This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Silvestri, G.
Right arrow Articles by Staprans, S. I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Silvestri, G.
Right arrow Articles by Staprans, S. I.

 Previous Article  |  Next Article 

Journal of Virology, April 2005, p. 4043-4054, Vol. 79, No. 7
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.7.4043-4054.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Divergent Host Responses during Primary Simian Immunodeficiency Virus SIVsm Infection of Natural Sooty Mangabey and Nonnatural Rhesus Macaque Hosts

Guido Silvestri,1,2 Andrew Fedanov,2 Stephanie Germon,2 Natalia Kozyr,2 William J. Kaiser,2 David A. Garber,1,2 Harold McClure,3,{dagger} Mark B. Feinberg,1,2,4 and Silvija I. Staprans1,2,4*

Departments of Medicine,1 Microbiology and Immunology,4 Emory Vaccine Center, Emory University School of Medicine,2 Yerkes National Primate Research Center of Emory University, Atlanta, Georgia3

Received 5 October 2004/ Accepted 11 November 2004

To understand how natural sooty mangabey hosts avoid AIDS despite high levels of simian immunodeficiency virus (SIV) SIVsm replication, we inoculated mangabeys and nonnatural rhesus macaque hosts with an identical inoculum of uncloned SIVsm. The unpassaged virus established infection with high-level viral replication in both macaques and mangabeys. A species-specific, divergent immune response to SIV was evident from the first days of infection and maintained in the chronic phase, with macaques showing immediate and persistent T-cell proliferation, whereas mangabeys displayed little T-cell proliferation, suggesting subdued cellular immune responses to SIV. Importantly, only macaques developed CD4+-T-cell depletion and AIDS, thus indicating that in mangabeys limited immune activation is a key mechanism to avoid immunodeficiency despite high levels of SIVsm replication. These studies demonstrate that it is the host response to infection, rather than properties inherent to the virus itself, that causes immunodeficiency in SIV-infected nonhuman primates.

* Corresponding author. Mailing address: Emory Vaccine Center, 954 Gatewood Rd., NE, Atlanta, GA 30329. Phone: (404) 727-8214. Fax: (404) 727-8199. E-mail: sstapr2{at}sph.emory.edu.

{dagger} Deceased.

