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Science 17 April 1998:
Vol. 280. no. 5362, pp. 427 - 431
DOI: 10.1126/science.280.5362.427
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Reports

Gastrointestinal Tract as a Major Site of CD4+ T Cell Depletion and Viral Replication in SIV Infection

Ronald S. Veazey, MaryAnn DeMaria, Laura V. Chalifoux, Daniel E. Shvetz, Douglas R. Pauley, Heather L. Knight, Michael Rosenzweig, R. Paul Johnson, Ronald C. Desrosiers, Andrew A. Lackner *

Human and simian immunodeficiency virus (HIV and SIV) replicate optimally in activated memory CD4+ T cells, a cell type that is abundant in the intestine. SIV infection of rhesus monkeys resulted in profound and selective depletion of CD4+ T cells in the intestine within days of infection, before any such changes in peripheral lymphoid tissues. The loss of CD4+ T cells in the intestine occurred coincident with productive infection of large numbers of mononuclear cells at this site. The intestine appears to be a major target for SIV replication and the major site of CD4+ T cell loss in early SIV infection.

New England Regional Primate Research Center, Harvard Medical School, 1 Pine Hill Drive, Post Office Box 9102, Southborough, MA 01772, USA.
*   To whom correspondence should be addressed. E-mail: alackner{at}warren.med.harvard.edu

