Cytolytic T-cell response to the PASD1 cancer testis antigen in patients with diffuse large B-cell lymphoma

British Journal of Haematology

Volumn 146, Issue 4, 2009, Pages 396-407

  Ait Tahar, Kamel ^a   Liggins, Amanda P ^a   Collins, Graham P ^a   Campbell, Andrew ^a   Barnardo, Martin ^b   Lawrie, Charles ^a   Moir, Donald ^c   Hatton, Chris ^a   Banham, Alison H ^a   Pulford, Karen ^a,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CHURCHILL HOSPITAL   (United Kingdom)

^c MILTON KEYNES GENERAL HOSPITAL   (United Kingdom)

^d JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

Cancer testis antigen; Cytotoxic T cell; Diffuse large B cell lymphoma; Immunotherapy; Lymphoma

Indexed keywords

ANTIGEN PASD1; CANCER TESTIS ANTIGEN; GAMMA INTERFERON; HLA A ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; UNCLASSIFIED DRUG;

ARTICLE; B CELL LYMPHOMA; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADULT; AGED; AGED, 80 AND OVER; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; ANTIGENS, NUCLEAR; CELL LINE, TUMOR; CYTOTOXICITY TESTS, IMMUNOLOGIC; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA-A ANTIGENS; HUMANS; IMMUNIZATION; INTERFERON-GAMMA; LYMPHOMA, B-CELL; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; MIDDLE AGED; T-LYMPHOCYTES; T-LYMPHOCYTES, CYTOTOXIC; YOUNG ADULT;

EID: 67749122288     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2009.07761.x     Document Type: Article

References (50)

