J. Exp. Med., Volume 187, Number 9, May 4, 1998 1373-1381

Analysis of Gag-specific Cytotoxic T Lymphocytes in Simian Immunodeficiency Virus-infected Rhesus Monkeys by Cell Staining with a Tetrameric Major Histocompatibility Complex Class I-Peptide Complex

By Marcelo J. Kuroda,^* Jörn E. Schmitz,^* Dan H. Barouch,^* Abie Craiu,^* Todd M. Allen,^§ Alessandro Sette, David I. Watkins,^§ Meryl A. Forman,^¶ and Norman L. Letvin^*

From the ^* Harvard Medical School, Division of Viral Pathogenesis, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, Massachusetts 02215;  Wisconsin Regional Primate Research Center and ^§ Department of Pathology and Laboratory Medicine, University of Wisconsin, Madison, Wisconsin 53715;  Eppimune, San Diego, California 92121; and the ^¶ Coulter Corporation, Miami, Florida 33116

A tetrameric recombinant major histocompatibility complex (MHC) class I-peptide complex was used as a staining reagent in flow cytometric analyses to quantitate and define the phenotype of Gag-specific cytotoxic T lymphocytes (CTLs) in the peripheral blood of simian immunodeficiency virus macaque (SIVmac)-infected rhesus monkeys. The heavy chain of the rhesus monkey MHC class I molecule Mamu-A*01 and ₂-microglobulin were refolded in the presence of an SIVmac Gag synthetic peptide (p11C, C-M) representing the optimal nine-amino acid peptide of Mamu-A*01-restricted predominant CTL epitope to create a tetrameric Mamu-A*01/p11C, C-M complex. Tetrameric Mamu-A*01/p11C, C-M complex bound to T cells of SIVmac-infected, Mamu-A*01⁺, but not uninfected, Mamu-A*01⁺, or infected, Mamu-A*01 rhesus monkeys. Specific staining of peripheral blood mononuclear cells (PBMC) from SIVmac-infected, Mamu-A*01⁺ rhesus monkeys was only found in the cluster of differentiation (CD)8/⁺ T lymphocyte subset and the percentage of CD8/⁺ T cells in the peripheral blood of four SIVmac-infected, Mamu-A*01⁺ rhesus monkeys staining with this complex ranged from 0.7 to 10.3%. Importantly, functional SIVmac Gag p11C-specific CTL activity was seen in sorted and expanded tetrameric Mamu-A*01/p11C, C-M complex-binding, but not nonbinding, CD8/⁺ T cells. Furthermore, the percentage of CD8/⁺ T cells binding this tetrameric Mamu-A*01/p11C, C-M complex correlated well with p11C-specific cytotoxic activity as measured in both bulk and limiting dilution effector frequency assays. Finally, phenotypic characterization of the cells binding this tetrameric complex indicated that this lymphocyte population is heterogeneous. These studies indicate the power of this approach for examining virus-specific CTLs in in vivo settings.

