Increased PRAME antigen-specific killing of malignant cell lines by low avidity CTL clones, following treatment with 5-aza-2′-Deoxycytidine

Cancer Immunology, Immunotherapy

Volumn 60, Issue 9, 2011, Pages 1243-1255

  Yan, Mengyong ^a   Himoudi, Nourredine ^a   Basu, B Piku ^a   Wallace, Rebecca ^a   Poon, Edmund ^a   Adams, Stuart ^b   Hasan, Fyeza ^a   Xue, Shao An ^c   Wilson, Natalie ^d   Dalgleish, Angus ^d   Williams, Owen ^a   Anderson, John ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^c University College London Royal Free Campus ^*  (United Kingdom)

^d ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

5 Aza 2 Deoxycytidine; Cancer; CTL; Decitabine; Leukaemia; PRAME

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CANCER TESTIS ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; FAS ANTIGEN; HLA A ANTIGEN; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; PRAME ANTIGEN; PREFERENTIALLY EXPRESSED ANTIGEN OF MELANOMA; PROGRAMMED DEATH 1 RECEPTOR; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CANCER CELL DESTRUCTION; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL KILLING; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE EXPRESSION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LYMPHOCYTE CLONE; MELANOMA; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; TARGET CELL; UPREGULATION;

ANTIBODY AFFINITY; ANTIGENS, NEOPLASM; ANTIMETABOLITES, ANTINEOPLASTIC; AZACITIDINE; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; HL-60 CELLS; HLA-A2 ANTIGEN; HUMANS; IMMUNOTHERAPY, ADOPTIVE; K562 CELLS; NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TRANSFECTION;

EID: 80054678677     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-1024-4     Document Type: Article

References (47)

