Epigenetic induction of adaptive immune response in multiple myeloma: Sequential azacitidine and lenalidomide generate cancer testis antigen-specific cellular immunity

British Journal of Haematology

Volumn 158, Issue 6, 2012, Pages 700-711

  Toor, Amir A ^a   Payne, Kyle K ^b   Chung, Harold M ^a   Sabo, Roy T ^b   Hazlett, Allison F ^a   Kmieciak, Maciej ^b   Sanford, Kimberly ^b   Williams, David C ^b   Clark, William B ^a   Roberts, Catherine H ^a   Mccarty, John M ^a   Manjili, Masoud H ^b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Adaptive immunity; Cancer testis antigens; Epigenetic induction; Multiple myeloma

Indexed keywords

AZACITIDINE; CANCER TESTIS ANTIGEN; LENALIDOMIDE; MELPHALAN; PLERIXAFOR; RECOMBINANT GRANULOCYTE COLONY STIMULATING FACTOR; RECOMBINANT GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; SYNDECAN 1;

ADAPTIVE IMMUNITY; ADULT; AGED; ANTIGEN SPECIFICITY; ARTICLE; AUTOLOGOUS LYMPHOCYTE INFUSION; BONE MARROW CELL; CANCER REGRESSION; CELLULAR IMMUNITY; CLINICAL ARTICLE; CRYOPRESERVATION; DRUG EFFICACY; DRUG MEGADOSE; ENGRAFTMENT; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; FEASIBILITY STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOTHERAPY; MALE; MULTIPLE CYCLE TREATMENT; MULTIPLE MYELOMA; OUTCOME ASSESSMENT; PATIENT SAFETY; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROSPECTIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL MOBILIZATION; T LYMPHOCYTE; TREATMENT RESPONSE; UPREGULATION;

ADULT; AGED; ANTIGENS, NEOPLASM; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; AZACITIDINE; BORONIC ACIDS; DEXAMETHASONE; DNA METHYLATION; DOXORUBICIN; DRUG ADMINISTRATION SCHEDULE; EPIGENESIS, GENETIC; FEMALE; HUMANS; IMMUNITY, CELLULAR; LYMPHOCYTE TRANSFUSION; MALE; MIDDLE AGED; MULTIPLE MYELOMA; PERIPHERAL BLOOD STEM CELL TRANSPLANTATION; PLASMA CELLS; PROSPECTIVE STUDIES; PYRAZINES; T-CELL ANTIGEN RECEPTOR SPECIFICITY; THALIDOMIDE; TRANSPLANTATION, AUTOLOGOUS;

EID: 84865553406     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2012.09225.x     Document Type: Article

References (44)