1. Abramson, J.S. (2007) T-cell/histiocyte-rich B-cell lymphoma and the paradox of the host immune response. Leukemia & Lymphoma, 48, 1670 1671.
2. Adams, S.P., Sahota, S.S., Mijovic, A., Czepulkowski, B., Padua, R.A., Mufti, G.J. Guinn, B.A. (2002) Frequent expression of HAGE in presentation chronic myeloid leukaemias. Leukemia, 16, 2238 2242.
3. Ait-Tahar, K., Cerundolo, V., Banham, A.H., Hatton, C., Blanchard, T.J., Kusec, R., Becker, M., Smith, G.L. Pulford, K. (2006) B and CTL responses to the ALK protein in patients with ALK-positive ALCL. International Journal of Cancer, 118, 688 695.
4. Atanackovic, D., Blum, I., Cao, Y., Wenzel, S., Bartels, K., Faltz, C., Hossfeld, D.K., Hegewisch-Becker, S., Bokemeyer, C. Leuwer, R. (2006) Expression of cancer-testis antigens as possible targets for antigen-specific immunotherapy in head and neck squamous cell carcinoma. Cancer Biology & Therapy, 5, 1218 1225.
5. Atanackovic, D., Arfsten, J., Cao, Y., Gnjatic, S., Schnieders, F., Bartels, K., Schilling, G., Faltz, C., Wolschke, C., Dierlamm, J., Ritter, G., Eiermann, T., Hossfeld, D.K., Zander, A.R., Jungbluth, A.A., Old, L.J., Bokemeyer, C. Kroger, N. (2007) Cancer-testis antigens are commonly expressed in multiple myeloma and induce systemic immunity following allogeneic stem cell transplantation. Blood, 109, 1103 1112.
6. Banham, A.H., Connors, J.M., Brown, P.J., Cordell, J.L., Ott, G., Sreenivasan, G., Farinha, P., Horsman, D.E. Gascoyne, R.D. (2005) Expression of the FOXP1 transcription factor is strongly associated with inferior survival in patients with diffuse large B-cell lymphoma. Clinical Cancer Research, 11, 1065 1072.
7. Barrow, C., Browning, J., MacGregor, D., Davis, I.D., Sturrock, S., Jungbluth, A.A. Cebon, J. (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clinical Cancer Research, 12, 764 771.
8. Baumgaertner, P., Rufer, N., Devevre, E., Derre, L., Rimoldi, D., Geldhof, C., Voelter, V., Lienard, D., Romero, P. Speiser, D.E. (2006) Ex vivo detectable human CD8 T-cell responses to cancer-testis antigens. Cancer Research, 66, 1912 1916.
9. Bunce, M., O'Neill, C.M., Barnardo, M.C., Krausa, P., Browning, M.J., Morris, P.J. Welsh, K.I. (1995) Phototyping: comprehensive DNA typing for HLA-A, B, C, DRB1, DRB3, DRB4, DRB5 & DQB1 by PCR with 144 primer mixes utilizing sequence-specific primers (PCR-SSP). Tissue Antigens, 46, 355 367.
10. Coiffier, D. (2005) State-of-the-art therapeutics: diffuse large B-cell lymphoma. Journal of Clinical Oncology, 23, 6387 6393.
11. Condomines, M., Hose, D., Raynaud, P., Hundemer, M., De Vos, J., Baudard, M., Moehler, T., Pantesco, V., Moos, M., Schved, J.F., Rossi, J.F., Reme, T., Goldschmidt, H. Klein, B. (2007) Cancer/testis genes in multiple myeloma: expression patterns and prognosis value determined by microarray analysis. Journal of Immunology, 178, 3307 3315.
12. Cooper, C.D., Liggins, A.P., Ait-Tahar, K., Roncador, G., Banham, A.H. Pulford, K. (2006) PASD1, a DLBCL-associated cancer testis antigen and candidate for lymphoma immunotherapy. Leukemia, 20, 2172 2174.
13. Dave, S.S., Wright, G., Tan, B., Rosenwald, A., Gascoyne, R.D., Chan, W.C., Fisher, R.I., Braziel, R.M., Rimsza, L.M., Grogan, T.M., Miller, T.P., LeBlanc, M., Greiner, T.C., Weisenburger, D.D., Lynch, J.C., Vose, J., Armitage, J.O., Smeland, E.B., Kvaloy, S., Holte, H., Delabie, J., Connors, J.M., Lansdorp, P.M., Ouyang, Q., Lister, T.A., Davies, A.J., Norton, A.J., Muller-Hermelink, H.K., Ott, G., Campo, E., Montserrat, E., Wilson, W.H., Jaffe, E.S., Simon, R., Yang, L., Powell, J., Zhao, H., Goldschmidt, N., Chiorazzi, M. Staudt, L.M. (2004) Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. The New England Journal of Medicine, 351, 2159 2169.
