Identification of tumor antigens and T-cell epitopes, and its clinical application

Cancer Immunology, Immunotherapy

Volumn 53, Issue 3, 2004, Pages 196-203

  Paschen, Annette ^a   Eichmuller, Stefan ^a   Schadendorf, Dirk ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Epitope; HLA molecule; Immunotherapy; T cell; Tumor antigen

Indexed keywords

ANTIBODY; BETA CATENIN; CANCER VACCINE; CARCINOEMBRYONIC ANTIGEN; CASPASE 8; CYCLIN DEPENDENT KINASE 4; EPITOPE; GLYCOPROTEIN GP 100; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; IMMUNOLOGICAL ADJUVANT; LIGAND; MELAN A; MELANOMA ANTIGEN 1; MELANOMA ANTIGEN 3; MONOPHENOL MONOOXYGENASE; MUCIN 1; PEPTIDE; SURVIVIN; TELOMERASE; TUMOR ANTIGEN; TYROSINASE RELATED PROTEIN 2; UNCLASSIFIED DRUG; VIRUS VECTOR;

ACTIVE IMMUNIZATION; ADOPTIVE TRANSFER; B LYMPHOCYTE; CANCER; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CELLULAR IMMUNITY; DENDRITIC CELL; DNA LIBRARY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HUMAN; IMMUNOGENICITY; LYMPHOCYTE FUNCTION; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TUMOR IMMUNOLOGY; VIRUS RECOMBINANT;

ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; EPITOPES, T-LYMPHOCYTE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS;

EID: 1542357604     PISSN: 03407004     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00262-003-0479-3     Document Type: Review

References (86)

1. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD (2001) IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410:1107
2. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, Topalian SL, Sherry R, Restifo NP, Hubicki AM, Robinson MR, Raffeld M, Duray P, Seipp CA, Rogers-Freezer L, Morton KE, Mavroukakis SA, White DE, Rosenberg SA (2002) Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298:850
3. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, Celis E, Greenberg PD (2002) Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A 99:16168
4. Schoenberger SP, Toes RE, van der Voort EI, Offringa R, Melief CJ (1998) T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393:480
5. Ridge JP, Di Rosa F, Matzinger P (1998) A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature 393:474
6. Bennett SR, Carbone FR, Karamalis F, Flavell RA, Miller JF, Heath WR (1998) Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393:478
7. Probst-Kepper M, Stroobant V, Kridel R, Gaugler B, Landry C, Brasseur F, Cosyns JP, Weynand B, Boon T, Van Den Eynde BJ (2001) An alternative open reading frame of the human macrophage colony-stimulating factor gene is independently translated and codes for an antigenic peptide of 14 amino acids recognized by tumor-infiltrating CD8 T lymphocytes. J Exp Med 193:1189
8. Yewdell JM and Bennink JR (2001) Cut and trim: generating MHC class I peptide ligands. Curr Opin Immunol 13:13
9. Belz GT, Carbone FR, Heath WR (2002) Cross-presentation of antigens by dendritic cells. Crit Rev Immunol 22:439
10. Watts C (2001) Antigen processing in the endocytic compartment. Curr Opin Immunol 13:26
11. Renkvist N, Castelli C, Robbins PF, Parmiani G (2001) A listing of human tumor antigens recognized by T cells. Cancer Immunol Immunother 50:3
12. Bourgault Villada I, Beneton N, Bony C, Connan F, Monsonego J, Bianchi A, Saiag P, Levy JP, Guillet JG, Choppin J (2000) Identification in humans of HPV-16 E6 and E7 protein epitopes recognized by cytolytic T lymphocytes in association with HLA-B18 and determination of the HLA-B18-specific binding motif. Eur J Immunol 30:2281
