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Originally published In Press as doi:10.1074/jbc.M305289200 on August 11, 2003

J. Biol. Chem., Vol. 278, Issue 43, 41624-41630, October 24, 2003
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Cell Entry of Hepatitis C Virus Requires a Set of Co-receptors That Include the CD81 Tetraspanin and the SR-B1 Scavenger Receptor*

Birke Bartosch{ddagger}§, Alessandra Vitelli§||, Christelle Granier{ddagger}, Caroline Goujon{ddagger}, Jean Dubuisson**, Simona Pascale||, Elisa Scarselli||, Riccardo Cortese||, Alfredo Nicosia§||, and François-Loïc Cosset{ddagger}§{ddagger}{ddagger}

From the {ddagger}Laboratoire de Vectorologie Rétrovirale et Thérapie Génique, INSERM U412, Institut Fédératif de Recherche 128, Ecole Normale Supérieure de Lyon, 46 allée d'Italie, 69364 Lyon Cedex 07, France, the ||Instituto di Recerche di Biologia Molecolare P. Angeletti, 00040 Pomezia, Roma, Italy, and the **CNRS-UPR2511, Institut de Biologie de Lille, Institut Pasteur de Lille, 1 rue Calmette, B. P. 447, 59021 Lille Cedex, France

Several cell surface molecules have been proposed as receptor candidates, mediating cell entry of hepatitis C virus (HCV) on the basis of their physical association with virions or with soluble HCV E2 glycoproteins. However, due to the lack of infectious HCV particles, evidence that these receptor candidates support infection was missing. Using our recently described infectious HCV pseudotype particles (HCVpp) that display functional E1E2 glycoprotein complexes, here we show that HCV is a pH-dependent virus, implying that its receptor component(s) mediate virion internalization by endocytosis. Expression of the CD81 tetraspanin in non-permissive CD81-negative hepato-carcinoma cells was sufficient to restore susceptibility to HCVpp infection, confirming its critical role as a cell attachment factor. As a cell surface molecule likely to mediate endosomal trafficking, we demonstrate that the human scavenger receptor class B type 1 (SR-B1), a high-density lipoprotein-internalization molecule that we previously proposed as a novel HCV receptor candidate due to its affinity with E2 glycoproteins, is required for infection of CD81-expressing hepatic cells. By receptor competition assays, we found that SR-B1 antibodies that blocked binding of soluble E2 could prevent HCVpp infectivity. Furthermore, we establish that the hyper-variable region 1 of the HCV E2 glycoprotein is a critical determinant mediating entry in SR-B1-positive cells. Finally, by correlating expression of HCV receptors and infectivity, we suggest that, besides CD81 and SR-B1, additional hepatocyte-specific co-factor(s) are necessary for HCV entry.

Received for publication, May 20, 2003 , and in revised form, July 8, 2003.

* This work was supported by Agence Nationale pour la Recherche contre le SIDA (ANRS), the European Community (contracts QLK3 1999-00859 and QLRT-2000-01120), the Association pour la Recherche contre le Cancer (ARC), the Centre National de la Recherche Scientifique (CNRS), the Réseau National Hépatite C, and the Institut National de la Santé Et de la Recherche Médicale (INSERM, Action Thé-matique Concertée, Hépatite C). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ These authors have contributed equally to this study.

Supported by a Marie Curie Fellowship from the European Community.

{ddagger}{ddagger} To whom correspondence should be addressed: Laboratoire de Vectorologie Rétrovirale et Thérapie Génique, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon Cedex 07, France. Tel.: 33-472-72-87-32; Fax: 33-472-72-80-80; E-mail: flcosset{at}ens-lyon.fr.


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Intracellular Versus Cell Surface Assembly of Retroviral Pseudotypes Is Determined by the Cellular Localization of the Viral Glycoprotein, Its Capacity to Interact with Gag, and the Expression of the Nef Protein
J. Biol. Chem., January 6, 2006; 281(1): 528 - 542.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
N. Callens, 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., December 15, 2005; 79(24): 15331 - 15341.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
S. Griffin, D. Clarke, C. McCormick, D. Rowlands, and M. Harris
Signal Peptide Cleavage and Internal Targeting Signals Direct the Hepatitis C Virus p7 Protein to Distinct Intracellular Membranes
J. Virol., December 15, 2005; 79(24): 15525 - 15536.
[Abstract] [Full Text] [PDF]

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 J. Gen. Virol.Home page
V. Sandrin, P. Boulanger, F. Penin, C. Granier, F.-L. Cosset, and B. Bartosch
Assembly of functional hepatitis C virus glycoproteins on infectious pseudoparticles occurs intracellularly and requires concomitant incorporation of E1 and E2 glycoproteins
J. Gen. Virol., December 1, 2005; 86(12): 3189 - 3199.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
Z.-Y. Keck, T.-K. Li, J. Xia, B. Bartosch, F.-L. Cosset, J. Dubuisson, and S. K. H. Foung
Analysis of a Highly Flexible Conformational Immunogenic Domain A in Hepatitis C Virus E2
J. Virol., November 1, 2005; 79(21): 13199 - 13208.
[Abstract] [Full Text] [PDF]

