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Originally published In Press as doi:10.1074/jbc.M210115200 on December 16, 2002

J. Biol. Chem., Vol. 278, Issue 10, 8725-8732, March 7, 2003
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HIV-1 Nef Stabilizes the Association of Adaptor Protein Complexes with Membranes*

Katy JanvierDagger §, Heather Craig§, Douglas Hitchin, Ricardo MadridDagger , Nathalie Sol-Foulon||, Louis Renault**, Jacqueline Cherfils**, Dan CasselDagger Dagger , Serge BenichouDagger §§, and John Guatelli¶¶||||

From the Dagger  Institut Cochin, Department of Infectious Diseases, INSERM U567-CNRS UMR8104, Universite Paris V, 24 Rue du Faubourg Saint-Jacques, 75014 Paris, France, the  San Diego Veterans Affairs Healthcare System, San Diego, California 92121, the || Institut Pasteur, 25 rue du Dr Roux, 75015 Paris, France, the ** Laboratoire d'Enzymologie et Biochimie Structurales, CNRS, 91198 Gif/Yvette, France, the Dagger Dagger  Institute Curie, UMR 144, 26 rue d'Ulm, 75248 Paris Cedex 05, France, and the ¶¶ Department of Medicine, University of California, La Jolla, California 92093-0679

The maximal virulence of HIV-1 requires Nef, a virally encoded peripheral membrane protein. Nef binds to the adaptor protein (AP) complexes of coated vesicles, inducing an expansion of the endosomal compartment and altering the surface expression of cellular proteins including CD4 and class I major histocompatibility complex. Here, we show that Nef stabilizes the association of AP-1 and AP-3 with membranes. These complexes remained with Nef on juxtanuclear membranes despite the treatment of cells with brefeldin A, which induced the release of ADP-ribosylation factor 1 (ARF1) from these membranes to the cytosol. Nef also induced a persistent association of AP-1 and AP-3 with membranes despite the expression of dominant-negative ARF1 or the overexpression of an ARF1-GTPase activating protein. Mutational analysis indicated that the direct binding of Nef to the AP complexes is essential for this stabilization. The leucine residues of the EXXXLL motif found in Nef were required for binding to AP-1 and AP-3 in vitro and for the stabilization of these complexes on membranes in vivo, whereas the glutamic acid residue of this motif was required specifically for the binding and stabilization of AP-3. These data indicate that Nef mediates the persistent attachment of AP-1 and AP-3 to membranes by an ARF1-independent mechanism. The stabilization of these complexes on membranes may underlie the pleiotropic effects of Nef on protein trafficking within the endosomal system.

* This work was supported by grants from Agence Nationale de Recherche sur le SIDA and SIDACTION, Association pour la Recherche contre le Cancer subvention number 4244, National Institutes of Health Grant AI38201, Universitywide AIDS Research Program of the University of California Grant RD98-SD-051, University of California, San Diego, Center for AIDS Research National Institutes of Health Grant AI36214, the Research Center of AIDS and HIV Infection of the San Diego Veterans Affairs Medical Center, and National Center for Microscopy and Imaging Resource at the University of California, San Diego, National Institutes of Health Grant RR04050.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Contributed equally to the results of this work.

§§ Co-senior author. To whom correspondence may be addressed: INSERM U567, CNRS UMR8104, Universite Paris V, 27 Rue du Faubourg Saint-Jacques, 75014 Paris, France. Tel.: 33-1-40-51-65-78; Fax: 33-1-40-51-65-70; E-mail: benichou@cochin.inserm.fr.

|||| Co-senior author. To whom correspondence may be addressed: University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0679. Tel.: 858-552-7439; Fax: 858-552-7445; E-mail: jguatelli@ucsd.edu.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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