Vaccine-Induced CD4+ T Cell Responses to MAGE-3 Protein in Lung Cancer Patients

Journal of Immunology

Volumn 172, Issue 5, 2004, Pages 3289-3296

  Atanackovic, Djordje ^a   Altorki, Nasser K ^b   Stockert, Elisabeth ^a   Williamson, Barbara ^a   Jungbluth, Achim A ^a   Ritter, Erika ^a   Santiago, Darren ^a   Ferrara, Cathy A ^b   Matsuo, Mitsutoshi ^a   Selvakumar, Annamalai ^a   Dupont, Bo ^a   Chen, Yao Tseng ^a,b   Hoffman, Eric W ^a   Ritter, Gerd ^a   Old, Lloyd J ^a   Gnjatic, Sacha ^a,c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADJUVANT; ADJUVANT SYSTEM 2B; ALANYLARGINYLGLYCYLPROLYLGLUTAMYLSERYLARGINYLLEUCYLLEUCYLGLUTAMYLPHENYLALAN YLTYROSYLLEUCYLALANYLMETHIONYLPROLYLPHENYLALANYLALANYLTHREONYLPROLYLMETHIONYLGLU TAMYLLEUCYLALANYLARGINYLARGINYLSERYLLEUCINE; CANCER VACCINE; CD4 ANTIGEN; CD8 ANTIGEN; GLUTAMYLVALYLASPARTYLPROLYLISOLEUCYLGLYCYLHISTIDYLLEUCYLTYROSINE; HLA DP ANTIGEN; HLA DP4 ANTIGEN; LEUCYLMETHIONYLTRYPTOPHYLISOLEUCYLTHREONYLGLUTAMINYLCYSTINYLPHENYLALANYLLEU CINE; LYSYLLYSYLLEUCYLLEUCYLTHREONYLGLUTAMINYLHISTIDYLPHENYLALANYLVALYLGLUTAMINYL GLUTAMYLASPARAGINYLTYROSYLLEUCYLGLUTAMYLTYROSINE; MELANOMA ANTIGEN; MELANOMA ANTIGEN 3; PEPTIDE DERIVATIVE; PHENYLALANYLLEUCYLTRYPTOPHYLGLYCYLPROLYLARGINYLALANYLLEUCYLVALINE; PHENYLALANYLTRYPTOPHYLARGINYLGLYCYLGLUTAMYLASPARAGINYLGLYCYLARGINYLLYSYLTHR EONYLARGINYLISOLEUCYLALANYLTYROSYLGLUTAMYLARGINYLMETHIONYLCYSTEINYLASPARAGINYLIS OLEUCYLLYSYLGLYCYLLYSINE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG EFFECT; DRUG TARGETING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VIVO STUDY; LUNG CANCER; LUNG NON SMALL CELL CANCER; METHODOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TREATMENT OUTCOME; VACCINATION;

EID: 10744229438     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.5.3289     Document Type: Article

References (66)

1. Gaugler, B., B. Van den Eynde, P. van der Bruggen, P. Romero, J. J. Gaforio, E. De Plaen, B. Lethé, F. Brasseur, and T. Boon. 1994. Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes. J. Exp. Med. 179:921.
2. Van den Eynde, B. J., and P. van der Bruggen. 1997. T cell defined tumor antigens. Curr. Opin. Immunol. 9:684.
3. Jäger, E., Y. Nagata, S. Gnjatic, H. Wada, E. Stockert, J. Karbach, P. R. Dunbar, S. Y. Lee, A. Jungbluth, D. Jäger, et al. 2000. Monitoring CD8 T cell responses to NY-ESO-1: correlation of humoral and cellular immune responses. Proc. Natl. Acad. Sci. USA 97:4760.
4. + T cell responses against NY-ESO-1 in cancer patients: correlation with antibody responses. Proc. Natl. Acad. Sci. USA 100:8862.
5. Ferlazzo, G., M. Meta, M. Mesiti, G. Cangemi, R. Iemmo, G. Quartarone, E. Fecarotta, C. Semino, G. Pietra, and G. Melioli. 1996. Detection of MAGE-1, -2, and -3 messenger RNA in tissue samples derived from lung and mammary tumors. Ann. NY Acad. Sci. 784:448.
6. Yoshimatsu, T., I. Yoshino, A. Ohgami, M. Takenoyama, T. Hanagiri, K. Nomoto, and K. Yasumoto. 1998. Expression of the melanoma antigen-encoding gene in human lung cancer. J. Surg. Oncol. 67:126.
