Overexpression of MYC and EZH2 cooperates to epigenetically silence MST1 expression

Epigenetics

Volumn 9, Issue 4, 2014, Pages 634-643

  Kuser Abali, Gamze ^a   Alptekin, Ahmet ^a   Cinar, Bekir ^a,b  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DNA methylation; Epigenetics; EZH2 and MST1 Hippo; H3K27me3; MYC

Indexed keywords

3 DEAZANEPLANOCIN A; 5 AZA 2' DEOXYCYTIDINE; DIMETHYL SULFOXIDE; GSK126; METHYLTRANSFERASE INHIBITOR; MICRORNA; MICRORNA 26A; MICRORNA 26B; MYC PROTEIN; PROTEIN INHIBITOR; PROTEIN INHIBITOR JQ1; PROTEIN KINASE; PROTEIN KINASE MST1; RNA POLYMERASE II; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; EZH2 PROTEIN, HUMAN; HISTONE; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN SERINE THREONINE KINASE; STK4 PROTEIN, HUMAN;

ARTICLE; CELL GROWTH; CELL SURVIVAL; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; DOWN REGULATION; EPIGENETICS; GENE SILENCING; GENETIC TRANSFECTION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; CELL PROLIFERATION; GENETIC EPIGENESIS; GENETICS; MALE; METABOLISM; METHYLATION; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; EPIGENESIS, GENETIC; GENE SILENCING; HISTONES; HUMANS; MALE; METHYLATION; POLYCOMB REPRESSIVE COMPLEX 2; PROSTATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-MYC;

EID: 84899137905     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.27957     Document Type: Article

References (45)

