Histones and their modifications in ovarian cancer - drivers of disease and therapeutic targets

Frontiers in Oncology

Volumn 4 JUN, Issue , 2014, Pages

  Marsh, Deborah J ^a   Shah, Jaynish S ^a   Cole, Alexander J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Deubiquitinases; Histone; Histone deacetylase inhibitors; Histone methyltransferases; lncRNA; Ovarian cancer; Polycomb repressive complex; Splicing

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ANTINEOPLASTIC AGENT; BORTEZOMIB; CARFILZOMIB; CISPLATIN; DEUBIQUITINASE; EPZ005687; GSK126; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HISTONE DEACETYLASE INHIBITOR M344; HISTONE H2B; HISTONE METHYLTRANSFERASE; HOX TRANSCRIPT ANTISENSE INTERGENIC RNA; LONG UNTRANSLATED RNA; MICRORNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OLAPARIB; POLYCOMB GROUP PROTEIN; PROTEIN P53; ROMIDEPSIN; RUCAPARIB; SIRTUIN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EZH2; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VALPROIC ACID; VE465; VELIPARIB; VORINOSTAT;

CANCER THERAPY; DRUG TARGETING; EPIGENETICS; GENE EXPRESSION; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HISTONE SPLICING; HISTONE UBIQUITINATION; HUMAN; MOLECULAR INTERACTION; NONHUMAN; OVARY CANCER; OVARY CARCINOMA; PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; SEROUS EPITHELIAL OVARIAN CANCER;

EID: 84904604801     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00144     Document Type: Review

References (152)

1. Visintin I, Feng Z, Longton G, Ward DC, Alvero AB, Lai Y, et al. Diagnostic markers for early detection of ovarian cancer. Clin Cancer Res (2008) 14:1065-72. doi: 10.1158/1078-0432.CCR-07-1569
2. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin (2010) 60:277-300. doi:10.3322/caac.20073
3. Jordan S, Steer C, Defazio A, Quinn M, Obermair A, Friedlander M, et al. Patterns of chemotherapy treatment for women with invasive epithelial ovarian cancer-a population-based study. Gynecol Oncol (2013) 129:310-7. doi:10.1016/j.ygyno.2013.02.007
4. Monneret C. Platinum anticancer drugs. From serendipity to rational design. Ann Pharm Fr (2011) 69:286-95. doi:10.1016/j.pharma.2011.10.001
5. Wani MC, Horwitz SB. Nature as a remarkable chemist: a personal story of the discovery and development of Taxol. Anticancer Drugs (2014) 25:482-7. doi:10.1097/CAD.0000000000000063
6. Tangjitgamol S, Manusirivithaya S, Laopaiboon M, Lumbiganon P, Bryant A. Interval debulking surgery for advanced epithelial ovarian cancer. Cochrane Database Syst Rev (2013) 4:CD006014. doi:10.1002/14651858.CD006014.pub6
7. da Costa Miranda V, De Souza Fede AB, Dos Anjos CH, Da Silva JR, Sanchez FB,Dda Silva Bessa LR, et al. Neoadjuvant chemotherapy with six cycles of carboplatin and paclitaxel in advanced ovarian cancer patients unsuitable for primary surgery: safety and effectiveness. Gynecol Oncol (2014) 132:287-91. doi:10.1016/j.ygyno.2013.12.002
8. Sabbatini P. Consolidation therapy in ovarian cancer: a clinical update. Int J Gynecol Cancer (2009) 19(Suppl 2):S35-9. doi:10.1111/IGC.0b013e3181c14007
9. Vaughan S, Coward JI, Bast RC Jr, Berchuck A, Berek JS, Brenton JD, et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer (2011) 11:719-25. doi:10.1038/nrc3144
10. Levanon K, Crum C, Drapkin R. New insights into the pathogenesis of serous ovarian cancer and its clinical impact. J Clin Oncol (2008) 26:5284-93. doi:10.1200/JCO.2008.18.1107
11. Perets R, Wyant GA, Muto KW, Bijron JG, Poole BB, Chin KT, et al. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models. Cancer Cell (2013) 24:751-65. doi:10.1016/j.ccr.2013.10.013
12. Tothill RW, Tinker AV, George J, Brown R, Fox SB, Lade S, et al. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin Cancer Res (2008) 14:5198-208. doi:10.1158/1078-0432.CCR-08-0196
13. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature (2011) 474:609-15. doi:10.1038/nature10166
