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 Veazey, R. S.
Right arrow Articles by Lackner, A. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Veazey, R. S.
Right arrow Articles by Lackner, A. A.

 Previous Article  |  Next Article 

Journal of Virology, December 2000, p. 11001-11007, Vol. 74, No. 23
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Dynamics of CCR5 Expression by CD4+ T Cells in Lymphoid Tissues during Simian Immunodeficiency Virus Infection

Ronald S. Veazey,1,* Keith G. Mansfield,2 Irene C. Tham,1 Angela C. Carville,2 Daniel E. Shvetz,1 Amy E. Forand,3 and Andrew A. Lackner1

Divisions of Pathology,1 Primate Medicine,2 and Immunology,3 New England Regional Primate Research Center, Harvard Medical School, Southborough, Massachusetts 01772

Received 19 June 2000/Accepted 7 September 2000

Early viral replication and profound CD4+ T-cell depletion occur preferentially in intestinal tissues of macaques infected with simian immunodeficiency virus (SIV). Here we show that a much higher percentage of CD4+ T cells in the intestine express CCR5 compared with those found in the peripheral blood, spleen, or lymph nodes. In addition, the selectivity and extent of the CD4+ T-cell loss in SIV infection may depend upon these cells coexpressing CCR5 and having a "memory" phenotype (CD45RA-). Following intravenous infection with SIVmac251, memory CD4+ CCR5+ T cells were selectively eliminated within 14 days in all major lymphoid tissues (intestine, spleen, and lymph nodes). However, the effect on CD4+ T-cell numbers was most profound in the intestine, where cells of this phenotype predominate. The CD4+ T cells that remain after 14 days of infection lacked CCR5 and/or were naive (CD45RA+). Furthermore, when animals in the terminal stages of SIV infection (with AIDS) were examined, virtually no CCR5-expressing CD4+ T cells were found in lymphoid tissues, and all of the remaining CD4+ T cells were naive and coexpressed CXCR4. These findings suggest that chemokine receptor usage determines which cells are targeted for SIV infection and elimination in vivo.

* Corresponding author. Present address: Tulane Regional Primate Research Center, 18703 Three Rivers Rd., Covington, LA 70433. Phone: (504) 871-6228. Fax: (504) 893-1352. E-mail: veazey{at}tpc.tulane.edu.

