Histone H3 Lysine 36 Trimethylation Is Established over the Xist Promoter by Antisense Tsix Transcription and Contributes to Repressing Xist Expression

REFERENCES

• Schulz EG, Heard E. 2013. Role and control of X chromosome dosage in mammalian development. Curr Opin Genet Dev 23:109–115. http://dx.doi.org/10.1016/j.gde.2013.01.008.
   PubMedGoogle Scholar
• Lee JT, Davidow LS, Warshawsky D. 1999. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet 21:400–404. http://dx.doi.org/10.1038/7734.
   PubMed Web of Science ®Google Scholar
• Donohoe ME, Silva SS, Pinter SF, Xu N, Lee JT. 2009. The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature 460:128–132. http://dx.doi.org/10.1038/nature08098.
   PubMed Web of Science ®Google Scholar
• Gontan C, Achame EM, Demmers J, Barakat TS, Rentmeester E, van IJken W, 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
• Guyochin A, Maenner S, Chu ET, Hentati A, Attia M, Avner P, Clerc P. 2014. Live cell imaging of the nascent inactive X chromosome during the early differentiation process of naive ES cells towards epiblast stem cells. PLoS One 9:e116109. http://dx.doi.org/10.1371/journal.pone.0116109.
   PubMedGoogle Scholar
• Lee JT, Lu N. 1999. Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99:47–57. http://dx.doi.org/10.1016/S0092-8674(00)80061-6.
   PubMed Web of Science ®Google Scholar
• Luikenhuis S, Wutz A, Jaenisch R. 2001. Antisense transcription through the Xist locus mediates Tsix function in embryonic stem cells. Mol Cell Biol 21:8512–8520. http://dx.doi.org/10.1128/MCB.21.24.8512-8520.2001.
   PubMed Web of Science ®Google Scholar
• Sado T, Li E, Sasaki H. 2002. Effect of TSIX disruption on XIST expression in male ES cells. Cytogenet Genome Res 99:115–118. http://dx.doi.org/10.1159/000071582.
   PubMedGoogle Scholar
• Vigneau S, Augui S, Navarro P, Avner P, Clerc P. 2006. An essential role for the DXPas34 tandem repeat and Tsix transcription in the counting process of X chromosome inactivation. Proc Natl Acad Sci U S A 103:7390–7395. http://dx.doi.org/10.1073/pnas.0602381103.
   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
• Lee JT. 2000. Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell 103:17–27. http://dx.doi.org/10.1016/S0092-8674(00)00101-X.
   PubMedGoogle Scholar
• Sado T, Wang Z, Sasaki H, Li E. 2001. Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development 128:1275–1286.
   PubMed Web of Science ®Google Scholar
• Ohhata T, Hoki Y, Sasaki H, Sado T. 2006. Tsix-deficient X chromosome does not undergo inactivation in the embryonic lineage in males: implications for Tsix-independent silencing of Xist. Cytogenet Genome Res 113:345–349. http://dx.doi.org/10.1159/000090851.
   PubMedGoogle Scholar
• Migeon BR. 2003. Is Tsix repression of Xist specific to mouse? Nat Genet 33:337. http://dx.doi.org/10.1038/ng0303-337a. ( Reply, 33:337–338, http://dx.doi.org/10.1038/ng0303-337b.)
   PubMedGoogle Scholar
• Shibata S, Yokota T, Wutz A. 2008. Synergy of Eed and Tsix in the repression of Xist gene and X-chromosome inactivation. EMBO J 27:1816–1826. http://dx.doi.org/10.1038/emboj.2008.110.
   PubMedGoogle Scholar
• Montgomery ND, Yee D, Chen A, Kalantry S, Chamberlain SJ, Otte AP, Magnuson T. 2005. The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr Biol 15:942–947. http://dx.doi.org/10.1016/j.cub.2005.04.051.
   PubMedGoogle Scholar
• Sun BK, Deaton AM, Lee JT. 2006. A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol Cell 21:617–628. http://dx.doi.org/10.1016/j.molcel.2006.01.028.
