Exploiting tumor epigenetics to improve oncolytic virotherapy

Frontiers in Genetics

Volumn 4, Issue SEP, 2013, Pages

  Forbes, Nicole E ^a,b   Abdelbary, Hesham ^a,b   Lupien, Mathieu ^c,d,e   Bell, John C ^a,b   Diallo, Jean Simon ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Anti viral response; Antigen presentation; Cancer; Epigenetic modulation; Oncolytic virotherapy; Tumor heterogeneity

Indexed keywords

EID: 84885983827     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00184     Document Type: Review

References (116)

1. Akhtar-Zaidi, B., Cowper-Sal-Lari, R., Corradin, O., Saiakhova, A., Bartels, C. F., Balasubramanian, D., et al. (2012). Epigenomic enhancer profiling defines a signature of colon cancer. Science 336, 736-739. doi:10.1126/science.1217277.
2. Alvarez-Breckenridge, C. A., Yu, J., Price, R., Wei, M., Wang, Y., Nowicki, M. O., et al. (2012). The histone deacetylase inhibitor valproic acid lessens NK cell action against oncolytic virus-infected glioblastoma cells by inhibition of STAT5/T-BET signaling and generation of gamma interferon. J. Virol. 86, 4566-4577. doi:10.1128/JVI.05545-11.
3. Asada, T. (1974). Treatment of human cancer with mumps virus. Cancer 34, 1907-1928. doi:10.1002/1097-0142(197412)34:6<1907::AID-CNCR2820340609>3.0.CO;2-4.
4. Bae, S. I., Cheriyath, V., Jacobs, B. S., Reu, F. J., and Borden, E. C. (2008). Reversal of methylation silencing of Apo2L/TRAIL receptor 1 (DR4) expression overcomes resistance of SK-MEL-3 and SK-MEL-28 melanoma cells to interferons (IFNs) or Apo2L/TRAIL. Oncogene 27, 490-498.
5. Bannister, A. J., and Kouzarides, T. (2011). Regulation of chromatin by histone modifications. Cell Res. 21, 381-395. doi:10.1038/cr.2011.22.
6. Bateman, A., Bullough, F., Murphy, S., Emiliusen, L., Lavillette, D., Cosset, F. L., et al. (2000). Fusogenic membrane glycoproteins as a novel class of genes for the local and immune-mediated control of tumor growth. Cancer Res. 60, 1492-1497.
7. Bateman, A. R., Harrington, K. J., Kottke, T., Ahmed, A., Melcher, A. A., Gough, M. J., et al. (2002). Viral fusogenic membrane glycoproteins kill solid tumor cells by non-apoptotic mechanisms that promote cross presentation of tumor antigens by dendritic cells. Cancer Res. 62, 6566-6578.
8. Baylin, S. B., and Jones, P. A. (2011). A decade of exploring the cancer epigenome-biological and translational implications. Nat. Rev. Cancer 11, 726-734.
9. Bennani-Baiti, I. M., Machado, I., Llombart-Bosch, A., and Kovar, H. (2012). Lysine-specific demethylase 1 (LSD1/KDM1A/AOF2/BHC110) is expressed and is an epigenetic drug target in chondrosarcoma, Ewing's sarcoma, osteosarcoma, and rhabdomyosarcoma. Hum. Pathol. 43, 1300#x02013;1307.
10. Borden, E. C. (2007). Augmentation of effects of interferon-stimulated genes by reversal of epigenetic silencing:potential application to melanoma. Cytokine Growth Factor Rev. 18, 491-501. doi:10.1016/j.cytogfr.2007.06.022.
11. Borden, E. C., Sen, G. C., Uze, G., Silverman, R. H., Ransohoff, R. M., Foster, G. R., et al. (2007). Interferons at age 50:past, current, and future impact on biomedicine. Nat. Rev. Drug Discov. 6, 975-990. doi:10.1038/nrd2422.
12. Breitbach, C. J., Burke, J., Jonker, D., Stephenson, J., Haas, A. R., Chow, L. Q., et al. (2011). Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans. Nature 477, 99-102. doi:10.1038/nature10358.
13. Bridle, B. W., Chen, L., Lemay, C. G., Diallo, J.-S., Pol, J., Nguyen, A., et al. (2013). HDAC inhibition suppresses primary immune responses, enhances secondary immune responses, and abrogates autoimmunity during tumor immunotherapy. Mol. Ther. 21, 887-894. doi:10.1038/mt.2012.265.
