. M. (2004) Structural biology of hepatitis C virus. Hepatology 39, 5-19.
127. Yagnik, A. T., Lahm, A., Meola, A., Roccasecca, R. M., Ercole, B. B., Nicosia, A. and Tramontano, A. (2000) A model for the hepatitis C virus envelope glycoprotein E2. Proteins 40, 355-366.
128. Flint, M., Thomas, J. M., Maidens C. M., Shotton, C., Levy, S., Barclay, W. S. and McKeating, J. A. (1999) Functional analysis of cell surface-expressed hepatitis C virus E2 glycoprotein. J. Virol. 73, 6782-6790.
129. Drummer, H. E., Boo, I. and Poumbourios, P. (2007) Mutagenesis of a conserved fusion peptide-like motif and membrane-proximal heptad-repeat region of hepatitis C virus glycoprotein E1. J. Gen. Virol. 88, 1144-1148.
130. Garry, R. F. and Dash, S. (2003) Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. Virology 307, 255-265.
131. Michalak, J.-P., Wychowski, C., Choukhi, A., Meunier, J.-C., Ung, S., Rice, C. M. and Dubuisson, J. (1997) Characterization of truncated forms of hepatitis C virus glycoproteins. J. Gen. Virol. 78, 2299-2306.
132. Brazzoli, M., Helenius, A., Foung, S. K., Houghton, M., Abrignani, S. and Merola, M. (2005) Folding and dimerization of hepatitis C virus E1 and E2 glycoproteins in stably transfected CHO cells. Virology 332, 438-453.
133. Perez-Berna, A. J., Moreno, M. R., Guillen, J., Bernabeu, A. and Villalain, J. (2006) The membrane-active regions of the hepatitis C virus E1 and E2 envelope glycoproteins. Biochemistry 45, 3755-3768.
134. Lavillette, D., Pecheur, E. I., Donot, P., Fresquet, J., Molle, J., Corbau, R., Dreux, M., Penin, F. and Cosset, F. L. (2007) 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, 8752-8765.
135. Bertaux, C., Daelemans, D., Meertens, L., Cormier, E. G., Reinus, J. F., Peumans, W. J., Van, Damme, E. J., Igarashi, Y., Oki, T., Schols, D., Dragic, T. and Balzarini, J. (2007) Entry of hepatitis C virus and human immunodeficiency virus is selectively inhibited by carbohydrate-binding agents but not by polyanions. Virology 366, 40-50.
136. Boriskin, Y. S., Pecheur, E. I. and Polyak, S. J. (2006) Arbidol: a broad-spectrum antiviral that inhibits acute and chronic HCV infection. Virol. J. 3, 56-64.
137. Helle, F., Wychowski, C., Vu-Dac, N., Gustafson, K. R., Voisset, C. and Dubuisson, J. (2006) Cyanovirin-N inhibits hepatitis C virus entry by binding to envelope protein glycans. J. Biol. Chem. 281, 25177-25183.
138. Pecheur, E. I., Lavillette, D., Alcaras, F., Molle, J., Boriskin, Y. S., Roberts, M., Cosset, F. L. and Polyak, S. J. (2007) Biochemical mechanism of hepatitis C virus inhibition by the broad-spectrum antiviral arbidol. Biochemistry 46, 6050-6059.