14. Dhodapkar, M.V., Osman, K., Teruya-Feldstein, J., Filippa, D., Hedvat, C.V., Iversen, K., Kolb, D., Geller, M.D., Hassoun, H., Kewalramani, T., Comenzo, R.L., Coplan, K., Chen, Y.T. Jungbluth, A.A. (2003) Expression of cancer/testis (CT) antigens MAGE-A1, MAGE-A3, MAGE-A4, CT-7, and NY-ESO-1 in malignant gammopathies is heterogeneous and correlates with site, stage and risk status of disease. Cancer Immunity, 3, 9.
15. Eichmuller, S., Usener, D., Thiel, D. Schadendorf, D. (2003) Tumor-specific antigens in cutaneous T-cell lymphoma: expression and sero-reactivity. International Journal of Cancer, 104, 482 487.
16. El Weshi, A., Akhtar, S., Mourad, W.A., Ajarim, D., Abdelsalm, M., Khafaga, Y., Bazarbashi, S. Maghfoor, I. (2007) T-cell/histiocyte-rich B-cell lymphoma: clinical presentation, management and prognostic factors: report on 61 patients and review of literature. Leukemia & Lymphoma, 48, 1764 1773.
17. Goodyear, O., Piper, K., Khan, N., Starczynski, J., Mahendra, P., Pratt, G. Moss, P. (2005) CD8+ T cells specific for cancer germline gene antigens are found in many patients with multiple myeloma, and their frequency correlates with disease burden. Blood, 106, 4217 4224.
18. Guinn, B.A., Bland, E.A., Lodi, U., Liggins, A.P., Tobal, K., Petters, S., Wells, J.W., Banham, A.H. Mufti, G.J. (2005) Humoral detection of leukaemia-associated antigens in presentation acute myeloid leukaemia. Biochemical and Biophysical Research Communications, 335, 1293 1304.
19. Haarer, C.F., Roberts, R.A., Frutiger, Y.M., Grogan, T.M. Rimsza, L.M. (2006) Immunohistochemical classification of de novo, transformed, and relapsed diffuse large B-cell lymphoma into germinal center B-cell and nongerminal center B-cell subtypes correlates with gene expression profile and patient survival. Archives of Pathology & Laboratory Medicine, 130, 1819 1824.
20. Hans, C.P., Weisenburger, D.D., Greiner, T.C., Gascoyne, R.D., Delabie, J., Ott, G., Muller-Hermelink, H.K., Campo, E., Braziel, R.M., Jaffe, E.S., Pan, Z., Farinha, P., Smith, L.M., Falini, B., Banham, A.H., Rosenwald, A., Staudt, L.M., Connors, J.M., Armitage, J.O. Chan, W.C. (2004) Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood, 103, 275 282.
21. Huang, S., Preuss, K.D., Xie, X., Regitz, E. Pfreundschuh, M. (2002) Analysis of the antibody repertoire of lymphoma patients. Cancer Immunology, Immunotherapy, 51, 655 662.
22. Hudolin, T., Juretic, A., Pasini, J., Tomas, D., Spagnoli, G.C., Heberer, M., Dimanovski, J. Kruslin, B. (2006) Immunohistochemical expression of tumor antigens MAGE-A1, MAGE-A3/4, and NY-ESO-1 in squamous cell carcinoma of the penis. Urology, 68, 205 207. (Pubitemid 44037716)
23. Inokuma, M., Dela Rosa, C., Schmitt, C., Haaland, P., Siebert, J., Petry, D., Tang, M., Suni, M.A., Ghanekar, S.A., Gladding, D., Dunne, J.F., Maino, V.C., Disis, M.L. Maecker, H.T. (2007) Functional T cell responses to tumor antigens in breast cancer patients have a distinct phenotype and cytokine signature. Journal of Immunology, 179, 2627 2633.
24. Jungbluth, A.A., Ely, S., DiLiberto, M., Niesvizky, R., Williamson, B., Frosina, D., Chen, Y.T., Bhardwaj, N., Chen-Kiang, S., Old, L.J. Cho, H.J. (2005) The cancer-testis antigens CT7 (MAGE-C1) and MAGE-A3/6 are commonly expressed in multiple myeloma and correlate with plasma-cell proliferation. Blood, 106, 167 174.
25. Liggins, A.P., Brown, P.J., Asker, K., Pulford, K. Banham, A.H. (2004a) A novel diffuse large B-cell lymphoma-associated cancer testis antigen encoding a PAS domain protein. British Journal of Cancer, 91, 141 149.
