Association of the Long Non-coding RNA Steroid Receptor RNA Activator (SRA) with TrxG and PRC2 Complexes

PLoS Genetics

Volumn 11, Issue 10, 2015, Pages

  Wongtrakoongate, Patompon ^a,b   Riddick, Gregory ^a   Fucharoen, Suthat ^b   Felsenfeld, Gary ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; LONG UNTRANSLATED RNA; NUCLEIC ACID BINDING PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; STEROID RECEPTOR RNA ACTIVATOR; TRANSCRIPTION FACTOR NANOG; TRITHORAX GROUP PROTEIN; UNCLASSIFIED DRUG; CCCTC-BINDING FACTOR; CHROMATIN; DNA BINDING PROTEIN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HOMEODOMAIN PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN; MLL PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; NANOG PROTEIN, HUMAN; PROTEIN KINASE R; REPRESSOR PROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING; FIBROBLAST; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; NUCLEAR REPROGRAMMING; NUCLEOTIDE BINDING SITE; PLURIPOTENT STEM CELL; PROTEIN NUCLEIC ACID INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; BINDING SITE; CHROMATIN; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

BINDING SITES; CHROMATIN; DNA-BINDING PROTEINS; EIF-2 KINASE; GENE EXPRESSION REGULATION; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HOMEODOMAIN PROTEINS; HUMANS; MULTIPROTEIN COMPLEXES; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NANOG HOMEOBOX PROTEIN; PLURIPOTENT STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 2; REPRESSOR PROTEINS; RNA, LONG NONCODING;

EID: 84946606813     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005615     Document Type: Article

References (51)