7. Stockert, E., E. Jäger, Y.-T. Chen, M. J. Scanlan, I. Gout, J. Karbach, M. Arand, A. Knuth, and L. J. Old. 1998. A survey of the humoral immune response of cancer patients to a panel of human tumor antigens. J. Exp. Med. 187:1349.
8. Dhodapkar, M. V., J. W. Young, P. B. Chapman, W. I. Cox, J. F. Fonteneau, S. Amigorena, A. N. Houghton, R. M. Steinman, and N. Bhardwaj. 2000. Paucity of functional T-cell memory to melanoma antigens in healthy donors and melanoma patients. Clin. Cancer Res. 6:4831.
9. Scheibenbogen, C., K.-H. Lee, S. Stevanovic, M. Witzens, M. Willhauck, V. Waldmann, H. Naeher, H.-G. Rammensee, and U. Keilholz. 1997. Analysis of the T cell response to tumor and viral peptide antigens by an IFN-γ-ELISPOT assay. Int. J. Cancer 71:932.
10. Herman, J., P. van der Bruggen, I. F. Luescher, S. Mandruzzato, P. Romero, J. Thonnard, K. Fleischhauer, T. Boon, and P. G. Coulie. 1996. A peptide encoded by the human MAGE3 gene and presented by HLA-B44 induces cytolytic T lymphocytes that recognize tumor cells expressing MAGE3. Immunogenetics 43:377.
11. Fleischhauer, K., D. Fruci, P. Van Endert, J. Herman, S. Tanzarella, H. J. Wallny, P. Coulie, C. Bordignon, and C. Traversari. 1996. Characterization of antigenic peptides presented by HLA-B44 molecules on tumor cells expressing the gene MAGE-3. Int. J. Cancer 68:622.
12. Tanaka, F., T. Fujie, K. Tahara, M. Mori, K. Takesako, A. Sette, E. Celis, and T. Akiyoshi. 1997. Induction of antitumor cytotoxic T lymphocytes with a MAGE-3-encoded synthetic peptide presented by human leukocytes antigen-A24. Cancer Res. 57:4465.
13. Kawashima, I., S. J. Hudson, V. Tsai, S. Southwood, K. Takesako, E. Appella, A. Sette, and E. Cells. 1998. The multi-epitope approach for immunotherapy for cancer: identification of several CTL epitopes from various tumor-associated antigens expressed on solid epithelial tumors. Hum. Immunol. 59:1.
14. Oiso, M., M. Eura, F. Katsura, M. Takiguchi, Y. Sobao, K. Masuyama, M. Nakashima, K. Itoh, and T. Ishikawa. 1999. A newly identified MAGE-3-derived epitope recognized by HLA-A24-restricted cytotoxic T lymphocytes. Int. J. Cancer 81:387.
15. Tanzarella, S., V. Russo, I. Lionello, P. Dalerba, D. Rigatti, C. Bordignon, and C. Traversari. 1999. Identification of a promiscuous T-cell epitope encoded by multiple members of the MAGE family. Cancer Res. 59:2668.
16. Russo, V., S. Tanzarella, P. Dalerba, D. Rigatti, P. Rovere, A. Villa, C. Bordignon, and C. Traversari. 2000. Dendritic cells acquire the MAGE-3 human tumor antigen from apoptotic cells and induce a class I-restricted T cell response. Proc. Natl. Acad. Sci. USA 97:2185.
17. Keogh, E., J. Fikes, S. Southwood, E. Celis, R. Chesnut, and A. Sette. 2001. Identification of new epitopes from four different tumor-associated antigens: recognition of naturally processed epitopes correlates with HLA-A*0201-binding affinity. J. Immunol. 167:787.
18. Schultz, E. S., J. Chapiro, C. Lurquin, S. Claverol, O. Burlet-Schiltz, G. Warnier, V. Russo, S. Morel, F. Levy, T. Boon, et al. 2002. The production of a new MAGE-3 peptide presented to cytolytic T lymphocytes by HLA-B40 requires the immunoproteasome. J. Exp. Med. 195:391.
19. Van der Bruggen, P., J. Bastin, T. Gajewski, P. G. Coulie, P. Boël, C. De Smet, C. Traversari, A. Townsend, and T. Boon. 1994. A peptide encoded by human gene MAGE-3 and presented by HLA-A2 induces cytolytic T lymphocytes that recognize tumor cells expressing MAGE-3. Eur. J. Immunol. 24:3038.
20. Marchand, M., N. van Baren, P. Weynants, V. Brichard, B. Dreno, M. H. Tessier, E. Rankin, G. Parmiani, F. Arienti, Y. Humblet, et al. 1999. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int. J. Cancer 80:219.
