J. Exp. Med., Volume 187, Number 8, April 20, 1998 1215-1224

Aminooxypentane-RANTES Induces CCR5 Internalization but Inhibits Recycling: A Novel Inhibitory Mechanism of HIV Infectivity

By Matthias Mack,^* Bruno Luckow,^* Peter J. Nelson,^* Josef Cihak, Graham Simmons,^§ Paul R. Clapham,^§ Nathalie Signoret, Mark Marsh, Manfred Stangassinger, Fréderic Borlat,^¶ Timothy N.C. Wells,^¶ Detlef Schlöndorff,^* and Amanda E.I. Proudfoot^¶

From the ^* Medizinische Poliklinik, Ludwig-Maximilians-University of Munich, 80336 Munich, Germany; the  Institute for Animal Physiology, University of Munich, 80539 Munich, Germany; the ^§ Section of Virology, Chester Beatty Laboratories, Institute of Cancer Research, London SW3 6JB, United Kingdom; the  Medical Research Council Laboratory for Molecular Cell Biology, University College London, London WC1E 6BT, United Kingdom; and the ^¶ Geneva Biomedical Research Institute, Glaxo Wellcome Research and Development SA, 1228 Plan-les-Ouates, Geneva, Switzerland

CCR5, a chemokine receptor expressed on T cells and macrophages, is the principal coreceptor for M-tropic HIV-1 strains. Recently, we described an NH₂-terminal modification of the CCR5 ligand regulated on activation, normal T cell expressed and secreted (RANTES), aminooxypentane-RANTES (AOP-RANTES), that showed potent inhibition of macrophage infection by HIV-1 under conditions where RANTES was barely effective. To investigate the mechanism of AOP-RANTES inhibition of HIV infectivity we examined the surface expression of CCR5 using a monoclonal anti-CCR5 antibody, MC-1. We demonstrate that AOP-RANTES rapidly caused >90% decrease in cell surface expression of CCR5 on lymphocytes, monocytes/ macrophages, and CCR5 transfected Chinese hamster ovary (CHO) cells. RANTES also caused a loss of cell surface CCR5, although its effect was less than with AOP-RANTES. Significantly, AOP-RANTES inhibited recycling of internalized CCR5 to the cell surface, whereas RANTES did not. When peripheral blood mononuclear cells are cultured for prolonged periods of time in the presence of RANTES, CCR5 expression is comparable to that seen on cells treated with control medium, whereas there is no CCR5 surface expression on cells cultured in the presence of AOP-RANTES. Immunofluorescence indicated that both AOP-RANTES and RANTES induced downmodulation of cell surface CCR5, and that the receptor was redistributed into endocytic organelles containing the transferrin receptor. When RANTES was removed, the internalized receptor was recycled to the cell surface; however, the receptor internalized in the presence of AOP-RANTES was retained in endosomes. Using human osteosarcoma (GHOST) 34/CCR5 cells, the potency of AOP-RANTES and RANTES to inhibit infection by the M-tropic HIV-1 strain, SF 162, correlated with the degree of downregulation of CCR5 induced by the two chemokines. These differences between AOP-RANTES and RANTES in their effect on receptor downregulation and recycling suggest a mechanism for the potent inhibition of HIV infection by AOP-RANTES. Moreover, these results support the notion that receptor internalization and inhibition of receptor recycling present new targets for therapeutic agents to prevent HIV infection.

