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Science 12 November 1999:
Vol. 286. no. 5443, pp. 1353 - 1357
DOI: 10.1126/science.286.5443.1353
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Reports

Sexual Transmission and Propagation of SIV and HIV in Resting and Activated CD4+ T Cells

Z.-Q. Zhang, 1 T. Schuler, 1 M. Zupancic, 1 S. Wietgrefe, 1 K. A. Staskus, 1 K. A. Reimann, 2 T. A. Reinhart, 3 M. Rogan, 1 W. Cavert, 1 C. J. Miller, 4 R. S. Veazey, 2 D. Notermans, 5 S. Little, 6 S. A. Danner, 5 D. D. Richman, 610 D. Havlir, 6 J. Wong, 610 H. L. Jordan, 2 T. W. Schacker, 7 P. Racz, 8 K. Tenner-Racz, 8 N. L. Letvin, 2 S. Wolinsky, 9 A. T. Haase 1*

In sexual transmission of simian immunodeficiency virus, and early and later stages of human immunodeficiency virus-type 1 (HIV-1) infection, both viruses were found to replicate predominantly in CD4+ T cells at the portal of entry and in lymphoid tissues. Infection was propagated not only in activated and proliferating T cells but also, surprisingly, in resting T cells. The infected proliferating cells correspond to the short-lived population that produces the bulk of HIV-1. Most of the HIV-1-infected resting T cells persisted after antiretroviral therapy. Latently and chronically infected cells that may be derived from this population pose challenges to eradicating infection and developing an effective vaccine.

1 Department of Microbiology, University of Minnesota Medical School, Minneapolis, MN 55455, USA.
2 Division of Viral Pathogenesis, Beth Israel Hospital, Harvard University, Boston, MA 02215, USA.
3 Department of Infectious Diseases and Microbiology, University of Pittsburgh, Pittsburgh, PA 15261, USA.
4 California Regional Primate Research Center, Davis, CA 95616, USA.
5 Division of Infectious Diseases, Tropical Medicine and AIDS, Academic Hospital, University of Amsterdam, Academic Medical Centre, Amsterdam, 1105 AZ, Netherlands.
6 Departments of Pathology and Medicine, University of California, San Diego, CA 92093, USA.
7 Department of Medicine, University of Minnesota Medical School, Minneapolis, MN 55455, USA.
8 Bernhard-Nocht Institute for Tropical Medicine, Hamburg 20359, Germany.
9 Division of Infectious Disease, Northwestern University Medical School, Chicago, IL 60611, USA.
10 San Diego VA Health Care System, San Diego, CA 92093, USA.
*   To whom correspondence should be addressed.

