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,
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Clinical Research Division, Fred Hutchinson Cancer Research Center, and Departments of Medicine and Immunology, University of Washington, Seattle, WA 98109;
The Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA 94305; and
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305
Immunogenic peptides of human tumor Ag have been used to generate antigen-specific CTL. However, the vast majority of these peptide-specific CTL clones are of low avidity and are peptide, but not tumor, reactive. Peptide-MHC tetramers have been shown to bind specific TCRs with sufficient affinity to be useful reagents for flow cytometry. In this paper we demonstrate that peptide-MHC tetramers can also be used to selectively identify high avidity tumor-reactive CTL and enrich, from a heterogeneous population, the subpopulation of peptide-reactive T cells that can lyse tumor targets. The melanoma proteins, MART-1 and gp100, were used to induce potentially tumor-reactive T cells, and the intensity of T cell staining by TCR binding of specific peptide-MHC tetramers was assessed. A range of fluorescence intensity was detected, and the magnitude of tetramer binding was correlated with T cell avidity. The population of peptide-reactive T cells was phenotypically similar with regard to expression of TCR and adhesion molecules, suggesting that this differential avidity for tumor cells reflected differential affinity of the TCR for its peptide-MHC ligand. Sorting, cloning, and expansion of tetramerhigh CTL from a heterogeneous population of peptide-stimulated PBMCs enabled rapid selection of high avidity tumor-reactive CTL clones, which retained their functional and tetramerhigh phenotype on re-expansion. These results demonstrate that the avidity of a T cell for its tumor target is due to the specific affinity of the TCR for its peptide-MHC ligand, that this interaction can be described using peptide-MHC tetramers and used to isolate high avidity tumor-reactive CTL.
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S. Yang, G. P. Linette, S. Longerich, and F. G. Haluska Antimelanoma Activity of CTL Generated from Peripheral Blood Mononuclear Cells After Stimulation with Autologous Dendritic Cells Pulsed with Melanoma gp100 Peptide G209-2M Is Correlated to TCR Avidity J. Immunol., July 1, 2002; 169(1): 531 - 539. [Abstract] [Full Text] [PDF]
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D. Valmori, V. Dutoit, V. Schnuriger, A.-L. Quiquerez, M. J. Pittet, P. Guillaume, V. Rubio-Godoy, P. R. Walker, D. Rimoldi, D. Lienard, et al. Vaccination with a Melan-A Peptide Selects an Oligoclonal T Cell Population with Increased Functional Avidity and Tumor Reactivity J. Immunol., April 15, 2002; 168(8): 4231 - 4240. [Abstract] [Full Text] [PDF]
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 T. F. Greten and J. P. Schneck Development and Use of Multimeric Major Histocompatibility Complex Molecules Clin. Vaccine Immunol., March 1, 2002; 9(2): 216 - 220. [Full Text] [PDF]
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V. Dutoit, V. Rubio-Godoy, M.-A. Doucey, P. Batard, D. Lienard, D. Rimoldi, D. Speiser, P. Guillaume, J.-C. Cerottini, P. Romero, et al. Functional Avidity of Tumor Antigen-Specific CTL Recognition Directly Correlates with the Stability of MHC/Peptide Multimer Binding to TCR J. Immunol., February 1, 2002; 168(3): 1167 - 1171. [Abstract] [Full Text] [PDF]
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M. J. Estcourt, A. J. Ramsay, A. Brooks, S. A. Thomson, C. J. Medveckzy, and I. A. Ramshaw Prime-boost immunization generates a high frequency, high-avidity CD8+ cytotoxic T lymphocyte population Int. Immunol., January 1, 2002; 14(1): 31 - 37. [Abstract] [Full Text] [PDF]
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K. Peggs, S. Verfuerth, A. Pizzey, J. Ainsworth, P. Moss, and S. Mackinnon Characterization of human cytomegalovirus peptide-specific CD8+ T-cell repertoire diversity following in vitro restimulation by antigen-pulsed dendritic cells Blood, January 1, 2002; 99(1): 213 - 223. [Abstract] [Full Text] [PDF]
