Chromatin-Mediated Reversible Silencing of Sense-Antisense Gene Pairs in Embryonic Stem Cells Is Consolidated upon Differentiation

REFERENCES

• Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, Suzuki H, Carninci P, Hayashizaki Y, Wells C, Frith M, Ravasi T, Pang KC, Hallinan J, Mattick J, Hume DA, Lipovich L, Batalov S, Engstrom PG, Mizuno Y, Faghihi MA, Sandelin A, Chalk AM, Mottagui-Tabar S, Liang Z, Lenhard B, Wahlestedt C, RIKEN Genome Exploration Research Group, Genome Science Group (Genome Network Project Core Group), FANTOM Consortium. 2005. Antisense transcription in the mammalian transcriptome. Science 309:1564–1566. http://dx.doi.org/10.1126/science.1112009.
   PubMed Web of Science ®Google Scholar
• Thakur N, Tiwari VK, Thomassin H, Pandey RR, Kanduri M, Gondor A, Grange T, Ohlsson R, Kanduri C. 2004. An antisense RNA regulates the bidirectional silencing property of the Kcnq1 imprinting control region. Mol Cell Biol 24:7855–7862. http://dx.doi.org/10.1128/MCB.24.18.7855-7862.2004.
   PubMed Web of Science ®Google Scholar
• Latos PA, Pauler FM, Koerner MV, Senergin HB, Hudson QJ, Stocsits RR, Allhoff W, Stricker SH, Klement RM, Warczok KE, Aumayr K, Pasierbek P, Barlow DP. 2012. Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing. Science 338:1469–1472. http://dx.doi.org/10.1126/science.1228110.
   PubMed Web of Science ®Google Scholar
• Williamson CM, Ball ST, Dawson C, Mehta S, Beechey CV, Fray M, Teboul L, Dear TN, Kelsey G, Peters J. 2011. Uncoupling antisense-mediated silencing and DNA methylation in the imprinted gnas cluster. PLoS Genet 7:e1001347. http://dx.doi.org/10.1371/journal.pgen.1001347.
   PubMedGoogle Scholar
• Sleutels F, Zwart R, Barlow DP. 2002. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415:810–813. http://dx.doi.org/10.1038/415810a.
   PubMed Web of Science ®Google Scholar
• Pandey R, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C. 2008. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 32:232–246. http://dx.doi.org/10.1016/j.molcel.2008.08.022.
   PubMed Web of Science ®Google Scholar
• Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, Fraser P. 2008. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322:1717–1720. http://dx.doi.org/10.1126/science.1163802.
   PubMed Web of Science ®Google Scholar
• Nesterova TB, Popova BC, Cobb BS, Norton S, Senner CE, Tang YA, Spruce T, Rodriguez TA, Sado T, Merkenschlager M, Brockdorff N. 2008. Dicer regulates Xist promoter methylation in ES cells indirectly through transcriptional control of Dnmt3a. Epigenetics Chromatin 1:2. http://dx.doi.org/10.1186/1756-8935-1-2.
   PubMedGoogle Scholar
• Sado T, Hoki Y, Sasaki H. 2005. Tsix silences Xist through modification of chromatin structure. Dev Cell 9:159–165. http://dx.doi.org/10.1016/j.devcel.2005.05.015.
   PubMed Web of Science ®Google Scholar
• Ohhata T, Hoki Y, Sasaki H, Sado T. 2008. Crucial role of antisense transcription across the Xist promoter in Tsix-mediated Xist chromatin modification. Development 135:227–235. http://dx.doi.org/10.1242/dev.008490.
   PubMed Web of Science ®Google Scholar
• Ladd PD, Smith LE, Rabaia NA, Moore JM, Georges SA, Hansen RS, Hagerman RJ, Tassone F, Tapscott SJ, Filippova GN. 2007. An antisense transcript spanning the CGG repeat region of FMR1 is upregulated in premutation carriers but silenced in full mutation individuals. Hum Mol Genet 16:3174–3187. http://dx.doi.org/10.1093/hmg/ddm293.
   PubMed Web of Science ®Google Scholar
• Brouwer JR, Willemsen R, Oostra BA. 2009. The FMR1 gene and fragile X-associated tremor/ataxia syndrome. Am J Med Genet B Neuropsychiatr Genet 150B:782–798. http://dx.doi.org/10.1002/ajmg.b.30910.
   PubMedGoogle Scholar
• Tufarelli C, Stanley JA, Garrick D, Sharpe JA, Ayyub H, Wood WG, Higgs DR. 2003. Transcription of antisense RNA leading to gene silencing and methylation as a novel cause of human genetic disease. Nat Genet 34:157–165. http://dx.doi.org/10.1038/ng1157.