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• 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]  
• Dzuris, J. L., Sidney, J., Horton, H., Correa, R., Carter, D., Chesnut, R. W., Watkins, D. I., Sette, A. (2001). Molecular Determinants of Peptide Binding to Two Common Rhesus Macaque Major Histocompatibility Complex Class II Molecules. J. Virol. 75: 10958-10968 [Abstract] [Full Text]  
• Charini, W. A., Kuroda, M. J., Schmitz, J. E., Beaudry, K. R., Lin, W., Lifton, M. A., Krivulka, G. R., Necker, A., Letvin, N. L. (2001). Clonally Diverse CTL Response to a Dominant Viral Epitope Recognizes Potential Epitope Variants. J. Immunol. 167: 4996-5003 [Abstract] [Full Text]  
• Staats, H. F., Bradney, C. P., Gwinn, W. M., Jackson, S. S., Sempowski, G. D., Liao, H.-X., Letvin, N. L., Haynes, B. F. (2001). Cytokine Requirements for Induction of Systemic and Mucosal CTL After Nasal Immunization. J. Immunol. 167: 5386-5394 [Abstract] [Full Text]  
• Barouch, D. H., Santra, S., Kuroda, M. J., Schmitz, J. E., Plishka, R., Buckler-White, A., Gaitan, A. E., Zin, R., Nam, J.-H., Wyatt, L. S., Lifton, M. A., Nickerson, C. E., Moss, B., Montefiori, D. C., Hirsch, V. M., Letvin, N. L. (2001). Reduction of Simian-Human Immunodeficiency Virus 89.6P Viremia in Rhesus Monkeys by Recombinant Modified Vaccinia Virus Ankara Vaccination. J. Virol. 75: 5151-5158 [Abstract] [Full Text]  
• Targoni, O. S., Baus, J., Hofstetter, H. H., Hesse, M. D., Karulin, A. Y., Boehm, B. O., Forsthuber, T. G., Lehmann, P. V. (2001). Frequencies of Neuroantigen-Specific T Cells in the Central Nervous System Versus the Immune Periphery During the Course of Experimental Allergic Encephalomyelitis. J. Immunol. 166: 4757-4764 [Abstract] [Full Text]  
• Vogel, T. U., Allen, T. M., Altman, J. D., Watkins, D. I. (2001). Functional Impairment of Simian Immunodeficiency Virus-Specific CD8+ T Cells during the Chronic Phase of Infection. J. Virol. 75: 2458-2461 [Abstract] [Full Text]  
• Barouch, D. H., Craiu, A., Santra, S., Egan, M. A., Schmitz, J. E., Kuroda, M. J., Fu, T.-M., Nam, J.-H., Wyatt, L. S., Lifton, M. A., Krivulka, G. R., Nickerson, C. E., Lord, C. I., Moss, B., Lewis, M. G., Hirsch, V. M., Shiver, J. W., Letvin, N. L. (2001). Elicitation of High-Frequency Cytotoxic T-Lymphocyte Responses against both Dominant and Subdominant Simian-Human Immunodeficiency Virus Epitopes by DNA Vaccination of Rhesus Monkeys. J. Virol. 75: 2462-2467 [Abstract] [Full Text]  
• Allen, T. M., Mothé, B. R., Sidney, J., Jing, P., Dzuris, J. L., Liebl, M. E., Vogel, T. U., O'Connor, D. H., Wang, X., Wussow, M. C., Thomson, J. A., Altman, J. D., Watkins, D. I., Sette, A. (2001). CD8+ Lymphocytes from Simian Immunodeficiency Virus-Infected Rhesus Macaques Recognize 14 Different Epitopes Bound by the Major Histocompatibility Complex Class I Molecule Mamu-A*01: Implications for Vaccine Design and Testing. J. Virol. 75: 738-749 [Abstract] [Full Text]  
