DNA demethylating agents synergize with oncolytic HSV1 against malignant gliomas

Clinical Cancer Research

Volumn 19, Issue 21, 2013, Pages 5952-5959

  Okemoto, Kazuo ^a   Kasai, Kazue ^c   Wagner, Benjamin ^a   Haseley, Amy ^a   Meisen, Hans ^a   Bolyard, Chelsea ^a   Mo, Xiaokui ^a   Wehr, Allison ^a   Lehman, Amy ^b   Fernandez, Soledad ^b   Kaur, Balveen ^a   Chiocca, E Antonio ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c Brigham and Women's/Faulkner Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; AZACITIDINE; ONCOLYTIC HERPES VIRUS; RQNESTIN34.5; UNCLASSIFIED DRUG; VALPROIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DNA METHYLATION; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; GLIOBLASTOMA; GLIOMA CELL; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL DESTRUCTION; TUMOR XENOGRAFT; VIRUS REPLICATION;

ANIMALS; AZACITIDINE; CELL LINE, TUMOR; CELL SURVIVAL; CPG ISLANDS; DISEASE MODELS, ANIMAL; DNA METHYLATION; ENHANCER ELEMENTS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, VIRAL; GENETIC THERAPY; GENETIC VECTORS; GLIOMA; HERPESVIRUS 1, HUMAN; HUMANS; MICE; NESTIN; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PROMOTER REGIONS, GENETIC; VIRAL PROTEINS; VIRUS REPLICATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84887116567     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-3588     Document Type: Article

References (35)

