A novel approach to characterize clonality and differentiation of human melanoma-specific T cell responses: Spontaneous priming and efficient boosting by vaccination

Journal of Immunology

Volumn 177, Issue 2, 2006, Pages 1338-1348

  Speiser, Daniel E ^a   Baumgaertner, Petra ^a   Barbey, Catherine ^a   Rubio Godoy, Verena ^a   Moulin, Alexandre ^b   Corthesy, Patricia ^c   Devevre, Estelle ^a   Dietrich, Pierre Yves ^d   Rimoldi, Donata ^b   Liénard, Danielle ^a   Cerottini, Jean Charles ^b   Romero, Pedro ^a   Rufer, Nathalie ^c  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; CD8 ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; FREUND ADJUVANT; GLUTAMYLLEUCYLALANYLGLYCYLISOLEUCYLGLYCYLISOLEUCYLTHREONYLVALINE; GLYCYLISOLEUCYLLEUCYLGLYCYLPHENYLALANYLVALYLPHENYLALANYLTHREONYLLEUCINE; MATRIX PROTEIN; MELAN A; PEPTIDE DERIVATIVE; T LYMPHOCYTE RECEPTOR; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BINDING AFFINITY; CANCER IMMUNOTHERAPY; CASE REPORT; CD8+ T LYMPHOCYTE; CELL COUNT; CELL KINETICS; CELL SELECTION; CELLULAR IMMUNITY; CLONAL VARIATION; CONTROLLED STUDY; DISEASE COURSE; EFFECTOR CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNIZATION; LYMPHOCYTE CLONE; LYMPHOCYTE DIFFERENTIATION; MELANOMA; MELANOMA CELL; MEMORY T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; T LYMPHOCYTE; TUMOR CELL; VACCINATION;

EID: 33745855138     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.2.1338     Document Type: Article

References (52)

1. Davis, M. M., and P. J. Bjorkman. 1988. T-cell antigen receptor genes and T-cell recognition. Nature 334: 395-402.
2. Kjer-Nielsen, L., C. S. Clements, A. W. Purcell, A. G. Brooks, J. C. Whisstock, S. R. Burrows, J. McCluskey, and J. Rossjohn. 2003. A structural basis for the selection of dominant αβ T cell receptors in antiviral immunity. Immunity 18: 53-64.
3. Stewart-Jones, G. B., A. J. McMichael, J. I. Bell, D. I. Stuart, and E. Y. Jones. 2003. A structural basis for immunodominant human T cell receptor recognition. Nat. Immunol. 4: 657-663.
4. + T cells with a predominant Vβ usage during the primary immune response to HIV. Nature 370: 463-467.
5. Kalams, S. A., R. P. Johnson, A. K. Trocha, M. J. Dynan, H. S. Ngo, R. T. D'Aquila, J. T. Kurnick, and B. D. Walker. 1994. Longitudinal analysis of T cell receptor (TCR) gene usage by human immunodeficiency virus 1 envelope-specific cytotoxic T lymphocyte clones reveals a limited TCR repertoire. J. Exp. Med. 179: 1261-1271.
6. Argaet, V. P., C. W. Schmidt, S. R. Burrows, S. L. Silins, M. G. Kurilla, D. L. Doolan, A. Suhrbier, D. J. Moss, E. Kieff, T. B. Sculley, and I. S. Misko. 1994. Dominant selection of an invariant T cell antigen receptor in response to persistent infection by Epstein-Barr virus. J. Exp. Med. 180: 2335-2340.
7. Wills, M. R., A. J. Carmichael, K. Mynard, X. Jin, M. P. Weekes, B. Plachter, and J. G. Sissons. 1996. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J. Virol. 70: 7569-7579.
8. Lehner, P. J., E. C. Wang, P. A. Moss, S. Williams, K. Platt, S. M. Friedman, J. I. Bell, and L. K. Borysiewicz. 1995. Human HLA-A0201-restricted cytotoxic T lymphocyte recognition of influenza A is dominated by T cells bearing the Vβ 17 gene segment. J. Exp. Med. 181: 79-91.
