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J. Biol. Chem., Vol. 281, Issue 27, 18285-18295, July 7, 2006
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High Density Lipoprotein Inhibits Hepatitis C Virus-neutralizing Antibodies by Stimulating Cell Entry via Activation of the Scavenger Receptor BI*
¶1¶¶¶6
From the
INSERM, U758, 69007 Lyon, France, Ecole Normale Supérieure de Lyon, 69007 Lyon, France, ¶IFR128 BioSciences Lyon-Gerland, 69007 Lyon, France, the ||Department of Molecular Virology, University of Heidelberg, D-69120 Heidelberg, Germany, **CNRS-UPR2511, Institut Pasteur de Lille, 59021 Lille, France, IBCP, UMR5086 CNRS-UCB Lyon-I, 69007 Lyon, France, Epixis SA, 69007 Lyon, France, and the ¶¶Department of Pathology, Stanford University School of Medicine, Stanford, California 94305
Hepatitis C virus (HCV) exploits serum-dependent mechanisms that inhibit neutralizing antibodies. Here we demonstrate that high density lipoprotein (HDL) is a key serum factor that attenuates neutralization by monoclonal and HCV patient-derived polyclonal antibodies of infectious pseudo-particles (HCVpp) harboring authentic E1E2 glycoproteins and cell culture-grown genuine HCV (HCVcc). Over 10-fold higher antibody concentrations are required to neutralize either HCV-enveloped particles in the presence of HDL or human serum, and less than 3–5-fold reduction of infectious titers are obtained at saturating antibody concentrations, in contrast to complete inhibition in serum-free conditions. We show that HDL interaction with the scavenger receptor BI (SR-BI), a proposed cell entry co-factor of HCV and a receptor mediating lipid transfer with HDL, strongly reduces neutralization of HCVpp and HCVcc. We found that HDL activation of target cells strongly stimulates cell entry of viral particles by accelerating their endocytosis, thereby suppressing a 1-h time lag during which cell-bound virions are not internalized and can be targeted by antibodies. Compounds that inhibit lipid transfer functions of SR-BI fully restore neutralization by antibodies in human serum. We demonstrate that this functional HDL/SR-BI interaction only interferes with antibodies blocking HCV-E2 binding to CD81, a major HCV receptor, reflecting its prominent role during the cell entry process. Moreover, we identify monoclonal antibodies targeted to epitopes in the E1E2 complex that are not inhibited by HDL. Consistently, we show that antibodies targeted to HCV-E1 efficiently neutralize HCVpp and HCVcc in the presence of human serum.
Received for publication, March 22, 2006 , and in revised form, May 3, 2006.
* This work was supported in part by La Ligue Nationale Contre le Cancer, "Agence Nationale pour la Recherche sur le SIDA et les Hépatites Virales," and the European Community Grant LSHB-CT-2004-005246 "COMPUVAC." 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.
1 Supported by a fellowship from the Région Rhône-Alpes.
2 Supported by an Agence Nationale Pour la Recherche sur le SIDA et les Hépatites Virales post-doc fellowship.
3 Supported by National Institutes of Health Grants AI47355 and HL079381.
4 An international scholar of the Howard Hughes Medical Institute.
5 Supported by the VIRGIL European Network of Excellence on Antiviral Drug Resistance Grant LSHM-CT-2004-503359 and the Bristol-Myers Squibb foundation.
6 To whom correspondence should be addressed: ENS de Lyon, 46 Allée d'Italie, 69007 Lyon, France. Tel.: 33472728732; Fax: 33472728080, E-mail: flcosset{at}neuf.fr.
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