1. Ascierto, M.L., Kmieciak, M., Idowu, M.O., Manjili, R., Zhao, Y., Grimes, M., Dumur, C., Wang, E., Ramakrishnan, V., Wang, X.Y., Bear, H.D., Marincola, F.M. & Manjili, M.H. (2012) A signature of immune function genes associated with recurrence-free survival in breast cancer patients. Breast Cancer Research and Treatment, 131, 871-880.
2. 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. & Kröger, N. (2007) Cancer-testis antigens are commonly expressed in multiple myeloma and induce systemic immunity following allogeneic stem cell transplantation. Blood, 109, 1103-1112.
3. Bao, L., Dunham, K. & Lucas, K. (2011) MAGE-A1, MAGE-A3, and NY-ESO-1 can be upregulated on neuroblastoma cells to facilitate cytotoxic T lymphocyte-mediated tumor cell killing. Cancer Immunology, Immunotherapy, 60, 1299-1307.
4. Barlogie, B., Tricot, G., Anaissie, E., Shaughnessy, J., Rasmussen, E., Van Rhee, F., Fassas, A., Zangari, M., Hollmig, K., Pineda-Roman, M., Lee, C., Talamo, G., Thertulien, R., Kiwan, E., Krishna, S., Fox, M. & Crowley, J. (2006) Thalidomide and hematopoietic-cell transplantation for multiple myeloma. New England Journal of Medicine, 354, 1021-1030.
5. Bellucci, R., Wu, C.J., Chiaretti, S., Weller, E., Davies, F.E., Alyea, E.P., Dranoff, G., Anderson, K.C., Munshi, N.C. & Ritz, J. (2004) Complete response to donor lymphocyte infusion in multiple myeloma is associated with antibody responses to highly expressed antigens. Blood, 103, 656-663.
6. Bellucci, R., Alyea, E.P., Chiaretti, S., Wu, C.J., Zorn, E., Weller, E., Wu, B., Canning, C., Schlossman, R., Munshi, N.C., Anderson, K.C. & Ritz, J. (2005) Graft-versus-tumor response in patients with multiple myeloma is associated with antibody response to BCMA, a plasma-cell membrane receptor. Blood, 105, 3945-3950.
7. Chim, C.S., Liang, R., Fung, T.K., Choi, C.L. & Kwong, Y.L. (2007) Epigenetic dysregulation of the death-associated protein kinase/p14/HDM2/p53/Apaf-1 apoptosis pathway in multiple myeloma. Journal of Clinical Pathology, 60, 664-669.
8. Condomines, M., Hose, D., Raynaud, P., Hundemer, M., De Vos, J., Baudard, M., Moehler, T., Pantesco, V., Moos, M., Schved, J., Rossi, J., Reme, T., Goldschmidt, H. & Klein, B. (2007) Cancer/testis genes in multiple myeloma: expression patterns and prognosis value determined by microarray analysis. The Journal of Immunology, 178, 3307-3315.
9. Coral, S., Sigalotti, L., Altomonte, M., Engelsberg, A., Colizzi, F., Cattarossi, I., Maraskovsky, E., Jager, E., Seliger, B. & Maio, M. (2002) 5-aza-2 '-deoxycytidine-induced expression of functional cancer testis antigens in human renal cell carcinoma: immunotherapeutic implications. Clinical Cancer Research, 8, 2690-2695.
10. Coral, S., Sigalotti, L., Colizzi, F., Spessotto, A., Nardi, G., Cortini, E., Pezzani, L., Fratta, E., Fonsatti, E., Di Giacomo, A.M., Nicotra, M.R., Natali, P.G., Altomonte, M. & Maio, M. (2006) Phenotypic and functional changes of human melanoma xenografts induced by DNA hypomethylation: immunotherapeutic implications. Journal of Cellular Physiology, 207, 58-66.
11. Corral, L., Haslett, P., Muller, G., Chen, R., Wong, L., Ocampo, C.J., Patterson, R.T., Stirling, D.I. & Kaplan, G. (1999) Differential cytokine modulation and T cell activation by two distinct classes of thalidomide analogues that are potent inhibitors of TNF-alpha. The Journal of Immunology, 163, 380-386.
12. Cruz, C.R., Gerdemann, U., Leen, A.M., Shafer, J.A., Ku, S., Tzou, B., Horton, T.M., Sheehan, A., Copeland, A., Younes, A., Rooney, C.M., Heslop, H.E. & Bollard, C.M. (2011) Improving T-cell therapy for relapsed EBV-negative Hodgkin lymphoma by targeting upregulated MAGE-A4. Clinical Cancer Research, 17, 7058-7066.
13. Davies, F., Raje, N., Hideshima, T., Lentzsch, S., Young, G., Tai, Y., Lin, B., Podar, K., Gupta, D., Chauhan, D., Treon, S.P., Richardson, P.G., Schlossman, R.L., Morgan, G.J., Muller, G.W., Stirling, D.I. & Anderson, K.C. (2001) Thalidomide and immunomodulatory derivatives augment natural killer cell cytotoxicity in multiple myeloma. Blood, 98, 210-216.