14. Bridle, B. W., Stephenson, K. B., Boudreau, J. E., Koshy, S., Kazdhan, N., Pullenayegum, E., et al. (2010). Potentiating cancer immunotherapy using an oncolytic virus. Mol. Ther. 18, 1430-1439. doi:10.1038/mt.2010.98.
15. Burton, T. R., Henson, E. S., Azad, M. B., Brown, M., Eisenstat, D. D., and Gibson, S. B. (2013). BNIP3 acts as transcriptional repressor of death receptor-5 expression and prevents TRAIL-induced cell death in gliomas. Cell Death Dis. 4, e587. doi:10.1038/cddis.2013.100.
16. Carroll, J. (2011). Amgen bets $1B on BioVex's dual-mechanism cancer therapy. Fierce Biotech. Available at:http://www.fiercebiotech.com/story/amgen-bets-1b-biovexs-dual-mechanism-cancer-therapy/2011-01-25 (accessed April 3, 2013).
17. Cedar, H., and Bergman, Y. (2009). Linking DNA methylation and histone modification:patterns and paradigms. Nat. Rev. Genet. 10, 295-304. doi:10.1038/nrg2540.
18. Chai, L., Liu, S., Mao, Q., Wang, D., Li, X., Zheng, X., et al. (2012). A novel conditionally replicating adenoviral vector with dual expression of IL-24 and arresten inserted in E1 and the region between E4 and fiber for improved melanoma therapy. Cancer Gene Ther. 19, 247-254. doi:10.1038/cgt.2011.84.
19. Chang, H. M., Paulson, M., Holko, M., Rice, C. M., Williams, B. R., Marie, I., et al. (2004). Induction of interferon-stimulated gene expression and antiviral responses require protein deacetylase activity. Proc. Natl. Acad. Sci. U.S.A. 101, 9578-9583. doi:10.1073/pnas.0400567101.
20. Chen, Q., Denard, B., Huang, H., and Ye, J. (2013). Epigenetic silencing of antiviral genes renders clones of Huh-7 cells permissive for hepatitis C virus replication. J. Virol. 87, 659-665. doi:10.1128/jvi.01984-12.
21. Chiocca, E. A. (2008). The host response to cancer virotherapy. Curr. Opin. Mol. Ther. 10, 38-45.
22. Cho, H., Proll, S. C., Szretter, K. J., Katze, M. G., Gale, M., and Diamond, M. S. (2013). Differential innate immune response programs in neuronal subtypes determine susceptibility to infection in the brain by positive-stranded RNA viruses. Nat. Med.
23. Chou, S. D. (2005). Histone acetylation regulates the cell type specific CIITA promoters, MHC class II expression and antigen presentation in tumor cells. Int. Immunol. 17, 1483-1494. doi:10.1093/intimm/dxh326.
24. De Carvalho, D. D., Sharma, S., You, J. S., Su, S. F., Taberlay, P. C., Kelly, T. K., et al. (2012). DNA methylation screening identifies driver epigenetic events of cancer cell. Cancer Cell 21, 655-667. doi:10.1016/j.ccr.2012.03.045.
25. Diallo, J. S., Le Boeuf, F., Lai, F., Cox, J., Vaha-Koskela, M., Abdelbary, H., et al. (2010). A high-throughput pharmacoviral approach identifies novel oncolytic virus sensitizers. Mol. Ther. 18, 1123-1129. doi:10.1038/mt.2010.67.
26. Diaz, R. M., Galivo, F., Kottke, T., Wongthida, P., Qiao, J., Thompson, J., et al. (2007). Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res. 67, 2840-2848. doi:10.1158/0008-5472.can-06-3974.
27. Dock, G. (1904). The influence of complicating diseases upon leukemia. Am. J. Med. Sci. 127, 563-592.
28. Dunn, G. P., Koebel, C. M., and Schreiber, R. D. (2006). Interferons, immunity, and cancer immunoediting. Nat. Rev. Immunol. 6, 836-848. doi:10.1038/nri1961.
29. Dunn, G. P., Sheehan, K. C., Old, L. J., and Schreiber, R. D. (2005). IFN unresponsiveness in LNCaP cells due to the lack of JAK1 gene expression. Cancer Res. 65, 3447-3453. doi:10.1158/0008-5472.can-04-4316.
