Lack of Transcription Triggers H3K27me3 Accumulation in the Gene Body

Cell Reports

Volumn 16, Issue 3, 2016, Pages 696-706

  Hosogane, Masaki ^a   Funayama, Ryo ^a   Shirota, Matsuyuki ^a   Nakayama, Keiko ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; RAS PROTEIN; SMAD6 PROTEIN; HISTONE;

ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; CPG ISLAND; DEACETYLATION; EPHX1 GENE; GENE; GENE SILENCING; GENETIC TRANSCRIPTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMAD6 GENE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; CHROMATIN; GENETICS; MOUSE; NEOPLASM; NIH 3T3 CELL LINE; ONCOGENE RAS; PHYSIOLOGY;

ANIMALS; CELL LINE; CHROMATIN; GENE SILENCING; GENES, RAS; HISTONES; MICE; NEOPLASMS; NIH 3T3 CELLS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 84989934651     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.06.034     Document Type: Article

References (43)

1. Bauer, M., Trupke, J., Ringrose, L., The quest for mammalian Polycomb response elements: are we there yet?. Chromosoma 125 (2016), 471–496.
2. Blackledge, N.P., Farcas, A.M., Kondo, T., King, H.W., McGouran, J.F., Hanssen, L.L., Ito, S., Cooper, S., Kondo, K., Koseki, Y., et al. Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell 157 (2014), 1445–1459.
3. Blackledge, N.P., Rose, N.R., Klose, R.J., Targeting Polycomb systems to regulate gene expression: modifications to a complex story. Nat. Rev. Mol. Cell Biol. 16 (2015), 643–649.
4. Bonnet, F., Vigneron, M., Bensaude, O., Dubois, M.F., Transcription-independent phosphorylation of the RNA polymerase II C-terminal domain (CTD) involves ERK kinases (MEK1/2). Nucleic Acids Res. 27 (1999), 4399–4404.
5. Brinkman, A.B., Gu, H., Bartels, S.J., Zhang, Y., Matarese, F., Simmer, F., Marks, H., Bock, C., Gnirke, A., Meissner, A., Stunnenberg, H.G., Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res. 22 (2012), 1128–1138.
6. Cifuentes-Rojas, C., Hernandez, A.J., Sarma, K., Lee, J.T., Regulatory interactions between RNA and polycomb repressive complex 2. Mol. Cell 55 (2014), 171–185.
7. da Rocha, S.T., Boeva, V., Escamilla-Del-Arenal, M., Ancelin, K., Granier, C., Matias, N.R., Sanulli, S., Chow, J., Schulz, E., Picard, C., et al. Jarid2 Is Implicated in the Initial Xist-Induced Targeting of PRC2 to the Inactive X Chromosome. Mol. Cell 53 (2014), 301–316.
8. Di Croce, L., Helin, K., Transcriptional regulation by Polycomb group proteins. Nat. Struct. Mol. Biol. 20 (2013), 1147–1155.
9. Dietrich, N., Lerdrup, M., Landt, E., Agrawal-Singh, S., Bak, M., Tommerup, N., Rappsilber, J., Södersten, E., Hansen, K., REST-mediated recruitment of polycomb repressor complexes in mammalian cells. PLoS Genet., 8, 2012, e1002494.
10. Dubois, M.F., Nguyen, V.T., Dahmus, M.E., Pagès, G., Pouysségur, J., Bensaude, O., Enhanced phosphorylation of the C-terminal domain of RNA polymerase II upon serum stimulation of quiescent cells: possible involvement of MAP kinases. EMBO J. 13 (1994), 4787–4797.
11. Dunham, I., Kundaje, A., Aldred, S.F., Collins, P.J., Davis, C.A., Doyle, F., Epstein, C.B., Frietze, S., Harrow, J., Kaul, R., et al., ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489 (2012), 57–74.
12. Ernst, J., Kheradpour, P., Mikkelsen, T.S., Shoresh, N., Ward, L.D., Epstein, C.B., Zhang, X., Wang, L., Issner, R., Coyne, M., et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473 (2011), 43–49.
13. Erokhin, M., Elizar'ev, P., Parshikov, A., Schedl, P., Georgiev, P., Chetverina, D., Transcriptional read-through is not sufficient to induce an epigenetic switch in the silencing activity of Polycomb response elements. Proc. Natl. Acad. Sci. USA 112 (2015), 14930–14935.
14. Filippakopoulos, P., Picaud, S., Mangos, M., Keates, T., Lambert, J.P., Barsyte-Lovejoy, D., Felletar, I., Volkmer, R., Müller, S., Pawson, T., et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 149 (2012), 214–231.
15. Hosogane, M., Funayama, R., Nishida, Y., Nagashima, T., Nakayama, K., Ras-induced changes in H3K27me3 occur after those in transcriptional activity. PLoS Genet., 9, 2013, e1003698.
16. Kalb, R., Latwiel, S., Baymaz, H.I., Jansen, P.W., Müller, C.W., Vermeulen, M., Müller, J., Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression. Nat. Struct. Mol. Biol. 21 (2014), 569–571.
17. Kaneda, A., Fujita, T., Anai, M., Yamamoto, S., Nagae, G., Morikawa, M., Tsuji, S., Oshima, M., Miyazono, K., Aburatani, H., Activation of Bmp2-Smad1 signal and its regulation by coordinated alteration of H3K27 trimethylation in Ras-induced senescence. PLoS Genet., 7, 2011, e1002359.