1. Ikeda H, Lethe B, Lehmann F, van Baren N, Baurain JF, de Smet C, Chambost H, Vitale M, Moretta A, Boon T, Coulie PG (1997) Characterization of an antigen that is recognized on a melanoma showing partial HLA loss by CTL expressing an NK inhibitory receptor. Immunity 6(2):199-208 (Pubitemid 27145564)
2. van Baren N, Chambost H, Ferrant A, Michaux L, Ikeda H, Millard I, Olive D, Boon T, Coulie PG (1998) PRAME, a gene encoding an antigen recognized on a human melanoma by cytolytic T cells, is expressed in acute leukaemia cells. Br J Haematol 102(5):1376-1379 (Pubitemid 28435230)
3. Van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415(6871):530-536 (Pubitemid 34130608)
4. Boon K, Edwards JB, Siu IM, Olschner D, Eberhart CG, Marra MA, Strausberg RL, Riggins GJ (2003) Comparison of medulloblastoma and normal neural transcriptomes identifies a restricted set of activated genes. Oncogene 22(48):7687-7694 (Pubitemid 37464103)
5. Oberthuer A, Hero B, Spitz R, Berthold F, Fischer M (2004) The tumor-associated antigen PRAME is universally expressed in high-stage neuroblastoma and associated with poor outcome. Clin Cancer Res 10(13):4307-4313 (Pubitemid 38878868)
6. Epping MT, Hart AA, Glas AM, Krijgsman O, Bernards R (2008) PRAME expression and clinical outcome of breast cancer. Br J Cancer 99(3):398-403
7. Neumann E, Engelsberg A, Decker J, Storkel S, Jaeger E, Huber C, Seliger B (1998) Heterogeneous expression of the tumorassociated antigens RAGE-1, PRAME, and glycoprotein 75 in human renal cell carcinoma: candidates for T-cell-based immunotherapies? Cancer Res 58(18):4090-4095 (Pubitemid 28440562)
8. Li CM, Guo M, Borczuk A, Powell CA, Wei M, Thaker HM, Friedman R, Klein U, Tycko B (2002) Gene expression in Wilms' tumor mimics the earliest committed stage in the metanephric mesenchymal-epithelial transition. Am J Pathol 160(6):2181-2190 (Pubitemid 34663409)
9. Steinbach D, Viehmann S, Zintl F, Gruhn B (2002) PRAME gene expression in childhood acute lymphoblastic leukemia. Cancer Genet Cytogenet 138(1):89-91 (Pubitemid 35292607)
10. Radich JP, Dai H, Mao M, Oehler V, Schelter J, Druker B, Sawyers C, Shah N, Stock W, Willman CL, Friend S, Linsley PS (2006) Gene expression changes associated with progression and response in chronic myeloid leukemia. Proc Natl Acad Sci USA 103(8):2794-2799
11. Epping MT, Wang L, Edel MJ, Carlee L, Hernandez M, Bernards R (2005) The human tumor antigen PRAME is a dominant repressor of retinoic acid receptor signaling. Cell 122(6):835-847 (Pubitemid 41345202)
12. Passeron T, Valencia JC, Namiki T, Vieira WD, Passeron H, Miyamura Y, Hearing VJ (2009) Upregulation of SOX9 inhibits the growth of human and mouse melanomas and restores their sensitivity to retinoic acid. J Clin Invest 119(4):954-963
13. 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 HLAA(*) 0201-presented cytotoxic T lymphocyte epitopes in the widely expressed tumor antigen PRAME by proteasome-mediated digestion analysis. J Exp Med 193(1):73-88 (Pubitemid 32060699)
14. Griffioen M, Kessler JH, Borghi M, van Soest RA, van der Minne CE, Nouta J, van der Burg SH, Medema JP, Schrier PI, Falkenburg JH, Osanto S, Melief CJ (2006) Detection and functional analysis of CD8 ? T cells specific for PRAME: a target for T-cell therapy. Clin Cancer Res 12(10):3130-3136 (Pubitemid 43837361)
15. Greiner J, Schmitt M, Li L, Giannopoulos K, Bosch K, Schmitt A, Dohner K, Schlenk RF, Pollack JR, Dohner H, Bullinger L (2006) Expression of tumor-associated antigens in acute myeloid leukemia: Implications for specific immunotherapeutic approaches. Blood 108(13):4109-4117 (Pubitemid 44913282)
16. Rezvani K, Yong AS, Tawab A, Jafarpour B, Eniafe R, Mielke S, Savani BN, Keyvanfar K, Li Y, Kurlander R, Barrett AJ (2009) Ex vivo characterization of polyclonal memory CD8 ? T-cell responses to PRAME-specific peptides in patients with acute lymphoblastic leukemia and acute and chronic myeloid leukemia. Blood 113(10):2245-2255