14. De Lerma Barbaro, A., De Ambrosis, A., Banelli, B., Li Pira, G., Aresu, O., Romani, M., Ferrini, S. & Accolla, R.S. (2008) Methylation of CIITA promoter IV causes loss of HLA-II inducibility by IFN-gamma in promyelocytic cells. International Immunology, 20, 1457-1466.
15. Durie, B.G., Harousseau, J.L., Miguel, J.S., Durie, B.G., Harousseau, J.L., Miguel, J.S., Bladé, J., Barlogie, B., Anderson, K., Gertz, M., Dimopoulos, M., Westin, J., Sonneveld, P., Ludwig, H., Gahrton, G., Beksac, M., Crowley, J., Belch, A., Boccadaro, M., Cavo, M., Turesson, I., Joshua, D., Vesole, D., Kyle, R., Alexanian, R., Tricot, G., Attal, M., Merlini, G., Powles, R., Richardson, P., Shimizu, K., Tosi, P., Morgan, G. & Rajkumar, S.V. (2006) International Myeloma Working Group. International uniform response criteria for multiple myeloma. Leukemia, 20, 1467-1473.
16. Fonsatti, E., Nicolay, H.J., Sigalotti, L., Calabrò, L., Pezzani, L., Colizzi, F., Altomonte, M., Guidoboni, M., Marincola, F.M. & Maio, M. (2007) Functional up-regulation of human leukocyte antigen class I antigens expression by 5-aza-2'-deoxycytidine in cutaneous melanoma: immunotherapeutic implications. Clinical Cancer Research, 13, 3333-3338.
17. 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, 1908-1918.
18. Guo, Z., Hong, J., Irvine, K., Chen, A.G., Spiess, P.J., Liu, Y., Zeng, G., Wunderlich, J.R., Nguyen, D.M., Restifo, N.P. & Schrump, D.S. (2006) De novo induction of a cancer/testis antigen by 5-aza-2 '-deoxycytidine augments adoptive immunotherapy in a murine tumor model RID A-5713-2008. Cancer Research, 66, 1105-1113.
19. Hayashi, T., Hideshima, T., Akiyama, M., Podar, K., Yasui, H., Raje, N., Kumar, S., Chauhan, D., Treon, S.P., Richardson, P. & Anderson, K.C. (2005) Molecular mechanisms whereby immunomodulatory drugs activate natural killer cells: clinical application. British Journal of Haematology, 128, 192-203.
20. Hofmann, O., Caballero, O.L., Stevenson, B.J., Chen, Y.T., Cohen, T., Chua, R., Maher, C.A., Panji, S., Schaefer, U., Kruger, A., Lehvaslaiho, M., Carninci, P., Hayashizaki, Y., Jongeneel, C.V., Simpson, A.J., Old, L.J. & Hide, W. (2008) Genome-wide analysis of cancer/testis gene expression. Proceedings of the National Academy of Sciences of the USA, 105, 20422-20427.
21. Hunder, N.N., Wallen, H., Cao, J., Hendricks, D.W., Reilly, J.Z., Rodmyre, R., Jungbluth, A., Gnjatic, S., Thompson, J.A. & Yee, C. (2008) Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. New England Journal of Medicine, 358, 2698-2703.
22. Jungbluth, A., Ely, S., DiLiberto, M., Niesvizky, R., Williamson, B., Frosina, D., Chen, Y., 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.
23. Kiziltepe, T., Hideshima, T., Catley, L., Raje, N., Yasui, H., Shiraishi, N., Okawa, Y., Ikeda, H., Vallet, S., Pozzi, S., Ishitsuka, K., Ocio, E.M., Chauhan, D. & Anderson, K.C. (2007) 5-Azacytidine, a DNA methyltransferase inhibitor, induces ATR-mediated DNA double-strand break responses, apoptosis, and synergistic cytotoxicity with doxorubicin and bortezomib against multiple myeloma cells. Molecular Cancer Therapeutics, 6, 1718-1727.
24. Klebanoff, C.A., Khong, H.T., Antony, P.A., Palmer, D.C. & Restifo, N.P. (2005) Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends in Immunology, 26, 111-117.
25. Kmieciak, M., Basu, D., Payne, K.K., Toor, A., Yacoub, A., Wang, X., Smith, L., Bear, H.D. & Manjili, M.H. (2011a) Activated NKT cells and NK cells render T cells resistant to myeloid-derived suppressor cells and result in an effective adoptive cellular therapy against breast cancer in the FVBN202 transgenic Mouse. The Journal of Immunology, 187, 708-717.
26. Kmieciak, M., Payne, K.K., Idowu, M.O., Grimes, M.M., Graham, L., Ascierto, M., Wang, E., Wang, X., Bear, H.D. & Manjili, M. (2011b) Tumor escape and progression of HER-2/neu negative breast cancer under immune pressure. Journal of Translational Medicine, 9, 35.
27. LeBlanc, R., Hideshima, T., Catley, L., Shringarpure, R., Burger, R., Mitsiades, N., Mitsiades, C., Cheema, P., Chauhan, D., Richardson, P.G., Anderson, K.C. & Munshi, N.C. (2004) Immunomodulatory drug costimulates T cells via the B7-CD28 pathway. Blood, 103, 1787-1790.
28. Lecoutre, B., Derzko, G. & Grouin, J.M. (1995) Bayesian predictive approach for inference about proportions. Statistics in Medicine, 14, 1057-1063.
