J. Exp. Med.
© The Rockefeller University Press
0022-1007/97/02/621/08 $2.00
Volume 185, Number 4, February 17, 1997 621-628

Change in Coreceptor Use Correlates with Disease Progression in HIV-1-Infected Individuals

By Ruth I. Connor, Kristine E. Sheridan, Daniel Ceradini, Sunny Choe, and Nathaniel R. Landau

From the Aaron Diamond AIDS Research Center and The Rockefeller University, New York, 10016

Recent studies have identified several coreceptors that are required for fusion and entry of Human Immunodeficiency Virus type 1 (HIV-1) into CD4⁺ cells. One of these receptors, CCR5, serves as a coreceptor for nonsyncytium inducing (NSI), macrophage-tropic strains of HIV-1, while another, fusin or CXCR-4, functions as a coreceptor for T cell line-adapted, syncytiuminducing (SI) strains. Using sequential primary isolates of HIV-1, we examined whether viruses using these coreceptors emerge in vivo and whether changes in coreceptor use are associated with disease progression. We found that isolates of HIV-1 from early in the course of infection predominantly used CCR5 for infection. However, in patients with disease progression, the virus expanded its coreceptor use to include CCR5, CCR3, CCR2b, and CXCR-4. Use of CXCR-4 as a coreceptor was only seen with primary viruses having an SI phenotype and was restricted by the env gene of the virus. The emergence of variants using this coreceptor was associated with a switch from NSI to SI phenotype, loss of sensitivity to chemokines, and decreasing CD4⁺ T cell counts. These results suggest that HIV-1 evolves during the course of infection to use an expanded range of coreceptors for infection, and that this adaptation is associated with progression to AIDS.

