Intergenic polycomb target sites are dynamically marked by non-coding transcription during lineage commitment

RNA Biology

Volumn 9, Issue 3, 2012, Pages 314-325

  Hekimoglu Balkan, Betül ^a,c   Aszodi, András ^b   Heinen, Robert ^a   Jaritz, Markus ^b   Ringrose, Leonie ^a  

^a INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

Embryonic stem cells; Intergenic; Neural differentiation; Non coding RNA; Polycomb

Indexed keywords

POLYCOMB GROUP PROTEIN; SPACER DNA; UNTRANSLATED RNA;

ANIMAL CELL; ARTICLE; CELL LINEAGE; CELL POPULATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CIS TRANS ISOMERISM; CONTROLLED STUDY; DIFFERENTIATION; DNA FLANKING REGION; GENE REPRESSION; GENE SILENCING; GENE SWITCHING; GENE TARGETING; IN VITRO STUDY; MOUSE; NONHUMAN; PROTEIN TARGETING; REPORTER GENE; RNA TRANSCRIPTION;

MURINAE; VERTEBRATA;

EID: 84860726465     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.19102     Document Type: Article

References (41)

1. Fisher CL, Fisher AG. Chromatin states in pluripotent, differentiated, and reprogrammed cells. Curr Opin Genet Dev 2011; 21:140-6; PMID:21316216; http:// dx.doi.org/10.1016/j.gde.2011.01.015
2. Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011; 469: 343-9; PMID:21248841; http://dx.doi.org/10.1038/nature09784
3. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, et al. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 2008; 30: 755-66; PMID:18514006; http://dx.doi.org/10.1016/j.molcel.2008.05.007
4. Schwartz YB, Pirrotta V. Polycomb complexes and epigenetic states. Curr Opin Cell Biol 2008; 20:266-73; PMID:18439810; http://dx.doi.org/10.1016/j.ceb. 2008.03.002
5. Schwartz YB, Kahn TG, Stenberg P, Ohno K, Bourgon R, Pirrotta V. Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet 2010; 6: e1000805; PMID:20062800; http://dx.doi.org/10.1371/journal.pgen.1000805
6. Bae E, Calhoun VC, Levine M, Lewis EB, Drewell RA. Characterization of the intergenic RNA profile at abdominal-A and Abdominal-B in the Drosophila bithorax complex. Proc Natl Acad Sci U S A 2002; 99:16847-52; PMID:12481037; http://dx.doi.org/10.1073/pnas.222671299
7. Sessa L, Breiling A, Lavorgna G, Silvestri L, Casari G, Orlando V. Noncoding RNA synthesis and loss of Polycomb group repression accompanies the colinear activation of the human HOXA cluster. RNA 2007; 13:223-39; PMID:17185360; http://dx.doi.org/10.1261/rna.266707
8. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007; 129:1311-23; PMID: 17604720; http://dx.doi.org/10. 1016/j.cell.2007.05.022
9. Enderle D, Beisel C, Stadler MB, Gerstung M, Athri P, Paro R. Polycomb preferentially targets stalled promoters of coding and noncoding transcripts. Genome Res 2011; 21:216-26; PMID:21177970; http://dx.doi. org/10.1101/gr.114348. 110
10. Hekimoglu B, Ringrose L. Non-coding RNAs in polycomb/trithorax regulation. RNA Biol 2009; 6:129- 37; PMID:19270511; http://dx.doi.org/10.4161/ rna.6.2.8178
11. Müller J, Kassis JA. Polycomb response elements and targeting of Polycomb group proteins in Drosophila. Curr Opin Genet Dev 2006; 16:476-84; PMID: 16914306; http://dx.doi.org/10.1016/j.gde.2006.08.005
12. Lempradl A, Ringrose L. How does noncoding transcription regulate Hox genes? Bioessays 2008; 30:110-21; PMID:18200528; http://dx.doi.org/10.1002/bies. 20704
13. Schmitt S, Prestel M, Paro R. Intergenic transcription through a polycomb group response element counteracts silencing. Genes Dev 2005; 19:697-708; PMID: 15741315; http://dx.doi.org/10.1101/gad.326205
14. Petruk S, Sedkov Y, Riley KM, Hodgson J, Schweisguth F, Hirose S, et al. Transcription of bxd noncoding RNAs promoted by trithorax represses Ubx in cis by transcriptional interference. Cell 2006; 127: 1209-21; PMID:17174895; http://dx.doi.org/10.1016/j.cell.2006.10.039
15. Sing A, Pannell D, Karaiskakis A, Sturgeon K, Djabali M, Ellis J, et al. A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell 2009; 138:885-97; PMID:19737517; http://dx.doi.org/10.1016/j. cell.2009.08.020
16. Woo CJ, Kharchenko PV, Daheron L, Park PJ, Kingston RE. A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 2010; 140:99-110; PMID:20085705; http://dx.doi.org/10.1016/j.cell.2009.12.022
17. Tanay A, O'Donnell AH, Damelin M, Bestor TH. Hyperconserved CpG domains underlie Polycombbinding sites. Proc Natl Acad Sci U S A 2007; 104: 5521-6; PMID:17376869; http://dx.doi.org/10.1073/pnas.0609746104
18. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 2008; 4:e1000242; PMID:18974828; http://dx.doi.org/10.1371/journal.pgen.1000242
19. Peng JC, Valouev A, Swigut T, Zhang J, Zhao Y, Sidow A, et al. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 2009; 139:1290-302; PMID: 20064375; http://dx.doi.org/10.1016/j.cell.2009.12.002
20. Mendenhall EM, Koche RP, Truong T, Zhou VW, Issac B, Chi AS, et al. GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet 2010; 6:e1001244; PMID:21170310; http://dx.doi.org/10.1371/journal.pgen.1001244
21. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008; 322:750-6; PMID: 18974356; http://dx.doi.org/10.1126/science.1163045
22. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, et al. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 2008; 32:232-46; PMID:18951091; http:// dx.doi.org/10.1016/j.molcel.2008.08.022
23. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 2009; 106:11667-72; PMID:19571010; http://dx.doi.org/10.1073/pnas.0904715106
24. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, et al. Genome-wide identification of polycomb- associated RNAs by RIP-seq. Mol Cell 2010; 40:939-53; PMID:21172659; http://dx.doi.org/10.1016/j.molcel.2010.12.011
25. Kanhere A, Viiri K, Araújo CC, Rasaiyaah J, Bouwman RD, Whyte WA, et al. Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol Cell 2010; 38: 675-88; PMID:20542000; http://dx.doi.org/10.1016/j.molcel.2010.03.019
26. Kaneko S, Li G, Son J, Xu CF, Margueron R, Neubert TA, et al. Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev 2010; 24:2615-20; PMID: 21123648; http://dx.doi.org/10.1101/gad.1983810
27. Jeon Y, Lee JT. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 2011; 146:119-33; PMID: 21729784; http://dx.doi.org/10.1016/j.cell.2011. 06.026
28. Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, et al. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 2008; 18:1433-45; PMID: 18562676; http://dx.doi.org/10.1101/gr.078378.108
29. ∅rom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 2010; 143:46-58; PMID:20887892; http://dx.doi.org/10.1016/j.cell.2010.09.001
30. Wang KC, Yang YW, Liu B, Sanyal A, Corces- Zimmerman R, Chen Y, et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 2011; 472:120-4; PMID: 21423168; http://dx.doi.org/10.1038/ nature09819
31. Pollard SM, Benchoua A, Lowell S. Neural stem cells, neurons, and glia. Methods Enzymol 2006; 418:151-69; PMID:17141035; http://dx.doi.org/10.1016/ S0076-6879(06)18010-6
32. Ying QL, Smith AG. Defined conditions for neural commitment and differentiation. Methods Enzymol 2003; 365:327-41; PMID:14696356; http://dx.doi.org/10.1016/S0076-6879(03)65023-8
33. Aubert J, StavridisMP, Tweedie S,O'ReillyM, Vierlinger K, Li M, et al. Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc Natl Acad Sci U S A 2003; 100(Suppl 1):11836-41; PMID: 12923295; http://dx.doi.org/10. 1073/pnas.1734197100
34. Tucker KL, Meyer M, Barde YA. Neurotrophins are required for nerve growth during development. Nat Neurosci 2001; 4:29-37; PMID:11135642; http://dx.doi.org/10.1038/82868
35. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006; 441:349-53; PMID: 16625203; http://dx.doi.org/10.1038/ nature04733
36. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, 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
37. Shilatifard A. Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr Opin Cell Biol 2008; 20:341-8; PMID: 18508253; http://dx.doi.org/10.1016/j.ceb.2008.03.019
38. Barrera LO, Li Z, Smith AD, Arden KC, Cavenee WK, Zhang MQ, et al. Genome-wide mapping and analysis of active promoters in mouse embryonic stem cells and adult organs. Genome Res 2008; 18:46-59; PMID: 18042645; http://dx.doi.org/10.1101/gr.6654808
39. Sanchez-Elsner T, Gou D, Kremmer E, Sauer F. Noncoding RNAs of trithorax response elements recruit Drosophila Ash1 to Ultrabithorax. Science 2006; 311:1118-23; PMID:16497925; http://dx.doi.org/10.1126/science.1117705
40. Shen X, Kim W, Fujiwara Y, Simon MD, Liu Y, Mysliwiec MR, et al. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 2009; 139:1303-14; PMID:20064376; http://dx.doi.org/10.1016/j.cell. 2009.12.003
41. Martens JHA, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 2005; 24:800-12; PMID: 15678104; http://dx.doi.org/10.1038/sj.emboj.7600545