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J. Virol. 81, 5202-5211
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Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts.
I. Pandrea, C. Apetrei, S. Gordon, J. Barbercheck, J. Dufour, R. Bohm, B. Sumpter, P. Roques, P. A. Marx, V. M. Hirsch, et al. (2007)
Blood 109, 1069-1076
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Massive infection and loss of CD4+ T cells occurs in the intestinal tract of neonatal rhesus macaques in acute SIV infection.
X. Wang, T. Rasmussen, B. Pahar, B. Poonia, X. Alvarez, A. A. Lackner, and R. S. Veazey (2007)
Blood 109, 1174-1181
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Mechanisms of Gastrointestinal CD4+ T-Cell Depletion during Acute and Early Human Immunodeficiency Virus Type 1 Infection.
S. Mehandru, M. A. Poles, K. Tenner-Racz, V. Manuelli, P. Jean-Pierre, P. Lopez, A. Shet, A. Low, H. Mohri, D. Boden, et al. (2007)
J. Virol. 81, 599-612
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Loss of Naive Cells Accompanies Memory CD4+ T-Cell Depletion during Long-Term Progression to AIDS in Simian Immunodeficiency Virus-Infected Macaques.
Y. Nishimura, T. Igarashi, A. Buckler-White, C. Buckler, H. Imamichi, R. M. Goeken, W. R. Lee, B. A. P. Lafont, R. Byrum, H. C. Lane, et al. (2007)
J. Virol. 81, 893-902
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Fusion-Induced Apoptosis Contributes to Thymocyte Depletion by a Pathogenic Human Immunodeficiency Virus Type 1 Envelope in the Human Thymus.
E. G. Meissner, L. Zhang, S. Jiang, and L. Su (2006)
J. Virol. 80, 11019-11030
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Going Wild: Lessons from Naturally Occurring T-Lymphotropic Lentiviruses.
S. VandeWoude and C. Apetrei (2006)
Clin. Microbiol. Rev. 19, 728-762
   Abstract »    Full Text »    PDF »
Biology of CCR5 and its role in HIV infection and treatment..
M. M. Lederman, A. Penn-Nicholson, M. Cho, and D. Mosier (2006)
JAMA 296, 815-826
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Viral Suppression and Immune Restoration in the Gastrointestinal Mucosa of Human Immunodeficiency Virus Type 1-Infected Patients Initiating Therapy during Primary or Chronic Infection..
M. Guadalupe, S. Sankaran, M. D. George, E. Reay, D. Verhoeven, B. L. Shacklett, J. Flamm, J. Wegelin, T. Prindiville, and S. Dandekar (2006)
J. Virol. 80, 8236-8247
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Vaccination preserves CD4 memory T cells during acute simian immunodeficiency virus challenge.
J. J. Mattapallil, D. C. Douek, A. Buckler-White, D. Montefiori, N. L. Letvin, G. J. Nabel, and M. Roederer (2006)
J. Exp. Med. 203, 1533-1541
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Receptor (SLAM [CD150]) Recognition and the V Protein Sustain Swift Lymphocyte-Based Invasion of Mucosal Tissue and Lymphatic Organs by a Morbillivirus..
V. von Messling, N. Svitek, and R. Cattaneo (2006)
J. Virol. 80, 6084-6092
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Lymphatic Tissue Fibrosis Is Associated with Reduced Numbers of Naive CD4+ T Cells in Human Immunodeficiency Virus Type 1 Infection..
T. W. Schacker, J. M. Brenchley, G. J. Beilman, C. Reilly, S. E. Pambuccian, J. Taylor, D. Skarda, M. Larson, D. C. Douek, and A. T. Haase (2006)
Clin. Vaccine Immunol. 13, 556-560
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Rapid dissemination of a pathogenic simian/human immunodeficiency virus to systemic organs and active replication in lymphoid tissues following intrarectal infection..
A. Miyake, K. Ibuki, Y. Enose, H. Suzuki, R. Horiuchi, M. Motohara, N. Saito, T. Nakasone, M. Honda, T. Watanabe, et al. (2006)
J. Gen. Virol. 87, 1311-1320
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Longitudinal Analysis of Monocyte/Macrophage Infection in Simian Immunodeficiency Virus-Infected, CD8+ T-Cell-Depleted Macaques that Develop Lentiviral Encephalitis.
S. J. Bissel, G. Wang, A. M. Trichel, M. Murphey-Corb, and C. A. Wiley (2006)
Am. J. Pathol. 168, 1553-1569
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Impact of vaccine-induced mucosal high-avidity CD8+CTLs in delay of AIDS viral dissemination from mucosa.
I. M. Belyakov, V. A. Kuznetsov, B. Kelsall, D. Klinman, M. Moniuszko, M. Lemon, P. D. Markham, R. Pal, J. D. Clements, M. G. Lewis, et al. (2006)
Blood 107, 3258-3264
   Abstract »    Full Text »    PDF »
Innate and Adaptive Mucosal Immunity in Protection against HIV Infection.
L.A. Bergmeier and T. Lehner (2006)
Advances in Dental Research 19, 21-28
   Abstract »    Full Text »    PDF »
Differential Mucosal Susceptibility in HIV-1 Transmission and Infection.
N.M. Moutsopoulos, T. Greenwell-Wild, and S.M. Wahl (2006)
Advances in Dental Research 19, 52-56
   Abstract »    Full Text »    PDF »
Perforin Expression in the Gastrointestinal Mucosa Is Limited to Acute Simian Immunodeficiency Virus Infection.
M. F. Quigley, K. Abel, B. Zuber, C. J. Miller, J. K. Sandberg, and B. L. Shacklett (2006)
J. Virol. 80, 3083-3087
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Comparative studies on mucosal and intravenous transmission of simian immunodeficiency virus (SIVsm): evolution of coreceptor use varies with pathogenic outcome..
A. Lauren, D. Vodros, R. Thorstensson, and E. M. Fenyo (2006)
J. Gen. Virol. 87, 581-594
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Comparative studies on mucosal and intravenous transmission of simian immunodeficiency virus (SIVsm): the kinetics of evolution to neutralization resistance are related to progression rate of disease..
A. Lauren, R. Thorstensson, and E. M. Fenyo (2006)
J. Gen. Virol. 87, 595-606
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Infectious Molecular Clones from a Simian Immunodeficiency Virus-Infected Rapid-Progressor (RP) Macaque: Evidence of Differential Selection of RP-Specific Envelope Mutations In Vitro and In Vivo.
T. Kuwata, H. Dehghani, C. R. Brown, R. Plishka, A. Buckler-White, T. Igarashi, J. Mattapallil, M. Roederer, and V. M. Hirsch (2006)
J. Virol. 80, 1463-1475
   Abstract »    Full Text »    PDF »
Expanded Tissue Targets for Foamy Virus Replication with Simian Immunodeficiency Virus-Induced Immunosuppression.
S. M. Murray, L. J. Picker, M. K. Axthelm, and M. L. Linial (2006)
J. Virol. 80, 663-670
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Detection of Immunoglobulin G Antibodies to Neospora caninum in Humans: High Seropositivity Rates in Patients Who Are Infected by Human Immunodeficiency Virus or Have Neurological Disorders.
J. Lobato, D. A. O. Silva, T. W. P. Mineo, J. D. H. F. Amaral, G. R. S. Segundo, J. M. Costa-Cruz, M. S. Ferreira, A. S. Borges, and J. R. Mineo (2006)
Clin. Vaccine Immunol. 13, 84-89
   Abstract »    Full Text »    PDF »
Improved Vaccine Protection from Simian AIDS by the Addition of Nonstructural Simian Immunodeficiency Virus Genes.
Z. Hel, W.-P. Tsai, E. Tryniszewska, J. Nacsa, P. D. Markham, M. G. Lewis, G. N. Pavlakis, B. K. Felber, J. Tartaglia, and G. Franchini (2006)
J. Immunol. 176, 85-96
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The majority of human immunodeficiency virus type 1 particles present within splenic germinal centres are produced locally.
M.-J. Dumaurier, S. Gratton, S. Wain-Hobson, and R. Cheynier (2005)
J. Gen. Virol. 86, 3369-3373
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Recombinant poxviruses as mucosal vaccine vectors.
M. M. Gherardi and M. Esteban (2005)
J. Gen. Virol. 86, 2925-2936
   Abstract »    Full Text »    PDF »
Distinct Chemokine Triggers and In Vivo Migratory Paths of Fluorescein Dye-Labeled T Lymphocytes in Acutely Simian Immunodeficiency Virus SIVmac251-Infected and Uninfected Macaques.
C. C. Clay, D. S. Rodrigues, D. J. Harvey, C. M. Leutenegger, and U. Esser (2005)
J. Virol. 79, 13759-13768
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Increased Expression of TLR3 in Lymph Nodes during Simian Immunodeficiency Virus Infection: Implications for Inflammation and Immunodeficiency.
S. K. Sanghavi and T. A. Reinhart (2005)
J. Immunol. 175, 5314-5323
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V3 Loop-Determined Coreceptor Preference Dictates the Dynamics of CD4+-T-Cell Loss in Simian-Human Immunodeficiency Virus-Infected Macaques.
S.-h. Ho, L. Shek, A. Gettie, J. Blanchard, and C. Cheng-Mayer (2005)
J. Virol. 79, 12296-12303
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Antigenic Stimulation Specifically Reactivates the Replication of Archived Simian Immunodeficiency Virus Genomes in Chronically Infected Macaques.
C. Renoux, S. Wain-Hobson, B. Hurtrel, and R. Cheynier (2005)
J. Virol. 79, 11231-11238
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HLA-A2 down-regulation on primary human macrophages infected with an M-tropic EGFP-tagged HIV-1 reporter virus.
A. Brown, S. Gartner, T. Kawano, N. Benoit, and C. Cheng-Mayer (2005)
J. Leukoc. Biol. 78, 675-685
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