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Macrophage HIV-1 infection and the gastrointestinal tract reservoir.
P. D. Smith, G. Meng, J. F. Salazar-Gonzalez, and G. M. Shaw (2003)
J. Leukoc. Biol. 74, 642-649
   Abstract »    Full Text »    PDF »
The role of dendritic cell C-type lectin receptors in HIV pathogenesis.
S. Turville, J. Wilkinson, P. Cameron, J. Dable, and A. L. Cunningham (2003)
J. Leukoc. Biol. 74, 710-718
   Abstract »    Full Text »    PDF »
Immunodeficiency virus exploitation of dendritic cells in the early steps of infection.
N. Teleshova, I. Frank, and M. Pope (2003)
J. Leukoc. Biol. 74, 683-690
   Abstract »    Full Text »    PDF »
Identification of T cell-signaling pathways that stimulate latent HIV in primary cells.
D. G. Brooks, P. A. Arlen, L. Gao, C. M. R. Kitchen, and J. A. Zack (2003)
PNAS 100, 12955-12960
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Human T lymphocytes transduced by lentiviral vectors in the absence of TCR activation maintain an intact immune competence.
S. Cavalieri, S. Cazzaniga, M. Geuna, Z. Magnani, C. Bordignon, L. Naldini, and C. Bonini (2003)
Blood 102, 497-505
   Abstract »    Full Text »    PDF »
Rigorous pre-clinical evaluation of topical microbicides to prevent transmission of human immunodeficiency virus.
M. J. Keller, M. E. Klotman, and B. C. Herold (2003)
J. Antimicrob. Chemother. 51, 1099-1102
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Transcriptional Suppression of In Vitro-Integrated Human Immunodeficiency Virus Type 1 Does Not Correlate with Proviral DNA Methylation.
M. Pion, A. Jordan, A. Biancotto, F. Dequiedt, F. Gondois-Rey, S. Rondeau, R. Vigne, J. Hejnar, E. Verdin, and I. Hirsch (2003)
J. Virol. 77, 4025-4032
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nef Gene Is Required for Robust Productive Infection by Simian Immunodeficiency Virus of T-Cell-Rich Paracortex in Lymph Nodes.
C. Sugimoto, K. Tadakuma, I. Otani, T. Moritoyo, H. Akari, F. Ono, Y. Yoshikawa, T. Sata, S. Izumo, and K. Mori (2003)
J. Virol. 77, 4169-4180
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HIV Envelope Induces Virus Expression from Resting CD4+ T Cells Isolated from HIV-Infected Individuals in the Absence of Markers of Cellular Activation or Apoptosis.
A. L. Kinter, C. A. Umscheid, J. Arthos, C. Cicala, Y. Lin, R. Jackson, E. Donoghue, L. Ehler, J. Adelsberger, R. L. Rabin, et al. (2003)
J. Immunol. 170, 2449-2455
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Simian immunodeficiency virus dramatically alters expression of homeostatic chemokines and dendritic cell markers during infection in vivo.
Y. K. Choi, B. A. Fallert, M. A. Murphey-Corb, and T. A. Reinhart (2003)
Blood 101, 1684-1691
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Gene expression and viral prodution in latently infected, resting CD4+ T cells in viremic versus aviremic HIV-infected individuals.
T.-W. Chun, J. S. Justement, R. A. Lempicki, J. Yang, G. Dennis Jr., C. W. Hallahan, C. Sanford, P. Pandya, S. Liu, M. McLaughlin, et al. (2003)
PNAS 100, 1908-1913
   Abstract »    Full Text »    PDF »
Latency in Human Immunodeficiency Virus Type 1 Infection: No Easy Answers.
D. Persaud, Y. Zhou, J. M. Siliciano, and R. F. Siliciano (2003)
J. Virol. 77, 1659-1665
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Mamu-A*01 Allele-Mediated Attenuation of Disease Progression in Simian-Human Immunodeficiency Virus Infection.
Z.-Q. Zhang, T.-M. Fu, D. R. Casimiro, M.-E. Davies, X. Liang, W. A. Schleif, L. Handt, L. Tussey, M. Chen, A. Tang, et al. (2002)
J. Virol. 76, 12845-12854
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Endogenously Expressed nef Uncouples Cytokine and Chemokine Production from Membrane Phenotypic Maturation in Dendritic Cells.
D. Messmer, J.-M. Jacque, C. Santisteban, C. Bristow, S.-Y. Han, L. Villamide-Herrera, E. Mehlhop, P. A. Marx, R. M. Steinman, A. Gettie, et al. (2002)
J. Immunol. 169, 4172-4182
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Immunohistochemical Localization of Feline Immunodeficiency Virus Using Native Species Antibodies.
A. B. Rogers, C. K. Mathiason, and E. A. Hoover (2002)
Am. J. Pathol. 161, 1143-1151
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Increased Macrophage Infection upon Subcutaneous Inoculation of Rhesus Macaques with Simian Immunodeficiency Virus-Loaded Dendritic Cells or T Cells but Not with Cell-Free Virus.
R. Ignatius, K. Tenner-Racz, D. Messmer, A. Gettie, J. Blanchard, A. Luckay, C. Russo, S. Smith, P. A. Marx, R. M. Steinman, et al. (2002)
