Immunomodulatory action of the DNA methyltransferase inhibitor SGI-110 in epithelial ovarian cancer cells and xenografts

References

• Odunsi K, Jungbluth AA, Stockert E, Qian F, Gnjatic S, Tammela J, Intengan M, Beck A, Keitz B, Santiago D, et al. NY-ESO-1 and LAGE-1 cancer-testis antigens are potential targets for immunotherapy in epithelial ovarian cancer. Cancer Res 2003; 63:6076-83; PMID:14522938
   PubMed Web of Science ®Google Scholar
• Woloszynska-Read A, Mhawech-Fauceglia P, Yu J, Odunsi K, Karpf AR. Intertumor and intratumor NY-ESO-1 expression heterogeneity is associated with promoter-specific and global DNA methylation status in ovarian cancer. Clin Cancer Res 2008; 14:3283-90; PMID:18519754; http://dx.doi.org/10.1158/1078-0432.CCR-07-5279
   PubMed Web of Science ®Google Scholar
• Imura M, Yamashita S, Cai LY, Furuta J, Wakabayashi M, Yasugi T, Ushijima T. Methylation and expression analysis of 15 genes and three normally-methylated genes in 13 ovarian cancer cell lines. Cancer Lett 2006; 241:213-20; PMID:16303245; http://dx.doi.org/10.1016/j.canlet.2005.10.010
   PubMed Web of Science ®Google Scholar
• Gnjatic S, Atanackovic D, Jager E, Matsuo M, Selvakumar A, Altorki NK, Maki RG, Dupont B, Ritter G, Chen YT, et al. Survey of naturally occurring CD4+ T cell responses against NY-ESO-1 in cancer patients: Correlation with antibody responses. Proc Natl Acad Sci U S A 2003; 100:8862-7; PMID:12853579; http://dx.doi.org/10.1073/pnas.1133324100
   PubMed Web of Science ®Google Scholar
• Stone B, Schummer M, Paley PJ, Thompson L, Stewart J, Ford M, Crawford M, Urban N, O'Briant K, Nelson BH. Serologic analysis of ovarian tumor antigens reveals a bias toward antigens encoded on 17q. Int J Cancer 2003; 104:73-84; PMID:12532422; http://dx.doi.org/10.1002/ijc.10900
   PubMed Web of Science ®Google Scholar
• Huarte E, Karbach J, Gnjatic S, Bender A, Jager D, Arand M, Atanackovic D, Skipper J, Ritter G, Chen YT, et al. HLA-DP4 expression and immunity to NY-ESO-1: Correlation and characterization of cytotoxic CD4+ CD25- CD8- T cell clones. Cancer Immun 2004; 4:15; PMID:15600300
   PubMedGoogle Scholar
• Qian F, Gnjatic S, Jager E, Santiago D, Jungbluth A, Grande C, Schneider S, Keitz B, Driscoll D, Ritter G, et al. Th1/Th2 CD4+ T cell responses against NY-ESO-1 in HLA-DPB1*0401/0402 patients with epithelial ovarian cancer. Cancer Immun 2004; 4:12; PMID:15521719
   PubMedGoogle Scholar
• Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, Jungbluth AA, Frosina D, Gnjatic S, Ambrosone C, et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 2005; 102:18538-43; PMID:16344461; http://dx.doi.org/10.1073/pnas.0509182102
   PubMed Web of Science ®Google Scholar
• Odunsi K, Qian F, Matsuzaki J, Mhawech-Fauceglia P, Andrews C, Hoffman EW, Pan L, Ritter G, Villella J, Thomas B, et al. Vaccination with an NY-ESO-1 peptide of HLA class I/II specificities induces integrated humoral and T cell responses in ovarian cancer. Proc Natl Acad Sci U S A 2007; 104:12837-42; PMID:17652518; http://dx.doi.org/10.1073/pnas.0703342104
   PubMed Web of Science ®Google Scholar
• Karbach J, Gnjatic S, Bender A, Neumann A, Weidmann E, Yuan J, Ferrara CA, Hoffmann E, Old LJ, Altorki NK, et al. Tumor-reactive CD8+ T-cell responses after vaccination with NY-ESO-1 peptide, CpG 7909 and montanide ISA-51: Association with survival. Int J Cancer 2010; 126:909-18; PMID:19728336; http://dx.doi.org/10.1002/ijc.24850