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T. N. J. Bullock, D. W. Mullins, T. A. Colella, and V. H. Engelhard Manipulation of Avidity to Improve Effectiveness of Adoptively Transferred CD8+ T Cells for Melanoma Immunotherapy in Human MHC Class I-Transgenic Mice J. Immunol., November 15, 2001; 167(10): 5824 - 5831. [Abstract] [Full Text] [PDF]
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P. M. Gray, G. D. Parks, and M. A. Alexander-Miller A Novel CD8-Independent High-Avidity Cytotoxic T-Lymphocyte Response Directed against an Epitope in the Phosphoprotein of the Paramyxovirus Simian Virus 5 J. Virol., November 1, 2001; 75(21): 10065 - 10072. [Abstract] [Full Text] [PDF]
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M. Evans, L. K. Borysiewicz, A. S. Evans, M. Rowe, M. Jones, U. Gileadi, V. Cerundolo, and S. Man Antigen Processing Defects in Cervical Carcinomas Limit the Presentation of a CTL Epitope from Human Papillomavirus 16 E6 J. Immunol., November 1, 2001; 167(9): 5420 - 5428. [Abstract] [Full Text] [PDF]
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A. Lamikanra, Z.-K. Pan, S. N. Isaacs, T.-C. Wu, and Y. Paterson Regression of Established Human Papillomavirus Type 16 (HPV-16) Immortalized Tumors In Vivo by Vaccinia Viruses Expressing Different Forms of HPV-16 E7 Correlates with Enhanced CD8+ T-Cell Responses That Home to the Tumor Site J. Virol., October 15, 2001; 75(20): 9654 - 9664. [Abstract] [Full Text] [PDF]
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W. Kuon, H.-G. Holzhutter, H. Appel, M. Grolms, S. Kollnberger, A. Traeder, P. Henklein, E. Weiss, A. Thiel, R. Lauster, et al. Identification of HLA-B27-Restricted Peptides from the Chlamydia trachomatis Proteome with Possible Relevance to HLA-B27-Associated Diseases J. Immunol., October 15, 2001; 167(8): 4738 - 4746. [Abstract] [Full Text] [PDF]
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K. Y. Tsang, M. Zhu, J. Even, J. Gulley, P. Arlen, and J. Schlom The Infection of Human Dendritic Cells with Recombinant Avipox Vectors Expressing a Costimulatory Molecule Transgene (CD80) to Enhance the Activation of Antigen-specific Cytolytic T Cells Cancer Res., October 1, 2001; 61(20): 7568 - 7576. [Abstract] [Full Text] [PDF]
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J. A. Gebe, E. J. Novak, W. W. Kwok, A. G. Farr, G. T. Nepom, and J. H. Buckner T Cell Selection and Differential Activation on Structurally Related HLA-DR4 Ligands J. Immunol., September 15, 2001; 167(6): 3250 - 3256. [Abstract] [Full Text] [PDF]
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K. Kuzushima, N. Hayashi, H. Kimura, and T. Tsurumi Efficient identification of HLA-A*2402-restricted cytomegalovirus-specific CD8+ T-cell epitopes by a computer algorithm and an enzyme-linked immunospot assay Blood, September 15, 2001; 98(6): 1872 - 1881. [Abstract] [Full Text] [PDF]
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A. G. Cawthon, H. Lu, and M. A. Alexander-Miller Peptide Requirement for CTL Activation Reflects the Sensitivity to CD3 Engagement: Correlation with CD8{alpha}{beta} Versus CD8{alpha}{alpha} Expression J. Immunol., September 1, 2001; 167(5): 2577 - 2584. [Abstract] [Full Text] [PDF]
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V. Dutoit, V. Rubio-Godoy, P.-Y. Dietrich, A.-L. Quiqueres, V. Schnuriger, D. Rimoldi, D. Lienard, D. Speiser, P. Guillaume, P. Batard, et al. Heterogeneous T-Cell Response to MAGE-A10254-262: High Avidity-specific Cytolytic T Lymphocytes Show Superior Antitumor Activity Cancer Res., August 1, 2001; 61(15): 5850 - 5856. [Abstract] [Full Text] [PDF]
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R. W. Tindle, K. Herd, T. Doan, G. Bryson, G. R. Leggatt, P. Lambert, I. H. Frazer, and M. Street Nonspecific Down-Regulation of CD8+ T-Cell Responses in Mice Expressing Human Papillomavirus Type 16 E7 Oncoprotein from the Keratin-14 Promoter J. Virol., July 1, 2001; 75(13): 5985 - 5997. [Abstract] [Full Text] [PDF]
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C. S. Gricks, E. Rawlings, L. Foroni, J. A. Madrigal, and P. L. Amlot Somatically Mutated Regions of Immunoglobulin on Human B-Cell Lymphomas Code for Peptides That Bind to Autologous Major Histocompatibility Complex Class I, Providing a Potential Target for Cytotoxic T Cells Cancer Res., July 1, 2001; 61(13): 5145 - 5152. [Abstract] [Full Text] [PDF]