J. Virol. 76, 9787-9797
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HIV-1 in peripheral blood monocytes: an underrated viral source.
T. Zhu (2002)
J. Antimicrob. Chemother. 50, 309-311
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Neuropathogenesis of Lentiviral Infection in Macaques : Roles of CXCR4 and CCR5 Viruses and Interleukin-4 in Enhancing Monocyte Chemoattractant Protein-1 Production in Macrophages.
A. Hicks, R. Potula, Y. J. Sui, F. Villinger, D. Pinson, I. Adany, Z. Li, C. Long, P. Cheney, J. Marcario, et al. (2002)
Am. J. Pathol. 161, 813-822
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Restricted SIV Replication in Rhesus Macaque Lung Tissues During the Acute Phase of Infection.
C. L. Fuller, Y. K. Choi, B. A. Fallert, S. Capuano III, P. Rajakumar, M. Murphey-Corb, and T. A. Reinhart (2002)
Am. J. Pathol. 161, 969-978
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Memory CD4+ T Cells Are the Earliest Detectable Human Immunodeficiency Virus Type 1 (HIV-1)-Infected Cells in the Female Genital Mucosal Tissue during HIV-1 Transmission in an Organ Culture System.
P. Gupta, K. B. Collins, D. Ratner, S. Watkins, G. J. Naus, D. V. Landers, and B. K. Patterson (2002)
J. Virol. 76, 9868-9876
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Modalities of Interleukin-7-Induced Human Immunodeficiency Virus Permissiveness in Quiescent T Lymphocytes.
O. Ducrey-Rundquist, M. Guyader, and D. Trono (2002)
J. Virol. 76, 9103-9111
   Abstract »    Full Text »    PDF »
Quantitative Expression and Virus Transmission Analysis of DC-SIGN on Monocyte-Derived Dendritic Cells.
F. Baribaud, S. Pohlmann, G. Leslie, F. Mortari, and R. W. Doms (2002)
J. Virol. 76, 9135-9142
   Abstract »    Full Text »    PDF »
Molecular Characterization of Preintegration Latency in Human Immunodeficiency Virus Type 1 Infection.
T. C. Pierson, Y. Zhou, T. L. Kieffer, C. T. Ruff, C. Buck, and R. F. Siliciano (2002)
J. Virol. 76, 8518-8531
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HIV envelope induces a cascade of cell signals in non-proliferating target cells that favor virus replication.
C. Cicala, J. Arthos, S. M. Selig, G. Dennis Jr., D. A. Hosack, D. Van Ryk, M. L. Spangler, T. D. Steenbeke, P. Khazanie, N. Gupta, et al. (2002)
PNAS 99, 9380-9385
   Abstract »    Full Text »    PDF »
Increased expression of the inflammatory chemokine CXC chemokine ligand 9/monokine induced by interferon-gamma in lymphoid tissues of rhesus macaques during simian immunodeficiency virus infection and acquired immunodeficiency syndrome.
T. A. Reinhart, B. A. Fallert, M. E. Pfeifer, S. Sanghavi, S. Capuano III, P. Rajakumar, M. Murphey-Corb, R. Day, C. L. Fuller, and T. M Schaefer (2002)
Blood 99, 3119-3128
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Interleukin-7-treated naive T cells can be productively infected by T-cell-adapted and primary isolates of human immunodeficiency virus 1.
C. M. Steffens, E. Z. Managlia, A. Landay, and L. Al-Harthi (2002)
Blood 99, 3310-3318
   Abstract »    Full Text »    PDF »
Infectious and Whole Inactivated Simian Immunodeficiency Viruses Interact Similarly with Primate Dendritic Cells (DCs): Differential Intracellular Fate of Virions in Mature and Immature DCs.
I. Frank, M. Piatak Jr., H. Stoessel, N. Romani, D. Bonnyay, J.D. Lifson, and M. Pope (2002)
J. Virol. 76, 2936-2951
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The Simian Immunodeficiency Virus {Delta}nef Vaccine, after Application to the Tonsils of Rhesus Macaques, Replicates Primarily within CD4+ T Cells and Elicits a Local Perforin-Positive CD8+ T-Cell Response.
C. Stahl-Hennig, R. M. Steinman, P. Ten Haaft, K. Uberla, N. Stolte, S. Saeland, K. Tenner-Racz, and P. Racz (2002)
J. Virol. 76, 688-696
   Abstract »    Full Text »    PDF »
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.
T. Zhu, D. Muthui, S. Holte, D. Nickle, F. Feng, S. Brodie, Y. Hwangbo, J. I. Mullins, and L. Corey (2002)
J. Virol. 76, 707-716
   Abstract »    Full Text »    PDF »
VEGF Receptor Signal Transduction.
T. Matsumoto and L. Claesson-Welsh (2001)
Sci. STKE 2001, re21
   Abstract »    Full Text »    PDF »
Induction of TAK (Cyclin T1/P-TEFb) in Purified Resting CD4+ T Lymphocytes by Combination of Cytokines.
R. Ghose, L.-Y. Liou, C. H. Herrmann, and A. P. Rice (2001)
J. Virol. 75, 11336-11343
   Abstract »    Full Text »


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