• Goulder, P. J.R., Tang, Y., Brander, C., Betts, M. R., Altfeld, M., Annamalai, K., Trocha, A., He, S., Rosenberg, E. S., Ogg, G., O'Callaghan, C. A., Kalams, S. A., McKinney, R. E. , Jr., Mayer, K., Koup, R. A., Pelton, S. I., Burchett, S. K., McIntosh, K., Walker, B. D. (2000). Functionally Inert HIV-specific Cytotoxic T Lymphocytes Do Not Play a Major Role in Chronically Infected Adults and Children. JEM 192: 1819-1832 [Abstract] [Full Text]  
• Santra, S., Barouch, D. H., Jackson, S. S., Kuroda, M. J., Schmitz, J. E., Lifton, M. A., Sharpe, A. H., Letvin, N. L. (2000). Functional Equivalency of B7-1 and B7-2 for Costimulating Plasmid DNA Vaccine-Elicited CTL Responses. J. Immunol. 165: 6791-6795 [Abstract] [Full Text]  
• Lim, D.-G., Bieganowska Bourcier, K., Freeman, G. J., Hafler, D. A. (2000). Examination of CD8+ T Cell Function in Humans Using MHC Class I Tetramers: Similar Cytotoxicity but Variable Proliferation and Cytokine Production Among Different Clonal CD8+ T Cells Specific to a Single Viral Epitope. J. Immunol. 165: 6214-6220 [Abstract] [Full Text]  
• Varga, S. M., Wissinger, E. L., Braciale, T. J. (2000). The Attachment (G) Glycoprotein of Respiratory Syncytial Virus Contains a Single Immunodominant Epitope That Elicits Both Th1 and Th2 CD4+ T Cell Responses. J. Immunol. 165: 6487-6495 [Abstract] [Full Text]  
• Barouch, D. H., Santra, S., Schmitz, J. E., Kuroda, M. J., Fu, T.-M., Wagner, W., Bilska, M., Craiu, A., Zheng, X. X., Krivulka, G. R., Beaudry, K., Lifton, M. A., Nickerson, C. E., Trigona, W. L., Punt, K., Freed, D. C., Guan, L., Dubey, S., Casimiro, D., Simon, A., Davies, M.-E., Chastain, M., Strom, T. B., Gelman, R. S., Montefiori, D. C., Lewis, M. G., Emini, E. A., Shiver, J. W., Letvin, N. L. (2000). Control of Viremia and Prevention of Clinical AIDS in Rhesus Monkeys by Cytokine-Augmented DNA Vaccination. Science 290: 486-492 [Abstract] [Full Text]  
• Marshall, N. A., Howe, J. G., Formica, R., Krause, D., Wagner, J. E., Berliner, N., Crouch, J., Pilip, I., Cooper, D., Blazar, B. R., Seropian, S., Pamer, E. G. (2000). Rapid reconstitution of Epstein-Barr virus-specific T lymphocytes following allogeneic stem cell transplantation. Blood 96: 2814-2821 [Abstract] [Full Text]  
• Kuroda, M. J., Schmitz, J. E., Lekutis, C., Nickerson, C. E., Lifton, M. A., Franchini, G., Harouse, J. M., Cheng-Mayer, C., Letvin, N. L. (2000). Human Immunodeficiency Virus Type 1 Envelope Epitope-Specific CD4+ T Lymphocytes in Simian/Human Immunodeficiency Virus-Infected and Vaccinated Rhesus Monkeys Detected Using a Peptide-Major Histocompatibility Complex Class II Tetramer. J. Virol. 74: 8751-8756 [Abstract] [Full Text]  
• Evans, D. T., Jing, P., Allen, T. M., O'Connor, D. H., Horton, H., Venham, J. E., Piekarczyk, M., Dzuris, J., Dykhuzen, M., Mitchen, J., Rudersdorf, R. A., Pauza, C. D., Sette, A., Bontrop, R. E., DeMars, R., Watkins, D. I. (2000). Definition of Five New Simian Immunodeficiency Virus Cytotoxic T-Lymphocyte Epitopes and Their Restricting Major Histocompatibility Complex Class I Molecules: Evidence for an Influence on Disease Progression. J. Virol. 74: 7400-7410 [Abstract] [Full Text]  