26. Liggins, A.P., Guinn, B.A., Hatton, C.S., Pulford, K. Banham, A.H. (2004b) Serologic detection of diffuse large B-cell lymphoma-associated antigens. International Journal of Cancer, 110, 934.
27. Lim, S.H., Wang, Z., Chiriva-Internati, M. Xue, Y. (2001) Sperm protein 17 is a novel cancer-testis antigen in multiple myeloma. Blood, 97, 1508 1510.
28. Luckey, C.J., King, G.M., Marto, J.A., Venketeswaran, S., Maier, B.F., Crotzer, V.L., Colella, T.A., Shabanowitz, J., Hunt, D.F. Engelhard, V.H. (1998) Proteasomes can either generate or destroy MHC class I epitopes: evidence for nonproteasomal epitope generation in the cytosol. Journal of Immunology, 161, 112 121.
29. Nakagawa, K., Noguchi, Y., Uenaka, A., Sato, S., Okumura, H., Tanaka, M., Shimono, M., Ali Eldib, A.M., Ono, T., Ohara, N., Yoshino, T., Yamashita, K., Tsunoda, T., Aoe, M., Shimizu, N. Nakayama, E. (2005) XAGE-1 expression in non-small cell lung cancer and antibody response in patients. Clinical Cancer Research, 11, 5496 5503. (Pubitemid 41060826)
30. Passoni, L., Gallo, B., Biganzoli, E., Stefanoni, R., Massimino, M., Di Nicola, M., Gianni, A.M. Gambacorti-Passerini, C. (2006) In vivo T-cell immune response against anaplastic lymphoma kinase in patients with anaplastic large cell lymphomas. Haematologica, 91, 48 55.
31. Pellat-Deceunynck, C., Mellerin, M.P., Labarriere, N., Jego, G., Moreau-Aubry, A., Harousseau, J.L., Jotereau, F. Bataille, R. (2000) The cancer germ-line genes MAGE-1, MAGE-3 and PRAME are commonly expressed by human myeloma cells. European Journal of Immunology, 30, 803 809.
32. Porter, D.L. Antin, J.H. (2006) Donor leukocyte infusions in myeloid malignancies: new strategies. Best Practice & Research. Clinical Haematology, 19, 737 755.
33. Preuss, K.D., Zwick, C., Bormann, C., Neumann, F. Pfreundschuh, M. (2002) Analysis of the B-cell repertoire against antigens expressed by human neoplasms. Immunological Reviews, 188, 43 50. (Pubitemid 35398864)
34. van Rhee, F., Szmania, S.M., Zhan, F., Gupta, S.K., Pomtree, M., Lin, P., Batchu, R.B., Moreno, A., Spagnoli, G., Shaughnessy, J. Tricot, G. (2005) NY-ESO-1 is highly expressed in poor-prognosis multiple myeloma and induces spontaneous humoral and cellular immune responses. Blood, 105, 3939 3944.
35. Rimsza, L.M., Roberts, R.A., Miller, T.P., Unger, J.M., LeBlanc, M., Braziel, R.M., Weisenberger, D.D., Chan, W.C., Muller-Hermelink, H.K., Jaffe, E.S., Gascoyne, R.D., Campo, E., Fuchs, D.A., Spier, C.M., Fisher, R.I., Delabie, J., Rosenwald, A., Staudt, L.M. Grogan, T.M. (2004) Loss of MHC class II gene and protein expression in diffuse large B-cell lymphoma is related to decreased tumor immunosurveillance and poor patient survival regardless of other prognostic factors: a follow-up study from the Leukemia and Lymphoma Molecular Profiling Project. Blood, 103, 4251 4258.
36. Rosenwald, A., Wright, G., Chan, W.C., Connors, J.M., Campo, E., Fisher, R.I., Gascoyne, R.D., Muller-Hermelink, H.K., Smeland, E.B., Giltnane, J.M., Hurt, E.M., Zhao, H., Averett, L., Yang, L., Wilson, W.H., Jaffe, E.S., Simon, R., Klausner, R.D., Powell, J., Duffey, P.L., Longo, D.L., Greiner, T.C., Weisenburger, D.D., Sanger, W.G., Dave, B.J., Lynch, J.C., Vose, J., Armitage, J.O., Montserrat, E., Lopez-Guillermo, A., Grogan, T.M., Miller, T.P., LeBlanc, M., Ott, G., Kvaloy, S., Delabie, J., Holte, H., Krajci, P., Stokke, T. Staudt, L.M. (2002) The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. The New England Journal of Medicine, 346, 1937 1947.