   PubMed Web of Science ®Google Scholar
• Jonkers I, Barakat TS, Achame EM, Monkhorst K, Kenter A, Rentmeester E, Grosveld F, Grootegoed JA, Gribnau J. 2009. RNF12 is an X-encoded dose-dependent activator of X chromosome inactivation. Cell 139:999–1011. http://dx.doi.org/10.1016/j.cell.2009.10.034.
   PubMed Web of Science ®Google Scholar
• Navarro P, Chambers I, Karwacki-Neisius V, Chureau C, Morey C, Rougeulle C, Avner P. 2008. Molecular coupling of Xist regulation and pluripotency. Science 321:1693–1695. http://dx.doi.org/10.1126/science.1160952.
   PubMed Web of Science ®Google Scholar
• Navarro P, Oldfield A, Legoupi J, Festuccia N, Dubois A, Attia M, Schoorlemmer J, Rougeulle C, Chambers I, Avner P. 2010. Molecular coupling of Tsix regulation and pluripotency. Nature 468:457–460. http://dx.doi.org/10.1038/nature09496.
   PubMed Web of Science ®Google Scholar
• Barakat TS, Gunhanlar N, Pardo CG, 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
• Minkovsky A, Barakat TS, Sellami N, Chin MH, Gunhanlar N, Gribnau J, Plath K. 2013. The pluripotency factor-bound intron 1 of Xist is dispensable for X chromosome inactivation and reactivation in vitro and in vivo. Cell Rep 3:905–918. http://dx.doi.org/10.1016/j.celrep.2013.02.018.
   PubMedGoogle Scholar
• Tian D, Sun S, Lee JT. 2010. The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143:390–403. http://dx.doi.org/10.1016/j.cell.2010.09.049.
   PubMed Web of Science ®Google Scholar
• Sun S, Del Rosario BC, Szanto A, Ogawa Y, Jeon Y, Lee JT. 2013. Jpx RNA activates Xist by evicting CTCF. Cell 153:1537–1551. http://dx.doi.org/10.1016/j.cell.2013.05.028.
   PubMed Web of Science ®Google Scholar
• Chureau C, Chantalat S, Romito A, Galvani A, Duret L, Avner P, Rougeulle C. 2011. Ftx is a non-coding RNA which affects Xist expression and chromatin structure within the X-inactivation center region. Hum Mol Genet 20:705–718. http://dx.doi.org/10.1093/hmg/ddq516.
   PubMed Web of Science ®Google Scholar
• Soma M, Fujihara Y, Okabe M, Ishino F, Kobayashi S. 2014. Ftx is dispensable for imprinted X-chromosome inactivation in preimplantation mouse embryos. Sci Rep 4:5181. http://dx.doi.org/10.1038/srep05181.
   PubMedGoogle Scholar
• Augui S, Filion GJ, Huart S, Nora E, Guggiari M, Maresca M, Stewart AF, Heard E. 2007. Sensing X chromosome pairs before X inactivation via a novel X-pairing region of the Xic. Science 318:1632–1636. http://dx.doi.org/10.1126/science.1149420.
   PubMed Web of Science ®Google Scholar
• Bacher CP, Guggiari M, Brors B, Augui S, Clerc P, Avner P, Eils R, Heard E. 2006. Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation. Nat Cell Biol 8:293–299. http://dx.doi.org/10.1038/ncb1365.
   PubMed Web of Science ®Google Scholar
• Xu N, Tsai CL, Lee JT. 2006. Transient homologous chromosome pairing marks the onset of X inactivation. Science 311:1149–1152. http://dx.doi.org/10.1126/science.1122984.
   PubMed Web of Science ®Google Scholar
• Wutz A, Jaenisch R. 2000. A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol Cell 5:695–705. http://dx.doi.org/10.1016/S1097-2765(00)80248-8.
   PubMed Web of Science ®Google Scholar
• Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A. 2008. The ground state of embryonic stem cell self-renewal. Nature 453:519–523. http://dx.doi.org/10.1038/nature06968.
