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¹ Aaron Diamond AIDS Research Center and The Rockefeller University, New York, NY 10016
² New York University School of Medicine, New York, NY 10016
³ Bernhard-Nocht Institut Fur Tropenmedizin, 20359 Hamburg, Germany

Address correspondence to Martin Markowitz, Aaron Diamond AIDS Research Center, The Rockefeller University, 455 First Ave., 7th Fl., New York, NY 10016. Phone: (212) 448-5020; Fax: (212) 725-1126; email: mmarkowitz{at}adarc.org

Given its population of CCR5-expressing, immunologically activated CD4⁺ T cells, the gastrointestinal (GI) mucosa is uniquely susceptible to human immunodeficiency virus (HIV)-1 infection. We undertook this study to assess whether a preferential depletion of mucosal CD4⁺ T cells would be observed in HIV-1–infected subjects during the primary infection period, to examine the anatomic subcompartment from which these cells are depleted, and to examine whether suppressive highly active antiretroviral therapy could result in complete immune reconstitution in the mucosal compartment. Our results demonstrate that a significant and preferential depletion of mucosal CD4⁺ T cells compared with peripheral blood CD4⁺ T cells is seen during primary HIV-1 infection. CD4⁺ T cell loss predominated in the effector subcompartment of the GI mucosa, in distinction to the inductive compartment, where HIV-1 RNA was present. Cross-sectional analysis of a cohort of primary HIV-1 infection subjects showed that although chronic suppression of HIV-1 permits near-complete immune recovery of the peripheral blood CD4⁺ T cell population, a significantly greater CD4⁺ T cell loss remains in the GI mucosa, despite up to 5 yr of fully suppressive therapy. Given the importance of the mucosal compartment in HIV-1 pathogenesis, further study to elucidate the significance of the changes observed here is critical.

Key Words: primary HIV-1 • GALT • CD4⁺ T cells

A portion of this data was presented in abstract forms at Digestive Disease Week, May 2004 (New Orleans, LA) and the second international workshop for acute and early HIV-1 infection, May 2004 (Bethesda, MD). No similar paper has been or will be submitted elsewhere.

Abbreviations used in this paper: GALT, gut-associated lymphoid tissue; GI, gastrointestinal; HAART, highly active antiretroviral therapy; MMC, mucosal mononuclear cell; SIV, simian immunodeficiency.