14. Kobayashi N, Abedini M, Sakuragi N, Tsang BK. PRIMA-1 increases cisplatin sensitivity in chemoresistant ovarian cancer cells with p53 mutation: a requirement for Akt down-regulation. J Ovarian Res (2013) 6:7. doi:10.1186/1757-2215-6-7
15. Domcke S, Sinha R, Levine DA, Sander C, Schultz N. Evaluating cell lines as tumour models by comparison of genomic profiles. Nat Commun (2013) 4:2126. doi:10.1038/ncomms3126
16. Chionh F, Mitchell G, Lindeman GJ, Friedlander M, Scott CL. The role of poly adenosine diphosphate ribose polymerase inhibitors in breast and ovarian cancer: current status and future directions. Asia Pac J Clin Oncol (2011) 7:197-211. doi:10.1111/j.1743-7563.2011.01430.x
17. Itamochi H, Kigawa J. Clinical trials and future potential of targeted therapy for ovarian cancer. Int J Clin Oncol (2012) 17:430-40. doi:10.1007/s10147-012-0459-8
18. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell (2010) 40:179-204. doi:10.1016/j.molcel.2010.09.019
19. Alsop K, Fereday S, Meldrum C, Defazio A, Emmanuel C, George J, et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J Clin Oncol (2012) 30:2654-63. doi:10.1200/JCO.2011.39.8545
20. O'Sullivan CC, Moon DH, Kohn EC, Lee JM. Beyond breast and ovarian cancers: PARP inhibitors for BRCA mutation-associated and BRCA-like solid tumors. Front Oncol (2014) 4:42. doi:10.3389/fonc.2014.00042
21. Nowsheen S, Cooper T, Bonner JA, Lobuglio AF, Yang ES. HER2 overexpression renders human breast cancers sensitive to PARP inhibition independently of any defect in homologous recombination DNA repair. Cancer Res (2012) 72:4796-806. doi:10.1158/0008-5472.CAN-12-1287
22. Barber LJ, Sandhu S, Chen L, Campbell J, Kozarewa I, Fenwick K, et al. Secondary mutations in BRCA2 associated with clinical resistance to a PARP inhibitor. J Pathol (2013) 229:422-9. doi:10.1002/path.4140
23. Fojo T, Bates S. Mechanisms of resistance to PARP inhibitors-three and counting. Cancer Discov (2013) 3:20-3. doi:10.1158/2159-8290.CD-12-0514
24. Wang Z, Wang F, Tang T, Guo C. The role of PARP1 in the DNA damage response and its application in tumor therapy. Front Med (2012) 6:156-64. doi:10.1007/s11684-012-0197-3
25. Kwon MJ, Shin YK. Epigenetic regulation of cancer-associated genes in ovarian cancer. Int J Mol Sci (2011) 12:983-1008. doi:10.3390/ijms12020983
26. Zeller C, Dai W, Steele NL, Siddiq A, Walley AJ, Wilhelm-Benartzi CS, et al. Candidate DNA methylation drivers of acquired cisplatin resistance in ovarian cancer identified by methylome and expression profiling. Oncogene (2012) 31:4567-76. doi:10.1038/onc.2011.611
27. Baldwin RL, Nemeth E, Tran H, Shvartsman H, Cass I, Narod S, et al. BRCA1 promoter region hypermethylation in ovarian carcinoma: a population-based study. Cancer Res (2000) 60:5329-33.
28. Schondorf T, Ebert MP, Hoffmann J, Becker M, Moser N, Pur S, et al. Hypermethylation of the PTEN gene in ovarian cancer cell lines. Cancer Lett (2004) 207:215-20. doi:10.1016/j.canlet.2003.10.028
29. Baba T, Convery PA, Matsumura N, Whitaker RS, Kondoh E, Perry T, et al. Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene (2009) 28:209-18. doi:10.1038/onc.2008.374
30. Izutsu N, Maesawa C, Shibazaki M, Oikawa H, Shoji T, Sugiyama T, et al. Epigenetic modification is involved in aberrant expression of class III beta-tubulin, TUBB3, in ovarian cancer cells. Int J Oncol (2008) 32:1227-35.
31. Cheng W, Jiang Y, Liu C, Shen O, Tang W, Wang X. Identification of aberrant promoter hypomethylation of HOXA10 in ovarian cancer. J Cancer Res Clin Oncol (2010) 136:1221-7. doi:10.1007/s00432-010-0772-4
32. Gifford G, Paul J, Vasey PA, Kaye SB, Brown R. The acquisition of hMLH1 methylation in plasma DNA after chemotherapy predicts poor survival for ovarian cancer patients. Clin Cancer Res (2004) 10:4420-6. doi:10.1158/1078-0432.CCR-03-0732
33. Plumb JA, Strathdee G, Sludden J, Kaye SB, Brown R. Reversal of drug resistance in human tumor xenografts by 2'-deoxy-5-azacytidine-induced demethylation of the hMLH1 gene promoter. Cancer Res (2000) 60:6039-44.