29. Lim, S.Y., Laxmanan, S., Stuart, G. & Ghosh, S.K. (2001) Anti-lymphoma immunity: relative efficacy of peptide and recombinant DNA vaccine. Cancer Detection and Prevention, 25, 470-478.
30. Martinez-Garcia, E., Popovic, R., Min, D.J., Sweet, S.M.M., Thomas, P.M., Zamdborg, L., Heffner, A., Will, C., Lamy, L., Staudt, L.M., Levens, D.L., Kelleher, N.L. & Licht, J.D. (2011) The MMSET histone methyl transferase switches global histone methylation and alters gene expression in t(4;14) multiple myeloma cells. Blood, 117, 211-220.
31. McLarnon, A., Piper, K.P., Goodyear, O.C., Arrazi, J.M., Mahendra, P., Cook, M., Clark, F., Pratt, G., Craddock, C. & Moss, P.A.H. (2010) CD8(+) T-cell immunity against cancer-testis antigens develops following allogeneic stem cell transplantation and reveals a potential mechanism for the graft-versus-leukemia effect. Haematologica, 95, 1572-1578.
32. Meklat, F., Li, Z., Wang, Z., Zhang, Y., Zhang, J., Jewell, A. & Lim, S.H. (2007) Cancer-testis antigens in haematological malignancies. British Journal of Haematology, 136, 769-776.
33. Miklos, D.B., Kim, H.T., Miller, K.H., Guo, L., Zorn, E., Lee, S.J., Hochberg, E.P., Wu, C.J., Alyea, E.P., Cutler, C., Ho, V., Soiffer, R.J., Antin, J.H. & Ritz, J. (2005) Antibody responses to H-Y minor histocompatibility antigens correlate with chronic graft-versus-host disease and disease remission. Blood, 105, 2973-2978.
34. Moreno-Bost, A., Szmania, S., Stone, K., Garg, T., Hoerring, A., Szymonifka, J., Shaughnessy, J., Barlogie, B., Prentice, H.G. & Van Rhee, F. (2011) 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, 13, 618-628.
35. 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. International Journal of Cancer, 122, 2542-2553.
36. Nojima, M., Maruyama, R., Yasui, H., Suzuki, H., Maruyama, Y., Tarasawa, I., Sasaki, Y., Asaoku, H., Sakai, H., Hayashi, T., Mori, M., Imai, K., Tokino, T., Ishida, T., Toyota, M. & Shinomura, Y. (2009) Genomic screening for genes silenced by DNA methylation revealed an association between RASD1 inactivation and dexamethasone resistance in multiple myeloma. Clinical Cancer Research, 15, 4356-4364.
37. Rapoport, A.P., Stadtmauer, E.A., Aqui, N., Badros, A., Cotte, J., Chrisley, L., Veloso, E., Zheng, Z., Westphal, S., Mair, R., Chi, N., Ratterree, B., Pochran, M.F., Natt, S., Hinkle, J., Sickles, C., Sohal, A., Ruehle, K., Lynch, C., Zhang, L., Porter, D.L., Luge, S., Guo, C., Fang, H., Blackwelder, W., Hankey, K., Mann, D., Edelman1, R., Frasch, C., Levine, B.L., Cross, A. & June, C.H. (2005) Restoration of immunity in lymphopenic individuals with cancer by vaccination and adoptive T-cell transfer. Nature Medicine, 11, 1230-1237.
38. Rapoport, A.P., Stadtmauer, E.A., Aqui, N., Vogl, D., Chew, A., Fang, H., Janofsky, S., Yager, K., Veloso, E., Zheng, Z., Milliron, T., Westphal, S., Cotte, J., Huynh, H., Cannon, A., Yanovich, S., Akpekl, G., Tan, M., Virts, K., Ruehle, K., Harris, C., Phillip, S., Vonderheide, R.H., Levine, B.L. & June, C.H. (2009) Rapid Immune Recovery and graft-versus-host disease-like engraftment syndrome following adoptive transfer of costimulated autologous T cells. Clinical Cancer Research, 15, 4499-4507.
39. Shlomchik, W.D. (2007) Graft-versus-host disease. Nature reviews. Immunology, 7, 340-352.
40. 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.
41. Sloand, E.M., Kim, S., Maciejewski, J.P., Van Rhee, F., Chaudhuri, A., Barrett, J. & Young, N.S. (2000) Pharmacologic doses of granulocyte colony-stimulating factor affect cytokine production by lymphocytes in vitro and in vivo. Blood, 95, 2269-2274.
42. Tatetsu, H., Ueno, S., Hata, H., Yamada, Y., Takeya, M., Mitsuya, H., Tenen, D.G. & Okuno, Y. (2007) Down-regulation of PU.1 by methylation of distal regulatory elements and the promoter is required for myeloma cell growth. Cancer Research, 67, 5328-5336.
43. Van Rhee, F., Szmania, S., 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.
44. Wang, Z., Zhang, Y., Liu, H., Salati, E., Chiriva-Internati, M. & Lim, S.H. (2003) Gene expression and immunologic consequence of SPAN-Xb in myeloma and other hematologic malignancies. Blood, 101, 955-960.