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• Blanpain, C., Migeotte, I., Lee, B., Vakili, J., Doranz, B. J., Govaerts, C., Vassart, G., Doms, R. W., Parmentier, M. (1999). CCR5 Binds Multiple CC-Chemokines: MCP-3 Acts as a Natural Antagonist. Blood 94: 1899-1905 [Abstract] [Full Text]  
• Klasse, P. J., Rosenkilde, M. M., Signoret, N., Pelchen-Matthews, A., Schwartz, T. W., Marsh, M. (1999). CD4-Chemokine Receptor Hybrids in Human Immunodeficiency Virus Type 1 Infection. J. Virol. 73: 7453-7466 [Abstract] [Full Text]  
• Trkola, A., Gordon, C., Matthews, J., Maxwell, E., Ketas, T., Czaplewski, L., Proudfoot, A. E. I., Moore, J. P. (1999). The CC-Chemokine RANTES Increases the Attachment of Human Immunodeficiency Virus Type 1 to Target Cells via Glycosaminoglycans and Also Activates a Signal Transduction Pathway That Enhances Viral Infectivity. J. Virol. 73: 6370-6379 [Abstract] [Full Text]  
• Nibbs, R. J. B., Yang, J., Landau, N. R., Mao, J.-H., Graham, G. J. (1999). LD78beta , A Non-allelic Variant of Human MIP-1alpha (LD78alpha ), Has Enhanced Receptor Interactions and Potent HIV Suppressive Activity. J. Biol. Chem. 274: 17478-17483 [Abstract] [Full Text]  
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• Mörner, A., Björndal, A., Albert, J., KewalRamani, V. N., Littman, D. R., Inoue, R., Thorstensson, R., Fenyö, E. M., Björling, E. (1999). Primary Human Immunodeficiency Virus Type 2 (HIV-2) Isolates, Like HIV-1 Isolates, Frequently Use CCR5 but Show Promiscuity in Coreceptor Usage. J. Virol. 73: 2343-2349 [Abstract] [Full Text]  
• Rodriguez-Frade, J. M., Vila-Coro, A. J., Martin, A., Nieto, M., Sanchez-Madrid, F., Proudfoot, A. E.I., Wells, T. N.C., Martinez-A, C., Mellado, M. (1999). Similarities and Differences in RANTES- and (AOP)-RANTES-triggered Signals: Implications for Chemotaxis. J. Cell Biol. 144: 755-765 [Abstract] [Full Text]  
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• Loetscher, P., Pellegrino, A., Gong, J.-H., Mattioli, I., Loetscher, M., Bardi, G., Baggiolini, M., Clark-Lewis, I. (2001). The Ligands of CXC Chemokine Receptor 3, I-TAC, Mig, and IP10, Are Natural Antagonists for CCR3. J. Biol. Chem. 276: 2986-2991 [Abstract] [Full Text]  
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• Proudfoot, A. E. I., Fritchley, S., Borlat, F., Shaw, J. P., Vilbois, F., Zwahlen, C., Trkola, A., Marchant, D., Clapham, P. R., Wells, T. N. C. (2001). The BBXB Motif of RANTES Is the Principal Site for Heparin Binding and Controls Receptor Selectivity. J. Biol. Chem. 276: 10620-10626 [Abstract] [Full Text]  
• Blanpain, C., Wittamer, V., Vanderwinden, J.-M., Boom, A., Renneboog, B., Lee, B., Le Poul, E., El Asmar, L., Govaerts, C., Vassart, G., Doms, R. W., Parmentier, M. (2001). Palmitoylation of CCR5 Is Critical for Receptor Trafficking and Efficient Activation of Intracellular Signaling Pathways. J. Biol. Chem. 276: 23795-23804 [Abstract] [Full Text]  
• Vila-Coro, A. J., Mellado, M., Martin de Ana, A., Lucas, P., del Real, G., Martinez-A., C., Rodriguez-Frade, J. M. (2000). HIV-1 infection through the CCR5 receptor is blocked by receptor dimerization. Proc. Natl. Acad. Sci. USA 97: 3388-3393 [Abstract] [Full Text]  
• Blanpain, C., Vanderwinden, J.-M., Cihak, J., Wittamer, V., Le Poul, E., Issafras, H., Stangassinger, M., Vassart, G., Marullo, S., Schlondorff, D., Parmentier, M., Mack, M. (2002). Multiple Active States and Oligomerization of CCR5 Revealed by Functional Properties of Monoclonal Antibodies. Mol. Biol. Cell 13: 723-737 [Abstract] [Full Text]  

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