1. Hu D, Garruss AS, Gao X, Morgan MA, Cook M, Smith ER, et al. The Mll2 branch of the COMPASS family regulates bivalent promoters in mouse embryonic stem cells. Nature structural & molecular biology. 2013;20(9):1093–7. Epub 2013/08/13. doi: 10.1038/nsmb.2653 23934151; PubMed Central PMCID: PMCPMC3805109.
2. Denissov S, Hofemeister H, Marks H, Kranz A, Ciotta G, Singh S, et al. Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant. Development. 2014;141(3):526–37. Epub 2014/01/16. doi: 10.1242/dev.102681 24423662.
3. Voigt P, Tee WW, Reinberg D, A double take on bivalent promoters. Genes Dev. 2013;27(12):1318–38. Epub 2013/06/22. doi: 10.1101/gad.219626.113 23788621; PubMed Central PMCID: PMCPMC3701188.
4. Ang YS, Tsai SY, Lee DF, Monk J, Su J, Ratnakumar K, et al. Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell. 2011;145(2):183–97. Epub 2011/04/12. doi: 10.1016/j.cell.2011.03.003 21477851; PubMed Central PMCID: PMC3097468.
5. Mo R, Rao SM, Zhu YJ, Identification of the MLL2 complex as a coactivator for estrogen receptor alpha. The Journal of biological chemistry. 2006;281(23):15714–20. Epub 2006/04/11. doi: 10.1074/jbc.M513245200 16603732.
6. Li T, Hu JF, Qiu X, Ling J, Chen H, Wang S, et al. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop. Molecular and cellular biology. 2008;28(20):6473–82. Epub 2008/07/30. doi: 10.1128/mcb.00204-08 18662993; PubMed Central PMCID: PMCPMC2577414.
7. Kaneko S, Son J, Shen SS, Reinberg D, Bonasio R, PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nature structural & molecular biology. 2013;20(11):1258–64. Epub 2013/10/22. doi: 10.1038/nsmb.2700 24141703; PubMed Central PMCID: PMCPMC3839660.
8. Kanhere A, Viiri K, Araujo 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(5):675–88. Epub 2010/06/15. doi: 10.1016/j.molcel.2010.03.019 20542000; PubMed Central PMCID: PMCPMC2886029.
9. Davidovich C, Zheng L, Goodrich KJ, Cech TR, Promiscuous RNA binding by Polycomb repressive complex 2. Nature structural & molecular biology. 2013;20(11):1250–7. Epub 2013/10/01. doi: 10.1038/nsmb.2679 24077223; PubMed Central PMCID: PMC3823624.
10. Davidovich C, Wang X, Cifuentes-Rojas C, Goodrich KJ, Gooding AR, Lee JT, et al. Toward a consensus on the binding specificity and promiscuity of PRC2 for RNA. Mol Cell. 2015;57(3):552–8. Epub 2015/01/21. doi: 10.1016/j.molcel.2014.12.017 25601759; PubMed Central PMCID: PMCPmc4320675.
11. Rinn JL, Chang HY, Genome regulation by long noncoding RNAs. Annual review of biochemistry. 2012;81:145–66. Epub 2012/06/06. doi: 10.1146/annurev-biochem-051410-092902 22663078.
12. 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(7341):120–4. Epub 2011/03/23. doi: 10.1038/nature09819 21423168; PubMed Central PMCID: PMCPMC3670758.
13. Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S, Monack DM, et al. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell. 2013;152(4):743–54. Epub 2013/02/19. doi: 10.1016/j.cell.2013.01.015 23415224; PubMed Central PMCID: PMCPMC3577098.
14. Herriges MJ, Swarr DT, Morley MP, Rathi KS, Peng T, Stewart KM, et al. Long noncoding RNAs are spatially correlated with transcription factors and regulate lung development. Genes Dev. 2014;28(12):1363–79. Epub 2014/06/19. doi: 10.1101/gad.238782.114 24939938; PubMed Central PMCID: PMCPmc4066405.
15. 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(5902):750–6. Epub 2008/11/01. 322/5902/750 [pii] doi: 10.1126/science.1163045 18974356; PubMed Central PMCID: PMC2748911.
16. 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(7):1311–23. Epub 2007/07/03. doi: 10.1016/j.cell.2007.05.022 17604720; PubMed Central PMCID: PMCPMC2084369.
17. Klattenhoff CA, Scheuermann JC, Surface LE, Bradley RK, Fields PA, Steinhauser ML, et al. Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell. 2013;152(3):570–83. Epub 2013/01/29. doi: 10.1016/j.cell.2013.01.003 23352431; PubMed Central PMCID: PMCPMC3563769.
18. Cifuentes-Rojas C, Hernandez AJ, Sarma K, Lee JT, Regulatory interactions between RNA and polycomb repressive complex 2. Mol Cell. 2014;55(2):171–85. Epub 2014/06/03. doi: 10.1016/j.molcel.2014.05.009 24882207; PubMed Central PMCID: PMCPmc4107928.
19. Chu C, Qu K, Zhong FL, Artandi SE, Chang HY, Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell. 2011;44(4):667–78. Epub 2011/10/04. doi: 10.1016/j.molcel.2011.08.027 21963238; PubMed Central PMCID: PMC3249421.
20. Simon MD, Pinter SF, Fang R, Sarma K, Rutenberg-Schoenberg M, Bowman SK, et al. High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature. 2013. Epub 2013/10/29. doi: 10.1038/nature12719 24162848.
21. Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K, Surka C, et al. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science. 2013;341(6147):1237973. Epub 2013/07/06. doi: 10.1126/science.1237973 23828888; PubMed Central PMCID: PMCPMC3778663.
22. Colley SM, Leedman PJ, Steroid Receptor RNA Activator—A nuclear receptor coregulator with multiple partners: Insights and challenges. Biochimie. 2011;93(11):1966–72. Epub 2011/08/03. doi: 10.1016/j.biochi.2011.07.004 21807064.
23. Ghosh SK, Patton JR, Spanjaard RA, A Small RNA Derived from RNA Coactivator SRA Blocks Steroid Receptor Signaling via Inhibition of Pus1p-Mediated Pseudouridylation of SRA: Evidence of a Novel RNA Binding Domain in the N-Terminus of Steroid Receptors. Biochemistry. 2012. Epub 2012/09/25. doi: 10.1021/bi300602r 22998747.
24. Lanz RB, McKenna NJ, Onate SA, Albrecht U, Wong J, Tsai SY, et al. A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell. 1999;97(1):17–27. Epub 1999/04/13. 10199399.
25. Caretti G, Schiltz RL, Dilworth FJ, Di Padova M, Zhao P, Ogryzko V, et al. The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell. 2006;11(4):547–60. Epub 2006/10/03. doi: 10.1016/j.devcel.2006.08.003 17011493.