30. Egger, G., Liang, G., Aparicio, A., and Jones, P. A. (2004). Epigenetics in human disease and prospects for epigenetic therapy. Nature 429, 457-463. doi:10.1038/nature02625.
31. Fang, T. C., Schaefer, U., Mecklenbrauker, I., Stienen, A., Dewell, S., Chen, M. S., et al. (2012). Histone H3 lysine 9 di-methylation as an epigenetic signature of the interferon response. J. Exp. Med. 209, 661-669. doi:10.1084/jem.20112343.
32. Farassati, F., Yang, A. D., and Lee, P. W. (2001). Oncogenes in Ras signalling pathway dictate host-cell permissiveness to herpes simplex virus 1. Nat. Cell Biol. 3, 745-750. doi:10.1038/35087061.
33. Fridman, A. L., Tang, L., Kulaeva, O. I., Ye, B., Li, Q., Nahhas, F., et al. (2006). Expression profiling identifies three pathways altered in cellular immortalization:interferon, cell cycle, and cytoskeleton. J. Gerontol. A Biol. Sci. Med. Sci. 61, 879-889. doi:10.1093/gerona/61.9.879.
34. Fritz, V., and Fajas, L. (2010). Metabolism and proliferation share common regulatory pathways in cancer cells. Oncogene 29, 4369-4377. doi:10.1038/onc.2010.182.
35. Galanis, E., Markovic, S. N., Suman, V. J., Nuovo, G. J., Vile, R. G., Kottke, T. J., et al. (2012). Phase II trial of intravenous administration of Reolysin(®) (Reovirus Serotype-3-dearing Strain) in patients with metastatic melanoma. Mol. Ther. 20, 1998-2003. doi:10.1038/mt.2012.146.
36. Génin, P., Morin, P., and Civas, A. (2003). Impairment of interferon-induced IRF-7 gene expression due to inhibition of ISGF3 formation by trichostatin A. J. Virol. 77, 7113-7119. doi:10.1128/JVI.77.12.7113-7119.2003.
37. Glasspool, R. M., Teodoridis, J. M., and Brown, R. (2006). Epigenetics as a mechanism driving polygenic clinical drug resistance. Br. J. Cancer 94, 1087-1092. doi:10.1038/sj.bjc.6603024.
38. Gomez, J. A., Wapinski, O. L., Yang, Y. W., Bureau, J.-F., Gopinath, S., Monack, D. M., et al. (2013). The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-? locus. Cell 152, 743-754. doi:10.1016/j.cell.2013.01.015.
39. Hacker, S., Dittrich, A., Mohr, A., Schweitzer, T., Rutkowski, S., Krauss, J., et al. (2009). Histone deacetylase inhibitors cooperate with IFN-gamma to restore caspase-8 expression and overcome TRAIL resistance in cancers with silencing of caspase-8. Oncogene 28, 3097-3110. doi:10.1038/onc.2009.161.
40. Hatziapostolou, M., and Iliopoulos, D. (2011). Epigenetic aberrations during oncogenesis. Cell. Mol. Life. Sci. 68, 1681-1702. doi:10.1007/s00018-010-0624-z.
41. Heo, J., Reid, T., Ruo, L., Breitbach, C. J., Rose, S., Bloomston, M., et al. (2013). Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat. Med. 19, 329-336. doi:10.1038/nm.3089.
42. Holling, T. M., Bergevoet, M. W., Wilson, L., Van Eggermond, M. C., Schooten, E., Steenbergen, R. D., et al. (2007). A role for EZH2 in silencing of IFN-gamma inducible MHC2TA transcription in uveal melanoma. J. Immunol. 179, 5317-5325.
43. Hoti, N., Chowdhury, W., Hsieh, J. T., Sachs, M. D., Lupold, S. E., and Rodriguez, R. (2006). Valproic acid, a histone deacetylase inhibitor, is an antagonist for oncolytic adenoviral gene therapy. Mol. Ther. 14, 768-778.
44. Huang, P. Y., Guo, J. H., and Hwang, L. H. (2012). Oncolytic Sindbis virus targets tumors defective in the interferon response and induces significant bystander antitumor immunity in vivo. Mol. Ther. 20, 298-305. doi:10.1038/mt.2011.245.
