J. Exp. Med., Volume 189, Number 11, June 7, 1999 1735-1746

Cytokine Signals Are Sufficient for HIV-1 Infection of Resting Human T Lymphocytes

By Derya Unutmaz,^* Vineet N. KewalRamani,^* Shana Marmon,^* and Dan R. Littman^*

From the ^* Molecular Pathogenesis Program, Skirball Institute of Biomolecular Medicine, New York University Medical Center, and the  Howard Hughes Medical Institute, New York 10016

Lentiviral vectors have been advocated to be effective vehicles for the delivery and stable expression of genes in nondividing primary cells. However, certain cell types, such as resting T lymphocytes, are resistant to infection with HIV-1. Establishing parameters for stable gene delivery into primary human lymphocytes and approaches to overcome the resistance of resting T cells to HIV infection may permit potential gene therapy applications, genetic studies of primary cells in vitro, and a better understanding of the stages of the lentiviral life cycle. Here we demonstrate that an HIV-1-derived vector can be used for stable delivery of genes into activated human T cells as well as natural killer and dendritic cells. Remarkably, a sizeable fraction of resting T cells was stably transduced with the HIV-1 vector when cultured with the cytokine interleukin (IL)-2, IL-4, IL-7, or IL-15, or, at a lower level, with IL-6, in the absence of any other stimuli. Resting T cells stimulated with these cytokines could also be infected with replication-competent HIV-1. To test the utility of this system for performing structure-function analysis in primary T cells, we introduced wild-type as well as a mutant form of murine CD28 into human T cells and showed a requirement for the CD28 cytoplasmic domain in costimulatory signaling. The ability to stably express genes of interest in primary T cells will be a valuable tool for genetic and structure-function studies that previously have been limited to transformed cell lines. In addition, the finding that cytokine signals are sufficient to permit transduction of resting T cells with HIV may be relevant for understanding mechanism of HIV-1 transmission and pathogenesis.

