Improving T-cell therapy for relapsed EBV-negative Hodgkin lymphoma by targeting upregulated MAGE-A4

Clinical Cancer Research

Volumn 17, Issue 22, 2011, Pages 7058-7066

  Cruz, Conrad R ^a   Gerdemann, Ulrike ^a   Leen, Ann M ^a   Shafer, Jessica A ^a   Ku, Stephanie ^a   Tzou, Benjamin ^a   Horton, Terzah M ^b   Sheehan, Andrea ^b   Copeland, Amanda ^c   Younes, Anas ^c   Rooney, Cliona M ^a   Heslop, Helen E ^a   Bollard, Catherine M ^a  

^a TEXAS CHILDREN S HOSPITAL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; GAMMA INTERFERON; MELANOMA ANTIGEN 4;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANTIGEN EXPRESSION; ARTICLE; CANCER RELAPSE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; EPIGENETICS; EPSTEIN BARR VIRUS; HODGKIN DISEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOSTIMULATION; IN VIVO STUDY; PRIORITY JOURNAL;

ANTIGENS, NEOPLASM; ANTIMETABOLITES, ANTINEOPLASTIC; AZACITIDINE; CELL LINE, TUMOR; EPIGENESIS, GENETIC; EPITOPES; FEASIBILITY STUDIES; HERPESVIRUS 4, HUMAN; HODGKIN DISEASE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MOLECULAR TARGETED THERAPY; NEOPLASM PROTEINS; RECURRENCE; T-LYMPHOCYTES; UP-REGULATION;

EID: 81255143446     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-1873     Document Type: Article

References (49)