26. Yao H, Brick K, Evrard Y, Xiao T, Camerini-Otero RD, Felsenfeld G, Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev. 2010;24(22):2543–55. Epub 2010/10/23. gad.1967810 [pii] doi: 10.1101/gad.1967810 20966046; PubMed Central PMCID: PMC2975930.
27. 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(6):939–53. Epub 2010/12/22. doi: 10.1016/j.molcel.2010.12.011 21172659; PubMed Central PMCID: PMCPMC3021903.
28. Vicent GP, Nacht AS, Zaurin R, Font-Mateu J, Soronellas D, Le Dily F, et al. Unliganded progesterone receptor-mediated targeting of an RNA-containing repressive complex silences a subset of hormone-inducible genes. Genes Dev. 2013;27(10):1179–97. Epub 2013/05/24. doi: 10.1101/gad.215293.113 23699411; PubMed Central PMCID: PMCPMC3672650.
29. Foulds CE, Tsimelzon A, Long W, Le A, Tsai SY, Tsai MJ, et al. Research resource: expression profiling reveals unexpected targets and functions of the human steroid receptor RNA activator (SRA) gene. Mol Endocrinol. 2010;24(5):1090–105. Epub 2010/03/12. me.2009-0427 [pii] doi: 10.1210/me.2009-0427 20219889; PubMed Central PMCID: PMC2870939.
30. Novikova IV, Hennelly SP, Sanbonmatsu KY, Structural architecture of the human long non-coding RNA, steroid receptor RNA activator. Nucleic Acids Res. 2012;40(11):5034–51. Epub 2012/03/01. doi: 10.1093/nar/gks071 22362738; PubMed Central PMCID: PMCPMC3367176.
31. 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(2):301–13. Epub 2006/04/25. doi: 10.1016/j.cell.2006.02.043 16630818; PubMed Central PMCID: PMCPMC3773330.
32. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005;122(6):947–56. Epub 2005/09/13. doi: 10.1016/j.cell.2005.08.020 16153702; PubMed Central PMCID: PMC3006442.
33. Onder TT, Kara N, Cherry A, Sinha AU, Zhu N, Bernt KM, et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature. 2012;483(7391):598–602. Epub 2012/03/06. doi: 10.1038/nature10953 22388813; PubMed Central PMCID: PMCPMC3501145.
34. Pereira CF, Piccolo FM, Tsubouchi T, Sauer S, Ryan NK, Bruno L, et al. ESCs require PRC2 to direct the successful reprogramming of differentiated cells toward pluripotency. Cell stem cell. 2010;6(6):547–56. Epub 2010/06/24. doi: 10.1016/j.stem.2010.04.013 20569692.
35. Grote P, Wittler L, Hendrix D, Koch F, Wahrisch S, Beisaw A, et al. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell. 2013;24(2):206–14. Epub 2013/02/02. doi: 10.1016/j.devcel.2012.12.012 23369715.
36. Sarma K, Cifuentes-Rojas C, Ergun A, Del Rosario A, Jeon Y, White F, et al. ATRX directs binding of PRC2 to Xist RNA and Polycomb targets. Cell. 2014;159(4):869–83. Epub 2014/11/25. doi: 10.1016/j.cell.2014.10.019 25417162.
37. Zaehres H, Lensch MW, Daheron L, Stewart SA, Itskovitz-Eldor J, Daley GQ, High-efficiency RNA interference in human embryonic stem cells. Stem cells (Dayton, Ohio). 2005;23(3):299–305. Epub 2005/03/08. doi: 10.1634/stemcells.2004-0252 15749924.
38. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003;113(5):643–55. Epub 2003/06/06. 12787505.
39. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell. 2003;113(5):631–42. Epub 2003/06/06. 12787504.
40. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, Barrandon O, et al. Nanog is the gateway to the pluripotent ground state. Cell. 2009;138(4):722–37. Epub 2009/08/26. doi: 10.1016/j.cell.2009.07.039 19703398; PubMed Central PMCID: PMCPMC3437554.
41. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science. 2010;329(5992):689–93. Epub 2010/07/10. science.1192002 [pii] doi: 10.1126/science.1192002 20616235; PubMed Central PMCID: PMC2967777.
42. Chu C, Quinn J, Chang HY, Chromatin isolation by RNA purification (ChIRP). Journal of visualized experiments: JoVE. 2012;25(61). Epub 2012/04/05. 10.3791/3912. 22472705; PubMed Central PMCID: PMC3460573.
43. Simon MD, Wang CI, Kharchenko PV, West JA, Chapman BA, Alekseyenko AA, et al. The genomic binding sites of a noncoding RNA. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(51):20497–502. Epub 2011/12/07. doi: 10.1073/pnas.1113536108 22143764; PubMed Central PMCID: PMCPMC3251105.
44. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics (Oxford, England). 2009;25(16):2078–9. Epub 2009/06/10. doi: 10.1093/bioinformatics/btp352 19505943; PubMed Central PMCID: PMCPMC2723002.
45. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome biology. 2008;9(9):R137. Epub 2008/09/19. doi: 10.1186/gb-2008-9-9-r137 18798982; PubMed Central PMCID: PMCPMC2592715.
46. Zhu LJ, Gazin C, Lawson ND, Pages H, Lin SM, Lapointe DS, et al. ChIPpeakAnno: a Bioconductor package to annotate ChIP-seq and ChIP-chip data. BMC bioinformatics. 2010;11:237. Epub 2010/05/13. doi: 10.1186/1471-2105-11-237 20459804; PubMed Central PMCID: PMCPMC3098059.
47. Quinlan AR, Hall IM, BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics (Oxford, England). 2010;26(6):841–2. Epub 2010/01/30. doi: 10.1093/bioinformatics/btq033 20110278; PubMed Central PMCID: PMCPMC2832824.
48. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nature biotechnology. 2011;29(1):24–6. Epub 2011/01/12. doi: 10.1038/nbt.1754 21221095; PubMed Central PMCID: PMCPMC3346182.
49. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, et al. GREAT improves functional interpretation of cis-regulatory regions. Nature biotechnology. 2010;28(5):495–501. Epub 2010/05/04. doi: 10.1038/nbt.1630 20436461.
50. RCoreTeam. R: A language and environment for statistical computing2013.
51. Wongtrakoongate P, Li J, Andrews PW, DNMT3B inhibits the re-expression of genes associated with induced pluripotency. Experimental cell research. 2014;321(2):231–9. Epub 2013/12/18. doi: 10.1016/j.yexcr.2013.11.024 24333507; PubMed Central PMCID: PMC24333507.