17. Quintarelli C, Dotti G, De Angelis B, Hoyos V, Mims M, Luciano L, Heslop HE, Rooney CM, Pane F, Savoldo B (2008) Cytotoxic T lymphocytes directed to the preferentially expressed antigen of melanoma (PRAME) target chronic myeloid leukemia. Blood 112(5):1876-1885
18. Weiser TS, Ohnmacht GA, Guo ZS, Fischette MR, Chen GA, Hong JA, Nguyen DM, Schrump DS (2001) Induction of MAGE- 3 expression in lung and esophageal cancer cells. Ann Thorac Surg 71(1):295-301 (discussion 301-292)
19. Adair SJ, Hogan KT (2009) Treatment of ovarian cancer cell lines with 5-aza-2′-deoxycytidine upregulates the expression of cancer-testis antigens and class I major histocompatibility complex- encoded molecules. Cancer Immunol Immunother 58(4):589-601
20. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo JA, Navarro G, Jose-Eneriz ES, Garate L, Cordeu L, Cervantes F, Prosper F, Heiniger A, Torres A (2007) Epigenetic regulation of PRAME gene in chronic myeloid leukemia. Leuk Res 31(11):1521-1528 (Pubitemid 350010966)
21. Weiser TS, Guo ZS, Ohnmacht GA, Parkhurst ML, Tong-On P, Marincola FM, Fischette MR, Yu X, Chen GA, Hong JA, Stewart JH, Nguyen DM, Rosenberg SA, Schrump DS (2001) Sequential 5-Aza-2′deoxycytidine-depsipeptide FR901228 treatment induces apoptosis preferentially in cancer cells and facilitates their recognition by cytolytic T lymphocytes specific for NYESO- 1. J Immunother 24(2):151-161 (Pubitemid 32183061)
22. Blum KA, Liu Z, Lucas DM, Chen P, Xie Z, Baiocchi R, Benson DM, Devine SM, Jones J, Andritsos L, Flynn J, Plass C, Marcucci G, Chan KK, Grever MR, Byrd JC (2010) Phase I trial of low dose decitabine targeting DNA hypermethylation in patients with chronic lymphocytic leukaemia and non-Hodgkin lymphoma: dose-limiting myelosuppression without evidence of DNA hypomethylation. Br J Haematol 150(2):189-195
23. Blum W, Klisovic RB, Hackanson B, Liu Z, Liu S, Devine H, Vukosavljevic T, Huynh L, Lozanski G, Kefauver C, Plass C, Devine SM, Heerema NA, Murgo A, Chan KK, Grever MR, Byrd JC, Marcucci G (2007) Phase I study of decitabine alone or in combination with valproic acid in acute myeloid leukemia. J Clin Oncol 25(25):3884-3891 (Pubitemid 47477265)
24. Dubovsky JA, McNeel DG, Powers JJ, Gordon J, Sotomayor EM, Pinilla-Ibarz JA (2009) Treatment of chronic lymphocytic leukemia with a hypomethylating agent induces expression of NXF2, an immunogenic cancer testis antigen. Clin Cancer Res 15(10):3406-3415
25. Kozbor D, Roder JC (1981) Requirements for the establishment of high-titered human monoclonal antibodies against tetanus toxoid using the Epstein-Barr virus technique. J Immunol 127(4):1275-1280 (Pubitemid 11020986)
26. Schultze JL, Michalak S, Seamon MJ, Dranoff G, Jung K, Daley J, Delgado JC, Gribben JG, Nadler LM (1997) CD40-activated human B cells: an alternative source of highly efficient antigen presenting cells to generate autologous antigen-specific T cells for adoptive immunotherapy. J Clin Invest 100(11):2757-2765 (Pubitemid 28007544)
27. 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(6):673-679 (Pubitemid 29302920)
28. Yan M, Himoudi N, Pule M, Sebire N, Poon E, Blair A, Williams O, Anderson J (2008) Development of cellular immune responses against PAX5, a novel target for cancer immunotherapy. Cancer Res 68(19):8058-8065
29. Sigalotti L, Fratta E, Coral S, Tanzarella S, Danielli R, Colizzi F, Fonsatti E, Traversari C, Altomonte M, Maio M (2004) Intratumor heterogeneity of cancer/testis antigens expression in human cutaneous melanoma is methylation-regulated and functionally reverted by 5-aza-2′-deoxycytidine. Cancer Res 64(24):9167-9171 (Pubitemid 39665532)
30. Weber J, Salgaller M, Samid D, Johnson B, Herlyn M, Lassam N, Treisman J, Rosenberg SA (1994) Expression of the MAGE-1 tumor antigen is up-regulated by the demethylating agent 5-aza-2′deoxycytidine. Cancer Res 54(7):1766-1771