37. Sahota, S.S., Goonewardena, C.M., Cooper, C.D., Liggins, A.P., Ait-Tahar, K., Zojer, N., Stevenson, F.K., Banham, A.H. Pulford, K. (2006) PASD1 is a potential multiple myeloma-associated antigen. Blood, 108, 3953 3955.
38. Scanlan, M.J., Simpson, A.J. Old, L.J. (2004) The cancer/testis genes: review, standardization, and commentary. Cancer Immunity, 4, 1.
39. Schmitt, M., Schmitt, A., Rojewski, M.T., Chen, J., Giannopoulos, K., Fei, F., Yu, Y., Gotz, M., Heyduk, M., Ritter, G., Speiser, D.E., Gnjatic, S., Guillaume, P., Ringhoffer, M., Schlenk, R.F., Liebisch, P., Bunjes, D., Shiku, H., Dohner, H. Greiner, J. (2008) RHAMM-R3 peptide vaccination in patients with acute myeloid leukemia, myelodysplastic syndrome, and multiple myeloma elicits immunologic and clinical responses. Blood, 111, 1357 1365.
40. Shipp, M.A., Ross, K.N., Tamayo, P., Weng, A.P., Kutok, J.L., Aguiar, R.C.T., Gaasenbeek, M., Angelo, M., Reich, M., Pinkus, G.S., Ray, T.S., Koval, M.A., Last, K.W., Norton, A., Lister, A., Mesirov, J., Neuberg, D.S., Lander, E.S., Aster, J.C. Golub, T.R. (2002) Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nature Medicine, 8, 68 74.
41. Simpson, A.J., Caballero, O.L., Jungbluth, A., Chen, Y.T. Old, L.J. (2005) Cancer/testis antigens, gametogenesis and cancer. Nature Reviews. Cancer, 5, 615 625.
42. Stein, H., Chan, J., Warnke, R., Gatter, K., Chan, W., Campo, E. Jaffe, E. (2008) Diffuse large B-cell lymphoma, not otherwise specified. In : WHO classification of tumours of Haematopoeitic and lymphoid tissues (ed. by S.H. Swerdlow, E. Campo, N.L. Harris, E.S. Jaffe, S.A. Pileri, H. Stein, J. Thiele J.W. Vardiman pp. 233 237. International Agency for Research on Cancer, Lyon, France.
43. Sugita, Y., Wada, H., Fujita, S., Nakata, T., Sato, S., Noguchi, Y., Jungbluth, A.A., Yamaguchi, M., Chen, Y.T., Stockert, E., Gnjatic, S., Williamson, B., Scanlan, M.J., Ono, T., Sakita, I., Yasui, M., Miyoshi, Y., Tamaki, Y., Matsuura, N., Noguchi, S., Old, L.J., Nakayama, E. Monden, M. (2004) NY-ESO-1 expression and immunogenicity in malignant and benign breast tumors. Cancer Research, 64, 2199 2204.
44. Suri, A. (2006) Cancer testis antigens - their importance in immunotherapy and in the early detection of cancer. Expert Opinion on Biological Therapy, 6, 379 389.
45. Szmania, S., Tricot, G. van Rhee, F. (2006) NY-ESO-1 immunotherapy for multiple myeloma. Leukemia & Lymphoma, 47, 2037 2048.
46. Theurillat, J.P., Ingold, F., Frei, C., Zippelius, A., Varga, Z., Seifert, B., Chen, Y.T., Jager, D., Knuth, A. Moch, H. (2007) NY-ESO-1 protein expression in primary breast carcinoma and metastases: correlation with CD8+ T-cell and CD79a+ plasmacytic/B-cell infiltration. International Journal of Cancer, 120, 2411 2417.
47. Vierboom, M.P., Zwaveling, S., Bos, G.M.J., Ooms, M., Krietemeijer, G.M., Melief, C.J. Offringa, R. (2000) High steady-state levels of p53 are not a prerequisite for tumor eradication by wild-type p53-specific cytotoxic T lymphocytes. Cancer Research, 60, 5508 5513.
48. Xie, X., Wacker, H.H., Huang, S., Regitz, E., Preuss, K.D., Romeike, B., Parwaresch, R., Tiemann, M. Pfreundschuh, M. (2003) Differential expression of cancer testis genes in histological subtypes of non-Hodgkin's lymphomas. Clinical Cancer Research, 9, 167 173.
49. Zeng, G. (2001) MHC class II-restricted tumor antigens recognized by CD4+ T cells: new strategies for cancer vaccine design. Journal of Immunotherapy, 1997, 24.
50. Zhang, Y., Wang, Z., Liu, H., Giles, F.J. Lim, S.H. (2003) Pattern of gene expression and immune responses to Semenogelin 1 in chronic hematologic malignancies. Journal of Immunotherapy, 1997, 26.