High Frequencies of Naive Melan-A/MART-1–specific CD8+ T Cells in a Large Proportion of Human Histocompatibility Leukocyte Antigen (HLA)-A2 Individuals

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© The Rockefeller University Press, 0022-1007/1999/9/705/ $5.00
The Journal of Experimental Medicine, Volume 190, Number 5, September 6, 1999 705-716

High Frequencies of Naive Melan-A/MART-1–specific CD8⁺ T Cells in a Large Proportion of Human Histocompatibility Leukocyte Antigen (HLA)-A2 Individuals

Mikaël J. Pittet^a, Danila Valmori^a, P. Rod Dunbar^c, Daniel E. Speiser^a, Danielle Liénard^a,b, Ferdy Lejeune^b, Katharina Fleischhauer^d, Vincenzo Cerundolo^c, Jean-Charles Cerottini^a, and Pedro Romero^a
^a From the Division of Clinical Onco-Immunology, Ludwig Institute for Cancer Research, Lausanne Branch,
^b Multidisciplinary Oncology Center, Centre Hospitalier Universitaire Vaudois, 1011 Lausanne, Switzerland
^c Institute of Molecular Medicine, Nuffield Department of Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, United Kingdom
^d Tissue Typing Laboratory, Department of Biology and Biotechnology (DIBIT), Istituto Scientifico H.S. Raffaele, 20132 Milano, Italy

Correspondence to: Pedro Romero, Division of Clinical Onco-Immunology, Ludwig Institute for Cancer Research, Centre Hospitalier Universitaire Vaudois – BH 19-602, 1011 Lausanne, Switzerland. Tel:41-21-314-01-78 Fax:41-21-314-74-77 E-mail:pedro.romero{at}isrec.unil.ch.

Using fluorescent HLA-A*0201 tetramers containing the immunodominantMelan-A/MART-1 (Melan-A) tumor-associated antigen (Ag), we previouslyobserved that metastatic lymph nodes of melanoma patients containhigh numbers of Ag-experienced Melan-A–specific cytolyticT lymphocytes (CTLs). In this paper, we enumerated and characterizedex vivo Melan-A–specific cells in peripheral blood samplesfrom both melanoma patients and healthy individuals. High frequencies( $>=$ 1 in 2,500 CD8⁺ T cells) of Melan-A–specific cells werefound in 10 out of 13 patients, and, surprisingly, in 6 outof 10 healthy individuals. Virtually all Melan-A–specificcells from 6 out of 6 healthy individuals and from 7 out of10 patients displayed a naive CD45RA^hi/RO^- phenotype, whereasvariable proportions of Ag-experienced CD45RA^lo/RO⁺ Melan-A–specificcells were observed in the remaining 3 patients. In contrast,ex vivo influenza matrix–specific CTLs from all individualsexhibited a CD45RA^lo/RO⁺ memory phenotype as expected. Ag specificityof tetramer-sorted A2/Melan-A⁺ cells from healthy individualswas confirmed after mitogen-driven expansion. Likewise, functionallimiting dilution analysis and interferon ${gamma}$ ELISPOT assays independentlyconfirmed that most of the Melan-A–specific cells werenot Ag experienced. Thus, it appears that high frequencies ofnaive Melan-A–specific CD8⁺ T cells can be found in alarge proportion of HLA-A*0201⁺ individuals. Furthermore, asdemonstrated for one patient followed over time, dramatic phenotypechanges of circulating Melan-A–specific cells can occurin vivo.