13. Welters MJ, de Jong A, van den Eeden SJ, van der Hulst JM, Kwappenberg KM, Hassane S, Franken KL, Drijfhout JW, Fleuren GJ, Kenter G, Melief CJ, Offringa R, van der Burg SH (2003) Frequent display of human papillomavirus type 16 E6-specific memory t-Helper cells in the healthy population as witness of previous viral encounter. Cancer Res 63:636
14. Kawakami Y, Eliyahu S, Delgado CH, Robbins PF, Rivoltini L, Topalian SL, Miki T, Rosenberg SA (1994) Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc Natl Acad Sci U S A 91:3515
15. Bakker AB, Schreurs MW, de Boer AJ, Kawakami Y, Rosenberg SA, Adema GJ, Figdor CG (1994) Melanocyte lineage-specific antigen gp100 is recognized by melanoma-derived tumor-infiltrating lymphocytes. J Exp Med 179:1005
16. Brichard V, Van Pel A, Wolfel T, Wolfel C, De Plaen E, Lethe B, Coulie P, Boon T (1993) The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J Exp Med 178:489
17. Wang RF, Appella E, Kawakami Y, Kang X, Rosenberg SA (1996) Identification of TRP-2 as a human tumor antigen recognized by cytotoxic T lymphocytes. J Exp Med 184:2207
18. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, Knuth A, Boon T (1991) A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254:1643
19. Wang RF, Wang X, Atwood AC, Topalian SL, Rosenberg SA (1999) Cloning genes encoding MHC class II-restricted antigens: mutated CDC27 as a tumor antigen. Science 284:1351
20. Wang RF, Wang X, Rosenberg SA (1999) Identification of a novel major histocompatibility complex class II-restricted tumor antigen resulting from a chromosomal rearrangement recognized by CD4(+) T cells. J Exp Med 189:1659
21. Vonderheide RH, Hahn WC, Schultze JL, Nadler LM (1999) The telomerase catalytic subunit is a widely expressed tumor-associated antigen recognized by cytotoxic T lymphocytes. Immunity 10:673
22. Schmitz M, Diestelkoetter P, Weigle B, Schmachtenberg F, Stevanovic S, Ockert D, Rammensee HG, Rieber EP (2000) Generation of survivin-specific CD8+ T effector cells by dendritic cells pulsed with protein or selected peptides. Cancer Res 60:4845
23. Sahin U, Tureci O, Schmitt H, Cochlovius B, Johannes T, Schmits R, Stenner F, Luo G, Schobert I, Pfreundschuh M (1995) Human neoplasms elicit multiple specific immune responses in the autologous host. Proc Natl Acad Sci U S A 92:11810
24. Chen YT, Scanlan MJ, Sahin U, Tureci O, Gure AO, Tsang S, Williamson B, Stockert E, Pfreundschuh M, Old LJ (1997) A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc Natl Acad Sci U S A 94:1914
25. Jager E, Chen YT, Drijfhout JW, Karbach J, Ringhoffer M, Jager D, Arand M, Wada H, Noguchi Y, Stockert E, Old LJ, Knuth A (1998) Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J Exp Med 187:265
26. Jager E, Jager D, Karbach J, Chen YT, Ritter G, Nagata Y, Gnjatic S, Stockert E, Arand M, Old LJ, Knuth A (2000) Identification of NY-ESO-1 epitopes presented by human histocompatibility antigen (HLA)-DRB4*0101-0103 and recognized by CD4(+) T lymphocytes of patients with NY-ESO-1-expressing melanoma. J Exp Med 191:625
27. Zeng G, Touloukian CE, Wang X, Restifo NP, Rosenberg SA, Wang RF (2000) Identification of CD4+ T cell epitopes from NY-ESO-1 presented by HLA-DR molecules. J Immunol 165:1153
28. Jager E, Nagata Y, Gnjatic S, Wada H, Stockert E, Karbach J, Dunbar PR, Lee SY, Jungbluth A, Jager D, Arand M, Ritter G, Cerundolo V, Dupont B, Chen YT, Old LJ, Knuth A (2000) Monitoring CD8 T cell responses to NY-ESO-1: correlation of humoral and cellular immune responses. Proc Natl Acad Sci U S A 97:4760