Journal of Virology, December 2000, p. 11001-11007, Vol. 74, No. 23
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • 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]  
  • Wang, X., Das, A., Lackner, A. A., Veazey, R. S., Pahar, B. (2008). Intestinal double-positive CD4+CD8+ T cells of neonatal rhesus macaques are proliferating, activated memory cells and primary targets for SIVMAC251 infection. Blood 112: 4981-4990 [Abstract] [Full Text]  
  • Kader, M., Hassan, W. M., Eberly, M., Piatak, M., Lifson, J. D., Roederer, M., Mattapallil, J. J. (2008). Antiretroviral Therapy prior to Acute Viral Replication Preserves CD4 T Cells in the Periphery but Not in Rectal Mucosa during Acute Simian Immunodeficiency Virus Infection. J. Virol. 82: 11467-11471 [Abstract] [Full Text]  
  • Tasca, S., Ho, S.-H., Cheng-Mayer, C. (2008). R5X4 Viruses Are Evolutionary, Functional, and Antigenic Intermediates in the Pathway of a Simian-Human Immunodeficiency Virus Coreceptor Switch. J. Virol. 82: 7089-7099 [Abstract] [Full Text]  
  • Veazey, R. S., Acierno, P. M., McEvers, K. J., Baumeister, S. H. C., Foster, G. J., Rett, M. D., Newberg, M. H., Kuroda, M. J., Williams, K., Kim, E.-Y., Wolinsky, S. M., Rieber, E. P., Piatak, M. Jr., Lifson, J. D., Montefiori, D. C., Brown, C. R., Hirsch, V. M., Schmitz, J. E. (2008). Increased Loss of CCR5+ CD45RA- CD4+ T Cells in CD8+ Lymphocyte-Depleted Simian Immunodeficiency Virus-Infected Rhesus Monkeys. J. Virol. 82: 5618-5630 [Abstract] [Full Text]  
  • Verhoeven, D., Sankaran, S., Silvey, M., Dandekar, S. (2008). Antiviral Therapy during Primary Simian Immunodeficiency Virus Infection Fails To Prevent Acute Loss of CD4+ T Cells in Gut Mucosa but Enhances Their Rapid Restoration through Central Memory T Cells. J. Virol. 82: 4016-4027 [Abstract] [Full Text]  
  • Monceaux, V., Viollet, L., Petit, F., Cumont, M. C., Kaufmann, G. R., Aubertin, A. M., Hurtrel, B., Silvestri, G., Estaquier, J. (2007). CD4+ CCR5+ T-Cell Dynamics during Simian Immunodeficiency Virus Infection of Chinese Rhesus Macaques. J. Virol. 81: 13865-13875 [Abstract] [Full Text]  
  • Tsukamoto, T., Yuasa, M., Yamamoto, H., Kawada, M., Takeda, A., Igarashi, H., Matano, T. (2007). Induction of CD8+ Cells Able To Suppress CCR5-Tropic Simian Immunodeficiency Virus SIVmac239 Replication by Controlled Infection of CXCR4-Tropic Simian-Human Immunodeficiency Virus in Vaccinated Rhesus Macaques. J. Virol. 81: 11640-11649 [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]  
  • Wilson, D. P., Mattapallil, J. J., Lay, M. D. H., Zhang, L., Roederer, M., Davenport, M. P. (2007). Estimating the Infectivity of CCR5-Tropic Simian Immunodeficiency Virus SIVmac251 in the Gut. J. Virol. 81: 8025-8029 [Abstract] [Full Text]  
  • Belyakov, I. M., Isakov, D., Zhu, Q., Dzutsev, A., Berzofsky, J. A. (2007). A Novel Functional CTL Avidity/Activity Compartmentalization to the Site of Mucosal Immunization Contributes to Protection of Macaques against Simian/Human Immunodeficiency Viral Depletion of Mucosal CD4+ T Cells. J. Immunol. 178: 7211-7221 [Abstract] [Full Text]  
  • Kawada, M., Tsukamoto, T., Yamamoto, H., Takeda, A., Igarashi, H., Watkins, D. I., Matano, T. (2007). Long-Term Control of Simian Immunodeficiency Virus Replication with Central Memory CD4+ T-Cell Preservation after Nonsterile Protection by a Cytotoxic T-Lymphocyte-Based Vaccine. J. Virol. 81: 5202-5211 [Abstract] [Full Text]  