9. Dong, T., G. Stewart-Jones, N. Chen, P. Easterbrook, X. Xu, L. Papagno, V. Appay, M. Weekes, C. Conlon, C. Spina, et al. 2004. HIV-specific cytotoxic T cells from long-term survivors select a unique T cell receptor. J. Exp. Med. 200: 1547-1557.
10. + T cell populations specific for persistent DNA viruses. J. Exp. Med. 202: 1349-1361.
11. Trautmann, L., M. Rimbert, K. Echasserieau, X. Saulquin, B. Neveu, J. Dechanet, V. Cerundolo, and M. Bonneville. 2005. Selection of T cell clones expressing high-affinity public TCRs within human cytomegalovirus-specific CD8 T cell responses. J. Immunol. 175: 6123-6132.
12. Zippelius, A., P. Batard, V. Rubio-Godoy, G. Bioley, D. Lienard, F. Lejeune, D. Rimoldi, P. Guillaume, N. Meidenbauer, A. Mackensen, et al. 2004. Effector function of human tumor-specific CD8 T cells in melanoma lesions: a state of local functional tolerance. Cancer Res. 64: 2865-2873.
13. Lienard, D., D. Rimoldi, M. Marchand, P. Y. Dietrich, N. van Baren, C. Geldhof, P. Batard, P. Guillaume, M. Ayyoub, M. J. Pittet, et al. 2004. Ex vivo detectable activation of Melan-A-specific T cells correlating with inflammatory skin reactions in melanoma patients vaccinated with peptides in IFA. Cancer Immun. 4: 4.
14. Lonchay, C., P. van der Bruggen, T. Connerotte, T. Hanagiri, P. Coulie, D. Colau, S. Lucas, A. Van Pel, K. Thielemans, N. van Baren, and T. Boon. 2004. Correlation between tumor regression and T cell responses in melanoma patients vaccinated with a MAGE antigen. Proc. Natl. Acad. Sci. USA 101(Suppl. 2): 14631-14638.
15. Stuge, T. B., S. P. Holmes, S. Saharan, A. Tuettenberg, M. Roederer, J. S. Weber, and P. P. Lee. 2004. Diversity and recognition efficiency of T cell responses to cancer. Plos. Med. 1: e28.
16. - effector subset exerting ex vivo tumor-specific cytolytic activity. Cancer Res. 62: 1743-1750.
17. Meidenbauer, N., A. Zippelius, M. J. Pittet, M. Laumer, S. Vogl, J. Heymann, M. Rehli, B. Seliger, S. Schwarz, F. A. Le Gal, et al. 2004. High frequency of functionally active Melan-a-specific T cells in a patient with progressive immunoproteasome-deficient melanoma. Cancer Res. 64: 6319-6326.
18. Speiser, D. E., M. J. Pittet, D. Rimoldi, P. Guillaume, I. F. Luescher, D. Lienard, F. Lejeune, J. C. Cerottini, and P. Romero. 2003. Evaluation of melanoma vaccines with molecularly defined antigens by ex vivo monitoring of tumor-specific T cells. Semin. Cancer Biol. 13: 461-472.
19. Sensi, M., C. Traversari, M. Radrizzani, S. Salvi, C. Maccalli, R. Mortarini, L. Rivoltini, C. Farina, G. Nicolini, T. Wolfel, et al. 1995. Cytotoxic T-lymphocyte clones from different patients display limited T-cell-receptor variable-region gene usage in HLA-A2-restricted recognition of the melanoma antigen Melan-A/MART-1. Proc. Natl. Acad. Sci. USA 92: 5674-5678.