29. Mischo A, Wadle A, Watzig K, Jager D, Stockert E, Santiago D, Ritter G, Regitz E, Jager E, Knuth A, Old L, Pfreundschuh M, Renner C (2003) Recombinant antigen expression on yeast surface (RAYS) for the detection of serological immune responses in cancer patients. Cancer Immun 3:5
30. Eichmuller S, Usener D, Dummer R, Stein A, Thiel D, Schadendorf D (2001) Serological detection of cutaneous T-cell lymphoma-associated antigens. Proc Natl Acad Sci USA 98:629
31. Usener D, Schadendorf D, Koch J, Dubel S, Eichmuller S (2003) cTAGE: a cutaneous T cell lymphoma associated antigen family with tumor-specific splicing. J Invest Dermatol 121:198
32. Traversari C, van der Bruggen P, Luescher IF, Lurquin C, Chomez P, Van Pel A, De Plaen E, Amar-Costesec A, Boon T (1992) A nonapeptide encoded by human gene MAGE-1 is recognized on HLA-A1 by cytolytic T lymphocytes directed against tumor antigen MZ2-E. J Exp Med 176:1453
33. Lupetti R, Pisarra P, Verrecchia A, Farina C, Nicolini G, Anichini A, Bordignon C, Sensi M, Parmiani G, Traversari C (1998) Translation of a retained intron in tyrosinase-related protein (TRP) 2 mRNA generates a new cytotoxic T lymphocyte (CTL)-defined and shared human melanoma antigen not expressed in normal cells of the melanocytic lineage. J Exp Med 188:1005
34. Castelli C, Tarsini P, Mazzocchi A, Rini F, Rivoltini L, Ravagnani F, Gallino F, Belli F, Parmiani G (1999) Novel HLA-Cw8-restricted T cell epitopes derived from tyrosinase-related protein-2 and gp100 melanoma antigens. J Immunol 162:1739
35. Harada M, Li YF, El-Gamil M, Rosenberg SA, Robbins PF (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
36. Khong HT, Rosenberg SA (2002) Pre-existing immunity to tyrosinase-related protein (TRP)-2, a new TRP-2 isoform, and the NY-ESO-1 melanoma antigen in a patient with a dramatic response to immunotherapy. J Immunol 168:951
37. Sun Y, Song M, Stevanovic S, Jankowiak C, Paschen A, Rammensee HG, Schadendorf D (2000) Identification of a new HLA-A*0201-restricted T-cell epitope from the tyrosinase-related protein 2 (TRP2) melanoma antigen. Int J Cancer 87:399
38. Scheibenbogen C, Sun Y, Keilhoz U, Song M, Stevanovic S, Asemissen AM, Thiel E, Nagorsen D, Rammensee HG, Schadendorf D (2002) Identification of known and novel immunogenic T cell epitopes from tumor antigens recognized by peripheral blood T cells from patients responding to IL-2 based treatment. Int J Cancer 98:409
39. Noppen C, Levy F, Burri L, Zajac P, Remmel E, Schaefer C, Luscher U, Heberer M, Spagnoli GC (2000) Naturally processed and concealed HLA-A2.1-restricted epitopes from tumor-associated antigen tyrosinase-related protein-2. Int J Cancer 87:241
40. Sun Y, Sijts A, Song M, Janke K, Nussbaum A, Kral S, Schirle M, Stevanovic S, Paschen A, Schild H, Kloetzel PM, Schadendorf D (2002) Expression of the proteasome activator PA28 rescues the presentation of a cytotoxic T lymphocyte epitope on human melanoma cells. Cancer Res 62:2875
41. Kessler JH, Beekman NJ, Bres-Vloemans SA, Verdijk P, van Veelen PA, Kloosterman-Joosten AM, Vissers DC, ten Bosch GJ, Kester MG, Sijts A, Wouter Drijfhout J, Ossendorp F, Offringa R, Melief CJ (2001) Efficient identification of novel HLA-A(*)0201-presented cytotoxic T lymphocyte epitopes in the widely expressed tumor antigen PRAME by proteasome-mediated digestion analysis. J Exp Med 193:73