  • Sun, Z., Denton, P. W., Estes, J. D., Othieno, F. A., Wei, B. L., Wege, A. K., Melkus, M. W., Padgett-Thomas, A., Zupancic, M., Haase, A. T., Garcia, J. V. (2007). Intrarectal transmission, systemic infection, and CD4+ T cell depletion in humanized mice infected with HIV-1. JEM 204: 705-714 [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]  
  • Wang, X., Rasmussen, T., Pahar, B., Poonia, B., Alvarez, X., Lackner, A. A., Veazey, R. S. (2007). Massive infection and loss of CD4+ T cells occurs in the intestinal tract of neonatal rhesus macaques in acute SIV infection. Blood 109: 1174-1181 [Abstract] [Full Text]  
  • Zaunders, J. J., Ip, S., Munier, M. L., Kaufmann, D. E., Suzuki, K., Brereton, C., Sasson, S. C., Seddiki, N., Koelsch, K., Landay, A., Grey, P., Finlayson, R., Kaldor, J., Rosenberg, E. S., Walker, B. D., Fazekas de St. Groth, B., Cooper, D. A., Kelleher, A. D., on Behalf of the PHAEDRA Study Team, (2006). Infection of CD127+ (Interleukin-7 Receptor+) CD4+ Cells and Overexpression of CTLA-4 Are Linked to Loss of Antigen-Specific CD4 T Cells during Primary Human Immunodeficiency Virus Type 1 Infection.. J. Virol. 80: 10162-10172 [Abstract] [Full Text]  
  • Abel, K., Pahar, B., Van Rompay, K. K. A., Fritts, L., Sin, C., Schmidt, K., Colon, R., McChesney, M., Marthas, M. L. (2006). Rapid virus dissemination in infant macaques after oral simian immunodeficiency virus exposure in the presence of local innate immune responses.. J. Virol. 80: 6357-6367 [Abstract] [Full Text]  
  • Miyake, A., Ibuki, K., Enose, Y., Suzuki, H., Horiuchi, R., Motohara, M., Saito, N., Nakasone, T., Honda, M., Watanabe, T., Miura, T., Hayami, M. (2006). Rapid dissemination of a pathogenic simian/human immunodeficiency virus to systemic organs and active replication in lymphoid tissues following intrarectal infection.. J. Gen. Virol. 87: 1311-1320 [Abstract] [Full Text]  
  • Ho, S.-h., Shek, L., Gettie, A., Blanchard, J., Cheng-Mayer, C. (2005). V3 Loop-Determined Coreceptor Preference Dictates the Dynamics of CD4+-T-Cell Loss in Simian-Human Immunodeficiency Virus-Infected Macaques. J. Virol. 79: 12296-12303 [Abstract] [Full Text]  
  • Reynolds, M. R., Rakasz, E., Skinner, P. J., White, C., Abel, K., Ma, Z.-M., Compton, L., Napoe, G., Wilson, N., Miller, C. J., Haase, A., Watkins, D. I. (2005). CD8+ T-Lymphocyte Response to Major Immunodominant Epitopes after Vaginal Exposure to Simian Immunodeficiency Virus: Too Late and Too Little. J. Virol. 79: 9228-9235 [Abstract] [Full Text]  
  • Picker, L. J., Hagen, S. I., Lum, R., Reed-Inderbitzin, E. F., Daly, L. M., Sylwester, A. W., Walker, J. M., Siess, D. C., Piatak, M. Jr., Wang, C., Allison, D. B., Maino, V. C., Lifson, J. D., Kodama, T., Axthelm, M. K. (2004). Insufficient Production and Tissue Delivery of CD4+ Memory T Cells in Rapidly Progressive Simian Immunodeficiency Virus Infection. JEM 200: 1299-1314 [Abstract] [Full Text]  
  • Mehandru, S., Poles, M. A., Tenner-Racz, K., Horowitz, A., Hurley, A., Hogan, C., Boden, D., Racz, P., Markowitz, M. (2004). Primary HIV-1 Infection Is Associated with Preferential Depletion of CD4+ T Lymphocytes from Effector Sites in the Gastrointestinal Tract. JEM 200: 761-770 [Abstract] [Full Text]  
  • Brenchley, J. M., Schacker, T. W., Ruff, L. E., Price, D. A., Taylor, J. H., Beilman, G. J., Nguyen, P. L., Khoruts, A., Larson, M., Haase, A. T., Douek, D. C. (2004). CD4+ T Cell Depletion during all Stages of HIV Disease Occurs Predominantly in the Gastrointestinal Tract. JEM 200: 749-759 [Abstract] [Full Text]  