Journal of Virology, April 2005, p. 4043-4054, Vol. 79, No. 7
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.7.4043-4054.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Gaufin, T., Pattison, M., Gautam, R., Stoulig, C., Dufour, J., MacFarland, J., Mandell, D., Tatum, C., Marx, M. H., Ribeiro, R. M., Montefiori, D., Apetrei, C., Pandrea, I. (2009). Effect of B-Cell Depletion on Viral Replication and Clinical Outcome of Simian Immunodeficiency Virus Infection in a Natural Host. J. Virol. 83: 10347-10357 [Abstract] [Full Text]  
  • Gautam, R., Gaufin, T., Butler, I., Gautam, A., Barnes, M., Mandell, D., Pattison, M., Tatum, C., Macfarland, J., Monjure, C., Marx, P. A., Pandrea, I., Apetrei, C. (2009). Simian Immunodeficiency Virus SIVrcm, a Unique CCR2-Tropic Virus, Selectively Depletes Memory CD4+ T Cells in Pigtailed Macaques through Expanded Coreceptor Usage In Vivo. J. Virol. 83: 7894-7908 [Abstract] [Full Text]  
  • Koopman, G., Mortier, D., Hofman, S., Koutsoukos, M., Bogers, W. M. J. M., Wahren, B., Voss, G., Heeney, J. L. (2009). Acute-phase CD4+ T-cell proliferation and CD152 upregulation predict set-point virus replication in vaccinated simian-human immunodeficiency virus strain 89.6p-infected macaques. J. Gen. Virol. 90: 915-926 [Abstract] [Full Text]  
  • Souquiere, S., Onanga, R., Makuwa, M., Pandrea, I., Ngari, P., Rouquet, P., Bourry, O., Kazanji, M., Apetrei, C., Simon, F., Roques, P. (2009). Simian immunodeficiency virus types 1 and 2 (SIV mnd 1 and 2) have different pathogenic potentials in rhesus macaques upon experimental cross-species transmission. J. Gen. Virol. 90: 488-499 [Abstract] [Full Text]  
  • Paiardini, M., Cervasi, B., Engram, J. C., Gordon, S. N., Klatt, N. R., Muthukumar, A., Else, J., Mittler, R. S., Staprans, S. I., Sodora, D. L., Silvestri, G. (2009). Bone marrow-based homeostatic proliferation of mature T cells in nonhuman primates: implications for AIDS pathogenesis. Blood 113: 612-621 [Abstract] [Full Text]  
  • Elbim, C., Monceaux, V., Mueller, Y. M., Lewis, M. G., Francois, S., Diop, O., Akarid, K., Hurtrel, B., Gougerot-Pocidalo, M.-A., Levy, Y., Katsikis, P. D., Estaquier, J. (2008). Early Divergence in Neutrophil Apoptosis between Pathogenic and Nonpathogenic Simian Immunodeficiency Virus Infections of Nonhuman Primates. J. Immunol. 181: 8613-8623 [Abstract] [Full Text]  
  • Bibollet-Ruche, F., McKinney, B. A., Duverger, A., Wagner, F. H., Ansari, A. A., Kutsch, O. (2008). The Quality of Chimpanzee T-Cell Activation and Simian Immunodeficiency Virus/Human Immunodeficiency Virus Susceptibility Achieved via Antibody-Mediated T-Cell Receptor/CD3 Stimulation Is a Function of the Anti-CD3 Antibody Isotype. J. Virol. 82: 10271-10278 [Abstract] [Full Text]  
  • Jiang, Q., Zhang, L., Wang, R., Jeffrey, J., Washburn, M. L., Brouwer, D., Barbour, S., Kovalev, G. I., Unutmaz, D., Su, L. (2008). FoxP3+CD4+ regulatory T cells play an important role in acute HIV-1 infection in humanized Rag2-/-{gamma}C-/- mice in vivo. Blood 112: 2858-2868 [Abstract] [Full Text]  
  • Pandrea, I., Onanga, R., Souquiere, S., Mouinga-Ondeme, A., Bourry, O., Makuwa, M., Rouquet, P., Silvestri, G., Simon, F., Roques, P., Apetrei, C. (2008). Paucity of CD4+ CCR5+ T Cells May Prevent Transmission of Simian Immunodeficiency Virus in Natural Nonhuman Primate Hosts by Breast-Feeding. J. Virol. 82: 5501-5509 [Abstract] [Full Text]  
  • Estes, J. D., Gordon, S. N., Zeng, M., Chahroudi, A. M., Dunham, R. M., Staprans, S. I., Reilly, C. S., Silvestri, G., Haase, A. T. (2008). Early Resolution of Acute Immune Activation and Induction of PD-1 in SIV-Infected Sooty Mangabeys Distinguishes Nonpathogenic from Pathogenic Infection in Rhesus Macaques. J. Immunol. 180: 6798-6807 [Abstract] [Full Text]  