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• Audige, A., Schlaepfer, E., Bonanomi, A., Joller, H., Knuchel, M. C., Weber, M., Nadal, D., Speck, R. F. (2004). HIV-1 Does Not Provoke Alteration of Cytokine Gene Expression in Lymphoid Tissue after Acute Infection Ex Vivo. J. Immunol. 172: 2687-2696 [Abstract] [Full Text]  
• Jacobson, J. M., Israel, R. J., Lowy, I., Ostrow, N. A., Vassilatos, L. S., Barish, M., Tran, D. N. H., Sullivan, B. M., Ketas, T. J., O'Neill, T. J., Nagashima, K. A., Huang, W., Petropoulos, C. J., Moore, J. P., Maddon, P. J., Olson, W. C. (2004). Treatment of Advanced Human Immunodeficiency Virus Type 1 Disease with the Viral Entry Inhibitor PRO 542. Antimicrob. Agents Chemother. 48: 423-429 [Abstract] [Full Text]  
• Igarashi, T., Donau, O. K., Imamichi, H., Dumaurier, M.-J., Sadjadpour, R., Plishka, R. J., Buckler-White, A., Buckler, C., Suffredini, A. F., Lane, H. C., Moore, J. P., Martin, M. A. (2003). Macrophage-Tropic Simian/Human Immunodeficiency Virus Chimeras Use CXCR4, Not CCR5, for Infections of Rhesus Macaque Peripheral Blood Mononuclear Cells and Alveolar Macrophages. J. Virol. 77: 13042-13052 [Abstract] [Full Text]  
• Trkola, A., Kuster, H., Leemann, C., Ruprecht, C., Joos, B., Telenti, A., Hirschel, B., Weber, R., Bonhoeffer, S., Gunthard, H. F. (2003). Human Immunodeficiency Virus Type 1 Fitness Is a Determining Factor in Viral Rebound and Set Point in Chronic Infection. J. Virol. 77: 13146-13155 [Abstract] [Full Text]  
• Vogel, T. U., Reynolds, M. R., Fuller, D. H., Vielhuber, K., Shipley, T., Fuller, J. T., Kunstman, K. J., Sutter, G., Marthas, M. L., Erfle, V., Wolinsky, S. M., Wang, C., Allison, D. B., Rud, E. W., Wilson, N., Montefiori, D., Altman, J. D., Watkins, D. I. (2003). Multispecific Vaccine-Induced Mucosal Cytotoxic T Lymphocytes Reduce Acute-Phase Viral Replication but Fail in Long-Term Control of Simian Immunodeficiency Virus SIVmac239. J. Virol. 77: 13348-13360 [Abstract] [Full Text]  
• Jensen, M. A., Li, F.-S., van 't Wout, A. B., Nickle, D. C., Shriner, D., He, H.-X., McLaughlin, S., Shankarappa, R., Margolick, J. B., Mullins, J. I. (2003). Improved Coreceptor Usage Prediction and Genotypic Monitoring of R5-to-X4 Transition by Motif Analysis of Human Immunodeficiency Virus Type 1 env V3 Loop Sequences. J. Virol. 77: 13376-13388 [Abstract] [Full Text]  
• Yi, Y., Singh, A., Shaheen, F., Louden, A., Lee, C., Collman, R. G. (2003). Contrasting Use of CCR5 Structural Determinants by R5 and R5X4 Variants within a Human Immunodeficiency Virus Type 1 Primary Isolate Quasispecies. J. Virol. 77: 12057-12066 [Abstract] [Full Text]  
• Campbell, T. B., Schneider, K., Wrin, T., Petropoulos, C. J., Connick, E. (2003). Relationship between In Vitro Human Immunodeficiency Virus Type 1 Replication Rate and Virus Load in Plasma. J. Virol. 77: 12105-12112 [Abstract] [Full Text]  
• Kunstman, K. J., Puffer, B., Korber, B. T., Kuiken, C., Smith, U. R., Kunstman, J., Stanton, J., Agy, M., Shibata, R., Yoder, A. D., Pillai, S., Doms, R. W., Marx, P., Wolinsky, S. M. (2003). Structure and Function of CC-Chemokine Receptor 5 Homologues Derived from Representative Primate Species and Subspecies of the Taxonomic Suborders Prosimii and Anthropoidea. J. Virol. 77: 12310-12318 [Abstract] [Full Text]  
• Goodenow, M. M., Rose, S. L., Tuttle, D. L., Sleasman, J. W. (2003). HIV-1 fitness and macrophages. J. Leukoc. Biol. 74: 657-666 [Abstract] [Full Text]  
• Chang, T. L.-Y., Chang, C.-H., Simpson, D. A., Xu, Q., Martin, P. K., Lagenaur, L. A., Schoolnik, G. K., Ho, D. D., Hillier, S. L., Holodniy, M., Lewicki, J. A., Lee, P. P. (2003). Inhibition of HIV infectivity by a natural human isolate of Lactobacillus jensenii engineered to express functional two-domain CD4. Proc. Natl. Acad. Sci. USA 100: 11672-11677 [Abstract] [Full Text]  
• Harouse, J. M., Buckner, C., Gettie, A., Fuller, R., Bohm, R., Blanchard, J., Cheng-Mayer, C. (2003). CD8+ T cell-mediated CXC chemokine receptor 4-simian/human immunodeficiency virus suppression in dually infected rhesus macaques. Proc. Natl. Acad. Sci. USA 100: 10977-10982 [Abstract] [Full Text]  
• Roscic-Mrkic, B., Fischer, M., Leemann, C., Manrique, A., Gordon, C. J., Moore, J. P., Proudfoot, A. E. I., Trkola, A. (2003). RANTES (CCL5) uses the proteoglycan CD44 as an auxiliary receptor to mediate cellular activation signals and HIV-1 enhancement. Blood 102: 1169-1177 [Abstract] [Full Text]  