1. Quddus F, Armitage JO. Salvage therapy for Hodgkin's lymphoma. Cancer J 2009;15:161-3.
2. Sureda A. Autologous and allogeneic stem cell transplantation in Hodgkin's lymphoma. Hematol Oncol Clin North Am 2007;21:943-60. (Pubitemid 47484144)
3. Castellino SM, Geiger AM, Mertens AC, Leisenring WM, Tooze JA, Goodman P, et al. Morbidity and mortality in long-term survivors of Hodgkin lymphoma: a report from the Childhood Cancer Survivor Study. Blood 2011;117:1806-16.
4. Dunleavy K, Bollard CM. Sobering realities of surviving Hodgkin lymphoma. Blood 2011;117:1772-3.
5. BollardCM, Gottschalk S, Leen AM, Weiss H, Straathof KC, Carrum G, et al. Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. Blood 2007;110:2838-45. (Pubitemid 350006936)
6. Bollard CM, Aguilar L, Straathof KC, Gahn B, Huls MH, Rousseau A, et al. Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin's disease. J Exp Med 2004;200:1623-33. (Pubitemid 40094186)
7. Simpson AJ, Caballero OL, Jungbluth A, Chen YT, Old LJ. Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 2005;5: 615-25. (Pubitemid 41081387)
8. Chambost H, Van Baren N, Brasseur F, Godelaine D, Xerri L, Landi SJ, et al. Expression of gene MAGE-A4 in Reed-Sternberg cells. Blood 2000;95:3530-3. (Pubitemid 30428487)
9. Marcar L, Maclaine NJ, Hupp TR, Meek DW. Mage-A cancer/testis antigens inhibit p53 function by blocking its interaction with chromatin. Cancer Res 2010;70:10362-70.
10. Shafer JA, Cruz CR, Leen AM, Ku S, Lu A, Rousseau A, et al. Antigen-specific cytotoxic T lymphocytes can target chemoresistant sidepopulation tumor cells in Hodgkin lymphoma. Leuk Lymphoma 2010;51:870-80.
11. Aribi A, Borthakur G, Ravandi F, Shan J, Davisson J, Cortes J, et al. Activity of decitabine, a hypomethylating agent, in chronic myelomonocytic leukemia. Cancer 2007;109:713-7. (Pubitemid 46233232)
12. Fang F, Balch C, Schilder J, Breen T, Zhang S, Shen C, et al. A phase 1 and pharmacodynamic study of decitabine in combination with carboplatin in patients with recurrent, platinum-resistant, epithelial ovarian cancer. Cancer 2010;116:4043-53.
13. George RE, Lahti JM, Adamson PC, Zhu K, Finkelstein D, Ingle AM, et al. Phase I study of decitabine with doxorubicin and cyclophosphamide in children with neuroblastoma and other solid tumors: a Children's Oncology Group study. Pediatr Blood Cancer 2010;55: 629-38.
14. Piekarz RL, Frye R, Turner M, Wright JJ, Allen SL, Kirschbaum MH, et al. Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J Clin Oncol 2009;27:5410-7.
15. Mackay HJ, Hirte H, Colgan T, Covens A, MacAlpine K, Grenci P, et al. Phase II trial of the histone deacetylase inhibitor belinostat in women with platinum resistant epithelial ovarian cancer and micropapillary (LMP) ovarian tumours. Eur J Cancer 2010;46:1573-9.
16. Sigalotti L, Fratta E, Coral S, Cortini E, Covre A, Nicolay HJ, et al. Epigenetic drugs as pleiotropic agents in cancer treatment: biomolecular aspects and clinical applications. J Cell Physiol 2007;212: 330-44. (Pubitemid 47025622)
17. Maio M, Coral S, Fratta E, Altomonte M, Sigalotti L. Epigenetic targets for immune intervention in human malignancies. Oncogene 2003;22: 6484-8. (Pubitemid 37372328)
18. Moreno-Bost A, Szmania S, Stone K, Garg T, Hoerring A, Szymonifka J, et al. Epigenetic modulation of MAGE-A3 antigen expression in multiple myeloma following treatment with the demethylation agent 5-azacitidine and the histone deacetlyase inhibitor MGCD0103. Cytotherapy 2011;13:618-28.
19. Goodyear O, Agathanggelou A, Novitzky-Basso I, Siddique S, McSkeane T, Ryan G, et al. 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 2010;116:1908-18.
20. Einsele H, Rauser G, Grigoleit U, Hebart H, Sinzger C, Riegler S, et al. Induction ofCMV-specific T-cell lines using Ag-presenting cells pulsed with CMV protein or peptide. Cytotherapy 2002;4:49-54. (Pubitemid 34752391)
21. Jia ZC, Ni B, Huang ZM, Tian Y, Tang J, Wang JX, et al. Identification of two novel HLA-A-0201-restricted CTL epitopes derived from MAGEA4. Clin Dev Immunol 2010:567594.
22. Graff-Dubois S, Faure O, Gross DA, Alves P, Scardino A, Chouaib S, et al. Generation of CTL recognizing an HLA-A-0201-restricted epitope shared by MAGE-A1, -A2, -A3, -A4, -A6, -A10, and -A12 tumor antigens: implication in a broad-spectrum tumor immunotherapy. J Immunol 2002;169:575-80. (Pubitemid 34686181)
23. Adair SJ, Hogan KT. 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 2009;58:589-601.
24. Monte M, Simonatto M, Peche LY, Bublik DR, Gobessi S, Pierotti MA, et al. MAGE-A tumor antigens target p53 transactivation function through histone deacetylase recruitment and confer resistance to chemotherapeutic agents. Proc Natl Acad Sci U S A 2006;103: 11160-5. (Pubitemid 44156489)
25. Hussein YM, Gharib AF, Etewa RL, El-Shal AS, Abdel-Ghany ME, Elsawy WH. The melanoma-associated antigen-A3, -A4 genes: relation to the risk and clinicopathological parameters in breast cancer patients. Mol Cell Biochem 2011;351:261-8.
26. Cuffel C, Rivals JP, Zaugg Y, Salvi S, Seelentag W, Speiser DE, et al. Pattern and clinical significance of cancer-testis gene expression in head and neck squamous cell carcinoma. Int J Cancer 2011;128: 2625-34.