   PubMed Web of Science ®Google Scholar
• Shearwin KE, Callen BP, Egan JB. 2005. Transcriptional interference—a crash course. Trends Genet 21:339–345. http://dx.doi.org/10.1016/j.tig.2005.04.009.
   PubMed Web of Science ®Google Scholar
• Li J, Moazed D, Gygi SP. 2002. Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J Biol Chem 277:49383–49388. http://dx.doi.org/10.1074/jbc.M209294200.
   PubMedGoogle Scholar
• Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP, Workman JL. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581–592. http://dx.doi.org/10.1016/j.cell.2005.10.023.
   PubMed Web of Science ®Google Scholar
• Xie L, Pelz C, Wang W, Bashar A, Varlamova O, Shadle S, Impey S. 2011. KDM5B regulates embryonic stem cell self-renewal and represses cryptic intragenic transcription. EMBO J 30:1473–1484. http://dx.doi.org/10.1038/emboj.2011.91.
   PubMed Web of Science ®Google Scholar
• Dhayalan A, Rajavelu A, Rathert P, Tamas R, Jurkowska RZ, Ragozin S, Jeltsch A. 2010. The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J Biol Chem 285:26114–26120. http://dx.doi.org/10.1074/jbc.M109.089433.
   PubMed Web of Science ®Google Scholar
• Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y. 2003. Role of histone H3 lysine 27 methylation in X inactivation. Science 300:131–135. http://dx.doi.org/10.1126/science.1084274.
   PubMed Web of Science ®Google Scholar
• Gontan C, Achame EM, Demmers J, Barakat TS, Rentmeester E, van IW, Grootegoed JA, Gribnau J. 2012. RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nature 485:386–390. http://dx.doi.org/10.1038/nature11070.
   PubMed Web of Science ®Google Scholar
• Barakat TS, Gunhanlar N, Gontan Pardo C, Achame EM, Ghazvini M, Boers R, Kenter A, Rentmeester E, Grootegoed JA, Gribnau J. 2011. RNF12 activates Xist and is essential for X chromosome inactivation. PLoS Genet 7:e1002001. http://dx.doi.org/10.1371/journal.pgen.1002001.
   PubMedGoogle Scholar
• Friedrich G, Soriano P. 1991. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev 5:1513–1523. http://dx.doi.org/10.1101/gad.5.9.1513.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−delta delta C(T)) method. Methods 25:402–408. http://dx.doi.org/10.1006/meth.2001.1262.
   PubMed Web of Science ®Google Scholar
• Kumaki Y, Oda M, Okano M. 2008. QUMA: quantification tool for methylation analysis. Nucleic Acids Res 36:W170–W175. http://dx.doi.org/10.1093/nar/gkn294.
   PubMed Web of Science ®Google Scholar
• Alexopoulou AN, Couchman JR, Whiteford JR. 2008. The CMV early enhancer/chicken beta actin (CAG) promoter can be used to drive transgene expression during the differentiation of murine embryonic stem cells into vascular progenitors. BMC Cell Biol 9:2. http://dx.doi.org/10.1186/1471-2121-9-2.
   PubMedGoogle Scholar
• Ng HH, Robert F, Young RA, Struhl K. 2003. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11:709–719. http://dx.doi.org/10.1016/S1097-2765(03)00092-3.
   PubMed Web of Science ®Google Scholar
• Saxonov S, Berg P, Brutlag DL. 2006. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci U S A 103:1412–1417. http://dx.doi.org/10.1073/pnas.0510310103.
   PubMed Web of Science ®Google Scholar
• Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, Gnirke A, Jaenisch R, Lander ES. 2008. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454:766–770. http://dx.doi.org/10.1038/nature07107.
   PubMed Web of Science ®Google Scholar
• Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schubeler D. 2008. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30:755–766. http://dx.doi.org/10.1016/j.molcel.2008.05.007.
   PubMed Web of Science ®Google Scholar
• Jeong S, Stein A. 1994. Micrococcal nuclease digestion of nuclei reveals extended nucleosome ladders having anomalous DNA lengths for chromatin assembled on non-replicating plasmids in transfected cells. Nucleic Acids Res 22:370–375. http://dx.doi.org/10.1093/nar/22.3.370.
   PubMed Web of Science ®Google Scholar
• Hebbar PB, Archer TK. 2008. Altered histone H1 stoichiometry and an absence of nucleosome positioning on transfected DNA. J Biol Chem 283:4595–4601. http://dx.doi.org/10.1074/jbc.M709121200.