34. Fuks F. DNA methylation and histone modifications: teaming up to silence genes. Curr Opin Genet Dev (2005) 15:490-5. doi:10.1016/j.gde.2005.08.002
35. Balch C, Fang F, Matei DE, Huang TH, Nephew KP. Minireview: epigenetic changes in ovarian cancer. Endocrinology (2009) 150:4003-11. doi:10.1210/en.2009-0404
36. Asadollahi R, Hyde CA, Zhong XY. Epigenetics of ovarian cancer: from the lab to the clinic. Gynecol Oncol (2010) 118:81-7. doi:10.1016/j.ygyno.2010.03.015
37. Hendzel MJ, Greenberg RA. Conversations between chromatin modifications and DNA double strand break repair: a commentary. Mutat Res (2013) 750:1-4. doi:10.1016/j.mrfmmm.2013.08.003
38. Jones PA. At the tipping point for epigenetic therapies in cancer. J Clin Invest (2014) 124:14-6. doi:10.1172/JCI74145
39. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature (1997) 389:251-60. doi:10.1038/38444
40. Dawson MA, Kouzarides T, Huntly BJ. Targeting epigenetic readers in cancer. N Engl J Med (2012) 367:647-57. doi:10.1056/NEJMra1112635
41. Th'ng JP, Sung R, Ye M, Hendzel MJ. H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. J Biol Chem (2005) 280:27809-14. doi:10.1074/jbc.M501627200
42. Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell (2012) 150:12-27. doi:10.1016/j.cell.2012.06.013
43. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell (2007) 129:823-37. doi:10.1016/j.cell.2007.05.009
44. Abbosh PH, Montgomery JS, Starkey JA, Novotny M, Zuhowski EG, Egorin MJ, et al. Dominant-negative histone H3 lysine 27 mutant derepresses silenced tumor suppressor genes and reverses the drug-resistant phenotype in cancer cells. Cancer Res (2006) 66:5582-91. doi:10.1158/0008-5472.CAN-05-3575
45. Johnsen SA. The enigmatic role of H2Bub1 in cancer. FEBS Lett (2012) 586:1592-601. doi:10.1016/j.febslet.2012.04.002
46. Fuchs G, Oren M. Writing and reading H2B monoubiquitylation. Biochim Biophys Acta (2014). doi:10.1016/j.bbagrm.2014.01.002
47. Zhang K, Dent SY. Histone modifying enzymes and cancer: going beyond histones. J Cell Biochem (2005) 96:1137-48. doi:10.1002/jcb.20615
48. Verdin E, Dequiedt F, Kasler HG. Class II histone deacetylases: versatile regulators. Trends Genet (2003) 19:286-93. doi:10.1016/S0168-9525(03)00073-8
49. Ropero S, Esteller M. The role of histone deacetylases (HDACs) in human cancer. Mol Oncol (2007) 1:19-25. doi:10.1016/j.molonc.2007.01.001
50. Hayashi A, Horiuchi A, Kikuchi N, Hayashi T, Fuseya C, Suzuki A, et al. Type-specific roles of histone deacetylase (HDAC) overexpression in ovarian carcinoma: HDAC1 enhances cell proliferation and HDAC3 stimulates cell migration with downregulation of E-cadherin. Int J Cancer (2010) 127:1332-46. doi:10.1002/ijc.25151
51. Gatta R, Dolfini D, Zambelli F, Imbriano C, Pavesi G, Mantovani R. An acetylation-mono-ubiquitination switch on lysine 120 of H2B. Epigenetics (2011) 6:630-7. doi:10.4161/epi.6.5.15623
52. Yuan H, Su L, Chen WY. The emerging and diverse roles of sirtuins in cancer: a clinical perspective. Onco Targets Ther (2013) 6:1399-416. doi:10.2147/ott.s37750
53. Jang KY, Kim KS, Hwang SH, Kwon KS, Kim KR, Park HS, et al. Expression and prognostic significance of SIRT1 in ovarian epithelial tumours. Pathology (2009) 41:366-71. doi:10.1080/00313020902884451
54. Wang RH, Zheng Y, Kim HS, Xu X, Cao L, Luhasen T, et al. Interplay among BRCA1, SIRT1, and survivin during BRCA1-associated tumorigenesis. Mol Cell (2008) 32:11-20. doi:10.1016/j.molcel.2008.09.011
55. Wang Z, Chen W. Emerging roles of SIRT1 in cancer drug resistance. Genes Cancer (2013) 4:82-90. doi:10.1177/1947601912473826
56. Steffensen KD, Alvero AB, Yang Y, Waldstrom M, Hui P, Holmberg JC, et al. Prevalence of epithelial ovarian cancer stem cells correlates with recurrence in early-stage ovarian cancer. J Oncol (2011) 2011:620523. doi:10.1155/2011/620523
