EZH2-Mediated H3K27me3 Is Involved in Epigenetic Repression of Deleted in Liver Cancer 1 in Human Cancers

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Au, Sandy Leung Kuen ^a   Wong, Carmen Chak Lui ^a   Lee, Joyce Man Fong ^a   Wong, Chun Ming ^a   Ng, Irene Oi Lin ^a  

^a THE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

3 DEAZANEPLANOCIN A; 5 AZA 2' DEOXYCYTIDINE; DELETED IN LIVER CANCER 1 PROTEIN; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HISTONE METHYLTRANSFERASE OF THE POLYCOMB REPRESSIVE COMPLEX 2 CATALYZING HISTONE H3 LYSINE 27 TRI METHYLATION PROTEIN; MESSENGER RNA; PROTEIN; RHO FACTOR; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR EZH2; TRICHOSTATIN A; UNCLASSIFIED DRUG; 3-DEAZANEPLANOCIN; ADENOSINE; ANTINEOPLASTIC AGENT; DLC1 PROTEIN, HUMAN; EZH2 PROTEIN, HUMAN; HISTONE; TUMOR SUPPRESSOR PROTEIN;

ACTIN FILAMENT; ARTICLE; BREAST CANCER; CANCER TISSUE; CARCINOMA CELL; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EPIGENETIC REPRESSION; GENE EXPRESSION; GENE INACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CANCER; LUNG CANCER; METASTASIS; METHYLATION; OVARY CANCER; PROMOTER REGION; PROSTATE CANCER; PROTEIN DEPLETION; PROTEIN FAMILY; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; CELL MOTION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASMS; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ACTIN CYTOSKELETON; ADENOSINE; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL MOVEMENT; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; EPIGENETIC REPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GTPASE-ACTIVATING PROTEINS; HISTONES; HUMANS; METHYLATION; NEOPLASMS; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEINS;

EID: 84879536747     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068226     Document Type: Article

References (50)