  • Nishimura, Y., Igarashi, T., Donau, O. K., Buckler-White, A., Buckler, C., Lafont, B. A. P., Goeken, R. M., Goldstein, S., Hirsch, V. M., Martin, M. A. (2004). Highly pathogenic SHIVs and SIVs target different CD4+ T cell subsets in rhesus monkeys, explaining their divergent clinical courses. Proc. Natl. Acad. Sci. USA 101: 12324-12329 [Abstract] [Full Text]  
  • Ling, B., Apetrei, C., Pandrea, I., Veazey, R. S., Lackner, A. A., Gormus, B., Marx, P. A. (2004). Classic AIDS in a Sooty Mangabey after an 18-Year Natural Infection. J. Virol. 78: 8902-8908 [Abstract] [Full Text]  
  • Sadjadpour, R., Theodore, T. S., Igarashi, T., Donau, O. K., Plishka, R. J., Buckler-White, A., Martin, M. A. (2004). Induction of Disease by a Molecularly Cloned Highly Pathogenic Simian Immunodeficiency Virus/Human Immunodeficiency Virus Chimera Is Multigenic. J. Virol. 78: 5513-5519 [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]  
  • Igarashi, T., Endo, Y., Nishimura, Y., Buckler, C., Sadjadpour, R., Donau, O. K., Dumaurier, M.-J., Plishka, R. J., Buckler-White, A., Martin, M. A. (2003). Early Control of Highly Pathogenic Simian Immunodeficiency Virus/Human Immunodeficiency Virus Chimeric Virus Infections in Rhesus Monkeys Usually Results in Long-Lasting Asymptomatic Clinical Outcomes. J. Virol. 77: 10829-10840 [Abstract] [Full Text]  
  • Veazey, R. S., Lifson, J. D., Pandrea, I., Purcell, J., Piatak, M. Jr., Lackner, A. A. (2003). Simian Immunodeficiency Virus Infection in Neonatal Macaques. J. Virol. 77: 8783-8792 [Abstract] [Full Text]  
  • LaBonte, J. A., Madani, N., Sodroski, J. (2003). Cytolysis by CCR5-Using Human Immunodeficiency Virus Type 1 Envelope Glycoproteins Is Dependent on Membrane Fusion and Can Be Inhibited by High Levels of CD4 Expression. J. Virol. 77: 6645-6659 [Abstract] [Full Text]  
  • Sugimoto, C., Tadakuma, K., Otani, I., Moritoyo, T., Akari, H., Ono, F., Yoshikawa, Y., Sata, T., Izumo, S., Mori, K. (2003). nef Gene Is Required for Robust Productive Infection by Simian Immunodeficiency Virus of T-Cell-Rich Paracortex in Lymph Nodes. J. Virol. 77: 4169-4180 [Abstract] [Full Text]  
  • Kaur, A., Hale, C. L., Noren, B., Kassis, N., Simon, M. A., Johnson, R. P. (2002). Decreased Frequency of Cytomegalovirus (CMV)-Specific CD4+ T Lymphocytes in Simian Immunodeficiency Virus-Infected Rhesus Macaques: Inverse Relationship with CMV Viremia. J. Virol. 76: 3646-3658 [Abstract] [Full Text]  
  • Jameson, B., Baribaud, F., Pohlmann, S., Ghavimi, D., Mortari, F., Doms, R. W., Iwasaki, A. (2002). Expression of DC-SIGN by Dendritic Cells of Intestinal and Genital Mucosae in Humans and Rhesus Macaques. J. Virol. 76: 1866-1875 [Abstract] [Full Text]  
  • Pitcher, C. J., Hagen, S. I., Walker, J. M., Lum, R., Mitchell, B. L., Maino, V. C., Axthelm, M. K., Picker, L. J. (2002). Development and Homeostasis of T Cell Memory in Rhesus Macaque. J. Immunol. 168: 29-43 [Abstract] [Full Text]  
  • Schmitz, J. E., Veazey, R. S., Kuroda, M. J., Levy, D. B., Seth, A., Mansfield, K. G., Nickerson, C. E., Lifton, M. A., Alvarez, X., Lackner, A. A., Letvin, N. L. (2001). Simian immunodeficiency virus (SIV)-specific cytotoxic T lymphocytes in gastrointestinal tissues of chronically SIV-infected rhesus monkeys. Blood 98: 3757-3761 [Abstract] [Full Text]  
  • Veazey, R. S., Gauduin, M.-C., Mansfield, K. G., Tham, I. C., Altman, J. D., Lifson, J. D., Lackner, A. A., Johnson, R. P. (2001). Emergence and Kinetics of Simian Immunodeficiency Virus-Specific CD8+ T Cells in the Intestines of Macaques during Primary Infection. J. Virol. 75: 10515-10519 [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»