• Chen, Z. W., Shen, Y., Kou, Z., Ibegbu, C., Zhou, D., Shen, L., Morrison, P., Bogle, C., McClure, H. M., Nahmias, A. J., Sehgal, P. K., Letvin, N. L. (2000). Prolonged Dominance of Clonally Restricted CD4+ T Cells in Macaques Infected with Simian Immunodeficiency Viruses. J. Virol. 74: 7442-7450 [Abstract] [Full Text]  
• Egan, M. A., Charini, W. A., Kuroda, M. J., Schmitz, J. E., Racz, P., Tenner-Racz, K., Manson, K., Wyand, M., Lifton, M. A., Nickerson, C. E., Fu, T., Shiver, J. W., Letvin, N. L. (2000). Simian Immunodeficiency Virus (SIV) gag DNA-Vaccinated Rhesus Monkeys Develop Secondary Cytotoxic T-Lymphocyte Responses and Control Viral Replication after Pathogenic SIV Infection. J. Virol. 74: 7485-7495 [Abstract] [Full Text]  
• Goulder, P. J. R., Lechner, F., Klenerman, P., McIntosh, K., Walker, B. D. (2000). Characterization of a Novel Respiratory Syncytial Virus-Specific Human Cytotoxic T-Lymphocyte Epitope. J. Virol. 74: 7694-7697 [Abstract] [Full Text]  
• Nielsen, M.-B., Monsurro, V., Migueles, S. A., Wang, E., Perez-Diez, A., Lee, K.-H., Kammula, U., Rosenberg, S. A., Marincola, F. M. (2000). Status of Activation of Circulating Vaccine-Elicited CD8+ T Cells. J. Immunol. 165: 2287-2296 [Abstract] [Full Text]  
• Kuroda, M. J., Schmitz, J. E., Seth, A., Veazey, R. S., Nickerson, C. E., Lifton, M. A., Dailey, P. J., Forman, M. A., Racz, P., Tenner-Racz, K., Letvin, N. L. (2000). Simian immunodeficiency virus-specific cytotoxic T lymphocytes and cell-associated viral RNA levels in distinct lymphoid compartments of SIVmac-infected rhesus monkeys. Blood 96: 1474-1479 [Abstract] [Full Text]  
• Höhn, H., Pilch, H., Günzel, S., Neukirch, C., Freitag, K., Necker, A., Maeurer, M. J. (2000). Human Papillomavirus Type 33 E7 Peptides Presented by HLA-DR*0402 to Tumor-Infiltrating T Cells in Cervical Cancer. J. Virol. 74: 6632-6636 [Abstract] [Full Text]  
• Skinner, P. J., Daniels, M. A., Schmidt, C. S., Jameson, S. C., Haase, A. T. (2000). Cutting Edge: In Situ Tetramer Staining of Antigen-Specific T Cells in Tissues. J. Immunol. 165: 613-617 [Abstract] [Full Text]  
• Schmitz, J. E., Kuroda, M. J., Veazey, R. S., Seth, A., Taylor, W. M., Nickerson, C. E., Lifton, M. A., Dailey, P. J., Forman, M. A., Racz, P., Tenner-Racz, K., Letvin, N. L. (2000). Simian Immunodeficiency Virus (SIV)-Specific CTL Are Present in Large Numbers in Livers of SIV-Infected Rhesus Monkeys. J. Immunol. 164: 6015-6019 [Abstract] [Full Text]  
• Spencer, J. V., Braciale, T. J. (2000). Incomplete CD8+ T Lymphocyte Differentiation as a Mechanism for Subdominant Cytotoxic T Lymphocyte Responses to a Viral Antigen. JEM 191: 1687-1698 [Abstract] [Full Text]  
• Allen, T. M., Vogel, T. U., Fuller, D. H., Mothe, B. R., Steffen, S., Boyson, J. E., Shipley, T., Fuller, J., Hanke, T., Sette, A., Altman, J. D., Moss, B., McMichael, A. J., Watkins, D. I. (2000). Induction of AIDS Virus-Specific CTL Activity in Fresh, Unstimulated Peripheral Blood Lymphocytes from Rhesus Macaques Vaccinated with a DNA Prime/Modified Vaccinia Virus Ankara Boost Regimen. J. Immunol. 164: 4968-4978 [Abstract] [Full Text]  