• Chang, T. L.-Y., Francois, F., Mosoian, A., Klotman, M. E. (2003). CAF-Mediated Human Immunodeficiency Virus (HIV) Type 1 Transcriptional Inhibition Is Distinct from {alpha}-Defensin-1 HIV Inhibition. J. Virol. 77: 6777-6784 [Abstract] [Full Text]  
• Willey, S. J., Reeves, J. D., Hudson, R., Miyake, K., Dejucq, N., Schols, D., Clercq, E. D., Bell, J., McKnight, A., Clapham, P. R. (2003). Identification of a Subset of Human Immunodeficiency Virus Type 1 (HIV-1), HIV-2, and Simian Immunodeficiency Virus Strains Able To Exploit an Alternative Coreceptor on Untransformed Human Brain and Lymphoid Cells. J. Virol. 77: 6138-6152 [Abstract] [Full Text]  
• Dehghani, H., Puffer, B. A., Doms, R. W., Hirsch, V. M. (2003). Unique Pattern of Convergent Envelope Evolution in Simian Immunodeficiency Virus-Infected Rapid Progressor Macaques: Association with CD4-Independent Usage of CCR5. J. Virol. 77: 6405-6418 [Abstract] [Full Text]  
• Jekle, A., Keppler, O. T., De Clercq, E., Schols, D., Weinstein, M., Goldsmith, M. A. (2003). In Vivo Evolution of Human Immunodeficiency Virus Type 1 toward Increased Pathogenicity through CXCR4-Mediated Killing of Uninfected CD4 T Cells. J. Virol. 77: 5846-5854 [Abstract] [Full Text]  
• Ito, Y., Grivel, J.-C., Margolis, L. (2003). Real-Time PCR Assay of Individual Human Immunodeficiency Virus Type 1 Variants in Coinfected Human Lymphoid Tissues. J. Clin. Microbiol. 41: 2126-2131 [Abstract] [Full Text]  
• Cilliers, T., Nhlapo, J., Coetzer, M., Orlovic, D., Ketas, T., Olson, W. C., Moore, J. P., Trkola, A., Morris, L. (2003). The CCR5 and CXCR4 Coreceptors Are Both Used by Human Immunodeficiency Virus Type 1 Primary Isolates from Subtype C. J. Virol. 77: 4449-4456 [Abstract] [Full Text]  
• Kumar, S., Kwei, G. Y., Poon, G. K., Iliff, S. A., Wang, Y., Chen, Q., Franklin, R. B., Didolkar, V., Wang, R. W., Yamazaki, M., Chiu, S.-H. L., Lin, J. H., Pearson, P. G., Baillie, T. A. (2003). Pharmacokinetics and Interactions of a Novel Antagonist of Chemokine Receptor 5 (CCR5) with Ritonavir in Rats and Monkeys: Role of CYP3A and P-Glycoprotein. J. Pharmacol. Exp. Ther. 304: 1161-1171 [Abstract] [Full Text]  
• Ketas, T. J., Frank, I., Klasse, P. J., Sullivan, B. M., Gardner, J. P., Spenlehauer, C., Nesin, M., Olson, W. C., Moore, J. P., Pope, M. (2003). Human Immunodeficiency Virus Type 1 Attachment, Coreceptor, and Fusion Inhibitors Are Active against both Direct and trans Infection of Primary Cells. J. Virol. 77: 2762-2767 [Abstract] [Full Text]  
• Lin, G., Baribaud, F., Romano, J., Doms, R. W., Hoxie, J. A. (2002). Identification of gp120 Binding Sites on CXCR4 by Using CD4-Independent Human Immunodeficiency Virus Type 2 Env Proteins. J. Virol. 77: 931-942 [Abstract] [Full Text]  
• Hsu, M., Harouse, J. M., Gettie, A., Buckner, C., Blanchard, J., Cheng-Mayer, C. (2002). Increased Mucosal Transmission but Not Enhanced Pathogenicity of the CCR5-Tropic, Simian AIDS-Inducing Simian/Human Immunodeficiency Virus SHIVSF162P3 Maps to Envelope gp120. J. Virol. 77: 989-998 [Abstract] [Full Text]  
• Lin, Y.-L., Mettling, C., Portales, P., Reynes, J., Clot, J., Corbeau, P. (2002). Cell surface CCR5 density determines the postentry efficiency of R5 HIV-1 infection. Proc. Natl. Acad. Sci. USA 99: 15590-15595 [Abstract] [Full Text]  
• Farzan, M., Chung, S., Li, W., Vasilieva, N., Wright, P. L., Schnitzler, C. E., Marchione, R. J., Gerard, C., Gerard, N. P., Sodroski, J., Choe, H. (2002). Tyrosine-sulfated Peptides Functionally Reconstitute a CCR5 Variant Lacking a Critical Amino-terminal Region. J. Biol. Chem. 277: 40397-40402 [Abstract] [Full Text]  
• Konig, R. R., Flory, E., Steidl, S., Neumann, J., Coulibaly, C., Holznagel, E., Holzammer, S., Norley, S., Cichutek, K. (2002). Engineered CD4- and CXCR4-Using Simian Immunodeficiency Virus from African Green Monkeys Is Neutralization Sensitive and Replicates in Nonstimulated Lymphocytes. J. Virol. 76: 10627-10636 [Abstract] [Full Text]  
• Fouts, T., Godfrey, K., Bobb, K., Montefiori, D., Hanson, C. V., Kalyanaraman, V. S., DeVico, A., Pal, R. (2002). Crosslinked HIV-1 envelope-CD4 receptor complexes elicit broadly cross-reactive neutralizing antibodies in rhesus macaques. Proc. Natl. Acad. Sci. USA 99: 11842-11847 [Abstract] [Full Text]  
• Estes, J. D., Keele, B. F., Tenner-Racz, K., Racz, P., Redd, M. A., Thacker, T. C., Jiang, Y., Lloyd, M. J., Gartner, S., Burton, G. F. (2002). Follicular Dendritic Cell-Mediated Up-Regulation of CXCR4 Expression on CD4 T Cells and HIV Pathogenesis. J. Immunol. 169: 2313-2322 [Abstract] [Full Text]  

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