Polycomb repressive complex 2 regulates lineage fidelity during embryonic stem cell differentiation

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Thornton, Seraphim R ^a   Butty, Vincent L ^a   Levine, Stuart S ^a   Boyer, Laurie A ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 3A; HISTONE H3; NEUROMODULIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; POLYCOMB REPRESSIVE COMPLEX 2; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX17; TRANSCRIPTION FACTOR SOX3; HISTONE; SUZ12 PROTEIN, MOUSE;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL LINEAGE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EMBRYONIC STEM CELL; ENZYME MECHANISM; EPIGENETIC REPRESSION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE REPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; MOLECULAR INTERACTION; MOTONEURON; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SPINAL CORD MOTONEURON; ANIMAL; C57BL MOUSE; CELL LINE; CPG ISLAND; CYTOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; MOUSE; PROMOTER REGION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CPG ISLANDS; DNA METHYLATION; EMBRYONIC STEM CELLS; GENE EXPRESSION; HISTONES; MICE; MICE, INBRED C57BL; MOTOR NEURONS; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC;

EID: 84908191910     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110498     Document Type: Article

References (58)

1. Surface LE, Thornton SR, Boyer L.A. (2010) Polycomb group proteins set the stage for early lineage commitment. Cell Stem Cell 7: 288-298. doi:10.1016/j.stem.2010.08.004.
2. Simon JA, Kingston R.E. (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10: 697-708. doi:10.1038/nrm2763.
3. Di Croce L., Helin K. (2013) Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol 20: 1147-1155. doi:10.1038/nsmb.2669.
4. Pasini D, Bracken AP, Jensen M.R., Lazzerini Denchi E, Helin K. (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23: 4061-4071. doi:10.1038/sj.emboj.7600402.
5. Faust C, Schumacher A, Holdener B., Magnuson T. (1995) The eed mutation disrupts anterior mesoderm production in mice. Development 121: 273-285.
6. O'Carroll D., Erhardt S, Pagani M., Barton SC, Surani MA, et al. (2001) The polycomb-group gene Ezh2 is required for early mouse development. Mol Cell Biol 21: 4330-4336. doi:10.1128/MCB.21.13.4330-4336.2001.
7. 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.
8. Pengelly AR, Copur Ö, Jäckle H, Herzig A, Müller J (2013) A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science 339: 698-699. doi:10.1126/science.1231382.
9. Boyer LA, Plath K, Zeitlinger J., Brambrink T, Medeiros LA, et al (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nat Cell Biol 441: 349-353. doi:10.1038/nature04733.
10. Lee TI, Jenner RG, Boyer L.A., 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.
11. Bracken AP, Dietrich N, Pasini D., Hansen KH, Helin K. (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20: 1123-1136. doi:10.1101/gad.381706.
12. Tolhuis B, de Wit E, Muijrers I, Teunissen H., Talhout W, et al. (2006) Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38: 694-699. doi:10.1038/ng1792.
13. 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.
14. Mikkelsen TS, Ku M, Jaffe D.B., Issac B., Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560. doi:10.1038/nature06008.
15. Azuara V, Perry P, Sauer S., Spivakov M, Jørgensen HF, et al. (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8: 532-538. doi:10.1038/ncb1403.
16. Varley KE, Gertz J, Bowling K.M., Parker SL, Reddy TE, et al. (2013) Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res 23: 555-567. doi:10.1101/gr.147942.112.
17. Neri F, Krepelova A, Incarnato D., Maldotti M, Parlato C, et al (2013) Dnmt3L Antagonizes DNA Methylation at Bivalent Promoters and Favors DNA Methylation at Gene Bodies in ESCs. Cell 155: 121-134. doi:10.1016/j.cell.2013.08.056.
18. Hagarman JA, Motley MP, Kristjansdottir K, Soloway P.D. (2013) Coordinate regulation of DNA methylation and H3K27me3 in mouse embryonic stem cells. PLoS ONE 8: e53880. doi:10.1371/journal.pone.0053880.