42. Ayyoub M, Stevanovic S, Sahin U, Guillaume P, Servis C, Rimoldi D, Valmori D, Romero P, Cerottini JC, Rammensee HG, Pfreundschuh M, Speiser D, Levy F (2002) Proteasome-assisted identification of a SSX-2-derived epitope recognized by tumor-reactive CTL infiltrating metastatic melanoma. J Immunol 168:1717
43. Pascolo S, Schirle M, Guckel B, Dumrese T, Stumm S, Kayser S, Moris A, Wallwiener D, Rammensee HG, Stevanovic (2001) A MAGE-A1 HLA-A A*0201 epitope identified by mass spectrometry. Cancer Res 61:4072
44. Weinschenk T, Gouttefangeas C, Schirle M, Obermayr F, Walter S, Schoor O, Kurek R, Loeser W, Bichler KH, Wernet D, Stevanovic S, Rammensee HG (2002) Integrated functional genomics approach for the design of patient-individual antitumor vaccines. Cancer Res 62:5818
45. Chaux P, Luiten R, Demotte N, Vantomme V, Stroobant V, Traversari C, Russo V, Schultz E, Cornelis GR, Boon T, van der Bruggen P (1999) Identification of five MAGE-A1 epitopes recognized by cytolytic T lymphocytes obtained by in vitro stimulation with dendritic cells transduced with MAGE-A1. J Immunol 163:2928
46. Robbins PF, El-Gamil M, Li YF, Zeng G, Dudley M, Rosenberg SA (2002) Multiple HLA class II-restricted melanocyte differentiation antigens are recognized by tumor-infiltrating lymphocytes from a patient with melanoma. J Immunol 169:6036
47. Consogno G, Manici S, Facchinetti V, Bachi A, Hammer J, Conti-Fine BM, Rugarli C, Traversari C, Protti MP (2003) Identification of immunodominant regions among promiscuous HLA-DR-restricted CD4+ T-cell epitopes on the tumor antigen MAGE-3. Blood 101:103
48. Schroers R, Huang XF, Hammer J, Zhang J, Chen SY (2002) Identification of HLA DR7-restricted epitopes from human telomerase reverse transcriptase recognized by CD4+ T-helper cells. Cancer Res 62:2600
49. Chaux P, Vantomme V, Stroobant V, Thielemans K, Corthals J, Luiten R, Eggermont AM, Boon T, van der Bruggen P (1999) Identification of MAGE-3 epitopes presented by HLA-DR molecules to CD4(+) T lymphocytes. J Exp Med 189:767
50. Touloukian CE, Leitner WW, Topalian SL, Li YF, Robbins PF, Rosenberg SA, Restifo NP (2000) Identification of a MHC class II-restricted human gp100 epitope using DR4-IE transgenic mice. J Immunol 164:3535
51. Touloukian CE, Leitner WW, Robbins PF, Li YF, Kang X, Lapointe R, Hwu P, Rosenberg SA, Restifo NP (2002) Expression of a "self-"antigen by human tumor cells enhances tumor antigen-specific CD4(+) T-cell function. Cancer Res 62:5144
52. Bowne WB, Srinivasan R, Wolchok JD, Hawkins WG, Blachere NE, Dyall R, Lewis JJ, Houghton AN (1999) Coupling and uncoupling of tumor immunity and autoimmunity. J Exp Med 190:1717
53. Morel S, Levy F, Burlet-Schiltz O, Brasseur F, Probst-Kepper M, Peitrequin AL, Monsarrat B, Van Velthoven R, Cerottini JC, Boon T, Gairin JE, Van den Eynde BJ (2000) Processing of some antigens by the standard proteasome but not by the immunoproteasome results in poor presentation by dendritic cells. Immunity 12:107
54. Schultz ES, Chapiro J, Lurquin C, Claverol S, Burlet-Schiltz O, Warnier G, Russo V, Morel S, Levy F, Boon T, Van den Eynde BJ, van der Bruggen P (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
55. Sijts A, Sun Y, Janek K, Kral S, Paschen A, Schadendorf D, Kloetzel PM (2002) The role of the proteasome activator PA28 in MHC class I antigen processing. Mol Immunol 39:165
56. York IA, Mo AX, Lemerise K, Zeng W, Shen Y, Abraham CR, Saric T, Goldberg AL, Rock KL (2003) The cytosolic endopeptidase, thimet oligopeptidase, destroys antigenic peptides and limits the extent of MHC class I antigen presentation. Immunity 18:429