1. Harvey K, Tapon N. The Salvador-Warts-Hippo pathway-an emerging tumour-suppressor network. Nat Rev Cancer 2007; 7:182-91; PMID:17318211; http://dx.doi.org/10.1038/nrc2070
2. Lu L, Li Y, Kim SM, Bossuyt W, Liu P, Qiu Q, Wang Y, Halder G, Finegold MJ, Lee JS, et al. Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc Natl Acad Sci U S A 2010; 107:1437-42; PMID:20080689; http:// dx.doi.org/10.1073/pnas.0911427107
3. Song H, Mak KK, Topol L, Yun K, Hu J, Garrett L, Chen Y, Park O, Chang J, Simpson RM, et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc Natl Acad Sci U S A 2010; 107:1431-6; PMID:20080598; http://dx.doi.org/10.1073/ pnas.0911409107
4. Zhou D, Conrad C, Xia F, Park JS, Payer B, Yin Y, Lauwers GY, Thasler W, Lee JT, Avruch J, et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009; 16:425-38; PMID:19878874; http://dx.doi. org/10.1016/j.ccr.2009.09.026
5. Zhou D, Zhang Y, Wu H, Barry E, Yin Y, Lawrence E, Dawson D, Willis JE, Markowitz SD, Camargo FD, et al. Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc Natl Acad Sci U S A 2011; 108:E1312-20; PMID:22042863; http://dx.doi. org/10.1073/pnas.1110428108
6. Qiao M, Wang Y, Xu X, Lu J, Dong Y, Tao W, Stein J, Stein GS, Iglehart JD, Shi Q, et al. Mst1 is an interacting protein that mediates PHLPPs' induced apoptosis. Mol Cell 2010; 38:512-23; PMID:20513427; http://dx.doi.org/10.1016/j.molcel.2010.03.017
7. Steinmann K, Sandner A, Schagdarsurengin U, Dammann RH. Frequent promoter hypermethylation of tumor-related genes in head and neck squamous cell carcinoma. Oncol Rep 2009; 22:1519-26; PMID:19885608
8. Minoo P, Zlobec I, Baker K, Tornillo L, Terracciano L, Jass JR, Lugli A. Prognostic significance of mammalian sterile20-like kinase 1 in colorectal cancer. Mod Pathol 2007; 20:331-8; PMID:17277767; http://dx.doi.org/10.1038/modpathol.3800740
9. Lin X, Cai F, Li X, Kong X, Xu C, Zuo X, Yang Q. Prognostic significance of mammalian sterile 20-like kinase 1 in breast cancer. Tumour Biol 2013; 34:3239-43; PMID:23737290; http://dx.doi. org/10.1007/s13277-013-0895-8
10. Cinar B, Fang PK, Lutchman M, Di Vizio D, Adam RM, Pavlova N, Rubin MA, Yelick PC, Freeman MR. The pro-apoptotic kinase Mst1 and its caspase cleavage products are direct inhibitors of Akt1. EMBO J 2007; 26:4523-34; PMID:17932490; http://dx.doi. org/10.1038/sj.emboj.7601872
11. Cinar B, Collak FK, Lopez D, Akgul S, Mukhopadhyay NK, Kilicarslan M, Gioeli DG, Freeman MR. MST1 is a multifunctional caspaseindependent inhibitor of androgenic signaling. Cancer Res 2011; 71:4303-13; PMID:21512132; http://dx.doi.org/10.1158/0008-5472.CAN-10-4532
12. Collak FK, Yagiz K, Luthringer DJ, Erkaya B, Cinar B. Threonine-120 phosphorylation regulated by phosphoinositide-3-kinase/Akt and mammalian target of rapamycin pathway signaling limits the antitumor activity of mammalian sterile 20-like kinase 1. J Biol Chem 2012; 287:23698-709; PMID:22619175; http://dx.doi.org/10.1074/jbc.M112.358713
13. Nupponen NN, Kakkola L, Koivisto P, Visakorpi T. Genetic alterations in hormone-refractory recurrent prostate carcinomas. Am J Pathol 1998; 153:141-8; PMID:9665474; http://dx.doi.org/10.1016/ S0002-9440(10)65554-X
14. Visakorpi T, Kallioniemi AH, Syvänen AC, Hyytinen ER, Karhu R, Tammela T, Isola JJ, Kallioniemi OP. Genetic changes in primary and recurrent prostate cancer by comparative genomic hybridization. Cancer Res 1995; 55:342-7; PMID:7529134
15. Koh CM, Bieberich CJ, Dang CV, Nelson WG, Yegnasubramanian S, De Marzo AM. MYC and Prostate Cancer. Genes Cancer 2010; 1:617-28; PMID:21779461; http://dx.doi. org/10.1177/1947601910379132
16. Ellwood-Yen K, Graeber TG, Wongvipat J, Iruela-Arispe ML, Zhang J, Matusik R, Thomas GV, Sawyers CL. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 2003; 4:223-38; PMID:14522256; http://dx.doi.org/10.1016/S1535-6108(03)00197-1
17. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002; 298:1039-43; PMID:12351676; http://dx.doi.org/10.1126/science.1076997
18. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002; 419:624-9; PMID:12374981; http://dx.doi.org/10.1038/nature01075
19. Xu K, Wu ZJ, Groner AC, He HH, Cai C, Lis RT, Wu X, Stack EC, Loda M, Liu T, et al. EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycomb-independent. Science 2012; 338:1465-9; PMID:23239736; http://dx.doi. org/10.1126/science.1227604
20. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, Eden E, Yakhini Z, Ben-Shushan E, Reubinoff BE, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39:232-6; PMID:17200670; http://dx.doi. org/10.1038/ng1950
21. Patra SK, Patra A, Zhao H, Dahiya R. DNA methyltransferase and demethylase in human prostate cancer. Mol Carcinog 2002; 33:163-71; PMID:11870882; http://dx.doi.org/10.1002/ mc.10033
22. De Carvalho DD, Sharma S, You JS, Su SF, Taberlay PC, Kelly TK, Yang X, Liang G, Jones PA. DNA methylation screening identifies driver epigenetic events of cancer cell survival. Cancer Cell 2012; 21:655-67; PMID:22624715; http://dx.doi. org/10.1016/j.ccr.2012.03.045
23. Koh CM, Iwata T, Zheng Q, Bethel C, Yegnasubramanian S, De Marzo AM. Myc enforces overexpression of EZH2 in early prostatic neoplasia via transcriptional and post-transcriptional mechanisms. Oncotarget 2011; 2:669-83; PMID:21941025