45. Hurtubise, A., Bernstein, M. L., and Momparler, R. L. (2008). Preclinical evaluation of the antineoplastic action of 5-aza-2'-deoxycytidine and different histone deacetylase inhibitors on human Ewing's sarcoma cells. Cancer Cell Int. 8, 16. doi:10.1186/1475-2867-8-16.
46. Jain, R. K. (2005). Normalization of tumor vasculature:an emerging concept in antiangiogenic therapy. Science 307, 58-62. doi:10.1126/science.1104819.
47. Janson, P. C., Marits, P., Thorn, M., Ohlsson, R., and Winqvist, O. (2008). CpG methylation of the IFNG gene as a mechanism to induce immunosuppression [correction of immunosupression] in tumor-infiltrating lymphocytes. J. Immunol. 181, 2878-2886.
48. Johnsen, A. K., Templeton, D. J., Sy, M., and Harding, C. V. (1999). Deficiency of transporter for antigen presentation (TAP) in tumor cells allows evasion of immune surveillance and increases tumorigenesis. J. Immunol. 163, 4224-4231.
49. Johnsson, A., Durand-Dubief, M., Xue-Franzen, Y., Ronnerblad, M., Ekwall, K., and Wright, A. (2009). HAT-HDAC interplay modulates global histone H3K14 acetylation in gene-coding. EMBO Rep. 10, 1009-1014.
50. Kanaseki, T., Ikeda, H., Takamura, Y., Toyota, M., Hirohashi, Y., Tokino, T., et al. (2003). Histone deacetylation, but not hypermethylation, modifies class II transactivator and MHC class II gene expression in squamous cell carcinomas. J. Immunol. 170, 4980-4985.
51. Karpf, A. R., Peterson, P. W., Rawlins, J. T., Dalley, B. K., Yang, Q., Albertson, H., et al. (1999). Inhibition of DNA methyltransferase stimulates the expression of signal transducer and activator of transcription 1, 2, and 3 genes in colon tumor cells. Proc. Natl. Acad. Sci. U.S.A. 96, 14007-14012.
52. Katsura, T., Iwai, S., Ota, Y., Shimizu, H., Ikuta, K., and Yura, Y. (2009). The effects of trichostatin A on the oncolytic ability of herpes simplex virus for oral squamous cell carcinoma cells. Cancer Gene Ther. 16, 237-245. doi:10.1038/cgt.2008.81.
53. Kelly, E., and Russell, S. J. (2007). History of oncolytic viruses:genesis to genetic engineering. Mol. Ther. 15, 651-659. doi:10.1038/sj.mt.6300108.
54. Khan, A. N., Magner, W., and Tomasi, T. (2004). An epigenetically altered tumor cell vaccine. Cancer Immunol. Immunother. 53, 748-754. doi:10.1007/s00262-004-0513-0.
55. Khan, A. N. H., Magner, W. J., and Tomasi, T. B. (2007). An epigenetic vaccine model active in the prevention and treatment of melanoma. J. Transl. Med. 5, 64. doi:10.1186/1479-5876-5-64.
56. Klampfer, L., Huang, J., Swaby, L. A., and Augenlicht, L. (2004). Requirement of histone deacetylase activity for signaling by STAT1. J. Biol. Chem. 279, 30358-30368. doi:10.1074/jbc. M401359200.
57. Krecmerova, M., and Otmar, M. (2012). 5-azacytosine compounds in medicinal chemistry:current stage and future perspectives. Future Med. Chem. 4, 991-1005. doi:10.4155/fmc.12.36.
58. Kulaeva, O. I., Draghici, S., Tang, L., Kraniak, J. M., Land, S. J., and Tainsky, M. A. (2003). Epigenetic silencing of multiple interferon pathway genes after cellular immortalization. Oncogene 22, 4118-4127. doi:10.1038/sj.onc.1206594.
59. Lange, S., Lampe, J., Bossow, S., Zimmermann, M., Neubert, W., Bitzer, M., et al. (2013). A novel armed oncolytic measles vaccine virus for the treatment of cholangiocarcinoma. Hum. Gene Ther. 24, 554-564. doi:10.1089/hum.2012.136.
60. Lee, J., Goh, S.-H., Song, N., Hwang, J.-A., Nam, S., Choi, I. J., et al. (2012). Overexpression of IFITM1 has clinicopathologic effects on gastric cancer and is regulated by an epigenetic mechanism. Am. J. Pathol. 181, 43-52. doi:10.1016/j.ajpath.2012.03.027.