   PubMed Web of Science ®Google Scholar
• Odunsi K, Matsuzaki J, Karbach J, Neumann A, Mhawech-Fauceglia P, Miller A, Beck A, Morrison CD, Ritter G, Godoy H, et al. Efficacy of vaccination with recombinant vaccinia and fowlpox vectors expressing NY-ESO-1 antigen in ovarian cancer and melanoma patients. Proc Natl Acad Sci U S A 2012; 109:5797-802; PMID:22454499; http://dx.doi.org/10.1073/pnas.1117208109
   PubMed Web of Science ®Google Scholar
• Sabbatini P, Tsuji T, Ferran L, Ritter E, Sedrak C, Tuballes K, Jungbluth AA, Ritter G, Aghajanian C, Bell-McGuinn K, et al. Phase I trial of overlapping long peptides from a tumor self-antigen and poly-ICLC shows rapid induction of integrated immune response in ovarian cancer patients. Clin Cancer Res 2012; 18:6497-508; PMID:23032745; http://dx.doi.org/10.1158/1078-0432.CCR-12-2189
   PubMed Web of Science ®Google Scholar
• Nicholaou T, Chen W, Davis ID, Jackson HM, Dimopoulos N, Barrow C, Browning J, Macgregor D, Williams D, Hopkins W, et al. Immunoediting and persistence of antigen-specific immunity in patients who have previously been vaccinated with NY-ESO-1 protein formulated in ISCOMATRIX. Cancer Immunol Immunother 2011; 60:1625-37; PMID:21698545; http://dx.doi.org/10.1007/s00262-011-1041-3
   PubMed Web of Science ®Google Scholar
• De Smet C, Loriot A, Boon T. Promoter-dependent mechanism leading to selective hypomethylation within the 5′ region of gene MAGE-A1 in tumor cells. Mol Cell Biol 2004; 24:4781-90; PMID:15143172; http://dx.doi.org/10.1128/MCB.24.11.4781-4790.2004
   PubMed Web of Science ®Google Scholar
• Akers SN, Odunsi K, Karpf AR. Regulation of cancer germline antigen gene expression: Implications for cancer immunotherapy. Future Oncol 2010; 6:717-32; PMID:20465387; http://dx.doi.org/10.2217/fon.10.36
   PubMed Web of Science ®Google Scholar
• Loriot A, De Plaen E, Boon T, De Smet C. Transient down-regulation of DNMT1 methyltransferase leads to activation and stable hypomethylation of MAGE-A1 in melanoma cells. J Biol Chem 2006; 281:10118-26; PMID:16497664; http://dx.doi.org/ M510469200 [pii]
   PubMed Web of Science ®Google Scholar
• Weber J, Salgaller M, Samid D, Johnson B, Herlyn M, Lassam N, Treisman J, Rosenberg SA. Expression of the MAGE-1 tumor antigen is up-regulated by the demethylating agent 5-aza-2′-deoxycytidine. Cancer Res 1994; 54:1766-71; PMID:7511051
   PubMed Web of Science ®Google Scholar
• Karpf AR, Lasek AW, Ririe TO, Hanks AN, Grossman D, Jones DA. Limited gene activation in tumor and normal epithelial cells treated with the DNA methyltransferase inhibitor 5-aza-2′-deoxycytidine. Mol Pharmacol 2004; 65:18-27; PMID:14722233; http://dx.doi.org/10.1124/mol.65.1.18
   PubMed Web of Science ®Google Scholar
• Srivastava P, Paluch BE, Matsuzaki J, James SR, Collamat-Lai G, Karbach J, Nemeth MJ, Taverna P, Karpf AR, Griffiths EA. Immunomodulatory action of SGI-110, a hypomethylating agent, in acute myeloid leukemia cells and xenografts. Leuk Res 2014; 38:1332-41; PMID:25260825; http://dx.doi.org/10.1016/j.leukres.2014.09.001
   PubMed Web of Science ®Google Scholar
• 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; PMID:18791715; http://dx.doi.org/10.1007/s00262-008-0582-6
   PubMed Web of Science ®Google Scholar
• Coral S, Parisi G, Nicolay HJ, Colizzi F, Danielli R, Fratta E, Covre A, Taverna P, Sigalotti L, Maio M. Immunomodulatory activity of SGI-110, a 5-aza-2′-deoxycytidine-containing demethylating dinucleotide. Cancer Immunol Immunother 2013; 62:605-14; PMID:23138873; http://dx.doi.org/10.1007/s00262-012-1365-7