  • Dunham, R. M., Cervasi, B., Brenchley, J. M., Albrecht, H., Weintrob, A., Sumpter, B., Engram, J., Gordon, S., Klatt, N. R., Frank, I., Sodora, D. L., Douek, D. C., Paiardini, M., Silvestri, G. (2008). CD127 and CD25 Expression Defines CD4+ T Cell Subsets That Are Differentially Depleted during HIV Infection. J. Immunol. 180: 5582-5592 [Abstract] [Full Text]  
  • Pandrea, I., Ribeiro, R. M., Gautam, R., Gaufin, T., Pattison, M., Barnes, M., Monjure, C., Stoulig, C., Dufour, J., Cyprian, W., Silvestri, G., Miller, M. D., Perelson, A. S., Apetrei, C. (2008). Simian Immunodeficiency Virus SIVagm Dynamics in African Green Monkeys. J. Virol. 82: 3713-3724 [Abstract] [Full Text]  
  • Gordon, S. N., Dunham, R. M., Engram, J. C., Estes, J., Wang, Z., Klatt, N. R., Paiardini, M., Pandrea, I. V., Apetrei, C., Sodora, D. L., Lee, H. Y., Haase, A. T., Miller, M. D., Kaur, A., Staprans, S. I., Perelson, A. S., Feinberg, M. B., Silvestri, G. (2008). Short-Lived Infected Cells Support Virus Replication in Sooty Mangabeys Naturally Infected with Simian Immunodeficiency Virus: Implications for AIDS Pathogenesis. J. Virol. 82: 3725-3735 [Abstract] [Full Text]  
  • Cumont, M.-C., Diop, O., Vaslin, B., Elbim, C., Viollet, L., Monceaux, V., Lay, S., Silvestri, G., Le Grand, R., Muller-Trutwin, M., Hurtrel, B., Estaquier, J. (2008). Early Divergence in Lymphoid Tissue Apoptosis between Pathogenic and Nonpathogenic Simian Immunodeficiency Virus Infections of Nonhuman Primates. J. Virol. 82: 1175-1184 [Abstract] [Full Text]  
  • Kosub, D. A., Lehrman, G., Milush, J. M., Zhou, D., Chacko, E., Leone, A., Gordon, S., Silvestri, G., Else, J. G., Keiser, P., Jain, M. K., Sodora, D. L. (2008). Gamma/Delta T-Cell Functional Responses Differ after Pathogenic Human Immunodeficiency Virus and Nonpathogenic Simian Immunodeficiency Virus Infections. J. Virol. 82: 1155-1165 [Abstract] [Full Text]  
  • Pereira, L. E., Villinger, F., Wulff, H., Sankaranarayanan, A., Raman, G., Ansari, A. A. (2007). Pharmacokinetics, Toxicity, and Functional Studies of the Selective Kv1.3 Channel Blocker 5-(4-Phenoxybutoxy)Psoralen in Rhesus Macaques. Exp. Biol. Med. 232: 1338-1354 [Abstract] [Full Text]  
  • Okoye, A., Meier-Schellersheim, M., Brenchley, J. M., Hagen, S. I., Walker, J. M., Rohankhedkar, M., Lum, R., Edgar, J. B., Planer, S. L., Legasse, A., Sylwester, A. W., Piatak, M. Jr., Lifson, J. D., Maino, V. C., Sodora, D. L., Douek, D. C., Axthelm, M. K., Grossman, Z., Picker, L. J. (2007). Progressive CD4+ central-memory T cell decline results in CD4+ effector-memory insufficiency and overt disease in chronic SIV infection. JEM 204: 2171-2185 [Abstract] [Full Text]  
  • Gordon, S. N., Klatt, N. R., Bosinger, S. E., Brenchley, J. M., Milush, J. M., Engram, J. C., Dunham, R. M., Paiardini, M., Klucking, S., Danesh, A., Strobert, E. A., Apetrei, C., Pandrea, I. V., Kelvin, D., Douek, D. C., Staprans, S. I., Sodora, D. L., Silvestri, G. (2007). Severe Depletion of Mucosal CD4+ T Cells in AIDS-Free Simian Immunodeficiency Virus-Infected Sooty Mangabeys. J. Immunol. 179: 3026-3034 [Abstract] [Full Text]  
  • Pandrea, I. V., Gautam, R., Ribeiro, R. M., Brenchley, J. M., Butler, I. F., Pattison, M., Rasmussen, T., Marx, P. A., Silvestri, G., Lackner, A. A., Perelson, A. S., Douek, D. C., Veazey, R. S., Apetrei, C. (2007). Acute Loss of Intestinal CD4+ T Cells Is Not Predictive of Simian Immunodeficiency Virus Virulence. J. Immunol. 179: 3035-3046 [Abstract] [Full Text]  
  • Milush, J. M., Reeves, J. D., Gordon, S. N., Zhou, D., Muthukumar, A., Kosub, D. A., Chacko, E., Giavedoni, L. D., Ibegbu, C. C., Cole, K. S., Miamidian, J. L., Paiardini, M., Barry, A. P., Staprans, S. I., Silvestri, G., Sodora, D. L. (2007). Virally Induced CD4+ T Cell Depletion Is Not Sufficient to Induce AIDS in a Natural Host. J. Immunol. 179: 3047-3056 [Abstract] [Full Text]  