Key Words: melanoma, tetramer, influenza matrix, immunotherapy, tumor immunity

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Blanchet, J.-S., Valmori, D., Dufau, I., Ayyoub, M., Nguyen, C., Guillaume, P., Monsarrat, B., Cerottini, J.-C., Romero, P., Gairin, J. E. (2001). A New Generation of Melan-A/MART-1 Peptides That Fulfill Both Increased Immunogenicity and High Resistance to Biodegradation: Implication for Molecular Anti-Melanoma Immunotherapy. J. Immunol. 167: 5852-5861 [Abstract] [Full Text]
Vonderheide, R. H., Anderson, K. S., Hahn, W. C., Butler, M. O., Schultze, J. L., Nadler, L. M. (2001). Characterization of HLA-A3-restricted Cytotoxic T Lymphocytes Reactive against the Widely Expressed Tumor Antigen Telomerase. Clin. Cancer Res. 7: 3343-3348 [Abstract] [Full Text]
Sutmuller, R. P.M., van Duivenvoorde, L. M., van Elsas, A., Schumacher, T. N.M., Wildenberg, M. E., Allison, J. P., Toes, R. E.M., Offringa, R., Melief, C. J.M. (2001). Synergism of Cytotoxic T Lymphocyte-associated Antigen 4 Blockade and Depletion of CD25+ Regulatory T Cells in Antitumor Therapy Reveals Alternative Pathways for Suppression of Autoreactive Cytotoxic T Lymphocyte Responses. JEM 194: 823-832 [Abstract] [Full Text]
Kedl, R. M., Jordan, M., Potter, T., Kappler, J., Marrack, P., Dow, S. (2001). CD40 stimulation accelerates deletion of tumor-specific CD8+ T cells in the absence of tumor-antigen vaccination. Proc. Natl. Acad. Sci. USA 10.1073/pnas.191371898v1 [Abstract] [Full Text]
Coulie, P. G., Karanikas, V., Colau, D., Lurquin, C., Landry, C., Marchand, M., Dorval, T., Brichard, V., Boon, T. (2001). A monoclonal cytolytic T-lymphocyte response observed in a melanoma patient vaccinated with a tumor-specific antigenic peptide encoded by gene MAGE-3. Proc. Natl. Acad. Sci. USA 10.1073/pnas.161260098v1 [Abstract] [Full Text]
Salio, M., Shepherd, D., Dunbar, P. R., Palmowski, M., Murphy, K., Wu, L., Cerundolo, V. (2001). Mature Dendritic Cells Prime Functionally Superior Melan-A-Specific CD8+ Lymphocytes as Compared with Nonprofessional APC. J. Immunol. 167: 1188-1197 [Abstract] [Full Text]
Tsujimura, K., Obata, Y., Matsudaira, Y., Ozeki, S., Yoshikawa, K., Saga, S., Takahashi, T. (2001). The Binding of Thymus Leukemia (TL) Antigen Tetramers to Normal Intestinal Intraepithelial Lymphocytes and Thymocytes. J. Immunol. 167: 759-764 [Abstract] [Full Text]
Pittet, M. J., Zippelius, A., Speiser, D. E., Assenmacher, M., Guillaume, P., Valmori, D., Lienard, D., Lejeune, F., Cerottini, J.-C., Romero, P. (2001). Ex Vivo IFN-{{gamma}} Secretion by Circulating CD8 T Lymphocytes: Implications of a Novel Approach for T Cell Monitoring in Infectious and Malignant Diseases. J. Immunol. 166: 7634-7640 [Abstract] [Full Text]
Novak, E. J., Liu, A. W., Gebe, J. A., Falk, B. A., Nepom, G. T., Koelle, D. M., Kwok, W. W. (2001). Tetramer-Guided Epitope Mapping: Rapid Identification and Characterization of Immunodominant CD4+ T Cell Epitopes from Complex Antigens. J. Immunol. 166: 6665-6670 [Abstract] [Full Text]
Karanikas, V., Colau, D., Baurain, J.-F., Chiari, R., Thonnard, J., Gutierrez-Roelens, I., Goffinet, C., Schaftingen, E. V., Weynants, P., Boon, T., Coulie, P. G. (2001). High Frequency of Cytolytic T Lymphocytes Directed against a Tumor-specific Mutated Antigen Detectable with HLA Tetramers in the Blood of a Lung Carcinoma Patient with Long Survival. Cancer Res. 61: 3718-3724 [Abstract] [Full Text]
Clay, T. M., Hobeika, A. C., Mosca, P. J., Lyerly, H. K., Morse, M. A. (2001). Assays for Monitoring Cellular Immune Responses to Active Immunotherapy of Cancer. Clin. Cancer Res. 7: 1127-1135 [Abstract] [Full Text]
Dietrich, P.-Y., Walker, P. R., Quiquerez, A.-L., Perrin, G., Dutoit, V., Liénard, D., Guillaume, P., Cerottini, J.-C., Romero, P., Valmori, D. (2001). Melanoma Patients Respond to a Cytotoxic T Lymphocyte-defined Self-Peptide with Diverse and Nonoverlapping T-Cell Receptor Repertoires. Cancer Res. 61: 2047-2054 [Abstract] [Full Text]
Harada, M., Li, Y. F., El-Gamil, M., Rosenberg, S. A., Robbins, P. F. (2001). Use of an in Vitro Immunoselected Tumor Line to Identify Shared Melanoma Antigens Recognized by HLA-A*0201-restricted T Cells. Cancer Res. 61: 1089-1094 [Abstract] [Full Text]