• Maini, M. K., Boni, C., Lee, C. K., Larrubia, J. R., Reignat, S., Ogg, G. S., King, A. S., Herberg, J., Gilson, R., Alisa, A., Williams, R., Vergani, D., Naoumov, N. V., Ferrari, C., Bertoletti, A. (2000). The Role of Virus-specific CD8+ Cells in Liver Damage and Viral Control during Persistent Hepatitis B Virus Infection. JEM 191: 1269-1280 [Abstract] [Full Text]  
• Seth, A., Ourmanov, I., Schmitz, J. E., Kuroda, M. J., Lifton, M. A., Nickerson, C. E., Wyatt, L., Carroll, M., Moss, B., Venzon, D., Letvin, N. L., Hirsch, V. M. (2000). Immunization with a Modified Vaccinia Virus Expressing Simian Immunodeficiency Virus (SIV) Gag-Pol Primes for an Anamnestic Gag-Specific Cytotoxic T-Lymphocyte Response and Is Associated with Reduction of Viremia after SIV Challenge. J. Virol. 74: 2502-2509 [Abstract] [Full Text]  
• Urvater, J. A., Otting, N., Loehrke, J. H., Rudersdorf, R., Slukvin, I. I., Piekarczyk, M. S., Golos, T. G., Hughes, A. L., Bontrop, R. E., Watkins, D. I. (2000). Mamu-I: A Novel Primate MHC Class I B-Related Locus with Unusually Low Variability. J. Immunol. 164: 1386-1398 [Abstract] [Full Text]  
• Hernandez, J., Lee, P. P., Davis, M. M., Sherman, L. A. (2000). The Use of HLA A2.1/p53 Peptide Tetramers to Visualize the Impact of Self Tolerance on the TCR Repertoire. J. Immunol. 164: 596-602 [Abstract] [Full Text]  
• Yang, J., Lemas, V. M., Flinn, I. W., Krone, C., Ambinder, R. F. (2000). Application of the ELISPOT assay to the characterization of CD8+ responses to Epstein-Barr virus antigens. Blood 95: 241-248 [Abstract] [Full Text]  
• Lee, K.-H., Wang, E., Nielsen, M.-B., Wunderlich, J., Migueles, S., Connors, M., Steinberg, S. M., Rosenberg, S. A., Marincola, F. M. (1999). Increased Vaccine-Specific T Cell Frequency After Peptide-Based Vaccination Correlates with Increased Susceptibility to In Vitro Stimulation But Does Not Lead to Tumor Regression. J. Immunol. 163: 6292-6300 [Abstract] [Full Text]  
• Whelan, J. A., Dunbar, P. R., Price, D. A., Purbhoo, M. A., Lechner, F., Ogg, G. S., Griffiths, G., Phillips, R. E., Cerundolo, V., Sewell, A. K. (1999). Specificity of CTL Interactions with Peptide-MHC Class I Tetrameric Complexes Is Temperature Dependent. J. Immunol. 163: 4342-4348 [Abstract] [Full Text]  
• Furchner, M., Erickson, A. L., Allen, T., Watkins, D. I., Sette, A., Johnson, P. R., Walker, C. M. (1999). The Simian Immunodeficiency Virus Envelope Glycoprotein Contains Two Epitopes Presented by the Mamu-A*01 Class I Molecule. J. Virol. 73: 8035-8039 [Abstract] [Full Text]  
• Dalod, M., Dupuis, M., Deschemin, J.-C., Sicard, D., Salmon, D., Delfraissy, J.-F., Venet, A., Sinet, M., Guillet, J.-G. (1999). Broad, Intense Anti-Human Immunodeficiency Virus (HIV) Ex Vivo CD8+ Responses in HIV Type 1-Infected Patients: Comparison with Anti-Epstein-Barr Virus Responses and Changes during Antiretroviral Therapy. J. Virol. 73: 7108-7116 [Abstract] [Full Text]  