27. Svobodova S, Browning J, MacGregor D, Pollara G, Scolyer RA, Murali R, et al. Cancer-testis antigen expression in primary cutaneous melanoma has independent prognostic value comparable to that of Breslow thickness, ulceration and mitotic rate. Eur J Cancer 2011;47: 460-9.
28. Poppema S. Immunobiology and pathophysiology of Hodgkin lymphomas. Hematology Am Soc Hematol Educ Program 2005:231-8.
29. Steingrimsdottir H, Gruber A, Bjorkholm M, Svensson A, Hansson M. Immune reconstitution after autologous hematopoietic stem cell transplantation in relation to underlying disease, type of high-dose therapy and infectious complications. Haematologica 2000;85:832-8.
30. Canto E, Rodriguez-Sanchez JL, Vidal S. Distinctive response of naive lymphocytes from cord blood to primary activation via TCR. J Leukoc Biol 2003;74:998-1007. (Pubitemid 38040321)
31. Chao NJ, Emerson SG, Weinberg KI. Stem cell transplantation (cord blood transplants). Hematology Am Soc Hematol Educ Program 2004:354-71.
32. Hanley PJ, Cruz CR, Savoldo B, Leen AM, Stanojevic M, Khalil M, et al. Functionally active virus-specific T cells that target CMV, adenovirus, and EBV can be expanded from naive T-cell populations in cord blood and will target a range of viral epitopes. Blood 2009;114:1958-67.
33. Micklethwaite KP, Savoldo B, Hanley PJ, Leen AM, Demmler-Harrison GJ, Cooper LJ, et al. Derivation of human T lymphocytes from cord blood and peripheral blood with antiviral and antileukemic specificity from a single culture as protection against infection and relapse after stem cell transplantation. Blood 2010;115:2695-703.
34. Fratta E, Coral S, Covre A, Parisi G, Colizzi F, Danielli R, et al. The biology of cancer testis antigens: putative function, regulation and therapeutic potential. Mol Oncol 2011;5:164-82.
35. Gerdemann U, Tripic T, Cruz CR, Vera J, Christin AS, Heslop HE, et al. Multi-tumor-antigen specific cytotoxic T lymphocytes for therapy of lymphoma. Mol Ther. Epub 2011 Sep 13.
36. Svane IM, Boesen M, Engel AM. The role of cytotoxic T-lymphocytes in the prevention and immune surveillance of tumors-lessons from normal and immunodeficient mice. Med Oncol 1999;16:223-38. (Pubitemid 30055711)
37. Baron F, Storb R. The immune system as a foundation for immunologic therapy and hematologic malignancies: a historical perspective. Best Pract Res Clin Haematol 2006;19:637-53. (Pubitemid 44418027)
38. Almstedt M, Blagitko-Dorfs N, Duque-Afonso J, Karbach J, Pfeifer D, Jager E, et al. The DNA demethylating agent 5-aza-2′-deoxycytidine induces expression of NY-ESO-1 and other cancer/testis antigens in myeloid leukemia cells. Leuk Res 2010;34:899-905.
39. Hambach L, Ling KW, Pool J, Aghai Z, Blokland E, Tanke HJ, et al. Hypomethylating drugs convert HA-1-negative solid tumors into targets for stem cell-based immunotherapy. Blood 2009;113: 2715-22.
40. Choi J, Ritchey J, Prior JL, Holt M, Shannon WD, Deych E, et al. In vivo administration of hypomethylating agents mitigate graft-versus-host disease without sacrificing graft-versus-leukemia. Blood 2010;116: 129-39.
41. Sanchez-Abarca LI, Gutierrez-Cosio S, Santamaria C, Caballero-Velazquez T, Blanco B, Herrero-Sanchez C, et al. Immunomodulatory effect of 5-azacytidine (5-azaC): potential role in the transplantation setting. Blood 2010;115:107-21.
42. Cashen AF, Shah AK, Todt L, Fisher N, DiPersio J. Pharmacokinetics of decitabine administered as a 3-h infusion to patients with acute myeloid leukemia (AML) or myelodysplastic syndrome (MDS). Cancer Chemother Pharmacol 2008;61:759-66. (Pubitemid 351302031)
43. Song W, Tai YT, Tian Z, Hideshima T, Chauhan D, Nanjappa P, et al. HDAC inhibition by LBH589 affects the phenotype and function of human myeloid dendritic cells. Leukemia 2011;25:161-8.
44. Quddus J, Johnson KJ, Gavalchin J, Amento EP, Chrisp CE, Yung RL, et al. Treating activated CD4+ T cells with either of two distinct DNA methyltransferase inhibitors, 5-azacytidine or procainamide, is sufficient to cause a lupus-like disease in syngeneic mice. J Clin Invest 1993;92:38-53. (Pubitemid 23208979)
45. Brogdon JL, Xu Y, Szabo SJ, An S, Buxton F, Cohen D, et al. Histone deacetylase activities are required for innate immune cell control of Th1 but not Th2 effector cell function. Blood 2007;109:1123-30. (Pubitemid 46220659)
46. Nagar M, Vernitsky H, Cohen Y, Dominissini D, Berkun Y, Rechavi G, et al. Epigenetic inheritance of DNA methylation limits activationinduced expression of FOXP3 in conventional human CD25-CD4+ T cells. Int Immunol 2008;20:1041-55.
47. Tao R, de Zoeten EF, Ozkaynak E, Chen C, Wang L, Porrett PM, et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 2007;13:1299-307. (Pubitemid 350073591)
48. Daurkin I, Eruslanov E, Vieweg J, Kusmartsev S. Generation of antigenpresenting cells from tumor-infiltrated CD11b myeloid cells with DNA demethylating agent 5-aza-2'-deoxycytidine. Cancer Immunol Immunother 2010;59:697-706.
49. Kennedy-Nasser AA, Hanley P, Bollard CM. Hodgkin disease and the role of the immune system. Pediatr Hematol Oncol 2011;28:176-86.