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• Nishimura, Y., Igarashi, T., Buckler-White, A., Buckler, C., Imamichi, H., Goeken, R. M., Lee, W. R., Lafont, B. A. P., Byrum, R., Lane, H. C., Hirsch, V. M., Martin, M. A. (2007). Loss of Naive Cells Accompanies Memory CD4+ T-Cell Depletion during Long-Term Progression to AIDS in Simian Immunodeficiency Virus-Infected Macaques. J. Virol. 81: 893-902 [Abstract] [Full Text]  
• Ji, J., Chen, J. J-Y., Braciale, V. L., Cloyd, M. W. (2007). Apoptosis induced in HIV-1-exposed, resting CD4+ T cells subsequent to signaling through homing receptors is Fas/Fas ligand-mediated. J. Leukoc. Biol. 81: 297-305 [Abstract] [Full Text]  
• Verma-Gandhu, M., Verdu, E. F., Cohen-Lyons, D., Collins, S. M. (2007). Lymphocyte-mediated regulation of beta-endorphin in the myenteric plexus. Am. J. Physiol. Gastrointest. Liver Physiol. 292: G344-G348 [Abstract] [Full Text]  
• Soares, R., Foxall, R., Albuquerque, A., Cortesao, C., Garcia, M., Victorino, R. M. M., Sousa, A. E. (2006). Increased Frequency of Circulating CCR5+ CD4+ T Cells in Human Immunodeficiency Virus Type 2 Infection. J. Virol. 80: 12425-12429 [Abstract] [Full Text]  
• Maheshwari, A., Smythies, L. E., Wu, X., Novak, L., Clements, R., Eckhoff, D., Lazenby, A. J., Britt, W. J., Smith, P. D. (2006). Cytomegalovirus blocks intestinal stroma-induced down-regulation of macrophage HIV-1 infection.. J. Leukoc. Biol. 80: 1111-1117 [Abstract] [Full Text]  
• Epple, H.-J., Loddenkemper, C., Kunkel, D., Troger, H., Maul, J., Moos, V., Berg, E., Ullrich, R., Schulzke, J.-D., Stein, H., Duchmann, R., Zeitz, M., Schneider, T. (2006). Mucosal but not peripheral FOXP3+ regulatory T cells are highly increased in untreated HIV infection and normalize after suppressive HAART. Blood 108: 3072-3078 [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]  
• 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]  
• Zhao, X., Zhang, M., Li, Z., Frankel, F. R. (2006). Vaginal Protection and Immunity after Oral Immunization of Mice with a Novel Vaccine Strain of Listeria monocytogenes Expressing Human Immunodeficiency Virus Type 1 gag.. J. Virol. 80: 8880-8890 [Abstract] [Full Text]  
• Hammer, S. M., Saag, M. S., Schechter, M., Montaner, J. S. G., Schooley, R. T., Jacobsen, D. M., Thompson, M. A., Carpenter, C. C. J., Fischl, M. A., Gazzard, B. G., Gatell, J. M., Hirsch, M. S., Katzenstein, D. A., Richman, D. D., Vella, S., Yeni, P. G., Volberding, P. A. (2006). Treatment for Adult HIV Infection: 2006 Recommendations of the International AIDS Society-USA Panel. JAMA 296: 827-843 [Abstract] [Full Text]  
• Guadalupe, M., Sankaran, S., George, M. D., Reay, E., Verhoeven, D., Shacklett, B. L., Flamm, J., Wegelin, J., Prindiville, T., Dandekar, S. (2006). Viral Suppression and Immune Restoration in the Gastrointestinal Mucosa of Human Immunodeficiency Virus Type 1-Infected Patients Initiating Therapy during Primary or Chronic Infection.. J. Virol. 80: 8236-8247 [Abstract] [Full Text]  
• Mattapallil, J. J., Douek, D. C., Buckler-White, A., Montefiori, D., Letvin, N. L., Nabel, G. J., Roederer, M. (2006). Vaccination preserves CD4 memory T cells during acute simian immunodeficiency virus challenge. JEM 203: 1533-1541 [Abstract] [Full Text]  
• von Messling, V., Svitek, N., Cattaneo, R. (2006). Receptor (SLAM [CD150]) Recognition and the V Protein Sustain Swift Lymphocyte-Based Invasion of Mucosal Tissue and Lymphatic Organs by a Morbillivirus.. J. Virol. 80: 6084-6092 [Abstract] [Full Text]  
• Duvall, M. G., Jaye, A., Dong, T., Brenchley, J. M., Alabi, A. S., Jeffries, D. J., van der Sande, M., Togun, T. O., McConkey, S. J., Douek, D. C., McMichael, A. J., Whittle, H. C., Koup, R. A., Rowland-Jones, S. L. (2006). Maintenance of HIV-Specific CD4+ T Cell Help Distinguishes HIV-2 from HIV-1 Infection.. J. Immunol. 176: 6973-6981 [Abstract] [Full Text]  
• Schacker, T. W., Brenchley, J. M., Beilman, G. J., Reilly, C., Pambuccian, S. E., Taylor, J., Skarda, D., Larson, M., Douek, D. C., Haase, A. T. (2006). Lymphatic Tissue Fibrosis Is Associated with Reduced Numbers of Naive CD4+ T Cells in Human Immunodeficiency Virus Type 1 Infection.. CVI 13: 556-560 [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]  