61. Lee, K. Y., Geng, H., Ng, K. M., Yu, J., Van Hasselt, A., Cao, Y., et al. (2008). Epigenetic disruption of interferon-? response through silencing the tumor suppressor interferon regulatory factor 8 in nasopharyngeal, esophageal, and multiple other carcinomas. Oncogene 27, 5267-5276. doi:10.1038/onc.2008.147.
62. LeibundGut-Landmann, S., Waldburger, J.-M., Krawczyk, M., Otten, L. A., Suter, T., Fontana, A., et al. (2004). Mini-review:specificity and expression of CIITA, the master regulator of MHC class II genes. Eur. J. Immunol. 34, 1513-1525. doi:10.1002/eji.200424964.
63. Lemay, C. G., Rintoul, J. L., Kus, A., Paterson, J. M., Garcia, V., Falls, T. J., et al. (2012). Harnessing oncolytic virus-mediated antitumor immunity in an infected cell vaccine. Mol. Ther. 20, 1791-1799. doi:10.1038/mt.2012.128.
64. Li, K., Markosyan, R. M., Zheng, Y. M., Golfetto, O., Bungart, B., Li, M., et al. (2013). IFITM proteins restrict viral membrane hemifusion. PLoS Pathog. 9:e1003124. doi:10.1371/journal.ppat.1003124.
65. Li, Q., Tang, L., Roberts, P. C., Kraniak, J. M., Fridman, A. L., Kulaeva, O. I., et al. (2008). Interferon regulatory factors IRF5 and IRF7 inhibit growth and induce senescence in immortal Li-Fraumeni fibroblasts. Mol. Cancer Res. 6, 770-784. doi:10.1158/1541-7786.mcr-07-0114.
66. Liikanen, I., Monsurro, V., Ahtiainen, L., Raki, M., Hakkarainen, T., Diaconu, I., et al. (2011). Induction of interferon pathways mediates in vivo resistance to oncolytic adenovirus. Mol. Ther. 19, 1858-1866. doi:10.1038/mt.2011.144.
67. Londhe, P., Zhu, B., Abraham, J., Keller, C., and Davie, J. (2012). CIITA is silenced by epigenetic mechanisms that prevent the recruitment of transactivating factors in rhabdomyosarcoma cells. Int. J. Cancer 131, E437-E448. doi:10.1002/ijc.26478.
68. Lubieniecka, J. M., De Bruijn, D. R., Su, L., Van Dijk, A. H., Subramanian, S., Van De Rijn, M., et al. (2008). Histone deacetylase inhibitors reverse SS18-SSX-mediated polycomb silencing of the tumor suppressor early growth response 1 in synovial sarcoma. Cancer Res. 68, 4303-4310. doi:10.1158/0008-5472.can-08-0092.
69. Lund, P., Kotova, I., Kedinger, V., Khanwalkar, H., Voltz, E., Hahn, W. C., et al. (2011). Transformation-dependent silencing of tumor-selective apoptosis-inducing TRAIL by DNA hypermethylation is antagonized by decitabine. Mol. Cancer Ther. 10, 1611-1623. doi:10.1158/1535-7163.MCT-11-0140.
70. MacTavish, H., Diallo, J. S., Huang, B., Stanford, M., Le Boeuf, F., De Silva, N., et al. (2011). Enhancement of vaccinia virus based oncolysis with histone deacetylase inhibitors. PLoS ONE 5:e14462. doi:10.1371/journal.pone.0014462.
71. Magnani, L., Eeckhoute, J., and Lupien, M. (2011). Pioneer factors:directing transcriptional regulators within the chromatin environment. Trends Genet. 27, 465-474. doi:10.1016/j.tig.2011.07.002.
72. Magnani, L., Stoeck, A., Zhang, X., Lanczky, A., Mirabella, A. C., Wang, T. L., et al. (2013). Genome-wide reprogramming of the chromatin landscape underlies endocrine therapy resistance in breast cancer. Proc. Natl. Acad. Sci. U.S.A. 110, E1490-E1499. doi:10.1073/pnas.1219992110.