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E. J. Novak, S. A. Masewicz, A. W. Liu, A. Lernmark, W. W. Kwok, and G. T. Nepom Activated human epitope-specific T cells identified by class II tetramers reside within a CD4high, proliferating subset Int. Immunol., June 1, 2001; 13(6): 799 - 806. [Abstract] [Full Text] [PDF]
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M. A. Derby, J. Wang, D. H. Margulies, and J. A. Berzofsky Two intermediate-avidity cytotoxic T lymphocyte clones with a disparity between functional avidity and MHC tetramer staining Int. Immunol., June 1, 2001; 13(6): 817 - 824. [Abstract] [Full Text] [PDF]
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T. M. Clay, A. C. Hobeika, P. J. Mosca, H. K. Lyerly, and M. A. Morse Assays for Monitoring Cellular Immune Responses to Active Immunotherapy of Cancer Clin. Cancer Res., May 1, 2001; 7(5): 1127 - 1135. [Abstract] [Full Text]
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C. Ohlen, M. Kalos, D. J. Hong, A. C. Shur, and P. D. Greenberg Expression of a Tolerizing Tumor Antigen in Peripheral Tissue Does Not Preclude Recovery of High-Affinity CD8+ T Cells or CTL Immunotherapy of Tumors Expressing the Antigen J. Immunol., February 15, 2001; 166(4): 2863 - 2870. [Abstract] [Full Text] [PDF]
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M. A. Derby, M. A. Alexander-Miller, R. Tse, and J. A. Berzofsky High-Avidity CTL Exploit Two Complementary Mechanisms to Provide Better Protection Against Viral Infection Than Low-Avidity CTL J. Immunol., February 1, 2001; 166(3): 1690 - 1697. [Abstract] [Full Text] [PDF]
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T. O. Cameron, J. R. Cochran, B. Yassine-Diab, R.-P. Sekaly, and L. J. Stern Cutting Edge: Detection of Antigen-Specific CD4+ T Cells by HLA-DR1 Oligomers Is Dependent on the T Cell Activation State J. Immunol., January 15, 2001; 166(2): 741 - 745. [Abstract] [Full Text] [PDF]
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D. Schrama, M. H. Andersen, P. Terheyden, L. Schrøder, L. O. Pedersen, P. t. Straten, and J. C. Becker Oligoclonal T-Cell Receptor Usage of Melanocyte Differentiation Antigen-reactive T Cells in Stage IV Melanoma Patients Cancer Res., January 1, 2001; 61(2): 493 - 496. [Abstract] [Full Text]
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S. M. Smith, R. Brookes, M. R. Klein, A. S. Malin, P. T. Lukey, A. S. King, G. S. Ogg, A. V. S. Hill, and H. M. Dockrell Human CD8+ CTL Specific for the Mycobacterial Major Secreted Antigen 85A J. Immunol., December 15, 2000; 165(12): 7088 - 7095. [Abstract] [Full Text] [PDF]
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D. Rimoldi, V. Rubio-Godoy, V. Dutoit, D. Lienard, S. Salvi, P. Guillaume, D. Speiser, E. Stockert, G. Spagnoli, C. Servis, et al. Efficient Simultaneous Presentation of NY-ESO-1/LAGE-1 Primary and Nonprimary Open Reading Frame-Derived CTL Epitopes in Melanoma J. Immunol., December 15, 2000; 165(12): 7253 - 7261. [Abstract] [Full Text] [PDF]
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C. Yee, J. A. Thompson, P. Roche, D. R. Byrd, P. P. Lee, M. Piepkorn, K. Kenyon, M. M. Davis, S. R. Riddell, and P. D. Greenberg Melanocyte Destruction after Antigen-Specific Immunotherapy of Melanoma: Direct Evidence of T Cell-Mediated Vitiligo J. Exp. Med., December 4, 2000; 192(11): 1637 - 1644. [Abstract] [Full Text] [PDF]
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S. R. Burrows, N. Kienzle, A. Winterhalter, M. Bharadwaj, J. D. Altman, and A. Brooks Peptide-MHC Class I Tetrameric Complexes Display Exquisite Ligand Specificity J. Immunol., December 1, 2000; 165(11): 6229 - 6234. [Abstract] [Full Text] [PDF]
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M.-B. Nielsen, V. Monsurro, S. A. Migueles, E. Wang, A. Perez-Diez, K.-H. Lee, U. Kammula, S. A. Rosenberg, and F. M. Marincola Status of Activation of Circulating Vaccine-Elicited CD8+ T Cells J. Immunol., August 15, 2000; 165(4): 2287 - 2296. [Abstract] [Full Text] [PDF]
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