31. Natsume A, Wakabayashi T, Tsujimura K, Shimato S, Ito M, Kuzushima K, Kondo Y, Sekido Y, Kawatsura H, Narita Y, Yoshida J (2008) The DNA demethylating agent 5-aza-2′-deoxycytidine activates NY-ESO-1 antigenicity in orthotopic human glioma. Int J Cancer 122(11):2542-2553 (Pubitemid 351590488)
32. Leisegang M, Wilde S, Spranger S, Milosevic S, Frankenberger B, Uckert W, Schendel DJ (2010) MHC-restricted fratricide of human lymphocytes expressing survivin-specific transgenic T cell receptors. J Clin Invest 120(11):3869-3877. doi: 10.1172/JCI43437
33. McCormack SE, Warlick ED (2010) Epigenetic approaches in the treatment of myelodysplastic syndromes: clinical utility of azacitidine. Onco Targets Ther 3:157-165
34. Kantarjian H, Issa JP, Rosenfeld CS, Bennett JM, Albitar M, DiPersio J, Klimek V, Slack J, de Castro C, Ravandi F, Helmer R III, Shen L, Nimer SD, Leavitt R, Raza A, Saba H (2006) Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Cancer 106(8):1794-1803
35. Atallah E, Kantarjian H, Garcia-Manero G (2007) The role of decitabine in the treatment of myelodysplastic syndromes. Expert Opin Pharmacother 8(1):65-73 (Pubitemid 46070830)
36. Jain N, Rossi A, Garcia-Manero G (2009) Epigenetic therapy of leukemia: an update. Int J Biochem Cell Biol 41(1):72-80
37. Momparler RL (2005) Epigenetic therapy of cancer with 5-aza- 2′deoxycytidine (decitabine). Semin Oncol 32(5):443-451 (Pubitemid 41396420)
38. Oki Y, Issa JP (2006) Review: recent clinical trials in epigenetic therapy. Rev Recent Clin Trials 1(2):169-182
39. Coral S, Sigalotti L, Colizzi F, Spessotto A, Nardi G, Cortini E, Pezzani L, Fratta E, Fonsatti E, Di Giacomo AM, Nicotra MR, Natali PG, Altomonte M, MaioM(2006) Phenotypic and functional changes of human melanoma xenografts induced by DNA hypomethylation: immunotherapeutic implications. J Cell Physiol 207(1):58-66
40. Lubbert M, Bertz H, Ruter B, Marks R, Claus R, Wasch R, Finke J (2009) Non-intensive treatment with low-dose 5-aza-2′-deoxycytidine (DAC) prior to allogeneic blood SCT of older MDS/ AML patients. Bone Marrow Transplant 44(9):585-588
41. Czibere A, Bruns I, Kroger N, PlatzbeckerU, Lind J, Zohren F, Fenk R, Germing U, Schroder T, Graf T, Haas R, Kobbe G (2010) 5-Azacytidine for the treatment of patients with acute myeloid leukemia or myelodysplastic syndrome who relapse after allo-SCT: a retrospective analysis. Bone Marrow Transplant 45(5):872-876
42. Schenk T, Stengel S, Goellner S, Steinbach D, Saluz HP (2007) Hypomethylation of PRAME is responsible for its aberrant overexpression in human malignancies. Genes Chromosom Cancer 46(9):796-804 (Pubitemid 47106183)
43. Wargo JA, Robbins PF, Li Y, Zhao Y, El-Gamil M, Caragacianu D, Zheng Z, Hong JA, Downey S, Schrump DS, Rosenberg SA, Morgan RA (2009) Recognition of NY-ESO-1 ? tumor cells by engineered lymphocytes is enhanced by improved vector design and epigenetic modulation of tumor antigen expression. Cancer Immunol Immunother 58(3):383-394
44. Lu Q, Wu A, Ray D, Deng C, Attwood J, Hanash S, Pipkin M, Lichtenheld M, Richardson B (2003) DNA methylation and chromatin structure regulate T cell perforin gene expression. J Immunol 170(10):5124-5132 (Pubitemid 36554744)
45. Goodyear O, Agathanggelou A, Novitzky-Basso I, Siddique S, McSkeane T, Ryan G, Vyas P, Cavenagh J, Stankovic T, Moss P, Craddock C (2010) Induction of a CD8 ? T-cell response to the MAGE cancer testis antigen by combined treatment with azacitidine and sodium valproate in patients with acute myeloid leukemia and myelodysplasia. Blood 116(11):1908-1918
46. Sanchez-Abarca LI, Gutierrez-Cosio S, Santamaria C, Caballero- Velazquez T, Blanco B, Herrero-Sanchez C, Garcia JL, Carrancio S, Hernandez-Campo P, Gonzalez FJ, Flores T, Ciudad L, Ballestar E, Del Canizo C, San Miguel JF, Perez-Simon JA (2010) Immunomodulatory effect of 5-azacytidine (5-azaC): potential role in the transplantation setting. Blood 115(1):107-121
47. Lu D, Hoory T, Monie A, Wu A, Wang MC, Hung CF (2009) Treatment with demethylating agent, 5-aza-2′-deoxycytidine enhances therapeutic HPV DNA vaccine potency. Vaccine 27(32):4363-4369