   PubMed Web of Science ®Google Scholar
• Karpf AR. A potential role for epigenetic modulatory drugs in the enhancement of cancer/germ-line antigen vaccine efficacy. Epigenetics 2006; 1:116-20; PMID:17786175
   PubMed Web of Science ®Google Scholar
• Griffiths EA, Gore SD. Epigenetic therapies in MDS and AML. Adv Exp Med Biol 2013; 754:253-83; PMID:22956506; http://dx.doi.org/10.1007/978-1-4419-9967-2_13
   PubMed Web of Science ®Google Scholar
• Samlowski WE, Leachman SA, Wade M, Cassidy P, Porter-Gill P, Busby L, Wheeler R, Boucher K, Fitzpatrick F, Jones DA, et al. Evaluation of a 7-day continuous intravenous infusion of decitabine: Inhibition of promoter-specific and global genomic DNA methylation. J Clin Oncol 2005; 23:3897-905; PMID:15753459; http://dx.doi.org/ JCO.2005.06.118 [pii]
   PubMed Web of Science ®Google Scholar
• Sessa C, Suinink W, Stoter G, Renard J, Cavalli F. Phase II study of 5-aza-2′-deoxycytidine in advanced ovarian carcinoma. the EORTC early clinical trials group. Eur J Cancer 1990; 26:137-8; PMID:1691012
   PubMed Web of Science ®Google Scholar
• Bellet RE, Catalano RB, Mastrangelo MJ, Berd D. Phase II study of subcutaneously administered 5-azacytidine (NSC-102816) in patients with metastatic malignant melanoma. Med Pediatr Oncol 1978; 4:11-5; PMID:75498
   PubMedGoogle Scholar
• Yoo CB, Jeong S, Egger G, Liang G, Phiasivongsa P, Tang C, Redkar S, Jones PA. Delivery of 5-aza-2′-deoxycytidine to cells using oligodeoxynucleotides. Cancer Res 2007; 67:6400-8; PMID:17616700; http://dx.doi.org/ 67/13/6400 [pii]
   PubMed Web of Science ®Google Scholar
• Griffiths EA, Choy G, Redkar S, Taverna P, Azab M, Karpf AR. SGI-110. DNA methyltransferase inhibitor, oncolytic. Drugs Fut 2013; 38:535.
   PubMed Web of Science ®Google Scholar
• Stresemann C, Lyko F. Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int J Cancer 2008; 123:8-13; PMID:18425818; http://dx.doi.org/10.1002/ijc.23607
   PubMed Web of Science ®Google Scholar
• Woloszynska-Read A, Zhang W, Yu J, Link PA, Mhawech-Fauceglia P, Collamat G, Akers SN, Ostler KR, Godley LA, Odunsi K, et al. Coordinated cancer germline antigen promoter and global DNA hypomethylation in ovarian cancer: Association with the BORIS/CTCF expression ratio and advanced stage. Clin Cancer Res 2011; 17:2170-80; PMID:21296871; http://dx.doi.org/10.1158/1078-0432.CCR-10-2315
   PubMed Web of Science ®Google Scholar
• Kantarjian H, Roboz G, Rizzieri D, Stock W, O’Connell C, Griffiths EA, Yee K, Tibes R, Garcia-Manero G, Ravandi F, et al. Results from the dose escalation phase of a randomized phase 1–2 first-in-human (FIH) study of SGI-110, a novel low volume stable subcutaneous (SQ) second generation hypomethylating agent (HMA) in patients with relapsed/refractory MDS and AML. Blood 2012; 120:414
   Google Scholar
• De Plaen E, Arden K, Traversari C, Gaforio JJ, Szikora JP, De Smet C, Brasseur F, van der Bruggen P, Lethe B, Lurquin C. Structure, chromosomal localization, and expression of 12 genes of the MAGE family. Immunogenetics 1994; 40:360-9; PMID:7927540
   PubMed Web of Science ®Google Scholar
• Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, Roederer M, Koup RA. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 2003; 281:65-78; PMID:14580882
   PubMed Web of Science ®Google Scholar
