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J. Biol. Chem., Vol. 280, Issue 25, 23698-23708, June 24, 2005

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Dendritic Cell-specific Intercellular Adhesion Molecule 3-grabbing Non-integrin (DC-SIGN)-mediated Enhancement of Dengue Virus Infection Is Independent of DC-SIGN Internalization Signals^*

Pierre-Yves Lozach¶, Laura Burleigh||, Isabelle Staropoli, Erika Navarro-Sanchez**, Julie Harriague||, Jean-Louis Virelizier, Felix A. Rey, Philippe Desprès**, Fernando Arenzana-Seisdedos, and Ali Amara

From the Unité d'Immunologie Virale, ^**Unité Postulante Interactions Moléculaires Flavivirus-Hôtes, Institut Pasteur Paris, 25–28, rue du Dr Roux, 75724 Paris Cedex 15, France and the Unité Mixte de Recherche de Virologie Moléculaire et Structurale, CNRS 2472-INRA 1157, 14B, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette Cedex, France

Dengue virus (DV) is a mosquito-borne flavivirus that causes hemorrhagic fever in humans. In the natural infection, DV is introduced into human skin by an infected mosquito vector where it is believed to target immature dendritic cells (DCs) and Langerhans cells (LCs). We found that DV productively infects DCs but not LCs. We show here that the interactions between DV E protein, the sole mannosylated glycoprotein present on DV particles, and the C-type lectin dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN) are essential for DV infection of DCs. Binding of mannosylated N-glycans on DV E protein to DC-SIGN triggers a rapid and efficient internalization of the viral glycoprotein. However, we observed that endocytosis-defective DC-SIGN molecules allow efficient DV replication, indicating that DC-SIGN endocytosis is dispensable for the internalization step in DV entry. Together, these results argue in favor of a mechanism by which DC-SIGN enhances DV entry and infection in cis. We propose that DC-SIGN concentrates mosquito-derived DV particles at the cell surface to allow efficient interaction with an as yet unidentified entry factor that is ultimately responsible for DV internalization and pH-dependent fusion into DCs.

Received for publication, April 20, 2005

^* This work was supported in part by grants from the "Direction Générale de l'Armement" and "Pediatric Dengue Vaccine Initiative" and by the "Fondation Jacques Monod." 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 Pediatric Dengue Vaccine Initiative fellowship.

^|| Supported by a SIDACTION fellowship.

Supported by a Société Française d'Exportation des Ressources-Consejo Nacional de Ciencia y Tecnología fellowship.

To whom correspondence should be addressed: Unité d'Immunologie Virale, Institut Pasteur, 28 rue du Dr Roux, 75724 Paris Cedex 15, France. Tel.: 33-1-4061-3197; Fax: 33-1-4568-8941; E-mail: aamara{at}pasteur.fr.

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