CDKN1C (p57KIP2) is a direct target of EZH2 and suppressed by multiple epigenetic mechanisms in breast cancer cells

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  Yang, Xiaojing ^a,b   Karuturi, R K Murthy ^a   Sun, Feng ^a,c   Aau, Meiyee ^a   Yu, Kun ^d   Shao, Rongguang ^b   Miller, Lance D ^a   Tan, Patrick Boon Ooi ^a,d   Yu, Qiang ^a  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

^b INSTITUTE OF MEDICINAL BIOTECHNOLOGY   (China)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; ENHANCER OF ZESTE 2 PROTEIN; HISTONE H3; LYSINE; POLYCOMB GROUP PROTEIN; UNCLASSIFIED DRUG; CDKN1C PROTEIN, HUMAN; DNA BINDING PROTEIN; EZH2 PROTEIN, HUMAN; HYDROXAMIC ACID; TRANSCRIPTION FACTOR; TRICHOSTATIN A;

ARTICLE; BREAST CANCER; CANCER CELL; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE LOCUS; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; PROGNOSIS; PROTEIN METHYLATION; PROTEIN MODIFICATION; BREAST TUMOR; GENETIC EPIGENESIS; GENETICS; METABOLISM; PATHOLOGY; POLYMERASE CHAIN REACTION; PROMOTER REGION; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; HUMANS; HYDROXAMIC ACIDS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS;

EID: 64549090667     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005011     Document Type: Article

References (43)

1. Bachman KE, Park BH, Rhee I, Rajagopalan H, Herman JG, et al. (2003) Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell 3: 89-95.
2. Karnik SK, Hughes CM, Gu X, Rozenblatt-Rosen O, McLean GW, et al. (2005) Menin regulates pancreatic islet growth by promoting histone methylation and expression of genes encoding p27Kip1 and p18INK4c. Proc Natl Acad Sci U S A 102: 14659-14664.
3. Bracken AP, Kleine-Kohlbrecher D, Dietrich N, Pasini D, Gargiulo G, et al. (2007) The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev 21: 525-530.
4. Kotake Y, Cao R, Viatour P, Sage J, Zhang Y, et al. (2007) pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev 21: 49-54.
5. Jones PA, Taylor SM (1980) Cellular differentiation, cytidine analogs and DNA methylation. Cell 20: 85-93.
6. Marks PA, Richon VM, Miller T, Kelly WK (2004) Histone deacetylase inhibitors. Adv Cancer Res 91: 137-168.
7. Cameron EE, Bachman KE, Myohanen 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.
8. 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.
9. Bachmann IM, Halvorsen OJ, Collett K, Stefansson IM, Straume O, et al. (2006) EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. J Clin Oncol 24: 268-273.
10. 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.
11. Kirmizis A, Bartley SM, Kuzmichev A, Margueron R, Reinberg D, et al. (2004) Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev 18: 1592-1605.
12. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893-2905.
13. 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.
14. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, et al. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874.
15. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, et al. (2008) Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet 40: 741-750.
16. Jiang X, Tan J, Li J, Kivimae S, Yang X, et al. (2008) DACT3 is an epigenetic regulator of Wnt/beta-catenin signaling in colorectal cancer and is a therapeutic target of histone modifications. Cancer Cell 13: 529-541.
17. Gal-Yam EN, Egger G, Iniguez L, Holster H, Einarsson S, et al. (2008) Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc Natl Acad Sci U S A 105: 12979-12984.
18. McGarvey KM, Van Neste L, Cope L, Ohm JE, Herman JG, et al. (2008) Defining a chromatin pattern that characterizes DNA-hypermethylated genes in colon cancer cells. Cancer Res 68: 5753-5759.
19. Egger G, Aparicio AM, Escobar SG, Jones PA (2007) Inhibition of histone deacetylation does not block resilencing of p16 after 5-aza-2′-deoxycytidine treatment. Cancer Res 67: 346-353.
20. McGarvey KM, Fahrner JA, Greene E, Martens J, Jenuwein T, et al. (2006) Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Res 66: 3541-3549.
21. Pateras IS, Apostolopoulou K, Koutsami M, Evangelou K, Tsantoulis P, et al. (2006) Downregulation of the KIP family members p27(KIP1) and p57(KIP2) by SKP2 and the role of methylation in p57(KIP2) inactivation in nonsmall cell lung cancer. Int J Cancer 119: 2546-2556.
22. Li Y, Nagai H, Ohno T, Yuge M, Hatano S, et al. (2002) Aberrant DNA methylation of p57(KIP2) gene in the promoter region in lymphoid malignancies of B-cell phenotype. Blood 100: 2572-2577.
23. 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.
24. Yu J, Rhodes DR, Tomlins SA, Cao X, Chen G, et al. (2007) A polycomb repression signature in metastatic prostate cancer predicts cancer outcome. Cancer Res 67: 10657-10663.
25. Zhao X, Han X, Chew J, Liu J, Chiu K, 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 3: 286.
26. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
27. 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.
28. 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.
29. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
30. Soejima H, Nakagawachi T, Zhao W, Higashimoto K, Urano T, et al. (2004) Silencing of imprinted CDKN1C gene expression is associated with loss of CpG and histone H3 lysine 9 methylation at DMR-LIT1 in esophageal cancer. Oncogene 23: 4380-4388.
31. Wozniak RJ, Klimecki WT, Lau SS, Feinstein Y, Futscher BW (2007) 5-Aza-2′-deoxycytidine-mediated reductions in G9A histone methyltransferase and histone H3 K9 di-methylation levels are linked to tumor suppressor gene reactivation. Oncogene 26: 77-90.
32. Miller LD, Smeds J, George J, Vega VB, Vergara L, et al. (2005) An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc Natl Acad Sci U S A 102: 13550-13555.
33. Hall P, Ploner A, Bjohle J, Huang F, Lin CY, et al. (2006) Hormone-replacement therapy influences gene expression profiles and is associated with breast-cancer prognosis: a cohort study. BMC Med 4: 16.
34. McGarvey KM, Greene E, Fahrner JA, Jenuwein T, Baylin SB (2007) DNA methylation and complete transcriptional silencing of cancer genes persist after depletion of EZH2. Cancer Res 67: 5097-5102.
35. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, et al. (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39: 457-466.
36. Kondo Y, Shen L, Issa JP (2003) Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol Cell Biol 23: 206-215.
37. Nguyen CT, Weisenberger DJ, Velicescu M, Gonzales FA, Lin JC, et al. (2002) Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′-deoxycytidine. Cancer Res 62: 6456-6461.
38. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448: 714-717.
39. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, et al. (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8: 532-538.
40. 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.
41. 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.
42. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, et al. (2007) Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39: 232-236.
43. Ohm JE, Baylin SB (2007) Stem cell chromatin patterns: an instructive mechanism for DNA hypermethylation? Cell Cycle 6: 1040-1043.