• Oflazoglu E, Elliott M, Takita H, Ferrone S, Henderson RA, Repasky EA. Adoptively transferred human lung tumor specific cytotoxic T cells can control autologous tumor growth and shape tumor phenotype in a SCID mouse xenograft model. J Transl Med 2007; 5:29; PMID:17592641; http://dx.doi.org/ 1479-5876-5-29 [pii]
   PubMed Web of Science ®Google Scholar
• Natsume A, Wakabayashi T, Tsujimura K, Shimato S, Ito M, Kuzushima K, Kondo Y, Sekido Y, Kawatsura H, Narita Y, et al. The DNA demethylating agent 5-aza-2′-deoxycytidine activates NY-ESO-1 antigenicity in orthotopic human glioma. Int J Cancer 2008; 122:2542-53; PMID:18240144; http://dx.doi.org/10.1002/ijc.23407
   PubMed Web of Science ®Google Scholar
• Fang F, Munck J, Tang J, Taverna P, Wang Y, Miller DF, Pilrose J, Choy G, Azab M, Pawelczak KS, et al. The novel, small-molecule DNA methylation inhibitor SGI-110 as an ovarian cancer chemosensitizer. Clin Cancer Res 2014; 20:6504-16; PMID:25316809; http://dx.doi.org/10.1158/1078-0432.CCR-14-1553
   PubMed Web of Science ®Google Scholar
• Clinicaltrials.gov. A randomized, controlled, open-label, phase 2 trial of SGI-110 and carboplatin in subjects with platinum-resistant recurrent ovarian cancer: NCT01696032. 2014; 2014
   Google Scholar
• Odunsi K, Matsuzaki J, James SR, Mhawech-Fauceglia P, Tsuji T, Miller A, Zhang W, Akers SN, Griffiths EA, Miliotto A, et al. Epigenetic potentiation of NY-ESO-1 vaccine therapy in human ovarian cancer. Cancer Immunol Res 2014; 2:37-49
   PubMed Web of Science ®Google Scholar
• Matei D, Fang F, Shen C, Schilder J, Arnold A, Zeng Y, Berry WA, Huang T, Nephew KP. Epigenetic resensitization to platinum in ovarian cancer. Cancer Res 2012; 72:2197-205; PMID:22549947; http://dx.doi.org/10.1158/0008-5472.CAN-11-3909
   PubMed Web of Science ®Google Scholar
• Schrump DS, Fischette MR, Nguyen DM, Zhao M, Li X, Kunst TF, Hancox A, Hong JA, Chen GA, Pishchik V, et al. Phase I study of decitabine-mediated gene expression in patients with cancers involving the lungs, esophagus, or pleura. Clin Cancer Res 2006; 12:5777-85; PMID:17020984; http://dx.doi.org/10.1158/1078-0432.CCR-06-0669
   PubMed Web of Science ®Google Scholar
• Link PA, Gangisetty O, James SR, Woloszynska-Read A, Tachibana M, Shinkai Y, Karpf AR. Distinct roles for histone methyltransferases G9a and GLP in cancer germ-line antigen gene regulation in human cancer cells and murine embryonic stem cells. Mol Cancer Res 2009; 7:851-62; PMID:19531572; http://dx.doi.org/10.1158/1541-7786.MCR-08-0497
   PubMed Web of Science ®Google Scholar
• Wischnewski F, Pantel K, Schwarzenbach H. Promoter demethylation and histone acetylation mediate gene expression of MAGE-A1, -A2, -A3, and -A12 in human cancer cells. Mol Cancer Res 2006; 4:339-49; PMID:16687489; http://dx.doi.org/ 4/5/339 [pii]
   PubMed Web of Science ®Google Scholar
• James SR, Cedeno CD, Sharma A, Zhang W, Mohler JL, Odunsi K, Wilson EM, Karpf AR. DNA methylation and nucleosome occupancy regulate the cancer germline antigen gene MAGEA11. Epigenetics 2013; 8:849-63; PMID:23839233; http://dx.doi.org/10.4161/epi.25500
   PubMed Web of Science ®Google Scholar
• Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: A novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 1996; 93:9821-6; PMID:8790415
   PubMed Web of Science ®Google Scholar
• Li LC, Dahiya R. MethPrimer: Designing primers for methylation PCRs. Bioinformatics 2002; 18:1427-31; PMID:12424112
   PubMed Web of Science ®Google Scholar