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Lijun Wu^*, William A. Paxton, Nasim Kassam^*, Nancy Ruffing^*, James B. Rottman^*, Nancy Sullivan, Hyeryun Choe, Joseph Sodroski^,||, Walter Newman^*, Richard A. Koup, and Charles R. Mackay^*

From ^* LeukoSite, Inc., Cambridge, Massachusetts 02142; Aaron Diamond AIDS Research Center, The Rockefeller University, New York 10016; Division of Human Retrovirology, Dana-Faber Cancer Institute, Department of Pathology, Harvard Medical School, Boston, Massachusetts 02115; and ^|| Department of Cancer Biology, Harvard School of Public Health, Boston, Massachusetts 02115

Chemokine receptors serve as coreceptors for HIV entry into CD4⁺ cells. Their expression is thought to determine the tropism of viral strains for different cell types, and also to influence susceptibility to infection and rates of disease progression. Of the chemokine receptors, CCR5 is the most important for viral transmission, since CCR5 is the principal receptor for primary, macrophage-tropic viruses, and individuals homozygous for a defective CCR5 allele (32/ 32) are highly resistant to infection with HIV-1. In this study, CCR5-specific mAbs were generated using transfectants expressing high levels of CCR5. The specificity of these mAbs was confirmed using a broad panel of chemokine receptor transfectants, and by their non-reactivity with T cells from 32/32 individuals. CCR5 showed a distinct pattern of expression, being abundant on long-term activated, IL-2–stimulated T cells, on a subset of effector/memory T cells in blood, and on tissue macrophages. A comparison of normal and CCR5 32 heterozygotes revealed markedly reduced expression of CCR5 on T cells from the heterozygotes. There was considerable individual to individual variability in the expression of CCR5 on blood T cells, that related to factors other than CCR5 genotype. Low expression of CCR5 correlated with the reduced infectability of T cells with macrophage-tropic HIV-1, in vitro. Anti-CCR5 mAbs inhibited the infection of PBMC by macrophage-tropic HIV-1 in vitro, but did not inhibit infection by T cell–tropic virus. Anti-CCR5 mAbs were poor inhibitors of chemokine binding, indicating that HIV-1 and ligands bind to separate, but overlapping regions of CCR5. These results illustrate many of the important biological features of CCR5, and demonstrate the feasibility of blocking macrophage-tropic HIV-1 entry into cells with an anti-CCR5 reagent.

¹ Abbreviations used in this paper: MCP, monocyte chemotactic protein; MIP, macrophage inflammatory protein; MFI, mean fluorescence intensity; 7TMR, seven trans-membrane spanning receptor.

Some of the mAbs described here will be deposited with the National Institutes of Health AIDS Research and Reference Reagent Program (http: //www.niaid.nih.gov/reagent).