Valmori, D., Dutoit, V., Rubio-Godoy, V., Chambaz, C., Liénard, D., Guillaume, P., Romero, P., Cerottini, J.-C., Rimoldi, D. (2001). Frequent Cytolytic T-Cell Responses to Peptide MAGE-A10254-262 in Melanoma. Cancer Res. 61: 509-512 [Abstract] [Full Text]
Dhodapkar, M. V., Young, J. W., Chapman, P. B., Cox, W. I., Fonteneau, J. F., Amigorena, S., Houghton, A. N., Steinman, R. M., Bhardwaj, N. (2000). Paucity of Functional T-Cell Memory to Melanoma Antigens in Healthy Donors and Melanoma Patients. Clin. Cancer Res. 6: 4831-4838 [Abstract] [Full Text]
Dunbar, P. R., Smith, C. L., Chao, D., Salio, M., Shepherd, D., Mirza, F., Lipp, M., Lanzavecchia, A., Sallusto, F., Evans, A., Russell-Jones, R., Harris, A. L., Cerundolo, V. (2000). A Shift in the Phenotype of Melan-A-Specific CTL Identifies Melanoma Patients with an Active Tumor-Specific Immune Response. J. Immunol. 165: 6644-6652 [Abstract] [Full Text]
Bercovici, N., Duffour, M.-T., Agrawal, S., Salcedo, M., Abastado, J.-P. (2000). New Methods for Assessing T-Cell Responses. CVI 7: 859-864 [Full Text]
Anderson, B. W., Peoples, G. E., Murray, J. L., Gillogly, M. A., Gershenson, D. M., Ioannides, C. G. (2000). Peptide Priming of Cytolytic Activity to HER-2 Epitope 369-377 in Healthy Individuals. Clin. Cancer Res. 6: 4192-4200 [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]
Mylin, L. M., Schell, T. D., Roberts, D., Epler, M., Boesteanu, A., Collins, E. J., Frelinger, J. A., Joyce, S., Tevethia, S. S. (2000). Quantitation of CD8+ T-Lymphocyte Responses to Multiple Epitopes from Simian Virus 40 (SV40) Large T Antigen in C57BL/6 Mice Immunized with SV40, SV40 T-Antigen-Transformed Cells, or Vaccinia Virus Recombinants Expressing Full-Length T Antigen or Epitope Minigenes. J. Virol. 74: 6922-6934 [Abstract] [Full Text]
Valmori, D., Dutoit, V., Liénard, D., Rimoldi, D., Pittet, M. J., Champagne, P., Ellefsen, K., Sahin, U., Speiser, D., Lejeune, F., Cerottini, J.-C., Romero, P. (2000). Naturally Occurring Human Lymphocyte Antigen-A2 Restricted CD8+ T-Cell Response to the Cancer Testis Antigen NY-ESO-1 in Melanoma Patients. Cancer Res. 60: 4499-4506 [Abstract] [Full Text]
Valmori, D., Dutoit, V., Lienard, D., Lejeune, F., Speiser, D., Rimoldi, D., Cerundolo, V., Dietrich, P.-Y., Cerottini, J.-C., Romero, P. (2000). Tetramer-Guided Analysis of TCR {beta}-Chain Usage Reveals a Large Repertoire of Melan-A-Specific CD8+ T Cells in Melanoma Patients. J. Immunol. 165: 533-538 [Abstract] [Full Text]
Baurain, J.-F., Colau, D., van Baren, N., Landry, C., Martelange, V., Vikkula, M., Boon, T., Coulie, P. G. (2000). High Frequency of Autologous Anti-Melanoma CTL Directed Against an Antigen Generated by a Point Mutation in a New Helicase Gene. J. Immunol. 164: 6057-6066 [Abstract] [Full Text]
Whiteside, T. L. (2000). Monitoring of Antigen-Specific Cytolytic T Lymphocytes in Cancer Patients Receiving Immunotherapy. CVI 7: 327-332 [Full Text]
Gajewski, T. F. (2000). Monitoring Specific T-Cell Responses to Melanoma Vaccines: ELISPOT, Tetramers, and Beyond. CVI 7: 141-144 [Full Text]
Ludewig, B., Ochsenbein, A. F., Odermatt, B., Paulin, D., Hengartner, H., Zinkernagel, R. M. (2000). Immunotherapy with Dendritic Cells Directed against Tumor Antigens Shared with Normal Host Cells Results in Severe Autoimmune Disease. JEM 191: 795-804 [Abstract] [Full Text]
Pittet, M. J., Speiser, D. E., Valmori, D., Cerottini, J.-C., Romero, P. (2000). Cutting Edge: Cytolytic Effector Function in Human Circulating CD8+ T Cells Closely Correlates with CD56 Surface Expression. J. Immunol. 164: 1148-1152 [Abstract] [Full Text]
Coulie, P. G., Karanikas, V., Colau, D., Lurquin, C., Landry, C., Marchand, M., Dorval, T., Brichard, V., Boon, T. (2001). A monoclonal cytolytic T-lymphocyte response observed in a melanoma patient vaccinated with a tumor-specific antigenic peptide encoded by gene MAGE-3. Proc. Natl. Acad. Sci. USA 98: 10290-10295 [Abstract] [Full Text]
Kedl, R. M., Jordan, M., Potter, T., Kappler, J., Marrack, P., Dow, S. (2001). CD40 stimulation accelerates deletion of tumor-specific CD8+ T cells in the absence of tumor-antigen vaccination. Proc. Natl. Acad. Sci. USA 98: 10811-10816 [Abstract] [Full Text]
Hislop, A. D., Annels, N. E., Gudgeon, N. H., Leese, A. M., Rickinson, A. B. (2002). Epitope-specific Evolution of Human CD8+ T Cell Responses from Primary to Persistent Phases of Epstein-Barr Virus Infection. JEM 195: 893-905 [Abstract] [Full Text]