19. Hawkins RD, Hon GC, Lee L.K., Ngo Q., Lister R, et al. (2010) Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6: 479-491. doi:10.1016/j.stem.2010.03.018.
20. Lister R, Ecker J.R. (2009) Finding the fifth base: genome-wide sequencing of cytosine methylation. Genome Res 19: 959-966. doi:10.1101/gr.083451.108.
21. Mohn F, Weber M, Rebhan M., Roloff TC, Richter J, et al. (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30: 755-766. doi:10.1016/j.molcel.2008.05.007.
22. Pasini D, Bracken AP, Hansen J.B., Capillo M., Helin K. (2007) The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol Cell Biol 27: 3769-3779. doi:10.1128/MCB.01432-06.
23. Mazzoni EO, Mahony S, Peljto M., Patel T, Thornton SR, et al (2013) Saltatory remodeling of Hox chromatin in response to rostrocaudal patterning signals. Nat Neurosci 16: 1191-1198. doi:10.1038/nn.3490.
24. Chamberlain SJ, Yee D, Magnuson T. (2008) Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 26: 1496-1505. doi:10.1634/stemcells.2008-0102.
25. Ku M, Koche RP, Rheinbay E, Mendenhall E.M., Endoh M., et al. (2008) Genomewide Analysis of PRC1 and PRC2 Occupancy Identifies Two Classes of Bivalent Domains. PLoS Genet 4: e1000242. doi:10.1371/journal.-pgen.1000242.g004.
26. Yuan W, Wu T, Fu H., Dai C, Wu H, et al (2012) Dense Chromatin Activates Polycomb Repressive Complex 2 to Regulate H3 Lysine 27 Methylation. Science 337: 971-975. doi:10.1126/science.1225237.
27. Montgomery ND, Yee D, Chen A., Kalantry S, Chamberlain SJ, et al (2005) The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr Biol 15: 942-947. doi:10.1016/j.cub.2005.04.051.
28. Margueron R, Li G, Sarma K., Blais A, Zavadil J, et al (2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol Cell 32: 503-518. doi:10.1016/j.molcel.2008.11.004.
29. Shen X, Liu Y, Hsu Y-J, Fujiwara Y, Kim J., et al. (2008) EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell 32: 491-502. doi:10.1016/j.molcel.2008.10.016.
30. Wichterle H, Peljto M. (2008) Differentiation of mouse embryonic stem cells to spinal motor neurons. Curr Protoc Stem Cell Biol Chapter 1: Unit1H.1.1-1H.1.9. doi:10.1002/9780470151808.sc01h01s5.
31. Meissner A, Gnirke A, Bell G.W., Ramsahoye B., Lander ES, et al. (2005) Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Research 33: 5868-5877. doi:10.1093/nar/gki901.
32. Gu H, Smith ZD, Bock C, Boyle P., Gnirke A, et al. (2011) Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat Protoc 6: 468-481. doi:10.1038/nprot.2010.190.
33. Simon JA, Kingston R.E. (2013) Occupying Chromatin: Polycomb Mechanisms for Getting to Genomic Targets, Stopping Transcriptional Traffic, and Staying Put. Mol Cell 49: 808-824. doi:10.1016/j.molcel.2013.02.013.
34. Schmitges FW, Prusty AB, Faty M, Stützer A, Lingaraju G.M., et al. (2011) Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell 42: 330-341. doi:10.1016/j.molcel.2011.03.025.
35. Xu C, Bian C, Yang W., Galka M, Ouyang H, et al (2010) Binding of different histone marks differentially regulates the activity and specificity of polycomb repressive complex 2 (PRC2). Proc Natl Acad Sci USA 107: 19266-19271. doi:10.1073/pnas.1008937107.
36. Yuan W, Xu M, Huang C., Liu N, Chen S, et al (2011) H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem 286: 7983-7989. doi:10.1074/jbc.M110.194027.
37. Smith ZD, Meissner A. (2013) DNA methylation: roles in mammalian development. Nat Rev Genet 14: 204-220. doi:10.1038/nrg3354.