57. McAuliffe SM, Morgan SL, Wyant GA, Tran LT, Muto KW, Chen YS, et al. Targeting Notch, a key pathway for ovarian cancer stem cells, sensitizes tumors to platinum therapy. Proc Natl Acad Sci U S A (2012) 109:E2939-48. doi:10.1073/pnas.1206400109
58. Ahmed N, Abubaker K, Findlay J, Quinn M. Cancerous ovarian stem cells: obscure targets for therapy but relevant to chemoresistance. J Cell Biochem (2013) 114:21-34. doi:10.1002/jcb.24317
59. Chapman-Rothe N, Curry E, Zeller C, Liber D, Stronach E, Gabra H, et al. Chromatin H3K27me3/H3K4me3 histone marks define gene sets in high-grade serous ovarian cancer that distinguish malignant, tumour-sustaining and chemo-resistant ovarian tumour cells. Oncogene (2013) 32:4586-92. doi:10.1038/onc.2012.477
60. Li H, Zhang R. Role of EZH2 in epithelial ovarian cancer: from biological insights to therapeutic target. Front Oncol (2013) 3:47. doi:10.3389/fonc.2013.00047
61. Bibikova M, Laurent LC, Ren B, Loring JF, Fan JB. Unraveling epigenetic regulation in embryonic stem cells. Cell Stem Cell (2008) 2:123-34. doi:10.1016/j.stem.2008.01.005
62. Orkin SH, Hochedlinger K. Chromatin connections to pluripotency and cellular reprogramming. Cell (2011) 145:835-50. doi:10.1016/j.cell.2011.05.019
63. Wei Y, Xia W, Zhang Z, Liu J, Wang H, Adsay NV, et al. Loss of trimethylation at lysine 27 of histone H3 is a predictor of poor outcome in breast, ovarian, and pancreatic cancers. Mol Carcinog (2008) 47:701-6. doi:10.1002/mc.20413
64. Prenzel T, Begus-Nahrmann Y, Kramer F, Hennion M, Hsu C, Gorsler T, et al. Estrogen-dependent gene transcription in human breast cancer cells relies upon proteasome-dependent monoubiquitination of histone H2B. Cancer Res (2011) 71:5739-53. doi:10.1158/0008-5472.CAN-11-1896
65. Hahn MA, Dickson KA, Jackson S, Clarkson A, Gill AJ, Marsh DJ. The tumor suppressor CDC73 interacts with the ring finger proteins RNF20 and RNF40 and is required for the maintenance of histone 2B monoubiquitination. Hum Mol Genet (2012) 21:559-68. doi:10.1093/hmg/ddr490
66. Urasaki Y, Heath L, Xu CW. Coupling of glucose deprivation with impaired histone H2B monoubiquitination in tumors. PLoS One (2012) 7:e36775. doi:10.1371/journal.pone.0036775
67. Marsh DJ, Defazio A, Clarkson A, Kennedy C, Australian Ovarian Cancer Study G, Gard GG, et al. Loss of histone H2B monoubiquitination in ovarian cancer-new therapeutic targeting opportunities based on chromatin relaxation. AACR Advances in Ovarian Cancer Research: From Concepts to Clinic. Miami, FL: American Association for Cancer Research (2013).
68. Izzo A, Schneider R. Chatting histone modifications in mammals. Brief Funct Genomics (2010) 9:429-43. doi:10.1093/bfgp/elq024
69. Lee JS, Smith E, Shilatifard A. The language of histone crosstalk. Cell (2010) 142:682-5. doi:10.1016/j.cell.2010.08.011
70. Wood A, Schneider J, Shilatifard A. Cross-talking histones: implications for the regulation of gene expression and DNA repair. Biochem Cell Biol (2005) 83:460-7. doi:10.1139/o05-116
71. Kim J, Guermah M, Mcginty RK, Lee JS, Tang Z, Milne TA, et al. RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell (2009) 137:459-71. doi:10.1016/j.cell.2009.02.027
72. Smith E, Shilatifard A. The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol Cell (2010) 40:689-701. doi:10.1016/j.molcel.2010.11.031
73. Shilatifard A. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem (2012) 81:65-95. doi:10.1146/annurev-biochem-051710-134100
74. Kouskouti A, Talianidis I. Histone modifications defining active genes persist after transcriptional and mitotic inactivation. EMBO J (2005) 24:347-57. doi:10.1038/sj.emboj.7600516
75. Nakamura K, Kato A, Kobayashi J, Yanagihara H, Sakamoto S, Oliveira DV, et al. Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol Cell (2011) 41:515-28. doi:10.1016/j.molcel.2011.02.002
76. Min J, Feng Q, Li Z, Zhang Y, Xu RM. Structure of the catalytic domain of human DOT1L, a non-SET domain nucleosomal histone methyltransferase. Cell (2003) 112:711-23. doi:10.1016/S0092-8674(03)00114-4