• Belyakov, I. M., Kuznetsov, V. A., Kelsall, B., Klinman, D., Moniuszko, M., Lemon, M., Markham, P. D., Pal, R., Clements, J. D., Lewis, M. G., Strober, W., Franchini, G., Berzofsky, J. A. (2006). Impact of vaccine-induced mucosal high-avidity CD8+CTLs in delay of AIDS viral dissemination from mucosa. Blood 107: 3258-3264 [Abstract] [Full Text]  
• Herzberg, M.C., Weinberg, A., Wahl, S.M. (2006). (C3) The Oral Epithelial Cell and First Encounters with HIV-1. ADR 19: 158-166 [Abstract] [Full Text]  
• Quigley, M. F., Abel, K., Zuber, B., Miller, C. J., Sandberg, J. K., Shacklett, B. L. (2006). Perforin Expression in the Gastrointestinal Mucosa Is Limited to Acute Simian Immunodeficiency Virus Infection. J. Virol. 80: 3083-3087 [Abstract] [Full Text]  
• Herbeuval, J.-P., Grivel, J.-C., Boasso, A., Hardy, A. W., Chougnet, C., Dolan, M. J., Yagita, H., Lifson, J. D., Shearer, G. M. (2005). CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 106: 3524-3531 [Abstract] [Full Text]  
• Gherardi, M. M., Esteban, M. (2005). Recombinant poxviruses as mucosal vaccine vectors. J. Gen. Virol. 86: 2925-2936 [Abstract] [Full Text]  
• Clay, C. C., Rodrigues, D. S., Harvey, D. J., Leutenegger, C. M., Esser, U. (2005). Distinct Chemokine Triggers and In Vivo Migratory Paths of Fluorescein Dye-Labeled T Lymphocytes in Acutely Simian Immunodeficiency Virus SIVmac251-Infected and Uninfected Macaques. J. Virol. 79: 13759-13768 [Abstract] [Full Text]  
• Papasavvas, E., Sun, J., Luo, Q., Moore, E. C., Thiel, B., MacGregor, R. R., Minty, A., Mounzer, K., Kostman, J. R., Montaner, L. J. (2005). IL-13 Acutely Augments HIV-Specific and Recall Responses from HIV-1-Infected Subjects In Vitro by Modulating Monocytes. J. Immunol. 175: 5532-5540 [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]  
• Sheth, P. M., Danesh, A., Shahabi, K., Rebbapragada, A., Kovacs, C., Dimayuga, R., Halpenny, R., MacDonald, K. S., Mazzulli, T., Kelvin, D., Ostrowski, M., Kaul, R. (2005). HIV-Specific CD8+ Lymphocytes in Semen Are Not Associated with Reduced HIV Shedding. J. Immunol. 175: 4789-4796 [Abstract] [Full Text]  
• Karlsson, I., Grivel, J.-C., Chen, S. S., Karlsson, A., Albert, J., Fenyo, E. M., Margolis, L. B. (2005). Differential Pathogenesis of Primary CCR5-Using Human Immunodeficiency Virus Type 1 Isolates in Ex Vivo Human Lymphoid Tissue. J. Virol. 79: 11151-11160 [Abstract] [Full Text]  
• Zaunders, J. J., Munier, M. L., Kaufmann, D. E., Ip, S., Grey, P., Smith, D., Ramacciotti, T., Quan, D., Finlayson, R., Kaldor, J., Rosenberg, E. S., Walker, B. D., Cooper, D. A., Kelleher, A. D., on behalf of the PHAEDRA Study Team, (2005). Early proliferation of CCR5+ CD38+++ antigen-specific CD4+ Th1 effector cells during primary HIV-1 infection. Blood 106: 1660-1667 [Abstract] [Full Text]  
• Markel, H. (2005). The Search for Effective HIV Vaccines. NEJM 353: 753-757 [Full Text]  
• Rao, S., Hu, S., McHugh, L., Lueders, K., Henry, K., Zhao, Q., Fekete, R. A., Kar, S., Adhya, S., Hamer, D. H. (2005). From the Cover: Toward a live microbial microbicide for HIV: Commensal bacteria secreting an HIV fusion inhibitor peptide. Proc. Natl. Acad. Sci. USA 102: 11993-11998 [Abstract] [Full Text]  
• Golding, H., Khurana, S., Yarovinsky, F., King, L. R., Abdoulaeva, G., Antonsson, L., Owman, C., Platt, E. J., Kabat, D., Andersen, J. F., Sher, A. (2005). CCR5 N-terminal Region Plays a Critical Role in HIV-1 Inhibition by Toxoplasma gondii-derived Cyclophilin-18. J. Biol. Chem. 280: 29570-29577 [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]  
• Nishimura, Y., Brown, C. R., Mattapallil, J. J., Igarashi, T., Buckler-White, A., Lafont, B. A. P., Hirsch, V. M., Roederer, M., Martin, M. A. (2005). Resting naive CD4+ T cells are massively infected and eliminated by X4-tropic simian-human immunodeficiency viruses in macaques. Proc. Natl. Acad. Sci. USA 102: 8000-8005 [Abstract] [Full Text]  
• Gurney, K. B., Elliott, J., Nassanian, H., Song, C., Soilleux, E., McGowan, I., Anton, P. A., Lee, B. (2005). Binding and Transfer of Human Immunodeficiency Virus by DC-SIGN+ Cells in Human Rectal Mucosa. J. Virol. 79: 5762-5773 [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]  
• Veazey, R. S., Lackner, A. A. (2004). Getting to the Guts of HIV Pathogenesis. JEM 200: 697-700 [Abstract] [Full Text]  

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