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J. Biol. Chem., Vol. 278, Issue 42, 41003-41012, October 17, 2003
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Cellular Binding of Hepatitis C Virus Envelope Glycoprotein E2 Requires Cell Surface Heparan Sulfate*
From the
Department of Medicine II, University of Freiburg, D-79106 Freiburg, Germany, the ¶Departments of Chemistry, Medicinal and Natural Products Chemistry, and Chemical and Biochemical Engineering, University of Iowa, Iowa City, Iowa 52242, the ||Department of Analytical Chemistry, Chiba University, Chiba 263-8522, Japan, the **Department of Biochemistry, NCMLS, University Medical Center, 6500HB Nijmegen, The Netherlands, and Innogenetics N. V., B-9052 Ghent, Belgium
The conservation of positively charged residues in the N terminus of the hepatitis C virus (HCV) envelope glycoprotein E2 suggests an interaction of the viral envelope with cell surface glycosaminoglycans. Using recombinant envelope glycoprotein E2 and virus-like particles as ligands for cellular binding, we demonstrate that cell surface heparan sulfate proteoglycans (HSPG) play an important role in mediating HCV envelope-target cell interaction. Heparin and liver-derived highly sulfated heparan sulfate but not other soluble glycosaminoglycans inhibited cellular binding and entry of virus-like particles in a dose-dependent manner. Degradation of cell surface heparan sulfate by pretreatment with heparinases resulted in a marked reduction of viral envelope protein binding. Surface plasmon resonance analysis demonstrated a high affinity interaction (KD 5.2 x 10–9 M) of E2 with heparin, a structural homologue of highly sulfated heparan sulfate. Deletion of E2 hypervariable region-1 reduced E2-heparin interaction suggesting that positively charged residues in the N-terminal E2 region play an important role in mediating E2-HSPG binding. In conclusion, our results demonstrate for the first time that cellular binding of HCV envelope requires E2-HSPG interaction. Docking of E2 to cellular HSPG may be the initial step in the interaction between HCV and the cell surface resulting in receptor-mediated entry and initiation of infection.
Received for publication, March 5, 2003 , and in revised form, July 15, 2003.
* This work was supported in part by grants from the European Union, Brussels, Belgium QLK2-CT-1999-00356 and QLK2-CT-2002-01329), the Wilhelm Sander-Stiftung, Munich, Germany (99041.1), and the Deutsche Forschungsgemeinschaft (Ba1417/9-1). 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.
Supported by a Georg Forster fellowship of the Alexander von Humboldt-Foundation, Bonn, Germany.
To whom correspondence should be addressed: Dept. of Medicine II, University of Freiburg, Hugstetter Strasse 55, D-79106 Freiburg, Germany. Tel.: 49-761-270-3401; Fax: 49-761-270-3259; E-mail: tbaumert{at}ukl.uni-freiburg.de.
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