J. Exp. Med.
© The Rockefeller University Press
0022-1007/97/07/139/08 $2.00
Volume 186, Number 1, July 7, 1997 139-146

HIV Coreceptor Downregulation as Antiviral Principle: SDF-1-dependent Internalization of the Chemokine Receptor CXCR4 Contributes to Inhibition of HIV Replication

By Ali Amara,^* Sylvie Le Gall, Olivier Schwartz, Jean Salamero,^§ Monica Montes, Pius Loetscher,^¶ Marco Baggiolini,^¶ Jean-Louis Virelizier,^* and Fernando Arenzana-Seisdedos^*

From the ^* Unité d'Immunologie Virale and  Laboratoire Rétrovirus et Transfert Génétique, Institut Pasteur, 75724 Paris, Cedex 15, France; ^§ Laboratoire Mécanismes Moléculaires du Transport Intracellulaire, Centre National de la Recherche Scientifique UMR 144, Institut Curie, 75248 Paris Cedex 05, France;  Laboratoire d'Immunologie Cellulaire, Centre National de la Recherche Scientifique URA 625, CERVI, 75013 Paris, France; and ^¶ Theodor Kocher Institute, University of Bern, CH-3000 Bern 9, Switzerland

Ligation of CCR5 by the CC chemokines RANTES, MIP-1 or MIP-1, and of CXCR4 by the CXC chemokine SDF-1, profoundly inhibits the replication of HIV strains that use these coreceptors for entry into CD4⁺ T lymphocytes. The mechanism of entry inhibition is not known. We found a rapid and extensive downregulation of CXCR4 by SDF-1 and of CCR5 by RANTES or the antagonist RANTES(9-68). Confocal laser scanning microscopy showed that CCR5 and CXCR4, after binding to their ligands, are internalized into vesicles that qualify as early endosomes as indicated by colocalization with transferrin receptors. Internalization was not affected by treatment with Bordetella pertussis toxin, showing that it is independent of signaling via G_i-proteins. Removal of SDF-1 led to rapid, but incomplete surface reexpression of CXCR4, a process that was not inhibited by cycloheximide, suggesting that the coreceptor is recycling from the internalization pool. Deletion of the COOH-terminal, cytoplasmic domain of CXCR4 did not affect HIV entry, but prevented SDF-1-induced receptor downregulation and decreased the potency of SDF-1 as inhibitor of HIV replication. Our results indicate that the ability of the coreceptor to internalize is not required for HIV entry, but contributes to the HIV suppressive effect of CXC and CC chemokines.

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• Ebert, L. M., McColl, S. R. (2001). Coregulation of CXC Chemokine Receptor and CD4 Expression on T Lymphocytes During Allogeneic Activation. J. Immunol. 166: 4870-4878 [Abstract] [Full Text]  
• Buri, C., Korner, M., Scharli, P., Cefai, D., Uguccioni, M., Mueller, C., Laissue, J. A., Mazzucchelli, L. (2001). CC chemokines and the receptors CCR3 and CCR5 are differentially expressed in the nonneoplastic leukocytic infiltrates of Hodgkin disease. Blood 97: 1543-1548 [Abstract] [Full Text]  
• Shalekoff, S., Tiemessen, C. T. (2001). Duration of Sample Storage Dramatically Alters Expression of the Human Immunodeficiency Virus Coreceptors CXCR4 and CCR5. CVI 8: 432-436 [Abstract] [Full Text]  
• KENAKIN, T. (2001). Inverse, protean, and ligand-selective agonism: matters of receptor conformation. FASEB J. 15: 598-611 [Abstract] [Full Text]  
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• Breitfeld, D., Ohl, L., Kremmer, E., Ellwart, J., Sallusto, F., Lipp, M., Forster, R. (2000). Follicular B Helper T Cells Express CXC Chemokine Receptor 5, Localize to B Cell Follicles, and Support Immunoglobulin Production. JEM 192: 1545-1552 [Abstract] [Full Text]  
• Cocchi, F., DeVico, A. L., Yarchoan, R., Redfield, R., Cleghorn, F., Blattner, W. A., Garzino-Demo, A., Colombini-Hatch, S., Margolis, D., Gallo, R. C. (2000). Higher macrophage inflammatory protein (MIP)-1alpha and MIP-1beta levels from CD8+ T cells are associated with asymptomatic HIV-1 infection. Proc. Natl. Acad. Sci. USA 10.1073/pnas.240469997v1 [Abstract] [Full Text]  
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• Buckley, C. D., Amft, N., Bradfield, P. F., Pilling, D., Ross, E., Arenzana-Seisdedos, F., Amara, A., Curnow, S. J., Lord, J. M., Scheel-Toellner, D., Salmon, M. (2000). Persistent Induction of the Chemokine Receptor CXCR4 by TGF-{beta}1 on Synovial T Cells Contributes to Their Accumulation Within the Rheumatoid Synovium. J. Immunol. 165: 3423-3429 [Abstract] [Full Text]  
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• Tilton, B., Ho, L., Oberlin, E., Loetscher, P., Baleux, F., Clark-Lewis, I., Thelen, M. (2000). Signal Transduction by CXC Chemokine Receptor 4: Stromal Cell-derived Factor 1 Stimulates Prolonged Protein Kinase B and Extracellular Signal-regulated Kinase 2 Activation in T Lymphocytes. JEM 192: 313-324 [Abstract] [Full Text]  
• Gonzalo, J.-A., Lloyd, C. M., Peled, A., Delaney, T., Coyle, A. J., Gutierrez-Ramos, J.-C. (2000). Critical Involvement of the Chemotactic Axis CXCR4/Stromal Cell-Derived Factor-1{alpha} in the Inflammatory Component of Allergic Airway Disease. J. Immunol. 165: 499-508 [Abstract] [Full Text]  
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• Hasegawa, H., Nomura, T., Kohno, M., Tateishi, N., Suzuki, Y., Maeda, N., Fujisawa, R., Yoshie, O., Fujita, S. (2000). Increased chemokine receptor CCR7/EBI1 expression enhances the infiltration of lymphoid organs by adult T-cell leukemia cells. Blood 95: 30-38 [Abstract] [Full Text]  
• Daniels, G. M., Amara, S. G. (1999). Regulated Trafficking of the Human Dopamine Transporter. CLATHRIN-MEDIATED INTERNALIZATION AND LYSOSOMAL DEGRADATION IN RESPONSE TO PHORBOL ESTERS. J. Biol. Chem. 274: 35794-35801 [Abstract] [Full Text]  
• Burns, J. M., Lewis, G. K., DeVico, A. L. (1999). Soluble complexes of regulated upon activation, normal T cells expressed and secreted (RANTES) and glycosaminoglycans suppress HIV-1 infection but do not induce Ca2+ signaling. Proc. Natl. Acad. Sci. USA 96: 14499-14504 [Abstract] [Full Text]  
• Wang, J., Guan, E., Roderiquez, G., Norcross, M. A. (1999). Inhibition of CCR5 Expression by IL-12 Through Induction of {beta}-Chemokines in Human T Lymphocytes. J. Immunol. 163: 5763-5769 [Abstract] [Full Text]  
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