57. Stoltze L, Schirle M, Schwarz G, Schroter C, Thompson MW, Hersh LB, Kalbacher H, Stevanovic S, Rammensee HG, Schild H (2000) Two new proteases in the MHC class I processing pathway. Nat Immunol 1:413
58. York IA, Chang SC, Saric T, Keys JA, Favreau JM, Goldberg AL, Rock KL (2002) The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat Immunol 3:1177
59. Seifert U, Maranon C, Shmueli A, Desoutter JF, Wesoloski L, Janek K, Henklein P, Diescher S, Andrieu M, de la Salle H, Weinschenk T, Schild H, Laderach D, Galy A, Haas G, Kloetzel PM, Reiss Y, Hosmalin A (2003) An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat Immunol 4:375
60. Saric T, Chang SC, Hattori A, York IA, Markant S, Rock KL, Tsujimoto M, Goldberg AL (2002) An IFN-gamma-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat Immunol 3:1169
61. Parkhurst MR, Salgaller ML, Southwood S, Robbins PF, Sette A, Rosenberg SA, Kawakami Y (1996) Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. J Immunol 157:2539
62. Slansky JE, Rattis FM, Boyd LF, Fahmy T, Jaffee EM, Schneck JP, Margulies DH, Pardoll DM (2000) Enhanced antigen-specific antitumor immunity with altered peptide ligands that stabilize the MHC-peptide-TCR complex. Immunity 13:529
63. Hernandez J, Garcia-Pons F, Lone YC, Firat H, Schmidt JD, Langlade-Demoyen P, Zanetti M (2002) Identification of a human telomerase reverse transcriptase peptide of low affinity for HLA A2.1 that induces cytotoxic T lymphocytes and mediates lysis of tumor cells. Proc Natl Acad Sci U S A 99:12275
64. Rosenberg SA, Yang JC, Schwartzentruber DJ, Hwu P, Marincola FM, Topalian SL, Restifo NP, Dudley ME, Schwarz SL, Spiess PJ, Wunderlich JR, Parkhurst MR, Kawakami Y, Seipp CA, Einhorn JH, White DE (1998) Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat Med 4:321
65. Marchand M, van Baren N, Weynants P, Brichard V, Dreno B, Tessier MH, Rankin E, Parmiani G, Arienti F, Humblet Y, Bourlond A, Vanwijck R, Lienard D, Beauduin M, Dietrich PY, Russo V, Kerger J, Masucci G, Jager E, De Greve J, Atzpodien J, Brasseur F, Coulie PG, van der Bruggen P, Boon T (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
66. Coulie PG, 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 U S A 98:10290
67. Scheibenbogen C, Schmittel A, Keilholz U, Allgäuer T, Hofmann U, Max R, Thiel E, Schadendorf D (2000) Phase II trial for vaccination with tyrosinase peptides and GM-CSF in melanoma. J Immunother 23:275
68. Jager E, Hohn H, Necker A, Forster R, Karbach J, Freitag K, Neukirch C, Castelli C, Salter RD, Knuth A, Maeurer MJ (2002) Peptide-specific CD8+ T-cell evolution in vivo: response to peptide vaccination with Melan-A/MART-1. Int J Cancer 98:376
69. Scheibenbogen C, Schadendorf D, Bechrakis NE, Nagorsen D, Hofmann U, Servetopoulou F, Letsch A, Philipp A, Foerster MH, Schmittel A, Thiel E, Keilholz U (2003) Effects of granulocyte-macrophage colony-stimulating factor and foreign helper protein as immunological adjuvants on the T cell response to vaccination with tyrosinase peptides. Int J Cancer 104:188
70. Nestle FO, Alijagic S, Gilliet M, Sun Y, Grabbe S, Dummer R, Burg G, Schadendorf D (1998) Vaccination of melanoma patients with peptide-or tumor lysate-pulsed dendritic cells. Nat Med 4:328