1. Chiocca EA. Oncolytic viruses. Nat Rev Cancer 2002;2: 938-50.
2. Grandi P, Peruzzi P, Reinhart B, Cohen JB, Chiocca EA, Glorioso JC. Design and application of oncolytic HSV vectors for glioblastoma therapy. Expert Rev Neurother 2009;9: 505-17.
3. Mohyeldin A, Chiocca EA. Gene and viral therapy for glioblastoma: a review of clinical trials and future directions. Cancer J 2012;18: 82-8.
4. Aghi M, Visted T, Depinho RA, Chiocca EA. Oncolytic herpes virus with defective ICP6 specifically replicates in quiescent cells with homozygous genetic mutations in p16. Oncogene 2008;27: 4249-54.
5. Markert JM, Liechty PG, Wang W, Gaston S, Braz E, Karrasch M, et al. Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol Ther 2009;17: 199-207.
6. Bergbauer M, Kalla M, Schmeinck A, Gobel C, Rothbauer U, Eck S, et al. CpG-methylation regulates a class of Epstein-Barr virus promoters. PLoS Pathog 2010;6:e1001114.
7. Bloom DC, Giordani NV, Kwiatkowski DL. Epigenetic regulation of latent HSV-1 gene expression. Biochim Biophys Acta 2010;1799: 246-56.
8. Kwiatkowski DL, Thompson HW, Bloom DC. The polycomb group protein Bmi1 binds to the herpes simplex virus 1 latent genome and maintains repressive histone marks during latency. J Virol 2009;83: 8173-81.
9. Kubat NJ, Tran RK, McAnany P, Bloom DC. Specific histone tail modification and not DNA methylation is a determinant of herpes simplex virus type 1 latent gene expression. J Virol 2004;78: 1139-49.
10. Kambara H, Okano H, Chiocca EA, Saeki Y. An oncolytic HSV-1 mutant expressing ICP34.5 under control of a nestin promoter increases survival of animals even when symptomatic from a brain tumor. Cancer Res 2005;65: 2832-9.
11. Kambara H, Saeki Y, Chiocca EA. Cyclophosphamide allows for in vivo dose reduction of a potent oncolytic virus. Cancer Res 2005;65: 11255-8.
12. Otsuki A, Patel A, Kasai K, Suzuki M, Kurozumi K, Chiocca EA, et al. Histone deacetylase inhibitors augment antitumor efficacy of herpesbased oncolytic viruses. Mol Ther 2008;16: 1546-55.
13. Klein J, Moeschberger M. Survival analysis: techniques for censored and truncated data. 2nd ed. New York: Springer-Verlag; 2003.
14. Schiffer D, Annovazzi L, Caldera V, Mellai M. On the origin and growth of gliomas. Anticancer Res 2010;30: 1977-98.
15. Xie Z. Brain tumor stem cells. Neurochem Res 2009;34: 2055-66.
16. Dell'Albani P. Stem cell markers in gliomas. Neurochem Res 2008;33: 2407-15.
17. Singh SK, Clarke ID, Hide T, Dirks PB. Cancer stem cells in nervous system tumors. Oncogene 2004;23: 7267-73.
18. Detich N, Bovenzi V, Szyf M. Valproate induces replication-independent active DNA demethylation. J Biol Chem 2003;278: 27586-92.
19. Dong E, Chen Y, Gavin DP, Grayson DR, Guidotti A. Valproate induces DNA demethylation in nuclear extracts from adult mouse brain. Epigenetics 2010;5: 730-5.
20. Milutinovic S, D'Alessio AC, Detich N, Szyf M. Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes. Carcinogenesis 2007;28: 560-71.
21. Reid G, Metivier R, Lin CY, Denger S, Ibberson D, Ivacevic T, et al. Multiple mechanisms induce transcriptional silencing of a subset of genes, including oestrogen receptor alpha, in response to deacetylase inhibition by valproic acid and trichostatin A. Oncogene 2005;24: 4894-907.
22. Van Nifterik KA, Van den Berg J, Slotman BJ, Lafleur MV, Sminia P, Stalpers LJ. Valproic acid sensitizes human glioma cells for temozolomide and gamma-radiation. J Neurooncol 2012;107: 61-7.
23. Aghi M, KrammCM, Chou TC, Breakefield XO, Chiocca EA. Synergistic anticancer effects of ganciclovir/thymidine kinase and 5-fluorocytosine/cytosine deaminase gene therapies. J Natl Cancer Inst 1998; 90: 370-80.
24. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984;22: 27-55.
25. Ichikawa T, Chiocca EA. Comparative analyses of transgene delivery and expression in tumors inoculated with a replication-conditional or -defective viral vector. Cancer Res 2001;61: 5336-9.
26. Alvarez-Breckenridge CA, Yu J, Kaur B, Caligiuri MA, Chiocca EA. Deciphering the multifaceted relationship between oncolytic viruses and natural killer cells. Adv Virol 2012;2012: 702839.
27. Alvarez-Breckenridge CA, Yu J, Price R, Wei M, Wang Y, Nowicki MO, et al. 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 2012;86: 4566-77.
28. Kundakovic M, Chen Y, Guidotti A, Grayson DR. The reelin and GAD67 promoters are activated by epigenetic drugs that facilitate the disruption of local repressor complexes. Molecular pharmacology 2009;75: 342-54.
29. Foltz G, Yoon JG, Lee H, Ryken TC, Sibenaller Z, Ehrich M, et al. DNA methyltransferase-mediated transcriptional silencing in malignant glioma: a combined whole-genome microarray and promoter array analysis. Oncogene 2009;28: 2667-77.
30. Rajendran G, Shanmuganandam K, Bendre A, Muzumdar D, Goel A, Shiras A. Epigenetic regulation of DNA methyltransferases: DNMT1 and DNMT3B in gliomas. J Neurooncol 2011;104: 483-94.
31. Bartoli A, Fettucciari K, Fetriconi I, Rosati E, Di Ianni M, Tabilio A, et al. Effect of trichostatin a and 5'-azacytidine on transgene reactivation in U937 transduced cells. Pharmacol Res 2003;48: 111-8.
32. James CD, He J, Carlbom E, Nordenskjold M, Cavenee WK, Collins VP. Chromosome 9 deletion mapping reveals interferon alpha and interferon beta-1 gene deletions in human glial tumors. Cancer Res 1991;51: 1684-8.
33. Miyakoshi J, Dobler KD, Allalunis-Turner J, McKean JD, Petruk K, Allen PB, et al. Absence of IFNA and IFNB genes from human malignant glioma cell lines and lack of correlation with cellular sensitivity to interferons. Cancer Res 1990;50: 278-83.
34. Li Q, Tainsky MA. Epigenetic silencing of IRF7 and/or IRF5 in lung cancer cells leads to increased sensitivity to oncolytic viruses. PLoS One 2011;6:e28683.
35. Alvarez-Breckenridge C, Kaur B, Chiocca EA. Pharmacologic and chemical adjuvants in tumor virotherapy. Chem Rev 2009;109: 3125-40.