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• Messmer, D., Jacque, J.-M., Santisteban, C., Bristow, C., Han, S.-Y., Villamide-Herrera, L., Mehlhop, E., Marx, P. A., Steinman, R. M., Gettie, A., Pope, M. (2002). Endogenously Expressed nef Uncouples Cytokine and Chemokine Production from Membrane Phenotypic Maturation in Dendritic Cells. J. Immunol. 169: 4172-4182 [Abstract] [Full Text]  
• Zhu, T. (2002). HIV-1 in peripheral blood monocytes: an underrated viral source. J Antimicrob Chemother 50: 309-311 [Full Text]  
• Ducrey-Rundquist, O., Guyader, M., Trono, D. (2002). Modalities of Interleukin-7-Induced Human Immunodeficiency Virus Permissiveness in Quiescent T Lymphocytes. J. Virol. 76: 9103-9111 [Abstract] [Full Text]  
• Pierson, T. C., Zhou, Y., Kieffer, T. L., Ruff, C. T., Buck, C., Siliciano, R. F. (2002). Molecular Characterization of Preintegration Latency in Human Immunodeficiency Virus Type 1 Infection. J. Virol. 76: 8518-8531 [Abstract] [Full Text]  
• Pedroza-Martins, L., Boscardin, W. J., Anisman-Posner, D. J., Schols, D., Bryson, Y. J., Uittenbogaart, C. H. (2002). Impact of Cytokines on Replication in the Thymus of Primary Human Immunodeficiency Virus Type 1 Isolates from Infants. J. Virol. 76: 6929-6943 [Abstract] [Full Text]  
• Forshey, B. M., von Schwedler, U., Sundquist, W. I., Aiken, C. (2002). Formation of a Human Immunodeficiency Virus Type 1 Core of Optimal Stability Is Crucial for Viral Replication. J. Virol. 76: 5667-5677 [Abstract] [Full Text]  
• Maurice, M., Verhoeyen, E., Salmon, P., Trono, D., Russell, S. J., Cosset, F.-L. (2002). Efficient gene transfer into human primary blood lymphocytes by surface-engineered lentiviral vectors that display a T cell-activating polypeptide. Blood 99: 2342-2350 [Abstract] [Full Text]  
• Lundquist, C. A., Tobiume, M., Zhou, J., Unutmaz, D., Aiken, C. (2002). Nef-Mediated Downregulation of CD4 Enhances Human Immunodeficiency Virus Type 1 Replication in Primary T Lymphocytes. J. Virol. 76: 4625-4633 [Abstract] [Full Text]  
• Chang, T. L.-Y., Gordon, C. J., Roscic-Mrkic, B., Power, C., Proudfoot, A. E. I., Moore, J. P., Trkola, A. (2002). Interaction of the CC-Chemokine RANTES with Glycosaminoglycans Activates a p44/p42 Mitogen-Activated Protein Kinase-Dependent Signaling Pathway and Enhances Human Immunodeficiency Virus Type 1 Infectivity. J. Virol. 76: 2245-2254 [Abstract] [Full Text]  
• Brooks, D. G., Zack, J. A. (2002). Effect of Latent Human Immunodeficiency Virus Infection on Cell Surface Phenotype. J. Virol. 76: 1673-1681 [Abstract] [Full Text]  
• Zhu, T., Muthui, D., Holte, S., Nickle, D., Feng, F., Brodie, S., Hwangbo, Y., Mullins, J. I., Corey, L. (2002). Evidence for Human Immunodeficiency Virus Type 1 Replication In Vivo in CD14+ Monocytes and Its Potential Role as a Source of Virus in Patients on Highly Active Antiretroviral Therapy. J. Virol. 76: 707-716 [Abstract] [Full Text]  
• Ghose, R., Liou, L.-Y., Herrmann, C. H., Rice, A. P. (2001). Induction of TAK (Cyclin T1/P-TEFb) in Purified Resting CD4+ T Lymphocytes by Combination of Cytokines. J. Virol. 75: 11336-11343 [Abstract] [Full Text]  
• Wu, Y., Marsh, J. W. (2001). Selective Transcription and Modulation of Resting T Cell Activity by Preintegrated HIV DNA. Science 293: 1503-1506 [Abstract] [Full Text]  
• Dardalhon, V., Jaleco, S., Kinet, S., Herpers, B., Steinberg, M., Ferrand, C., Froger, D., Leveau, C., Tiberghien, P., Charneau, P., Noraz, N., Taylor, N. (2001). IL-7 differentially regulates cell cycle progression and HIV-1-based vector infection in neonatal and adult CD4+ T cells. Proc. Natl. Acad. Sci. USA 10.1073/pnas.161272698v1 [Abstract] [Full Text]  
• Neil, S., Martin, F., Ikeda, Y., Collins, M. (2001). Postentry Restriction to Human Immunodeficiency Virus-Based Vector Transduction in Human Monocytes. J. Virol. 75: 5448-5456 [Abstract] [Full Text]  
• Scales, D., Ni, H., Shaheen, F., Capodici, J., Cannon, G., Weissman, D. (2001). Nonproliferating Bystander CD4+ T Cells Lacking Activation Markers Support HIV Replication During Immune Activation. J. Immunol. 166: 6437-6443 [Abstract] [Full Text]  
• Marti, F., Krause, A., Post, N. H., Lyddane, C., Dupont, B., Sadelain, M., King, P. D. (2001). Negative-Feedback Regulation of CD28 Costimulation by a Novel Mitogen-Activated Protein Kinase Phosphatase, MKP6. J. Immunol. 166: 197-206 [Abstract] [Full Text]  
• Salmon, P., Kindler, V., Ducrey, O., Chapuis, B., Zubler, R. H., Trono, D. (2000). High-level transgene expression in human hematopoietic progenitors and differentiated blood lineages after transduction with improved lentiviral vectors. Blood 96: 3392-3398 [Abstract] [Full Text]  
• Unutmaz, D., Xiang, W., Sunshine, M. J., Campbell, J., Butcher, E., Littman, D. R. (2000). The Primate Lentiviral Receptor Bonzo/STRL33 Is Coordinately Regulated with CCR5 and Its Expression Pattern Is Conserved Between Human and Mouse. J. Immunol. 165: 3284-3292 [Abstract] [Full Text]  
• 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]  
• Chinnasamy, D., Chinnasamy, N., Enriquez, M. J., Otsu, M., Morgan, R. A., Candotti, F. (2000). Lentiviral-mediated gene transfer into human lymphocytes: role of HIV-1 accessory proteins. Blood 96: 1309-1316 [Abstract] [Full Text]  
• Dardalhon, V., Jaleco, S., Rebouissou, C., Ferrand, C., Skander, N., Swainson, L., Tiberghien, P., Spits, H., Noraz, N., Taylor, N. (2000). Highly efficient gene transfer in naive human T cells with a murine leukemia virus-based vector. Blood 96: 885-893 [Abstract] [Full Text]  
• Wang, J.-K., Kiyokawa, E., Verdin, E., Trono, D. (2000). The Nef protein of HIV-1 associates with rafts and primes T cells for activation. Proc. Natl. Acad. Sci. USA 97: 394-399 [Abstract] [Full Text]  
• Dardalhon, V., Jaleco, S., Kinet, S., Herpers, B., Steinberg, M., Ferrand, C., Froger, D., Leveau, C., Tiberghien, P., Charneau, P., Noraz, N., Taylor, N. (2001). IL-7 differentially regulates cell cycle progression and HIV-1-based vector infection in neonatal and adult CD4+ T cells. Proc. Natl. Acad. Sci. USA 98: 9277-9282 [Abstract] [Full Text]  
• Motsinger, A., Haas, D. W., Stanic, A. K., Van Kaer, L., Joyce, S., Unutmaz, D. (2002). CD1d-restricted Human Natural Killer T Cells Are Highly Susceptible to Human Immunodeficiency Virus 1 Infection. JEM 195: 869-879 [Abstract] [Full Text]  

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