77. Vardabasso C, Hasson D, Ratnakumar K, Chung CY, Duarte LF, Bernstein E. Histone variants: emerging players in cancer biology. Cell Mol Life Sci (2014) 71:379-404. doi:10.1007/s00018-013-1343-z
78. Zlatanova J, Bishop TC, Victor JM, Jackson V, Van Holde K. The nucleosome family: dynamic and growing. Structure (2009) 17:160-71. doi:10.1016/j.str.2008.12.016
79. Talbert PB, Henikoff S. Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol (2010) 11:264-75. doi:10.1038/nrm2861
80. Novikov L, Park JW, Chen H, Klerman H, Jalloh AS, Gamble MJ. QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation. Mol Cell Biol (2011) 31:4244-55. doi:10.1128/MCB.05244-11
81. Chauhan S, Boyd DD. Regulation of u-PAR gene expression by H2A.Z is modulated by the MEK-ERK/AP-1 pathway. Nucleic Acids Res (2012) 40:600-13. doi:10.1093/nar/gkr725
82. John S, Sabo PJ, Johnson TA, Sung MH, Biddie SC, Lightman SL, et al. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol Cell (2008) 29:611-24. doi:10.1016/j.molcel.2008.02.010
83. Gevry N, Hardy S, Jacques PE, Laflamme L, Svotelis A, Robert F, et al. Histone H2A.Z is essential for estrogen receptor signaling. Genes Dev (2009) 23:1522-33. doi:10.1101/gad.1787109
84. Gevry N, Chan HM, Laflamme L, Livingston DM, Gaudreau L. p21 Transcription is regulated by differential localization of histone H2A.Z. Genes Dev (2007) 21:1869-81. doi:10.1101/gad.1545707
85. Cantero D, Friess H, Deflorin J, Zimmermann A, Brundler MA, Riesle E, et al. Enhanced expression of urokinase plasminogen activator and its receptor in pancreatic carcinoma. Br J Cancer (1997) 75:388-95. doi:10.1038/bjc.1997.63
86. Morita S, Sato A, Hayakawa H, Ihara H, Urano T, Takada Y, et al. Cancer cells overexpress mRNA of urokinase-type plasminogen activator, its receptor and inhibitors in human non-small-cell lung cancer tissue: analysis by Northern blotting and in situ hybridization. Int J Cancer (1998) 78:286-92. doi:10.1002/(SICI)1097-0215(19981029)78:3<286::AID-IJC4>3.0.CO;2-R
87. Medrzycki M, Zhang Y, Mcdonald JF, Fan Y. Profiling of linker histone variants in ovarian cancer. Front Biosci (Landmark Ed) (2012) 17:396-406. doi:10.2741/3934
88. Tay Y, Rinn J, Pandolfi PP. The multilayered complexity of ceRNA crosstalk and competition. Nature (2014) 505:344-52. doi:10.1038/nature12986
89. Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, et al. MicroRNA signatures in human ovarian cancer. Cancer Res (2007) 67:8699-707. doi:10.1158/0008-5472.CAN-07-1936
90. Nam EJ, Yoon H, Kim SW, Kim H, Kim YT, Kim JH, et al. MicroRNA expression profiles in serous ovarian carcinoma. Clin Cancer Res (2008) 14:2690-5. doi:10.1158/1078-0432.CCR-07-1731
91. Zhang L, Volinia S, Bonome T, Calin GA, Greshock J, Yang N, et al. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc Natl Acad Sci U S A (2008) 105:7004-9. doi:10.1073/pnas.0801615105
92. Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, Dupont S, et al. A microRNA targeting dicer for metastasis control. Cell (2010) 141:1195-207. doi:10.1016/j.cell.2010.05.017
93. Hsu SD, Tseng YT, Shrestha S, Lin YL, Khaleel A, Chou CH, et al. miRTarBase update 2014: an information resource for experimentally validated miRNA-target interactions. Nucleic Acids Res (2014) 42:D78-85. doi:10.1093/nar/gkt1266
94. Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet (2009) 10:155-9. doi:10.1038/nrg2521
95. Gutschner T, Diederichs S. The hallmarks of cancer: a long non-coding RNA point of view. RNA Biol (2012) 9:703-19. doi:10.4161/rna.20481
96. Spizzo R, Almeida MI, Colombatti A, Calin GA. Long non-coding RNAs and cancer: a new frontier of translational research? Oncogene (2012) 31:4577-87. doi:10.1038/onc.2011.621
97. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A (2009) 106:11667-72. doi:10.1073/pnas.0904715106
98. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell (2007) 129:1311-23. doi:10.1016/j.cell.2007.05.022
99. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature (2010) 464:1071-6. doi:10.1038/nature08975
100. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science (2010) 329:689-93. doi:10.1126/science.1192002
101. Kogo R, Shimamura T, Mimori K, Kawahara K, Imoto S, Sudo T, et al. Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res (2011) 71:6320-6. doi:10.1158/0008-5472.CAN-11-1021
102. Kim K, Jutooru I, Chadalapaka G, Johnson G, Frank J, Burghardt R, et al. HOTAIR is a negative prognostic factor and exhibits pro-oncogenic activity in pancreatic cancer. Oncogene (2013) 32:1616-25. doi:10.1038/onc.2012.193
103. Lv XB, Lian GY, Wang HR, Song E, Yao H, Wang MH. Long noncoding RNA HOTAIR is a prognostic marker for esophageal squamous cell carcinoma progression and survival. PLoS One (2013) 8:e63516. doi:10.1371/journal.pone.0063516
104. He X, Bao W, Li X, Chen Z, Che Q, Wang H, et al. The long non-coding RNA HOTAIR is upregulated in endometrial carcinoma and correlates with poor prognosis. Int J Mol Med (2014) 33:325-32. doi:10.3892/ijmm.2013.1570
105. Qiu JJ, Lin YY, Ye LC, Ding JX, Feng WW, Jin HY, et al. Overexpression of long non-coding RNA HOTAIR predicts poor patient prognosis and promotes tumor metastasis in epithelial ovarian cancer. Gynecol Oncol (2014). doi:10.1016/j.ygyno.2014.03.556
106. Ozes AR, Miller D, Guio C, Bhattrai A, Liu Y, Nephew KP. The transcriptional regulation of the long non-coding RNA HOTAIR in ovarian cancer. Proceedings of the 104th Annual Meeting of the American Association for Cancer Research. Washington, DC (2013).
107. Padua Alves C, Fonseca AS, Muys BR, de Barros E Lima Bueno R, Burger MC, De Souza JE, et al. Brief report: the lincRNA Hotair is required for epithelial-to-mesenchymal transition and stemness maintenance of cancer cell lines. Stem Cells (2013) 31:2827-32. doi:10.1002/stem.1547
108. Margueron R, Reinberg D. The polycomb complex PRC2 and its mark in life. Nature (2011) 469:343-9. doi:10.1038/nature09784
109. Rao ZY, Cai MY, Yang GF, He LR, Mai SJ, Hua WF, et al. EZH2 supports ovarian carcinoma cell invasion and/or metastasis via regulation of TGF-beta1 and is a predictor of outcome in ovarian carcinoma patients. Carcinogenesis (2010) 31:1576-83. doi:10.1093/carcin/bgq150
110. Rizzo S, Hersey JM, Mellor P, Dai W, Santos-Silva A, Liber D, et al. Ovarian cancer stem cell-like side populations are enriched following chemotherapy and overexpress EZH2. Mol Cancer Ther (2011) 10:325-35. doi:10.1158/1535-7163.MCT-10-0788
111. Hu S, Yu L, Li Z, Shen Y, Wang J, Cai J, et al. Overexpression of EZH2 contributes to acquired cisplatin resistance in ovarian cancer cells in vitro and in vivo. Cancer Biol Ther (2010) 10:788-95. doi:10.4161/cbt.10.8.12913
112. Seward S, Semaan A, Qazi AM, Gruzdyn OV, Chamala S, Bryant CC, et al. EZH2 blockade by RNA interference inhibits growth of ovarian cancer by facilitating re-expression of p21(waf1/cip1) and by inhibiting mutant p53. Cancer Lett (2013) 336:53-60. doi:10.1016/j.canlet.2013.04.012
113. Wong CF, Tellam RL. MicroRNA-26a targets the histone methyltransferase enhancer of Zeste homolog 2 during myogenesis. J Biol Chem (2008) 283:9836-43. doi:10.1074/jbc.M709614200
114. Juan AH, Kumar RM, Marx JG, Young RA, Sartorelli V. Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells. Mol Cell (2009) 36:61-74. doi:10.1016/j.molcel.2009.08.008
115. Wang L, Zeng X, Chen S, Ding L, Zhong J, Zhao JC, et al. BRCA1 is a negative modulator of the PRC2 complex. EMBO J (2013) 32:1584-97. doi:10.1038/emboj.2013.95
116. Murphy SK. Targeting the epigenome in ovarian cancer. Future Oncol (2012) 8:151-64. doi:10.2217/fon.11.152
117. Zhou Q, Melkoumian ZK, Lucktong A, Moniwa M, Davie JR, Strobl JS. Rapid induction of histone hyperacetylation and cellular differentiation in human breast tumor cell lines following degradation of histone deacetylase-1. J Biol Chem (2000) 275:35256-63. doi:10.1074/jbc.M003106200