  • Apetrei, C., Gautam, R., Sumpter, B., Carter, A. C., Gaufin, T., Staprans, S. I., Else, J., Barnes, M., Cao, R. Jr., Garg, S., Milush, J. M., Sodora, D. L., Pandrea, I., Silvestri, G. (2007). Virus Subtype-Specific Features of Natural Simian Immunodeficiency Virus SIVsmm Infection in Sooty Mangabeys. J. Virol. 81: 7913-7923 [Abstract] [Full Text]  
  • Meier, A., Alter, G., Frahm, N., Sidhu, H., Li, B., Bagchi, A., Teigen, N., Streeck, H., Stellbrink, H.-J., Hellman, J., van Lunzen, J., Altfeld, M. (2007). MyD88-Dependent Immune Activation Mediated by Human Immunodeficiency Virus Type 1-Encoded Toll-Like Receptor Ligands. J. Virol. 81: 8180-8191 [Abstract] [Full Text]  
  • Kim, N., Dabrowska, A., Jenner, R. G., Aldovini, A. (2007). Human and Simian Immunodeficiency Virus-Mediated Upregulation of the Apoptotic Factor TRAIL Occurs in Antigen-Presenting Cells from AIDS-Susceptible but Not from AIDS-Resistant Species. J. Virol. 81: 7584-7597 [Abstract] [Full Text]  
  • Alter, G., Suscovich, T. J., Teigen, N., Meier, A., Streeck, H., Brander, C., Altfeld, M. (2007). Single-Stranded RNA Derived from HIV-1 Serves as a Potent Activator of NK Cells. J. Immunol. 178: 7658-7666 [Abstract] [Full Text]  
  • Bostik, P., Noble, E. S., Stephenson, S. T., Villinger, F., Ansari, A. A. (2007). CD4+ T Cells from Simian Immunodeficiency Virus Disease-Resistant Sooty Mangabeys Produce More IL-2 Than Cells from Disease-Susceptible Species: Involvement of p300 and CREB at the Proximal IL-2 Promoter in IL-2 Up-Regulation. J. Immunol. 178: 7720-7729 [Abstract] [Full Text]  
  • Barry, A. P., Silvestri, G., Safrit, J. T., Sumpter, B., Kozyr, N., McClure, H. M., Staprans, S. I., Feinberg, M. B. (2007). Depletion of CD8+ Cells in Sooty Mangabey Monkeys Naturally Infected with Simian Immunodeficiency Virus Reveals Limited Role for Immune Control of Virus Replication in a Natural Host Species. J. Immunol. 178: 8002-8012 [Abstract] [Full Text]  
  • Brown, C. R., Czapiga, M., Kabat, J., Dang, Q., Ourmanov, I., Nishimura, Y., Martin, M. A., Hirsch, V. M. (2007). Unique Pathology in Simian Immunodeficiency Virus-Infected Rapid Progressor Macaques Is Consistent with a Pathogenesis Distinct from That of Classical AIDS. J. Virol. 81: 5594-5606 [Abstract] [Full Text]  
  • Holmes, D., Knudsen, G., Mackey-Cushman, S., Su, L. (2007). FoxP3 Enhances HIV-1 Gene Expression by Modulating NF{kappa}B Occupancy at the Long Terminal Repeat in Human T Cells. J. Biol. Chem. 282: 15973-15980 [Abstract] [Full Text]  
  • Pereira, L. E., Villinger, F., Onlamoon, N., Bryan, P., Cardona, A., Pattanapanysat, K., Mori, K., Hagen, S., Picker, L., Ansari, A. A. (2007). Simian Immunodeficiency Virus (SIV) Infection Influences the Level and Function of Regulatory T Cells in SIV-Infected Rhesus Macaques but Not SIV-Infected Sooty Mangabeys. J. Virol. 81: 4445-4456 [Abstract] [Full Text]  
  • Vanderford, T. H., Demma, L. J., Feinberg, M. B., Staprans, S. I., Logsdon, J. M. Jr (2007). Adaptation of a Diverse Simian Immunodeficiency Virus Population to a New Host Is Revealed through a Systematic Approach to Identify Amino Acid Sites under Selection. Mol Biol Evol 24: 660-669 [Abstract] [Full Text]  
  • Sumpter, B., Dunham, R., Gordon, S., Engram, J., Hennessy, M., Kinter, A., Paiardini, M., Cervasi, B., Klatt, N., McClure, H., Milush, J. M., Staprans, S., Sodora, D. L., Silvestri, G. (2007). Correlates of Preserved CD4+ T Cell Homeostasis during Natural, Nonpathogenic Simian Immunodeficiency Virus Infection of Sooty Mangabeys: Implications for AIDS Pathogenesis. J. Immunol. 178: 1680-1691 [Abstract] [Full Text]  
  • Pandrea, I., Apetrei, C., Gordon, S., Barbercheck, J., Dufour, J., Bohm, R., Sumpter, B., Roques, P., Marx, P. A., Hirsch, V. M., Kaur, A., Lackner, A. A., Veazey, R. S., Silvestri, G. (2007). Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood 109: 1069-1076 [Abstract] [Full Text]  