38. Neri F, Incarnato D, Krepelova A., Rapelli S, Pagnani A, et al (2013) Genome-wide analysis identifies a functional association of Tet1 and Polycomb PRC2 in mouse embryonic stem cells. Genome Biol 14: R91. doi:10.1186/gb-2013-14-8-r91.
39. Dawlaty MM, Ganz K, Powell B.E., Hu Y-C, Markoulaki S, et al (2011) Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 9: 166-175. doi:10.1016/j.stem.2011.07.010.
40. Piunti A, Pasini D. (2011) Epigenetic factors in cancer development: Polycomb group proteins. Future Oncology 7: 57-75. doi:10.2217/fon.10.157.
41. Varambally S, Dhanasekaran SM, Zhou M, Barrette T.R., 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.
42. Collett K, Eide GE, Arnes J, Stefansson I.M., Eide J., et al. (2006) Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. Clin Cancer Res 12: 1168-1174. doi:10.1158/1078-0432.CCR-05-1533.
43. Raaphorst FM, van Kemenade FJ, Blokzijl T, Fieret E, Hamer K.M., et al. (2000) Coexpression of BMI-1 and EZH2 polycomb group genes in Reed-Sternberg cells of Hodgkin's disease. Am J Pathol 157: 709-715. doi:10.1016/S0002-9440(10)64583-X.
44. Li X, Gonzalez ME, Toy K, Filzen T., Merajver SD, et al. (2009) Targeted overexpression of EZH2 in the mammary gland disrupts ductal morphogenesis and causes epithelial hyperplasia. Am J Pathol 175: 1246-1254. doi:10.2353/ajpath.2009.090042.
45. McCabe MT, Ott HM, Ganji G, Korenchuk S., Thompson C, et al. (2012) EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 492: 108-112. doi:10.1038/nature11606.
46. Puppe J, Drost R, Liu X., Joosse SA, Evers B, et al. (2009) BRCA1-deficient mammary tumor cells are dependent on EZH2 expression and sensitive to Polycomb Repressive Complex 2-inhibitor 3-deazaneplanocin A. Breast Cancer Res 11: R63. doi:10.1186/bcr2354.
47. Bachmann IM, Puntervoll HE, Otte A.P., Akslen L.A. (2008) Loss of BMI-1 expression is associated with clinical progress of malignant melanoma. Mod Pathol 21: 583-590. doi:10.1038/modpathol.2008.17.
48. 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.
49. 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.
50. 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. doi:10.1038/ng1950.
51. Mohammad HP, Cai Y, Mcgarvey K.M., Easwaran H., van Neste L, et al. (2009) Polycomb CBX7 promotes initiation of heritable repression of genes frequently silenced with cancer-specific DNA hypermethylation. Cancer Res 69: 6322-6330. doi:10.1158/0008-5472.CAN-09-0065.
52. Wichterle H, Lieberam I, Porter J.A., Jessell T.M. (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110: 385-397.
53. Wamstad JA, Alexander JM, Truty R.M., Shrikumar A., Li F, et al. (2012) Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 151: 206-220. doi:10.1016/j.cell.2012.07.035.
54. Trapnell C, Roberts A, Goff L., Pertea G, Kim D, et al (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562-578. doi:10.1038/nprot.2012.016.
55. Lee TI, Johnstone SE, Young R.A. (2006) Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 1: 729-748. doi:10.1038/nprot.2006.98.
56. Schmidt D, Wilson MD, Spyrou C, Brown G.D., Hadfield J., et al. (2009) ChIP-seq: using high-throughput sequencing to discover protein-DNA interactions. Methods 48: 240-248. doi:10.1016/j.ymeth.2009.03.001.
57. Philipp S, Puchert M, Adam-Klages S, Tchikov V., Winoto-Morbach S, et al. (2010) The Polycomb group protein EED couples TNF receptor 1 to neutral sphingomyelinase. Proc Natl Acad Sci USA 107: 1112-1117. doi:10.1073/pnas.0908486107.
58. Schmittgen TD, Livak K.J. (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.