118. Takai N, Narahara H. Histone deacetylase inhibitor therapy in epithelial ovarian cancer. J Oncol (2010) 2010:458431. doi:10.1155/2010/458431
119. Takai N, Ueda T, Nishida M, Nasu K, Narahara H. M344 is a novel synthesized histone deacetylase inhibitor that induces growth inhibition, cell cycle arrest, and apoptosis in human endometrial cancer and ovarian cancer cells. Gynecol Oncol (2006) 101:108-13. doi:10.1016/j.ygyno.2005.09.044
120. Weberpals JI, O'Brien AM, Niknejad N, Garbuio KD, Clark-Knowles KV, Dimitroulakos J. The effect of the histone deacetylase inhibitor M344 on BRCA1 expression in breast and ovarian cancer cells. Cancer Cell Int (2011) 11:29. doi:10.1186/1475-2867-11-29
121. Muscolini M, Cianfrocca R, Sajeva A, Mozzetti S, Ferrandina G, Costanzo A, et al. Trichostatin A up-regulates p73 and induces Bax-dependent apoptosis in cisplatin-resistant ovarian cancer cells. Mol Cancer Ther (2008) 7:1410-9. doi:10.1158/1535-7163.MCT-08-0299
122. Takai N, Kawamata N, Gui D, Said JW, Miyakawa I, Koeffler HP. Human ovarian carcinoma cells: histone deacetylase inhibitors exhibit antiproliferative activity and potently induce apoptosis. Cancer (2004) 101:2760-70. doi:10.1002/cncr.20709
123. Sonnemann J, Gange J, Pilz S, Stotzer C, Ohlinger R, Belau A, et al. Comparative evaluation of the treatment efficacy of suberoylanilide hydroxamic acid (SAHA) and paclitaxel in ovarian cancer cell lines and primary ovarian cancer cells from patients. BMC Cancer (2006) 6:183. doi:10.1186/1471-2407-6-183
124. Cooper AL, Greenberg VL, Lancaster PS, Van Nagell JR Jr, Zimmer SG, Modesitt SC. In vitro and in vivo histone deacetylase inhibitor therapy with suberoylanilide hydroxamic acid (SAHA) and paclitaxel in ovarian cancer. Gynecol Oncol (2007) 104:596-601. doi:10.1016/j.ygyno.2006.09.011
125. Dietrich CS III, Greenberg VL, Desimone CP, Modesitt SC, Van Nagell JR, Craven R, et al. Suberoylanilide hydroxamic acid (SAHA) potentiates paclitaxel-induced apoptosis in ovarian cancer cell lines. Gynecol Oncol (2010) 116:126-30. doi:10.1016/j.ygyno.2009.09.039
126. Chen MY, Liao WS, Lu Z, Bornmann WG, Hennessey V, Washington MN, et al. Decitabine and suberoylanilide hydroxamic acid (SAHA) inhibit growth of ovarian cancer cell lines and xenografts while inducing expression of imprinted tumor suppressor genes, apoptosis, G2/M arrest, and autophagy. Cancer (2011) 117:4424-38. doi:10.1002/cncr.26073
127. Ong PS, Wang XQ, Lin HS, Chan SY, Ho PC. Synergistic effects of suberoylanilide hydroxamic acid combined with cisplatin causing cell cycle arrest independent apoptosis in platinum-resistant ovarian cancer cells. Int J Oncol (2012) 40:1705-13. doi:10.3892/ijo.2012.1354
128. Chen S, Zhao Y, Gou WF, Zhao S, Takano Y, Zheng HC. The anti-tumor effects and molecular mechanisms of suberoylanilide hydroxamic acid (SAHA) on the aggressive phenotypes of ovarian carcinoma cells. PLoS One (2013) 8:e79781. doi:10.1371/journal.pone.0079781
129. Richon VM. Cancer biology: mechanism of antitumour action of vorinostat (suberoylanilide hydroxamic acid), a novel histone deacetylase inhibitor. Br J Cancer (2006) 95:S2-6. doi:10.1038/sj.bjc.6603463
130. Modesitt SC, Sill M, Hoffman JS, Bender DP. A phase II study of vorinostat in the treatment of persistent or recurrent epithelial ovarian or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol (2008) 109:182-6. doi:10.1016/j.ygyno.2008.01.009
131. Lin CT, Lai HC, Lee HY, Lin WH, Chang CC, Chu TY, et al. Valproic acid resensitizes cisplatin-resistant ovarian cancer cells. Cancer Sci (2008) 99:1218-26. doi:10.1111/j.1349-7006.2008.00793.x
132. Shan Z, Feng-Nian R, Jie G, Ting Z. Effects of valproic acid on proliferation, apoptosis, angiogenesis and metastasis of ovarian cancer in vitro and in vivo. Asian Pac J Cancer Prev (2012) 13:3977-82. doi:10.7314/APJCP.2012.13.8.3977