73. Maldonado, A. R., Klanke, C., Jegga, A. G., Aronow, B. J., Mahller, Y. Y., Cripe, T. P., et al. (2010). Molecular engineering and validation of an oncolytic herpes simplex virus type 1 transcriptionally targeted to midkine-positive tumors. J. Gene Med. 12, 613-623. doi:10.1002/jgm.1479.
74. Meissner, M., Whiteside, T. L., Van Kuik-Romein, P., Valesky, E. M., Van Den Elsen, P. J., Kaufmann, R., et al. (2008). Loss of interferon-? inducibility of the MHC class II antigen processing pathway in head and neck cancer:evidence for post-transcriptional as well as epigenetic regulation. Br. J. Dermatol. 158, 930-940. doi:10.1111/j.1365-2133.2008.08465.x.
75. Merrick, A. E., Ilett, E. J., and Melcher, A. A. (2009). JX-594, a targeted oncolytic poxvirus for the treatment of cancer. Curr. Opin. Investig. Drugs 10, 1372-1382.
76. Morimoto, Y., Toyota, M., Satoh, A., Murai, M., Mita, H., Suzuki, H., et al. (2004). Inactivation of class II transactivator by DNA methylation and histone deacetylation associated with absence of HLA-DR induction by interferon-? in haematopoietic tumour cells. Br. J. Cancer 90, 844-852.
77. Morris, A. C., Spangler, W. E., and Boss, J. M. (2000). Methylation of class II trans-activator promoter IV:a novel mechanism of MHC class II gene control. J. Immunol. 164, 4143-4149.
78. Muhlethaler-Mottet, A., Di Berardino, W., Otten, L. A., and Mach, B. (1998). Activation of the MHC class II transactivator CIITA by interferon-gamma requires cooperative interaction between Stat1 and USF-1. Immunity8, 157-166.
79. Muntean, A. G., and Hess, J. L. (2009). Epigenetic dysregulation in cancer. Am. J. Pathol. 175, 1353-1361. doi:10.2353/ajpath.2009.081142.
80. Naka, K., Abe, K., Takemoto, K., Dansako, H., Ikeda, M., Shimotohno, K., et al. (2006). Epigenetic silencing of interferon-inducible genes is implicated in interferon resistance of hepatitis C virus replicon-harboring cells. J. Hepatol. 44, 869-878. doi:10.1016/j.jhep.2006.01.030.
81. Nguyen, T. L., Abdelbary, H., Arguello, M., Breitbach, C., Leveille, S., Diallo, J. S., et al. (2008). Chemical targeting of the innate antiviral response by histone deacetylase inhibitors renders refractory cancers sensitive to viral oncolysis. Proc. Natl. Acad. Sci. U.S.A. 105, 14981-14986. doi:10.1073/pnas.0803988105.
82. Norman, K., and Lee, P. (2000). Reovirus as a novel oncolytic agent. J. Clin. Invest. 105, 1035-1038. doi:10.1172/JCI9871.
83. Nusinzon, I., and Horvath, C. M. (2003). Interferon-stimulated transcription and innate antiviral immunity require deacetylase activity and histone deacetylase 1. Proc. Natl. Acad. Sci. U.S.A. 100, 14742-14747. doi:10.1073/pnas.2433987100.
84. Okemoto, K., Wagner, B. P., Haseley, A. M., Price, R. L., Kaur, B., and Chiocca, A. E. (2012). 5-Azacitydine augments the anti-glioma efficacy of Herpes-based oncolytic virotherapy. AACR 103rd Annual Meeting 2012:Cancer Research, Chicago.
85. Otsuki, A., Patel, A., Kasai, K., Suzuki, M., Kurozumi, K., Antonio Chiocca, E., et al. (2008). Histone deacetylase inhibitors augment antitumor efficacy of herpes-based oncolytic viruses. Mol. Ther. 16, 1546-1555. doi:10.1038/mt.2008.155.
86. Parato, K. A., Senger, D., Forsyth, P. A., and Bell, J. C. (2005). Recent progress in the battle between oncolytic viruses and tumours. Nat. Rev. Cancer 5, 965-976. doi:10.1038/nrc1750.
87. Patel, N., Black, J., Chen, X., Marcondes, A. M., Grady, W. M., Lawlor, E. R., et al. (2012). DNA methylation and gene expression profiling of ewing sarcoma primary tumors reveal genes that are potential targets of epigenetic inactivation. Sarcoma 2012, 498472. doi:10.1155/2012/498472.