71. Thurner B, Haendle I, Roder C, Dieckmann D, Keikavoussi P, Jonuleit H, Bender A, Maczek C, Schreiner D, von den Driesch P, Brocker EB, Steinman RM, Enk A, Kampgen E, Schuler G (1999) Vaccination with mage-3A1 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
72. Banchereau J, Palucka AK, Dhodapkar M, Burkeholder S, Taquet N, Rolland A, Taquet S, Coquery S, Wittkowski KM, Bhardwaj N, Pineiro L, Steinman R, Fay J (2001) Immune and clinical responses in patients with metastatic melanoma to CD34(+) progenitor-derived dendritic cell vaccine. Cancer Res 61:6451
73. Schuler-Thurner B, Schultz ES, Berger TG, Weinlich G, Ebner S, Woerl P, Bender A, Feuerstein B, Fritsch PO, Romani N, Schuler G (2002) Rapid induction of tumor-specific type 1 T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells. J Exp Med 195:1279
74. Rosenberg SA, Zhai Y, Yang JC, Schwartzentruber DJ, Hwu P, Marincola FM, Topalian SL, Restifo NP, Seipp CA, Einhorn JH, Roberts B, White DE (1998) Immunizing patients with metastatic melanoma using recombinant adenoviruses encoding MART-1 or gp100 melanoma antigens. J Natl Cancer Inst 90:1894
75. Eder JP, Kantoff PW, Roper K, Xu GX, Bubley GJ, Boyden J, Gritz L, Mazzara G, Oh WK, Arlen P, Tsang KY, Panicali D, Schlom J, Kufe DW (2000) A phase I trial of a recombinant vaccinia virus expressing prostate-specific antigen in advanced prostate cancer. Clin Cancer Res 6:1632
76. Jager E, Ringhoffer M, Karbach J, Arand M, Oesch F, Knuth A (1996) Inverse relationship of melanocyte differentiation antigen expression in melanoma tissues and CD8+ cytotoxic-T-cell responses: evidence for immunoselection of antigen-loss variants in vivo. Int J Cancer 66:470
77. Khong HT, Restifo NP (2002) Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat Immunol 3:999
78. Coulie PG, Bruggen P (2003) T-cell responses of vaccinated cancer patients. Curr Opin Immunol 15:131
79. Boel P, Wildmann C, Sensi ML, Brasseur R, Renauld JC, Coulie P, Boon T, van der Bruggen P (1995) BAGE: a new gene encoding an antigen recognized on human melanomas by cytolytic T lymphocytes. Immunity 2:167
80. Van den Eynde B, Peeters O, De Backer O, Gaugler B, Lucas S, Boon T (1995) A new family of genes coding for an antigen recognized by autologous cytolytic T lymphocytes on a human melanoma. J Exp Med 182:689
81. Wolfel T, Hauer M, Schneider J, Serrano M, Wolfel C, Klehmann-Hieb E, De Plaen E, Hankeln T, Meyer zum Buschenfelde KH, Beach D (1995) A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science 269:1281
82. Coulie PG, Lehmann F, Lethe B, Herman J, Lurquin C, Andrawiss M, Boon T (1995) A mutated intron sequence codes for an antigenic peptide recognized by cytolytic T lymphocytes on a human melanoma. Proc Natl Acad Sci U S A 92:7976
83. Robbins PF, El-Gamil M, Li YF, Kawakami Y, Loftus D, Appella E, Rosenberg SA (1996) A mutated beta-catenin gene encodes a melanoma-specific antigen recognized by tumor infiltrating lymphocytes. J Exp Med 183:1185
84. Mandruzzato S, Brasseur F, Andry G, Boon T, van der Bruggen P (1997) A CASP-8 mutation recognized by cytolytic T lymphocytes on a human head and neck carcinoma. J Exp Med 186:785
85. Domenech N, Henderson RA, Finn OJ (1995) Identification of an HLA-A11-restricted epitope from the tandem repeat domain of the epithelial tumor antigen mucin. J Immunol 155:4766
86. Tsang KY, Zaremba S, Nieroda CA, Zhu MZ, Hamilton JM, Schlom J (1995) Generation of human cytotoxic T cells specific for human carcinoembryonic antigen epitopes from patients immunized with recombinant vaccinia-CEA vaccine. J Natl Cancer Inst 87:982