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 J. Gen. Virol.Home page
E. Yamada, 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., September 1, 2005; 86(9): 2507 - 2512.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
F. Martin, D. M. Roth, D. A. Jans, C. W. Pouton, L. J. Partridge, P. N. Monk, and G. W. Moseley
Tetraspanins in Viral Infections: a Fundamental Role in Viral Biology?
J. Virol., September 1, 2005; 79(17): 10839 - 10851.
[Full Text] [PDF]

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 J. Virol.Home page
A. Owsianka, 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., September 1, 2005; 79(17): 11095 - 11104.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
S. Lecot, S. Belouzard, J. Dubuisson, and Y. Rouille
Bovine Viral Diarrhea Virus Entry Is Dependent on Clathrin-Mediated Endocytosis
J. Virol., August 15, 2005; 79(16): 10826 - 10829.
[Abstract] [Full Text] [PDF]

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 ScienceHome page
B. D. Lindenbach, 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, et al.
Complete Replication of Hepatitis C Virus in Cell Culture
Science, July 22, 2005; 309(5734): 623 - 626.
[Abstract] [Full Text] [PDF]

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 J. Gen. Virol.Home page
R. J. P. Brown, V. S. Juttla, A. W. Tarr, R. Finnis, W. L. Irving, S. Hemsley, D. R. Flower, P. Borrow, and J. K. Ball
Evolutionary dynamics of hepatitis C virus envelope genes during chronic infection
J. Gen. Virol., July 1, 2005; 86(7): 1931 - 1942.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
B. Bartosch, 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., July 1, 2005; 79(13): 8217 - 8229.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
H. Barth, R. Cerino, M. Arcuri, M. Hoffmann, P. Schurmann, M. I. Adah, B. Gissler, X. Zhao, V. Ghisetti, B. Lavezzo, et al.
Scavenger Receptor Class B Type I and Hepatitis C Virus Infection of Primary Tupaia Hepatocytes
J. Virol., May 1, 2005; 79(9): 5774 - 5785.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
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., March 4, 2005; 280(9): 7793 - 7799.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
K. K. Stein, P. Primakoff, and D. Myles
Sperm-egg fusion: events at the plasma membrane
J. Cell Sci., December 15, 2004; 117(26): 6269 - 6274.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
E. G. Cormier, 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
PNAS, September 28, 2004; 101(39): 14067 - 14072.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
Z.-Y. Keck, A. Op De Beeck, K. G. Hadlock, J. Xia, T.-K. Li, J. Dubuisson, and S. K. H. Foung
Hepatitis C Virus E2 Has Three Immunogenic Domains Containing Conformational Epitopes with Distinct Properties and Biological Functions
J. Virol., September 1, 2004; 78(17): 9224 - 9232.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
J. A. McKeating, L. Q. Zhang, C. Logvinoff, M. Flint, J. Zhang, J. Yu, D. Butera, D. D. Ho, L. B. Dustin, C. M. Rice, et al.
Diverse Hepatitis C Virus Glycoproteins Mediate Viral Infection in a CD81-Dependent Manner
J. Virol., August 15, 2004; 78(16): 8496 - 8505.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P.-Y. Lozach, 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., July 30, 2004; 279(31): 32035 - 32045.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. E. Drummer and P. Poumbourios
Hepatitis C Virus Glycoprotein E2 Contains a Membrane-proximal Heptad Repeat Sequence That Is Essential for E1E2 Glycoprotein Heterodimerization and Viral Entry
J. Biol. Chem., July 16, 2004; 279(29): 30066 - 30072.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
T.-H. Heo, J.-H. Chang, J.-W. Lee, S. K. H. Foung, J. Dubuisson, and C.-Y. Kang
Incomplete Humoral Immunity against Hepatitis C Virus Is Linked with Distinct Recognition of Putative Multiple Receptors by E2 Envelope Glycoprotein
J. Immunol., July 1, 2004; 173(1): 446 - 455.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
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
PNAS, May 11, 2004; 101(19): 7270 - 7274.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
A. Op De Beeck, C. Voisset, B. Bartosch, Y. Ciczora, L. Cocquerel, Z. Keck, S. Foung, F.-L. Cosset, and J. Dubuisson
Characterization of Functional Hepatitis C Virus Envelope Glycoproteins
J. Virol., March 15, 2004; 78(6): 2994 - 3002.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
B. Bartosch, 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
PNAS, November 25, 2003; 100(24): 14199 - 14204.
[Abstract] [Full Text] [PDF]


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