20. Romero, P., N. Gervois, J. Schneider, P. Escobar, D. Valmori, C. Pannetier, A. Steinle, T. Wolfel, D. Lienard, V. Brichard, et al. 1997. Cytolytic T lymphocyte recognition of the immunodominant HLA-A*0201- restricted Melan-A/MART-1 antigenic peptide in melanoma. J. Immunol. 159: 2366-2374.
21. Trautmann, L., N. Labarriere, F. Jotereau, V. Karanikas, N. Gervois, T. Connerotte, P. Coulie, and M. Bonneville. 2002. Dominant TCR Vα usage by virus and tumor-reactive T cells with wide affinity ranges for their specific antigens. Eur. J. Immunol. 32: 3181-3190.
22. Mandruzzato, S., E. Rossi, F. Bernardi, V. Tosello, B. Macino, G. Basso, V. Chiarion-Sileni, C. R. Rossi, C. Montesco, and P. Zanovello. 2002. Large and dissimilar repertoire of Melan-A/MART-1-specific CTL in metastatic lesions and blood of a melanoma patient. J. Immunol. 169: 4017-4024.
23. Karanikas, V., C. Lurquin, D. Colau, N. van Baren, C. De Smet, B. Lethe, T. Connerotte, V. Corbiere, M. A. Demoitie, D. Lienard, et al. 2003. Monoclonal anti-MAGE-3 CTL responses in melanoma patients displaying tumor regression after vaccination with a recombinant canarypox virus. J. Immunol. 171: 4898-4904.
24. Dietrich, P. Y., P. R. Walker, A. L. Quiquerez, G. Perrin, V. Dutoit, D. Lienard, P. Guillaume, J. C. Cerottini, P. Romero, and D. Valmori. 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.
25. Dietrich, P. Y., F. A. Le Gal, V. Dutoit, M. J. Pittet, L. Trautman, A. Zippelius, I. Cognet, V. Widmer, P. R. Walker, O. Michielin, et al. 2003. Prevalent role of TCR α-chain in the selection of the preimmune repertoire specific for a human tumor-associated self-antigen. J. Immunol. 170: 5103-5109.
26. Valmori, D., V. Dutoit, V. Schnuriger, A. L. Quiquerez, M. J. Pittet, P. Guillaume, V. Rubio-Godoy, P. R. Walker, D. Rimoldi, D. Lienard, et al. 2002. Vaccination with a Melan-A peptide selects an oligoclonal T cell population with increased functional avidity and tumor reactivity. J. Immunol. 168: 4231-4240.
27. Germeau, C., W. Ma, F. Schiavetti, C. Lurquin, E. Henry, N. Vigneron, F. Brasseur, B. Lethe, E. De Plaen, T. Velu, et al. 2005. High frequency of antitumor T cells in the blood of melanoma patients before and after vaccination with tumor antigens. J. Exp. Med. 201: 241-248.
28. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
29. + T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8: 379-385.
30. + T subsets with distinct replicative history and partial effector functions. Blood 102: 1779-1787.
31. + T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J. Clin. Invest. 115: 739-746.
32. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96.
33. Romero, P., P. R. Dunbar, D. Valmori, M. Pittet, G. S. Ogg, D. Rimoldi, J. L. Chen, D. Lienard, J. C. Cerottini, and V. Cerundolo. 1998. Ex vivo staining of metastatic lymph nodes by class I major histocompatibility complex tetramers reveals high numbers of antigen-experienced tumor-specific cytolytic T lymphocytes. J. Exp. Med. 188: 1641-1650.
34. + T subsets based on gene expression and replicative history analysis. Methods Mol. Med. 109: 265-284.
35. Arden, B., S. P. Clark, D. Kabelitz, and T. W. Mak. 1995. Human T-cell receptor variable gene segment families. Immunogenetics 42: 455-500.
36. Dumont-Girard, F., E. Roux, R. A. van Lier, G. Hale, C. Helg, B. Chapuis, M. Starobinski, and E. Roosnek. 1998. Reconstitution of the T-cell compartment after bone marrow transplantation: restoration of the repertoire by thymic emigrants. Blood 92: 4464-4471.