• Hanke, T., Samuel, R. V., Blanchard, T. J., Neumann, V. C., Allen, T. M., Boyson, J. E., Sharpe, S. A., Cook, N., Smith, G. L., Watkins, D. I., Cranage, M. P., McMichael, A. J. (1999). Effective Induction of Simian Immunodeficiency Virus-Specific Cytotoxic T Lymphocytes in Macaques by Using a Multiepitope Gene and DNA Prime-Modified Vaccinia Virus Ankara Boost Vaccination Regimen. J. Virol. 73: 7524-7532 [Abstract] [Full Text]  
• Rees, W., Bender, J., Teague, T. K., Kedl, R. M., Crawford, F., Marrack, P., Kappler, J. (1999). An inverse relationship between T cell receptor affinity and antigen dose during CD4+ T cell responses in vivo and in vitro. Proc. Natl. Acad. Sci. USA 96: 9781-9786 [Abstract] [Full Text]  
• Brochu, S., Rioux-Masse, B., Roy, J., Roy, D.-C., Perreault, C. (1999). Massive Activation-Induced Cell Death of Alloreactive T Cells With Apoptosis of Bystander Postthymic T Cells Prevents Immune Reconstitution in Mice With Graft-Versus-Host Disease. Blood 94: 390-400 [Abstract] [Full Text]  
• Egan, M. A., Kuroda, M. J., Voss, G., Schmitz, J. E., Charini, W. A., Lord, C. I., Forman, M. A., Letvin, N. L. (1999). Use of Major Histocompatibility Complex Class I/Peptide/beta 2M Tetramers To Quantitate CD8+ Cytotoxic T Lymphocytes Specific for Dominant and Nondominant Viral Epitopes in Simian-Human Immunodeficiency Virus-Infected Rhesus Monkeys. J. Virol. 73: 5466-5472 [Abstract] [Full Text]  
• Staprans, S. I., Dailey, P. J., Rosenthal, A., Horton, C., Grant, R. M., Lerche, N., Feinberg, M. B. (1999). Simian Immunodeficiency Virus Disease Course Is Predicted by the Extent of Virus Replication during Primary Infection. J. Virol. 73: 4829-4839 [Abstract] [Full Text]  
• Schmitz, J. E., Simon, M. A., Kuroda, M. J., Lifton, M. A., Ollert, M. W., Vogel, C.-W., Racz, P., Tenner-Racz, K., Scallon, B. J., Dalesandro, M., Ghrayeb, J., Rieber, E. P., Sasseville, V. G., Reimann, K. A. (1999). A Nonhuman Primate Model for the Selective Elimination of CD8+ Lymphocytes Using a Mouse-Human Chimeric Monoclonal Antibody. Am. J. Pathol. 154: 1923-1932 [Abstract] [Full Text]  
• Bousso, P., Levraud, J.-P., Kourilsky, P., Abastado, J.-P. (1999). The Composition of a Primary T Cell Response Is Largely Determined by the Timing of Recruitment of Individual T Cell Clones. JEM 189: 1591-1600 [Abstract] [Full Text]  
• He, X.-S., Rehermann, B., Lopez-Labrador, F. X., Boisvert, J., Cheung, R., Mumm, J., Wedemeyer, H., Berenguer, M., Wright, T. L., Davis, M. M., Greenberg, H. B. (1999). Quantitative analysis of hepatitis C virus-specific CD8+ T cells in peripheral blood and liver using peptide-MHC tetramers. Proc. Natl. Acad. Sci. USA 96: 5692-5697 [Abstract] [Full Text]  
• Kuroda, M. J., Schmitz, J. E., Charini, W. A., Nickerson, C. E., Lifton, M. A., Lord, C. I., Forman, M. A., Letvin, N. L. (1999). Emergence of CTL Coincides with Clearance of Virus During Primary Simian Immunodeficiency Virus Infection in Rhesus Monkeys. J. Immunol. 162: 5127-5133 [Abstract] [Full Text]  

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