88. Peserico, A., and Simone, C. (2010). Physical and functional HAT/HDAC interplay regulates protein acetylation balance. J. Biomed. Biotechnol. 2011, 371832.
89. Pol, J., Le Boeuf, F., and Diallo, J. S. (2013). [Genetic, immunological, and pharmacological strategies to generate improved oncolytic viruses]. Med. Sci. (Paris) 29, 165-173.
90. Pulido, J., Kottke, T., Thompson, J., Galivo, F., Wongthida, P., Diaz, R. M., et al. (2012). Using virally expressed melanoma cDNA libraries to identify tumor-associated antigens that cure melanoma. Nat. Biotechnol. 30, 337-343. doi:10.1038/nbt.2157.
91. Radosevich, M., Jager, M., and Ono, S. J. (2007). Inhibition of MHC class II gene expression in uveal melanoma cells is due to methylation of the CIITA gene or an upstream activator. Exp. Mol. Pathol. 82, 68-76. doi:10.1016/j.yexmp.2006.03.005.
92. Reu, F. J., Bae, S. I., Cherkassky, L., Leaman, D. W., Lindner, D., Beaulieu, N., et al. (2006a). Overcoming resistance to interferon-induced apoptosis of renal carcinoma and melanoma cells by DNA demethylation. J. Clin. Oncol. 24, 3771-3779. doi:10.1200/jco.2005.03.4074.
93. Reu, F. J., Leaman, D. W., Maitra, R. R., Bae, S. I., Cherkassky, L., Fox, M. W., et al. (2006b). Expression of RASSF1A, an epigenetically silenced tumor suppressor, overcomes resistance to apoptosis induction by interferons. Cancer Res. 66, 2785-2793. doi:10.1158/0008-5472.can-05-2303.
94. Rice, J. C., and Allis, C. D. (2001). Histone methylation versus histone acetylation:new insights into epigenetic regulation. Curr. Opin. Cell Biol. 13, 263-273. doi:10.1016/S0955-0674(00)00208-8.
95. Russell, S. J., Peng, K. W., and Bell, J. C. (2012). Oncolytic virotherapy. Nat. Biotechnol. 30, 658-670. doi:10.1038/nbt.2287.
96. Sakamoto, S., Potla, R., and Larner, A. C. (2004). Histone deacetylase activity is required to recruit RNA polymerase II to the promoters of selected interferon-stimulated early response genes. J. Biol. Chem. 279, 40362-40367. doi:10.1074/jbc. M406400200.
97. Satoh, A., Toyota, M., Ikeda, H., Morimoto, Y., Akino, K., Mita, H., et al. (2004). Epigenetic inactivation of class II transactivator (CIITA) is associated with the absence of interferon-?-induced HLA-DR expression in colorectal and gastric cancer cells. Oncogene 23, 8876-8886. doi:10.1038/sj.onc.1208144.
98. Schenk, T., Chen, W. C., Gollner, S., Howell, L., Jin, L., Hebestreit, K., et al. (2012). Inhibition of the LSD1 (KDM1A) demethylase reactivates the all-trans-retinoic acid differentiation pathway in acute myeloid leukemia. Nat. Med. 18, 605-611. doi:10.1038/nm.2661.
99. Schildhaus, H.-U., Riegel, R., Hartmann, W., Steiner, S., Wardelmann, E., Merkelbach-Bruse, S., et al. (2011). Lysine-specific demethylase 1 is highly expressed in solitary fibrous tumors, synovial sarcomas, rhabdomyosarcomas, desmoplastic small round cell tumors, and malignant peripheral nerve sheath tumors. Hum. Pathol. 42, 1667-1675. doi:10.1016/j.humpath.2010.12.025.
100. Setiadi, A. F., David, M. D., Seipp, R. P., Hartikainen, J. A., Gopaul, R., and Jefferies, W. A. (2007). Epigenetic control of the immune escape mechanisms in malignant carcinomas. Mol. Cell. Biol. 27, 7886-7894. doi:10.1128/mcb.01547-07.
101. Shmulevitz, M., Marcato, P., and Lee, P. W. (2005). Unshackling the links between reovirus oncolysis, Ras signaling, translational control and cancer. Oncogene 24, 7720-7728. doi:10.1038/sj.onc.1209041.