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• Thompson, S. D., Luyrink, L. K., Graham, T. B., Tsoras, M., Ryan, M., Passo, M. H., Glass, D. N. (2001). Chemokine Receptor CCR4 on CD4+ T Cells in Juvenile Rheumatoid Arthritis Synovial Fluid Defines a Subset of Cells with Increased IL-4:IFN-{{gamma}} mRNA Ratios. J. Immunol. 166: 6899-6906 [Abstract] [Full Text]  
• Hogan, C. M., Hammer, S. M. (2001). Host Determinants in HIV Infection and Disease: Part 2: Genetic Factors and Implications for Antiretroviral Therapeutics. ANN INTERN MED 134: 978-996 [Abstract] [Full Text]  
• Cotter, R. L., Zheng, J., Che, M., Niemann, D., Liu, Y., He, J., Thomas, E., Gendelman, H. E. (2001). Regulation of Human Immunodeficiency Virus Type 1 Infection, {beta}-Chemokine Production, and CCR5 Expression in CD40L-Stimulated Macrophages: Immune Control of Viral Entry. J. Virol. 75: 4308-4320 [Abstract] [Full Text]  
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• Martín, J., LaBranche, C. C., González-Scarano, F. (2001). Differential CD4/CCR5 Utilization, gp120 Conformation, and Neutralization Sensitivity between Envelopes from a Microglia-Adapted Human Immunodeficiency Virus Type 1 and Its Parental Isolate. J. Virol. 75: 3568-3580 [Abstract] [Full Text]  
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• Bouhlal, H., Galon, J., Kazatchkine, M. D., Fridman, W.-H., Sautes-Fridman, C., Haeffner Cavaillon, N. (2001). Soluble CD16 Inhibits CR3 (CD11b/CD18)-Mediated Infection of Monocytes/Macrophages by Opsonized Primary R5 HIV-1. J. Immunol. 166: 3377-3383 [Abstract] [Full Text]  
• Trkola, A., Ketas, T. J., Nagashima, K. A., Zhao, L., Cilliers, T., Morris, L., Moore, J. P., Maddon, P. J., Olson, W. C. (2001). Potent, Broad-Spectrum Inhibition of Human Immunodeficiency Virus Type 1 by the CCR5 Monoclonal Antibody PRO 140. J. Virol. 75: 579-588 [Abstract] [Full Text]  
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• Moir, S., Malaspina, A., Li, Y., Chun, T.-W., Lowe, T., Adelsberger, J., Baseler, M., Ehler, L. A., Liu, S., Davey, R. T. Jr., Mican, J. A. M., Fauci, A. S. (2000). B Cells of HIV-1-Infected Patients Bind Virions through Cd21-Complement Interactions and Transmit Infectious Virus to Activated T Cells. JEM 192: 637-646 [Abstract] [Full Text]  
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• Pierson, T., Hoffman, T. L., Blankson, J., Finzi, D., Chadwick, K., Margolick, J. B., Buck, C., Siliciano, J. D., Doms, R. W., Siliciano, R. F. (2000). Characterization of Chemokine Receptor Utilization of Viruses in the Latent Reservoir for Human Immunodeficiency Virus Type 1. J. Virol. 74: 7824-7833 [Abstract] [Full Text]  
• Brandes, M., Legler, D. F., Spoerri, B., Schaerli, P., Moser, B. (2000). Activation-dependent modulation of B lymphocyte migration to chemokines. Int Immunol 12: 1285-1292 [Abstract] [Full Text]  
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• Blanpain, C., Lee, B., Tackoen, M., Puffer, B., Boom, A., Libert, F., Sharron, M., Wittamer, V., Vassart, G., Doms, R. W., Parmentier, M. (2000). Multiple nonfunctional alleles of CCR5 are frequent in various human populations. Blood 96: 1638-1645 [Abstract] [Full Text]  
• Proost, P., Menten, P., Struyf, S., Schutyser, E., De Meester, I., Van Damme, J. (2000). Cleavage by CD26/dipeptidyl peptidase IV converts the chemokine LD78beta into a most efficient monocyte attractant and CCR1 agonist. Blood 96: 1674-1680 [Abstract] [Full Text]  
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• Jones, D., O'Hara, C., Kraus, M. D., Perez-Atayde, A. R., Shahsafaei, A., Wu, L., Dorfman, D. M. (2000). Expression pattern of T-cell-associated chemokine receptors and their chemokines correlates with specific subtypes of T-cell non-Hodgkin lymphoma. Blood 96: 685-690 [Abstract] [Full Text]  
• Liao, H.-X., Montefiori, D. C., Patel, D. D., Lee, D. M., Scott, W. K., Pericak-Vance, M., Haynes, B. F. (2000). Linkage of the CCR5{Delta}32 Mutation with a Functional Polymorphism of CD45RA. J. Immunol. 165: 148-157 [Abstract] [Full Text]  
• Hornung, F., Scala, G., Lenardo, M. J. (2000). TNF-{alpha}-Induced Secretion of C-C Chemokines Modulates C-C Chemokine Receptor 5 Expression on Peripheral Blood Lymphocytes. J. Immunol. 164: 6180-6187 [Abstract] [Full Text]  
• Giltay, E. J., Fonk, J. C. M., von Blomberg, B. M. E., Drexhage, H. A., Schalkwijk, C., Gooren, L. J. G. (2000). In Vivo Effects of Sex Steroids on Lymphocyte Responsiveness and Immunoglobulin Levels in Humans. J. Clin. Endocrinol. Metab. 85: 1648-1657 [Abstract] [Full Text]  
• Lopalco, L., Barassi, C., Pastori, C., Longhi, R., Burastero, S. E., Tambussi, G., Mazzotta, F., Lazzarin, A., Clerici, M., Siccardi, A. G. (2000). CCR5-Reactive Antibodies in Seronegative Partners of HIV-Seropositive Individuals Down-Modulate Surface CCR5 In Vivo and Neutralize the Infectivity of R5 Strains of HIV-1 In Vitro. J. Immunol. 164: 3426-3433 [Abstract] [Full Text]  
• Franchin, G., Zybarth, G., Dai, W. W., Dubrovsky, L., Reiling, N., Schmidtmayerova, H., Bukrinsky, M., Sherry, B. (2000). Lipopolysaccharide Inhibits HIV-1 Infection of Monocyte- Derived Macrophages Through Direct and Sustained Down-Regulation of CC Chemokine Receptor 5. J. Immunol. 164: 2592-2601 [Abstract] [Full Text]  
• Zhang, G X, Baker, C M, Kolson, D L, Rostami, A M (2000). Chemokines and chemokine receptors in the pathogenesis of multiple sclerosis. Mult Scler 6: 3-13 [Abstract]  
• Steinberger, P., Andris-Widhopf, J., Buhler, B., Torbett, B. E., Barbas, C. F. III (2000). Functional deletion of the CCR5 receptor by intracellular immunization produces cells that are refractory to CCR5-dependent HIV-1 infection and cell fusion. Proc. Natl. Acad. Sci. USA 97: 805-810 [Abstract] [Full Text]  

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