24. Kaur M, Cole MD. MYC acts via the PTEN tumor suppressor to elicit autoregulation and genomewide gene repression by activation of the Ezh2 methyltransferase. Cancer Res 2013; 73:695-705; PMID:23135913; http://dx.doi.org/10.1158/0008-5472.CAN-12-2522
25. Brenner C, Deplus R, Didelot C, Loriot A, Viré E, De Smet C, Gutierrez A, Danovi D, Bernard D, Boon T, et al. Myc represses transcription through recruitment of DNA methyltransferase corepressor. EMBO J 2005; 24:336-46; PMID:15616584; http://dx.doi. org/10.1038/sj.emboj.7600509
26. Zhang X, Zhao X, Fiskus W, Lin J, Lwin T, Rao R, Zhang Y, Chan JC, Fu K, Marquez VE, et al. Coordinated silencing of MYC-mediated miR-29 by HDAC3 and EZH2 as a therapeutic target of histone modification in aggressive B-Cell lymphomas. Cancer Cell 2012; 22:506-23; PMID:23079660; http://dx.doi.org/10.1016/j.ccr.2012.09.003
27. Seidel C, Schagdarsurengin U, Blümke K, Würl P, Pfeifer GP, Hauptmann S, Taubert H, Dammann R. Frequent hypermethylation of MST1 and MST2 in soft tissue sarcoma. Mol Carcinog 2007; 46:865-71; PMID:17538946; http://dx.doi.org/10.1002/ mc.20317
28. Bhat KP, Salazar KL, Balasubramaniyan V, Wani K, Heathcock L, Hollingsworth F, James JD, Gumin J, Diefes KL, Kim SH, et al. The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma. Genes Dev 2011; 25:2594-609; PMID:22190458; http://dx.doi.org/10.1101/ gad.176800.111
29. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, Karuturi RK, Tan PB, Liu ET, Yu Q. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev 2007; 21:1050-63; PMID:17437993; http://dx.doi.org/10.1101/ gad.1524107
30. rd, Diaz E, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 2012; 492:108-12; PMID:23051747; http://dx.doi.org/10.1038/ nature11606
31. Sampson VB, Rong NH, Han J, Yang Q, Aris V, Soteropoulos P, Petrelli NJ, Dunn SP, Krueger LJ. MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res 2007; 67:9762-70; PMID:17942906; http://dx.doi.org/10.1158/0008-5472.CAN-07-2462
32. Huang MJ, Cheng YC, Liu CR, Lin S, Liu HE. A small-molecule c-Myc inhibitor, 10058-F4, induces cell-cycle arrest, apoptosis, and myeloid differentiation of human acute myeloid leukemia. Exp Hematol 2006; 34:1480-9; PMID:17046567; http://dx.doi. org/10.1016/j.exphem.2006.06.019
33. Yin X, Giap C, Lazo JS, Prochownik EV. Low molecular weight inhibitors of Myc-Max interaction and function. Oncogene 2003; 22:6151-9; PMID:13679853; http://dx.doi.org/10.1038/ sj.onc.1206641
34. Delmore JE, Issa GC, Lemieux ME, Rahl PB, Shi J, Jacobs HM, Kastritis E, Gilpatrick T, Paranal RM, Qi J, et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 2011; 146:904-17; PMID:21889194; http://dx.doi.org/10.1016/j. cell.2011.08.017
35. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O, Morse EM, Keates T, Hickman TT, Felletar I, et al. Selective inhibition of BET bromodomains. Nature 2010; 468:1067-73; PMID:20871596; http://dx.doi.org/10.1038/nature09504
36. Sander S, Bullinger L, Klapproth K, Fiedler K, Kestler HA, Barth TF, Möller P, Stilgenbauer S, Pollack JR, Wirth T. MYC stimulates EZH2 expression by repression of its negative regulator miR-26a. Blood 2008; 112:4202-12; PMID:18713946; http:// dx.doi.org/10.1182/blood-2008-03-147645
37. Lu J, He ML, Wang L, Chen Y, Liu X, Dong Q, Chen YC, Peng Y, Yao KT, Kung HF, et al. MiR-26a inhibits cell growth and tumorigenesis of nasopharyngeal carcinoma through repression of EZH2. Cancer Res 2011; 71:225-33; PMID:21199804; http://dx.doi. org/10.1158/0008-5472.CAN-10-1850
38. Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439:871-4; PMID:16357870; http://dx.doi. org/10.1038/nature04431
39. Gao L, Schwartzman J, Gibbs A, Lisac R, Kleinschmidt R, Wilmot B, Bottomly D, Coleman I, Nelson P, McWeeney S, et al. Androgen receptor promotes ligand-independent prostate cancer progression through c-Myc upregulation. PLoS One 2013; 8:e63563; PMID:23704919; http://dx.doi. org/10.1371/journal.pone.0063563
40. Mukhopadhyay NK, Kim J, You S, Morello M, Hager MH, Huang WC, et al. Scaffold attachment factor B1 regulates the androgen receptor in concert with the growth inhibitory kinase MST1 and the methyltransferase EZH2. Oncogene 2013. PMID: 23893242.
41. Dang CV. MYC on the path to cancer. Cell 2012; 149:22-35; PMID:22464321; http://dx.doi. org/10.1016/j.cell.2012.03.003
42. Civenni G, Malek A, Albino D, Garcia-Escudero R, Napoli S, Di Marco S, Pinton S, Sarti M, Carbone GM, Catapano CV. RNAi-mediated silencing of Myc transcription inhibits stem-like cell maintenance and tumorigenicity in prostate cancer. Cancer Res 2013; 73:6816-27; PMID:24063893; http://dx.doi. org/10.1158/0008-5472.CAN-13-0615
43. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006; 125:301-13; PMID:16630818; http://dx.doi. org/10.1016/j.cell.2006.02.043
44. Lian I, Kim J, Okazawa H, Zhao J, Zhao B, Yu J, Chinnaiyan A, Israel MA, Goldstein LS, Abujarour R, et al. The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev 2010; 24:1106-18; PMID:20516196; http://dx.doi.org/10.1101/gad.1903310
45. Gartel AL, Shchors K. Mechanisms of c-myc-mediated transcriptional repression of growth arrest genes. Exp Cell Res 2003; 283:17-21; PMID:12565816; http://dx.doi.org/10.1016/S0014-4827(02)00020-4