  • Cervasi, B., Paiardini, M., Serafini, S., Fraternale, A., Menotta, M., Engram, J., Lawson, B., Staprans, S. I., Piedimonte, G., Perno, C. F., Silvestri, G., Magnani, M. (2006). Administration of Fludarabine-Loaded Autologous Red Blood Cells in Simian Immunodeficiency Virus-Infected Sooty Mangabeys Depletes pSTAT-1-Expressing Macrophages and Delays the Rebound of Viremia after Suspension of Antiretroviral Therapy.. J. Virol. 80: 10335-10345 [Abstract] [Full Text]  
  • VandeWoude, S., Apetrei, C. (2006). Going Wild: Lessons from Naturally Occurring T-Lymphotropic Lentiviruses. Clin. Microbiol. Rev. 19: 728-762 [Abstract] [Full Text]  
  • Dunham, R., Pagliardini, P., Gordon, S., Sumpter, B., Engram, J., Moanna, A., Paiardini, M., Mandl, J. N., Lawson, B., Garg, S., McClure, H. M., Xu, Y.-X., Ibegbu, C., Easley, K., Katz, N., Pandrea, I., Apetrei, C., Sodora, D. L., Staprans, S. I., Feinberg, M. B., Silvestri, G. (2006). The AIDS resistance of naturally SIV-infected sooty mangabeys is independent of cellular immunity to the virus. Blood 108: 209-217 [Abstract] [Full Text]  
  • Pandrea, I., Apetrei, C., Dufour, J., Dillon, N., Barbercheck, J., Metzger, M., Jacquelin, B., Bohm, R., Marx, P. A., Barre-Sinoussi, F., Hirsch, V. M., Muller-Trutwin, M. C., Lackner, A. A., Veazey, R. S. (2006). Simian Immunodeficiency Virus SIVagm.sab Infection of Caribbean African Green Monkeys: a New Model for the Study of SIV Pathogenesis in Natural Hosts.. J. Virol. 80: 4858-4867 [Abstract] [Full Text]  
  • Goldstein, S., Brown, C. R., Ourmanov, I., Pandrea, I., Buckler-White, A., Erb, C., Nandi, J. S., Foster, G. J., Autissier, P., Schmitz, J. E., Hirsch, V. M. (2006). Comparison of Simian Immunodeficiency Virus SIVagmVer Replication and CD4+ T-Cell Dynamics in Vervet and Sabaeus African Green Monkeys.. J. Virol. 80: 4868-4877 [Abstract] [Full Text]  
  • Onanga, R., Souquiere, S., Makuwa, M., Mouinga-Ondeme, A., Simon, F., Apetrei, C., Roques, P. (2006). Primary Simian Immunodeficiency Virus SIVmnd-2 Infection in Mandrills (Mandrillus sphinx).. J. Virol. 80: 3301-3309 [Abstract] [Full Text]  
  • Wang, Z., Metcalf, B., Ribeiro, R. M., McClure, H., Kaur, A. (2006). Th-1-Type Cytotoxic CD8+ T-Lymphocyte Responses to Simian Immunodeficiency Virus (SIV) Are a Consistent Feature of Natural SIV Infection in Sooty Mangabeys. J. Virol. 80: 2771-2783 [Abstract] [Full Text]  
  • Paiardini, M., Cervasi, B., Sumpter, B., McClure, H. M., Sodora, D. L., Magnani, M., Staprans, S. I., Piedimonte, G., Silvestri, G. (2006). Perturbations of Cell Cycle Control in T Cells Contribute to the Different Outcomes of Simian Immunodeficiency Virus Infection in Rhesus Macaques and Sooty Mangabeys. J. Virol. 80: 634-642 [Abstract] [Full Text]  
  • Santiago, M. L., Range, F., Keele, B. F., Li, Y., Bailes, E., Bibollet-Ruche, F., Fruteau, C., Noe, R., Peeters, M., Brookfield, J. F. Y., Shaw, G. M., Sharp, P. M., Hahn, B. H. (2005). Simian Immunodeficiency Virus Infection in Free-Ranging Sooty Mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d'Ivoire: Implications for the Origin of Epidemic Human Immunodeficiency Virus Type 2. J. Virol. 79: 12515-12527 [Abstract] [Full Text]  
  • Herbeuval, J.-P., Hardy, A. W., Boasso, A., Anderson, S. A., Dolan, M. J., Dy, M., Shearer, G. M. (2005). Regulation of TNF-related apoptosis-inducing ligand on primary CD4+ T cells by HIV-1: Role of type I IFN-producing plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. USA 102: 13974-13979 [Abstract] [Full Text]  
  • Munch, J., Schindler, M., Wildum, S., Rucker, E., Bailer, N., Knoop, V., Novembre, F. J., Kirchhoff, F. (2005). Primary Sooty Mangabey Simian Immunodeficiency Virus and Human Immunodeficiency Virus Type 2 nef Alleles Modulate Cell Surface Expression of Various Human Receptors and Enhance Viral Infectivity and Replication. J. Virol. 79: 10547-10560 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»