102. Sobol, P. T., Boudreau, J. E., Stephenson, K., Wan, Y., Lichty, B. D., and Mossman, K. L. (2011). Adaptive antiviral immunity is a determinant of the therapeutic success of oncolytic virotherapy. Mol. Ther. 19, 335-344. doi:10.1038/mt.2010.264.
103. Soncini, M., Santoro, F., Gutierrez, A., Frige, G., Romanenghi, M., Botrugno, O. A., et al. (2013). The DNA demethylating agent decitabine activates the TRAIL pathway and induces apoptosis in acute myeloid leukemia. Biochim. Biophys. Acta 1832, 114-120. doi:10.1016/j.bbadis.2012.10.001.
104. Stephenson, K. B., Barra, N. G., Davies, E., Ashkar, A. A., and Lichty, B. D. (2012). Expressing human interleukin-15 from oncolytic vesicular stomatitis virus improves survival in a murine metastatic colon adenocarcinoma model through the enhancement of anti-tumor immunity. Cancer Gene Ther. 19, 238-246. doi:10.1038/cgt.2011.81.
105. Stojdl, D. F., Lichty, B., Knowles, S., Marius, R., Atkins, H., Sonenberg, N., et al. (2000). Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6, 821-825. doi:10.1038/77558.
106. Stojdl, D. F., Lichty, B. D., Tenoever, B. R., Paterson, J. M., Power, A. T., Knowles, S., et al. (2003). VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4, 263-275. doi:10.1016/S1535-6108(03)00241-1.
107. Suh, H.-S., Choi, S., Khattar, P., Choi, N., and Lee, S. C. (2010). Histone deacetylase inhibitors suppress the expression of inflammatory and innate immune response genes in human microglia and astrocytes. J. Neuroimmune Pharmacol. 5, 521-532. doi:10.1007/s11481-010-9192-0.
108. Suva, M. L., Riggi, N., and Bernstein, B. E. (2013). Epigenetic reprogramming in cancer. Science 339, 1567-1570. doi:10.1126/science.1230184.
109. Taylor, B. S., Decarolis, P. L., Angeles, C. V., Brenet, F., Schultz, N., Antonescu, C. R., et al. (2011). Frequent alterations and epigenetic silencing of differentiation pathway genes in structurally rearranged liposarcomas. Cancer Discov. 1, 587-597. doi:10.1158/2159-8290.cd-11-0181.
110. Truax, A. D., Thakkar, M., and Greer, S. F. (2012). Dysregulated recruitment of the histone methyltransferase EZH2 to the class II transactivator (CIITA) promoter IV in breast cancer cells. PLoS ONE 7:e36013. doi:10.1371/journal.pone.0036013.
111. Vigneau, S., Levillayer, F., Crespeau, H., Cattolico, L., Caudron, B., Bihl, F., et al. (2001). Homology between a 173-kb region from mouse chromosome 10, telomeric to the Ifng locus, and human chromosome 12q15. Genomics 78, 206-213. doi:10.1006/geno.2001.6656.
112. Watanabe, T., Hioki, M., Fujiwara, T., Nishizaki, M., Kagawa, S., Taki, M., et al. (2006). Histone deacetylase inhibitor FR901228 enhances the antitumor effect of telomerase-specific replication-selective adenoviral agent OBP-301 in human lung cancer cells. Exp. Cell Res. 312, 256-265.
113. U.S. National Library of Medicine (2013). ClinicalTrials.gov [Online]. Available at:www.clinicaltrials.gov [accessed January 29, 2013].
114. Yamashita, M., Toyota, M., Suzuki, H., Nojima, M., Yamamoto, E., Kamimae, S., et al. (2010). DNA methylation of interferon regulatory factors in gastric cancer and non-cancerous gastric mucosae. Cancer Sci. 101, 1708-1716. doi:10.1111/j.1349-7006.2010.01581.x.
115. Yoo, C. B., and Jones, P. A. (2006). Epigenetic therapy of cancer:past, present, and future. Nat. Rev. Drug Discov. 5, 37-50. doi:10.1038/nrd1930.
116. Yu, F., Ng, S. S., Chow, B. K., Sze, J., Lu, G., Poon, W. S., et al. (2011). Knockdown of interferon-induced transmembrane protein 1 (IFITM1) inhibits proliferation, migration, and invasion of glioma cells. J. Neurooncol. 103, 187-195. doi:10.1007/s11060-010-0377-4.