21. Marchand, M., N. van Baren, P. Weynants, V. Brichard, B. Dreno, M. H. Tessier, E. Rankin, G. Parmiani, F. Arienti, Y. Humblet, et al. 1999. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int. J. Cancer 80:219.
22. Thurner, B., I. Haendle, C. Roder, D. Dieckmann, P. Keikavoussi, H. Jonuleit, A. Bender, C. Maczek, D. Schreiner, P. von den Driesch, et al. 1999. Vaccination with MAGE-3.A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J. Exp. Med. 190:1669.
23. + hematopoietic progenitor cells. Int. J. Cancer 86:385.
24. + progenitor-derived dendritic cell vaccine. Cancer Res. 61:6451.
25. Keene, J. A., and J. Forman. 1982. Helper activity is required for the in vivo generation of cytotoxic T lymphocytes. J. Exp. Med. 155:768.
26. Husmann, L. A., and M. J. Bevan. 1988. Cooperation between helper T cells and cytotoxic T lymphocyte precursors. Ann. NY Acad. Sci. 532:158.
27. Von Herrath, M. G., M. Yokoyama, J. Dockter, M. B. Oldstone, and J. L. Whitton. 1996. CD4-deficient mice have reduced levels of memory cytotoxic T lymphocytes after immunization and show diminished resistance to subsequent virus challenge. J. Virol. 70:1072.
28. + cytotoxic T-cell responses during chronic viral infection. J. Virol. 68:8056.
29. Walter, E. A., P. D. Greenberg, M. J. Gilbert, R. J. Finch, K. S. Watanabe, E. D. Thomas, and S. R. Riddell. 1995. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N. Engl. J. Med. 333:1038.
30. + T cells in the immune response to melanoma. Cancer Immunol. Immunother. 48:363.
31. Greten, T. F., and E. M. Jaffee. 1999. Cancer vaccines. J. Clin. Oncol. 17:1047.
32. + T lymphocytes. J. Exp. Med. 189:767.
33. + cytotoxic T cells in association with histocompatibility leukocyte antigen DRI 1. J. Exp. Med. 189:871.
34. Kobayashi, H., Y. Song, D. S. Hoon, E. Appella, and E. Celis. 2001. Tumor-reactive T helper lymphocytes recognize a promiscuous MAGE-A3 epitope presented by various major histocompatibility complex class 11 alleles. Cancer Res. 61:4773.
35. + T-cell epitopes on the tumor antigen MAGE-3. Blood 101:1038.
36. + cytolytic T lymphocytes. Cancer Res. 60:6272.
37. Schuler-Thurner, B., E. S. Schultz, T. G. Berger, G. Weinlich, S. Ebner, P. Woerl, A. Bender, B. Feuerstein, P. O. Fritsch, N. Romani, and G. Schuler. 2002. Rapid induction of tumor-specific type I T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells. J. Exp. Med. 195:1279.
38. Marchand, M., C. J. Punt, S. Aamdal, B. Escudier, W. H. Kruit, U. Keilholz, L. Hakansson, N. van Baren, Y. Humblet, P. Mulders, et al. 2003. Immunization of metastatic cancer patients with MAGE-3 protein combined with adjuvant SBAS-2: a clinical report. Eur. J. Cancer 39:70.
39. + T cells that were isolated from a melanoma patient vaccinated with a MAGE-3 protein. J. Immunol. 171:219.
40. + T cell responses against viral and tumor antigens using T cells as novel target APC. J. Immunol. Methods 278:57.
41. Gnjatic, S., Y. Nagata, E. Jäger, E. Stockert, S. Shankara, B. L. Roberts, G. P. Mazzara, S. Y. Lee, P. R. Dunbar, B. DuPont, et al. 2000. Strategy for monitoring T cell responses to NY-ESO-1 in patients with any HLA class I allele. Proc. Natl. Acad. Sci. USA 97:10917.
42. Melief, C. J. 1992. Tumor eradication by adoptive transfer of cytotoxic T lymphocytes. Adv. Cancer Res. 58:143.
43. + T lymphocytes. Proc. Natl. Acad. Sci. USA 96:2982.
44. Stern, B. V., B. O. Boehm, and M. Tary-Lehmann. 2002. Vaccination with tumor peptide in CpG adjuvant protects via IFN-γ-dependent CD4 cell immunity. J. Immunol. 168:6099.
45. + T cell subsets: the role of granule exocytosis. J. Immunol. 151:740.
46. + T lymphocytes, generated by mutant p21-ras (12Val) peptide vaccination of a patient, recognize 12Val-dependent nested epitopes present within the vaccine peptide and kill autologous tumor cells carrying this mutation. Int. J. Cancer 72:784.