   PubMed Web of Science ®Google Scholar
• Sado T, Fenner MH, Tan SS, Tam P, Shioda T, Li E. 2000. X inactivation in the mouse embryo deficient for Dnmt1: distinct effect of hypomethylation on imprinted and random X inactivation. Dev Biol 225:294–303. http://dx.doi.org/10.1006/dbio.2000.9823.
   PubMed Web of Science ®Google Scholar
• Borgel J, Guibert S, Li Y, Chiba H, Schubeler D, Sasaki H, Forne T, Weber M. 2010. Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 42:1093–1100. http://dx.doi.org/10.1038/ng.708.
   PubMed Web of Science ®Google Scholar
• Okano M, Bell DW, Haber DA, Li E. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257. http://dx.doi.org/10.1016/S0092-8674(00)81656-6.
   PubMed Web of Science ®Google Scholar
• Kristensen LH, Nielsen AL, Helgstrand C, Lees M, Cloos P, Kastrup JS, Helin K, Olsen L, Gajhede M. 2012. Studies of H3K4me3 demethylation by KDM5B/Jarid1B/PLU1 reveals strong substrate recognition in vitro and identifies 2,4-pyridine-dicarboxylic acid as an in vitro and in cell inhibitor. FEBS J 279:1905–1914. http://dx.doi.org/10.1111/j.1742-4658.2012.08567.x.
   PubMed Web of Science ®Google Scholar
• Hainer SJ, Pruneski JA, Mitchell RD, Monteverde RM, Martens JA. 2011. Intergenic transcription causes repression by directing nucleosome assembly. Genes Dev 25:29–40. http://dx.doi.org/10.1101/gad.1975011.
   PubMed Web of Science ®Google Scholar
• Thebault P, Boutin G, Bhat W, Rufiange A, Martens JA, Nourani A. 2011. Transcription regulation by the noncoding RNA SRG1 requires Spt2-dependent chromatin deposition in the wake of RNA polymerase II. Mol Cell Biol 31:1288–1300. http://dx.doi.org/10.1128/MCB.01083-10.
   PubMed Web of Science ®Google Scholar
• Eszterhas SK, Bouhassira EE, Martin DI, Fiering S. 2002. Transcriptional interference by independently regulated genes occurs in any relative arrangement of the genes and is influenced by chromosomal integration position. Mol Cell Biol 22:469–479. http://dx.doi.org/10.1128/MCB.22.2.469-479.2002.
   PubMedGoogle Scholar
• Houseley J, Rubbi L, Grunstein M, Tollervey D, Vogelauer M. 2008. A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster. Mol Cell 32:685–695. http://dx.doi.org/10.1016/j.molcel.2008.09.027.
   PubMed Web of Science ®Google Scholar
• Navarro P, Page DR, Avner P, Rougeulle C. 2006. Tsix-mediated epigenetic switch of a CTCF-flanked region of the Xist promoter determines the Xist transcription program. Genes Dev 20:2787–2792. http://dx.doi.org/10.1101/gad.389006.
   PubMed Web of Science ®Google Scholar
• Ohhata T, Senner CE, Hemberger M, Wutz A. 2011. Lineage-specific function of the noncoding Tsix RNA for Xist repression and Xi reactivation in mice. Genes Dev 25:1702–1715. http://dx.doi.org/10.1101/gad.16997911.
   PubMedGoogle Scholar
• Beard C, Li E, Jaenisch R. 1995. Loss of methylation activates Xist in somatic but not in embryonic cells. Genes Dev 9:2325–2334. http://dx.doi.org/10.1101/gad.9.19.2325.
   PubMed Web of Science ®Google Scholar
• Santoro F, Mayer D, Klement RM, Warczok KE, Stukalov A, Barlow DP, Pauler FM. 2013. Imprinted Igf2r silencing depends on continuous Airn lncRNA expression and is not restricted to a developmental window. Development 140:1184–1195. http://dx.doi.org/10.1242/dev.088849.
   PubMedGoogle Scholar
• Duhring U, Axmann IM, Hess WR, Wilde A. 2006. An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci U S A 103:7054–7058. http://dx.doi.org/10.1073/pnas.0600927103.
   PubMedGoogle Scholar
• Xu Z, Wei W, Gagneur J, Clauder-Munster S, Smolik M, Huber W, Steinmetz LM. 2011. Antisense expression increases gene expression variability and locus interdependency. Mol Syst Biol 7:468. http://dx.doi.org/10.1038/msb.2011.1.
   PubMedGoogle Scholar