1. Jones PA, Baylin SB, (2007) The epigenomics of cancer. Cell 128: 683-692. doi:10.1016/j.cell.2007.01.029. PubMed: 17320506.
2. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, et al. (2002) The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419: 624-629. doi:10.1038/nature01075. PubMed: 12374981.
3. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, et al. (2003) EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci U S A 100: 11606-11611. doi:10.1073/pnas.1933744100. PubMed: 14500907.
4. Simon JA, Lange CA, (2008) Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat Res 647: 21-29. doi:10.1016/j.mrfmmm.2008.07.010. PubMed: 18723033.
5. Chase A, Cross NC, (2011) Aberrations of EZH2 in cancer. Clin Cancer Res Off J Am Assoc Cancer Res 17: 2613-2618. doi:10.1158/1078-0432.CCR-10-2156. PubMed: 21367748.
6. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043. doi:10.1126/science.1076997. PubMed: 12351676.
7. Cao R, Zhang Y, (2004) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14: 155-164. doi:10.1016/j.gde.2004.02.001. PubMed: 15196462.
8. Cao Q, Yu J, Dhanasekaran SM, Kim JH, Mani RS, et al. (2008) Repression of E-cadherin by the polycomb group protein EZH2 in cancer. Oncogene 27: 7274-7284. doi:10.1038/onc.2008.333. PubMed: 18806826.
9. Fujii S, Ito K, Ito Y, Ochiai A, (2008) Enhancer of zeste homologue 2 (EZH2) down-regulates RUNX3 by increasing histone H3 methylation. J Biol Chem 283: 17324-17332. doi:10.1074/jbc.M800224200. PubMed: 18430739.
10. Yu J, Cao Q, Wu L, Dallol A, Li J, et al. (2010) The neuronal repellent SLIT2 is a target for repression by EZH2 in prostate cancer. Oncogene 29: 5370-5380. doi:10.1038/onc.2010.269. PubMed: 20622896.
11. Min J, Zaslavsky A, Fedele G, McLaughlin SK, Reczek EE, et al. (2010) An oncogene-tumor suppressor cascade drives metastatic prostate cancer by coordinately activating Ras and nuclear factor-kappaB. Nat Med 16: 286-294. doi:10.1038/nm.2100. PubMed: 20154697.
12. Taniguchi H, Jacinto FV, Villanueva A, Fernandez AF, Yamamoto H, et al. (2012) Silencing of Kruppel-like factor 2 by the histone methyltransferase EZH2 in human cancer. Oncogene 31: 1988-1994. doi:10.1038/onc.2011.387. PubMed: 21892211.
13. Au SL, Wong CC, Lee JM, Fan DN, Tsang FH, et al. (2012) Enhancer of zeste homolog 2 epigenetically silences multiple tumor suppressor microRNAs to promote liver cancer metastasis. Hepatology 56: 622-631. doi:10.1002/hep.25679. PubMed: 22370893.
14. Yuan BZ, Miller MJ, Keck CL, Zimonjic DB, Thorgeirsson SS, et al. (1998) Cloning, characterization, and chromosomal localization of a gene frequently deleted in human liver cancer (DLC-1) homologous to rat RhoGAP. Cancer Res 58: 2196-2199. PubMed: 9605766.
15. Liao YC, Si L, deVere White RW, Lo SH, (2007) The phosphotyrosine-independent interaction of DLC-1 and the SH2 domain of cten regulates focal adhesion localization and growth suppression activity of DLC-1. J Cell Biol 176: 43-49. doi:10.1083/jcb.200608015. PubMed: 17190795.
16. Yam JW, Ko FC, Chan CY, Jin DY, Ng IO, (2006) Interaction of deleted in liver cancer 1 with tensin2 in caveolae and implications in tumor suppression. Cancer Res 66: 8367-8372. doi:10.1158/0008-5472.CAN-05-2850. PubMed: 16951145.
17. Wong CM, Lee JM, Ching YP, Jin DY, Ng IO, (2003) Genetic and epigenetic alterations of DLC-1 gene in hepatocellular carcinoma. Cancer Res 63: 7646-7651. PubMed: 14633684.
18. Healy KD, Hodgson L, Kim TY, Shutes A, Maddileti S, et al. (2008) DLC-1 suppresses non-small cell lung cancer growth and invasion by RhoGAP-dependent and independent mechanisms. Mol Carcinog 47: 326-337. doi:10.1002/mc.20389. PubMed: 17932950.
19. Olson MF, Ashworth A, Hall A, (1995) An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science 269: 1270-1272. doi:10.1126/science.7652575. PubMed: 7652575.
20. Raftopoulou M, Hall A, (2004) Cell migration: Rho GTPases lead the way. Dev Biol 265: 23-32. doi:10.1016/j.ydbio.2003.06.003. PubMed: 14697350.
21. Wong CC, Wong CM, Ko FC, Chan LK, Ching YP, et al. (2008) Deleted in liver cancer 1 (DLC1) negatively regulates Rho/ROCK/MLC pathway in hepatocellular carcinoma. PLOS ONE 3: e2779. doi:10.1371/journal.pone.0002779. PubMed: 18648664.
22. Wong CC, Wong CM, Tung EK, Man K, Ng IO, (2009) Rho-kinase 2 is frequently overexpressed in hepatocellular carcinoma and involved in tumor invasion. Hepatology 49: 1583-1594. doi:10.1002/hep.22836. PubMed: 19205033.
23. Zhou X, Thorgeirsson SS, Popescu NC, (2004) Restoration of DLC-1 gene expression induces apoptosis and inhibits both cell growth and tumorigenicity in human hepatocellular carcinoma cells. Oncogene 23: 1308-1313. doi:10.1038/sj.onc.1207246. PubMed: 14647417.
24. Shih YP, Liao YC, Lin Y, Lo SH, (2010) DLC1 negatively regulates angiogenesis in a paracrine fashion. Cancer Res 70: 8270-8275. doi:10.1158/0008-5472.CAN-10-1174. PubMed: 20861185.