37. Chen, Y. T., E. Stockert, A. Jungbluth, S. Tsang, K. A. Coplan, M. J. Scanlan, and L. J. Old. 1996. Serological analysis of Melan-A(MART-1), a melanocyte-specific protein homogeneously expressed in human melanomas. Proc. Natl. Acad. Sci. USA 93: 5915-5919.
38. Rufer, N., W. Dragowska, G. Thornbury, E. Roosnek, and P. M. Lansdorp. 1998. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat. Biotechnol. 16: 743-747.
39. Rufer, N., M. Migliaccio, J. Antonchuk, R. K. Humphries, E. Roosnek, and P. M. Lansdorp. 2001. Transfer of the human telomerase reverse transcriptase (TERT) gene into T lymphocytes results in extension of replicative potential. Blood 98: 597-603.
40. Brady, G., and N. N. Iscove. 1993. Construction of cDNA libraries from single cells. Methods Enzymol. 225: 611-623.
41. Pannetier, C., J. Even, and P. Kourilsky. 1995. T-cell repertoire diversity and clonal expansions in normal and clinical samples. Immunol. Today 16: 176-181.
42. Valmori, D., J. F. Fonteneau, C. M. Lizana, N. Gervois, D. Lienard, D. Rimoldi, V. Jongeneel, F. Jotereau, J. C. Cerottini, and P. Romero. 1998. Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J. Immunol. 160: 1750-1758.
43. Harley, C. B., A. B. Futcher, and C. W. Greider. 1990. Telomeres shorten during ageing of human fibroblasts. Nature 345: 458-460.
44. Weng, N. P., B. L. Levine, C. H. June, and R. J. Hodes. 1995. Human naive and memory T lymphocytes differ in telomeric length and replicative potential. Proc. Natl. Acad. Sci. USA 92: 11091-11094.
45. Rufer, N., T. H. Brummendorf, S. Kolvraa, C. Bischoff, K. Christensen, L. Wadsworth, M. Schulzer, and P. M. Lansdorp. 1999. Telomere fluorescence measurements in granulocytes and T lymphocyte subsets point to a high turnover of hematopoietic stem cells and memory T cells in early childhood. J. Exp. Med. 190: 157-167.
46. Marincola, F. M., E. Wang, M. Herlyn, B. Seliger, and S. Ferrone. 2003. Tumors as elusive targets of T-cell-based active immunotherapy. Trends Immunol. 24: 335-342.
47. Baumgaertner, P., N. Rufer, E. Devevre, L. Derre, D. Rimoldi, C. Geldhof, V. Voelter, D. Lienard, P. Romero, and D. E. Speiser. 2006. Ex vivo detectable human CD8 T-cell responses to cancer-testis antigens. Cancer Res. 66: 1912-1916.
48. + CTL in persons with frequently recurring genital herpes. J. Immunol. 165: 1146-1152.
49. Lim, A., L. Trautmann, M. A. Peyrat, C. Couedel, F. Davodeau, F. Romagne, P. Kourilsky, and M. Bonneville. 2000. Frequent contribution of T cell clonotypes with public TCR features to the chronic response against a dominant EBV-derived epitope: application to direct detection of their molecular imprint on the human peripheral T cell repertoire. J. Immunol. 165: 2001-2011.
50. Dudley, M. E., J. R. Wunderlich, J. C. Yang, R. M. Sherry, S. L. Topalian, N. P. Restifo, R. E. Royal, U. Kammula, D. E. White, S. A. Mavroukakis, et al. 2005. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J. Clin. Oncol. 23: 2346-2357.
51. + T-cell responses to the tumor-specific antigen NY-ESO-1. J. Immunother. 28: 252-257.
52. + T cells by endogenous tumor antigen and peptide vaccines: a comparison to virus-specific T cells. Eur. J. Immunol. 32: 731-741.