18. Kaneko, S., Son, J., Shen, S.S., Reinberg, D., Bonasio, R., PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat. Struct. Mol. Biol. 20 (2013), 1258–1264.
19. Kaneko, S., Son, J., Bonasio, R., Shen, S.S., Reinberg, D., Nascent RNA interaction keeps PRC2 activity poised and in check. Genes Dev. 28 (2014), 1983–1988.
20. Karnoub, A.E., Weinberg, R.A., Ras oncogenes: split personalities. Nat. Rev. Mol. Cell Biol. 9 (2008), 517–531.
21. Kim, K.H., Roberts, C.W., Targeting EZH2 in cancer. Nat. Med. 22 (2016), 128–134.
22. Klose, R.J., Cooper, S., Farcas, A.M., Blackledge, N.P., Brockdorff, N., Chromatin sampling—an emerging perspective on targeting polycomb repressor proteins. PLoS Genet., 9, 2013, e1003717.
23. Konermann, S., Brigham, M.D., Trevino, A.E., Joung, J., Abudayyeh, O.O., Barcena, C., Hsu, P.D., Habib, N., Gootenberg, J.S., Nishimasu, H., et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517 (2015), 583–588.
24. Mendenhall, E.M., Koche, R.P., Truong, T., Zhou, V.W., Issac, B., Chi, A.S., Ku, M., Bernstein, B.E., GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet., 6, 2010, e1001244.
25. Musselman, C.A., Avvakumov, N., Watanabe, R., Abraham, C.G., Lalonde, M.E., Hong, Z., Allen, C., Roy, S., Nuñez, J.K., Nickoloff, J., et al. Molecular basis for H3K36me3 recognition by the Tudor domain of PHF1. Nat. Struct. Mol. Biol. 19 (2012), 1266–1272.
26. Pasini, D., Malatesta, M., Jung, H.R., Walfridsson, J., Willer, A., Olsson, L., Skotte, J., Wutz, A., Porse, B., Jensen, O.N., Helin, K., Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res. 38 (2010), 4958–4969.
27. Pauler, F.M., Sloane, M.A., Huang, R., Regha, K., Koerner, M.V., Tamir, I., Sommer, A., Aszodi, A., Jenuwein, T., Barlow, D.P., H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res. 19 (2009), 221–233.
28. Poux, S., Horard, B., Sigrist, C.J., Pirrotta, V., The Drosophila trithorax protein is a coactivator required to prevent re-establishment of polycomb silencing. Development 129 (2002), 2483–2493.
29. Ran, F.A., Hsu, P.D., Wright, J., Agarwala, V., Scott, D.A., Zhang, F., Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8 (2013), 2281–2308.
30. Reynolds, N., Salmon-Divon, M., Dvinge, H., Hynes-Allen, A., Balasooriya, G., Leaford, D., Behrens, A., Bertone, P., Hendrich, B., NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression. EMBO J. 31 (2012), 593–605.
31. Riising, E.M., Comet, I., Leblanc, B., Wu, X., Johansen, J.V., Helin, K., Gene silencing triggers polycomb repressive complex 2 recruitment to CpG islands genome wide. Mol. Cell 55 (2014), 347–360.
32. Sarma, K., Cifuentes-Rojas, C., Ergun, A., Del Rosario, A., Jeon, Y., White, F., Sadreyev, R., Lee, J.T., ATRX directs binding of PRC2 to Xist RNA and Polycomb targets. Cell 159 (2014), 869–883.
33. Schmitges, F.W., Prusty, A.B., Faty, M., Stützer, A., Lingaraju, G.M., Aiwazian, J., Sack, R., Hess, D., Li, L., Zhou, S., et al. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 42 (2011), 330–341.
34. Schmitt, S., Prestel, M., Paro, R., Intergenic transcription through a polycomb group response element counteracts silencing. Genes Dev. 19 (2005), 697–708.
35. Schwartz, Y.B., Pirrotta, V., Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8 (2007), 9–22.
36. Simon, J.A., Kingston, R.E., Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol. Cell 49 (2013), 808–824.
37. Steffen, P.A., Ringrose, L., What are memories made of? How Polycomb and Trithorax proteins mediate epigenetic memory. Nat. Rev. Mol. Cell Biol. 15 (2014), 340–356.
38. Surface, L.E., Thornton, S.R., Boyer, L.A., Polycomb group proteins set the stage for early lineage commitment. Cell Stem Cell 7 (2010), 288–298.
39. Tee, W.W., Shen, S.S., Oksuz, O., Narendra, V., Reinberg, D., Erk1/2 activity promotes chromatin features and RNAPII phosphorylation at developmental promoters in mouse ESCs. Cell 156 (2014), 678–690.
40. Yuan, W., Xu, M., Huang, C., Liu, N., Chen, S., Zhu, B., H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J. Biol. Chem. 286 (2011), 7983–7989.
41. Yuan, W., Wu, T., Fu, H., Dai, C., Wu, H., Liu, N., Li, X., Xu, M., Zhang, Z., Niu, T., et al. Dense chromatin activates Polycomb repressive complex 2 to regulate H3 lysine 27 methylation. Science 337 (2012), 971–975.
42. Zheng, Q., Cai, X., Tan, M.H., Schaffert, S., Arnold, C.P., Gong, X., Chen, C.Z., Huang, S., Precise gene deletion and replacement using the CRISPR/Cas9 system in human cells. Biotechniques 57 (2014), 115–124.
43. Zhu, J., Adli, M., Zou, J.Y., Verstappen, G., Coyne, M., Zhang, X., Durham, T., Miri, M., Deshpande, V., De Jager, P.L., et al. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152 (2013), 642–654.