25. Seng TJ, Low JS, Li H, Cui Y, Goh HK, et al. (2007) The major 8p22 tumor suppressor DLC1 is frequently silenced by methylation in both endemic and sporadic nasopharyngeal, esophageal, and cervical carcinomas, and inhibits tumor cell colony formation. Oncogene 26: 934-944. doi:10.1038/sj.onc.1209839. PubMed: 16862168.
26. Ullmannova V, Popescu NC, (2006) Expression profile of the tumor suppressor genes DLC-1 and DLC-2 in solid tumors. Int J Oncol 29: 1127-1132. PubMed: 17016643.
27. Li Y, Tang ZY, Ye SL, Liu YK, Chen J, et al. (2001) Establishment of cell clones with different metastatic potential from the metastatic hepatocellular carcinoma cell line MHCC97. World J Gastroenterol 7: 630-636. PubMed: 11819844.
28. Rhee I, Bachman KE, Park BH, Jair KW, Yen RW, et al. (2002) DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416: 552-556. doi:10.1038/416552a. PubMed: 11932749.
29. Tan J, Yang X, Zhuang L, Jiang X, Chen W, et al. (2007) Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev 21: 1050-1063. doi:10.1101/gad.1524107. PubMed: 17437993.
30. Miranda TB, Cortez CC, Yoo CB, Liang G, Abe M, et al. (2009) DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol Cancer Ther 8: 1579-1588. doi:10.1158/1535-7163.MCT-09-0013. PubMed: 19509260.
31. Au SL, Wong CC, Lee JM, Fan DN, Tsang FH, et al. (2012) Enhancer of zeste homolog 2 epigenetically silences multiple tumor suppressor microRNAs to promote liver cancer metastasis. Hepatology, 56: 622-31. PubMed: 22370893.
32. Bhattacharjee A, Richards WG, Staunton J, Li C, Monti S, et al. (2001) Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A 98: 13790-13795. doi:10.1073/pnas.191502998. PubMed: 11707567.
33. Richardson AL, Wang ZC, De Nicolo A, Lu X, Brown M, et al. (2006) X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9: 121-132. doi:10.1016/j.ccr.2006.01.013. PubMed: 16473279.
34. Vanaja DK, Cheville JC, Iturria SJ, Young CY, (2003) Transcriptional silencing of zinc finger protein 185 identified by expression profiling is associated with prostate cancer progression. Cancer Res 63: 3877-3882. PubMed: 12873976.
35. Adib TR, Henderson S, Perrett C, Hewitt D, Bourmpoulia D, et al. (2004) Predicting biomarkers for ovarian cancer using gene-expression microarrays. Br J Cancer 90: 686-692. doi:10.1038/sj.bjc.6601603. PubMed: 14760385.
36. Cameron EE, Bachman KE, Myöhänen S, Herman JG, Baylin SB, (1999) Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 21: 103-107. doi:10.1038/5047. PubMed: 9916800.
37. Kouzarides T, (2007) Chromatin modifications and their function. Cell 128: 693-705. doi:10.1016/j.cell.2007.02.005. PubMed: 17320507.
38. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313. doi:10.1016/j.cell.2006.02.043. PubMed: 16630818.
39. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, et al. (2007) Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1: 286-298. doi:10.1016/j.stem.2007.08.004. PubMed: 18371363.
40. Pan G, Tian S, Nie J, Yang C, Ruotti V, et al. (2007) Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1: 299-312. doi:10.1016/j.stem.2007.08.003. PubMed: 18371364.
41. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326. doi:10.1016/j.cell.2006.02.041. PubMed: 16630819.
42. Pietersen AM, van Lohuizen M, (2008) Stem cell regulation by polycomb repressors: postponing commitment. Curr Opin Cell Biol 20: 201-207. doi:10.1016/j.ceb.2008.01.004. PubMed: 18291635.
43. Durkin ME, Avner MR, Huh CG, Yuan BZ, Thorgeirsson SS, et al. (2005) DLC-1, a Rho GTPase-activating protein with tumor suppressor function, is essential for embryonic development. FEBS Lett 579: 1191-1196. doi:10.1016/j.febslet.2004.12.090. PubMed: 15710412.
44. Calvanese V, Horrillo A, Hmadcha A, Suarez-Alvarez B, Fernandez AF, et al. (2008) Cancer genes hypermethylated in human embryonic stem cells. PLOS ONE 3: e3294. doi:10.1371/journal.pone.0003294. PubMed: 18820729.
45. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, et al. (2007) A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 39: 237-242. doi:10.1038/ng1972. PubMed: 17211412.
46. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, et al. (2007) Epigenetic stem cell signature in cancer. Nat Genet 39: 157-158. doi:10.1038/ng1941. PubMed: 17200673.
47. Plimack ER, Kantarjian HM, Issa JP, (2007) Decitabine and its role in the treatment of hematopoietic malignancies. Leuk Lymphoma 48: 1472-1481. doi:10.1080/10428190701471981. PubMed: 17701577.
48. Marks PA, (2007) Discovery and development of SAHA as an anticancer agent. Oncogene 26: 1351-1356. doi:10.1038/sj.onc.1210204. PubMed: 17322921.
49. Chiba T, Suzuki E, Negishi M, Saraya A, Miyagi S, et al. (2012) 3-Deazaneplanocin A is a promising therapeutic agent for the eradication of tumor-initiating hepatocellular carcinoma cells. Int J Cancer 130: 2557-2567. doi:10.1002/ijc.26264. PubMed: 21717453.
50. Fiskus W, Wang Y, Sreekumar A, Buckley KM, Shi H, et al. (2009) Combined epigenetic therapy with the histone methyltransferase EZH2 inhibitor 3-deazaneplanocin A and the histone deacetylase inhibitor panobinostat against human AML cells. Blood 114: 2733-2743. doi:10.1182/blood-2009-03-213496. PubMed: 19638619.