133. Li Y, Liu T, Ivan C, Huang J, Shen DY, Kavanagh JJ, et al. Enhanced cytotoxic effects of combined valproic acid and the aurora kinase inhibitor VE465 on gynecologic cancer cells. Front Oncol (2013) 3:58. doi:10.3389/fonc.2013.00058
134. Monti B, Polazzi E, Contestabile A. Biochemical, molecular and epigenetic mechanisms of valproic acid neuroprotection. Curr Mol Pharmacol (2009) 2:95-109. doi:10.2174/1874-470210902010095
135. Ueda H, Nakajima H, Hori Y, Fujita T, Nishimura M, Goto T, et al. FR901228, a novel antitumor bicyclic depsipeptide produced by Chromobacterium violaceum no. 968. I. Taxonomy, fermentation, isolation, physico-chemical and biological properties, and antitumor activity. J Antibiot (Tokyo) (1994) 47:301-10. doi:10.7164/antibiotics.47.301
136. Wilson AJ, Cheng YQ, Khabele D. Thailandepsins are new small molecule class I HDAC inhibitors with potent cytotoxic activity in ovarian cancer cells: a preclinical study of epigenetic ovarian cancer therapy. J Ovarian Res (2012) 5:12. doi:10.1186/1757-2215-5-12
137. Wilson AJ, Lalani AS, Wass E, Saskowski J, Khabele D. Romidepsin (FK228) combined with cisplatin stimulates DNA damage-induced cell death in ovarian cancer. Gynecol Oncol (2012) 127:579-86. doi:10.1016/j.ygyno.2012.09.016
138. Braun S, Madhani HD. Shaping the landscape: mechanistic consequences of ubiquitin modification of chromatin. EMBO Rep (2012) 13:619-30. doi:10.1038/embor.2012.78
139. Colland F. The therapeutic potential of deubiquitinating enzyme inhibitors. Biochem Soc Trans (2010) 38:137-43. doi:10.1042/BST0380137
140. Nicholson B, Suresh Kumar KG. The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem Biophys (2011) 60:61-8. doi:10.1007/s12013-011-9185-5
141. Chauhan D, Tian Z, Nicholson B, Kumar KG, Zhou B, Carrasco R, et al. A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes bortezomib resistance. Cancer Cell (2012) 22:345-58. doi:10.1016/j.ccr.2012.08.007
142. Glinsky GV, Berezovska O, Glinskii AB. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest (2005) 115:1503-21. doi:10.1172/JCI23412
143. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, et al. Pharmacologic disruption of polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev (2007) 21:1050-63. doi:10.1101/gad.1524107
144. Miranda TB, Cortez CC, Yoo CB, Liang G, Abe M, Kelly TK, et al. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol Cancer Ther (2009) 8:1579-88. doi:10.1158/1535-7163.MCT-09-0013
145. Knutson SK, Wigle TJ, Warholic NM, Sneeringer CJ, Allain CJ, Klaus CR, et al. A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells. Nat Chem Biol (2012) 8:890-6. doi:10.1038/nchembio.1084
146. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature (2012) 492:108-12. doi:10.1038/nature11606
147. Qi W, Chan H, Teng L, Li L, Chuai S, Zhang R, et al. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proc Natl Acad Sci U S A (2012) 109:21360-5. doi:10.1073/pnas.1210371110
148. Kim W, Bird GH, Neff T, Guo G, Kerenyi MA, Walensky LD, et al. Targeted disruption of the EZH2-EED complex inhibits EZH2-dependent cancer. Nat Chem Biol (2013) 9:643-50. doi:10.1038/nchembio.1331
149. Avan A, Crea F, Paolicchi E, Funel N, Galvani E, Marquez VE, et al. Molecular mechanisms involved in the synergistic interaction of the EZH2 inhibitor 3-deazaneplanocin A with gemcitabine in pancreatic cancer cells. Mol Cancer Ther (2012) 11:1735-46. doi:10.1158/1535-7163.MCT-12-0037
150. Momparler RL, Idaghdour Y, Marquez VE, Momparler LF. Synergistic antileukemic action of a combination of inhibitors of DNA methylation and histone methylation. Leuk Res (2012) 36:1049-54. doi:10.1016/j.leukres.2012.03.001
151. Shen L, Cui J, Pang YX, Ma YH, Liu PS. 3-Deazaneplanocin A is a promising therapeutic agent for ovarian cancer cells. Asian Pac J Cancer Prev (2013) 14:2915-8. doi:10.7314/APJCP.2013.14.5.2915
152. Treppendahl MB, Kristensen LS, Gronbaek K. Predicting response to epigenetic therapy. J Clin Invest (2014) 124:47-55. doi:10.1172/JCI69737