47. + T cells kill HLA-class-II-antigen-positive melanoma cells presenting peptide in vitro. Cancer Immunol. Immunother. 48:621.
48. + T cells mediate tumor rejection. J. Immunol. 168:1.
49. Giuntoli, R. L., II, J. Lu, H. Kobayashi, R. Kennedy, and E. Celis. 2002. Direct costimulation of tumor-reactive CTL by helper T cells potentiates their proliferation, survival, and effector function. Clin. Cancer Res. 8:922.
50. + cytotoxic T lymphocytes from human naive precursors: helper effect requirement for efficient primary cytotoxic T lymphocyte induction in vitro. Int. J. Cancer 72:987.
51. Cella, M., D. Scheidegger, K. Palmer-Lehmann, P. Lane, A. Lanzavecchia, and G. Alber. 1996. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184:747.
52. + T-helper and a T-killer cell. Nature 393:474.
53. Schoenberger, S. P., R. E. Toes, E. I. van der Voort, R. Offringa, and C. J. Melief. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393:480.
54. Bennett, S. R., F. R. Carbone, F. Karamalis, R. A. Flavell, J. F. Miller, and W. R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393:478.
55. Diehl, L., A. T. den Boer, S. P. Schoenberger, E. I. van der Voort, T. N. Schumacher, C. J. Melief, R. Offringa, and R. E. Toes. 1999. CD40 activation in vivo overcomes peptide-induced peripheral cytotoxic T-lymphocyte tolerance and augments anti-tumor vaccine efficacy. Nat. Med. 5:774.
56. + T-cell tolerance to T-cell priming through in vivo ligation of CD40. Nat. Med. 5:780.
57. + T cells in the antitumor immune response. J. Exp. Med. 188:2357.
58. Strobel, I., M. Krumbholz, A. Menke, E. Hoffmann, P. R. Dunbar, A. Bender, G. Hobom, A. Steinkasserer, G. Schuler, and R. Grassmann. 2000. Efficient expression of the tumor-associated antigen MAGE-3 in human dendritic cells, using an avian influenza virus vector. Hum. Gene Ther. 11:2207.
59. Celis, E., V. Tsai, C. Crimi, R. DeMars, P. A. Wentworth, R. W. Chesnut, H. M. Grey, A. Sette, and H. M. Serra. 1994. Induction of anti-tumor cytotoxic T lymphocytes in normal humans using primary cultures and synthetic peptide epitopes. Proc. Natl. Acad. Sci. USA 91:2105.
60. Cangemi, G., E. Millo, G. Damonte, C. Semino, G. Pietra, U. Benatti, and G. Melioli. 2000. α-Interferon treatment induces quantitative modifications of HLA class I-associated peptides eluted from cultured cancer cell lines. Tissue Antigens 55:212.
61. Valmori, D., D. Lienard, G. Waanders, D. Rimoldi, J. C. Cerottini, and P. Romero. 1997. Analysis of MAGE-3-specific cytolytic T lymphocytes in human leukocyte antigen-A2 melanoma patients. Cancer Res. 57:735.
62. Valmori, D., U. Gileadi, C. Servis, P. R. Dunbar, J. C. Cerottini, P. Romero, V. Cerundolo, and F. Levy. 1999. Modulation of proteasomal activity required for the generation of a cytotoxic T lymphocyte-defined peptide derived from the tumor antigen MAGE-3. J. Exp. Med. 189:895.
63. Miconnet, I., C. Servis, J. C. Cerottini, P. Romero, and F. Levy. 2000. Amino acid identity and/or position determines the proteasomal cleavage of the HLA-A*0201-restricted peptide tumor antigen MAGE-3 271-279. J. Biol. Chem. 275:26892.
64. Berard, F., P. Blanco, J. Davoust, E. M. Neidhart-Berard, M. Nouri-Shirazi, N. Taquet, D. Rimoldi, J. C. Cerottini, J. Banchereau, and A. K. Palucka. 2000. Cross-priming of naive CD8 T cells against melanoma antigens using dendritic cells loaded with killed allogeneic melanoma cells. J. Exp. Med. 192:1535.
65. + T cells for efficient tumor cell lysis. Cancer Res. 60:4446.
66. Dhodapkar, K. M., J. Krasovsky, B. Williamson, and M. V. Dhodapkar. 2002. Antitumor monoclonal antibodies enhance cross-presentation of cellular antigens and the generation of myeloma-specific killer T cells by dendritic cells. J. Exp. Med. 195:125.