   PubMed Web of Science ®Google Scholar
• Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, Matsuoka C, Shimotohno K, Ishikawa F, Li E, Ueda HR, Nakayama J, Okano M. 2006. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 11:805–814. http://dx.doi.org/10.1111/j.1365-2443.2006.00984.x.
   PubMed Web of Science ®Google Scholar
• Leeb M, Wutz A. 2007. Ring1B is crucial for the regulation of developmental control genes and PRC1 proteins but not X inactivation in embryonic cells. J Cell Biol 178:219–229. http://dx.doi.org/10.1083/jcb.200612127.
   PubMedGoogle Scholar
• Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J. 2005. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123:917–929. http://dx.doi.org/10.1016/j.cell.2005.08.040.
   PubMed Web of Science ®Google Scholar
• Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, Koseki H, Brockdorff N, Fisher AG, Pombo A. 2007. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 9:1428–1435. http://dx.doi.org/10.1038/ncb1663.
   PubMed Web of Science ®Google 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
• Marks H, Kalkan T, Menafra R, Denissov S, Jones K, Hofemeister H, Nichols J, Kranz A, Stewart AF, Smith A, Stunnenberg HG. 2012. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149:590–604. http://dx.doi.org/10.1016/j.cell.2012.03.026.
   PubMed Web of Science ®Google Scholar
• Hayashi-Takanaka Y, Yamagata K, Wakayama T, Stasevich TJ, Kainuma T, Tsurimoto T, Tachibana M, Shinkai Y, Kurumizaka H, Nozaki N, Kimura H. 2011. Tracking epigenetic histone modifications in single cells using Fab-based live endogenous modification labeling. Nucleic Acids Res 39:6475–6488. http://dx.doi.org/10.1093/nar/gkr343.
   PubMedGoogle 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
• 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
• Atsuta T, Fujimura S, Moriya H, Vidal M, Akasaka T, Koseki H. 2001. Production of monoclonal antibodies against mammalian Ring1B proteins. Hybridoma 20:43–46. http://dx.doi.org/10.1089/027245701300060427.
   PubMedGoogle Scholar
• Leitch HG, McEwen KR, Turp A, Encheva V, Carroll T, Grabole N, Mansfield W, Nashun B, Knezovich JG, Smith A, Surani MA, Hajkova P. 2013. Naive pluripotency is associated with global DNA hypomethylation. Nat Struct Mol Biol 20:311–316. http://dx.doi.org/10.1038/nsmb.2510.
   PubMed Web of Science ®Google Scholar
• Rougeulle C, Chaumeil J, Sarma K, Allis CD, Reinberg D, Avner P, Heard E. 2004. Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol Cell Biol 24:5475–5484. http://dx.doi.org/10.1128/MCB.24.12.5475-5484.2004.
   PubMedGoogle Scholar
• Navarro P, Chantalat S, Foglio M, Chureau C, Vigneau S, Clerc P, Avner P, Rougeulle C. 2009. A role for non-coding Tsix transcription in partitioning chromatin domains within the mouse X-inactivation centre. Epigenet Chromatin 2:8. http://dx.doi.org/10.1186/1756-8935-2-8.
   PubMedGoogle Scholar
• Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, Presser A, Nusbaum C, Xie X, Chi AS, Adli M, Kasif S, Ptaszek LM, Cowan CA, Lander ES, Koseki H, Bernstein BE. 2008. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4:e1000242. http://dx.doi.org/10.1371/journal.pgen.1000242.
   PubMed Web of Science ®Google Scholar
• Schwartz YB, Pirrotta V. 2007. Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8:9–22. http://dx.doi.org/10.1038/nrg1981.
   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. Epigenet Chromatin 1:2. http://dx.doi.org/10.1186/1756-8935-1-2.
   PubMedGoogle 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.
   PubMed Web of Science ®Google Scholar
• Hagarman JA, Motley MP, Kristjansdottir K, Soloway PD. 2013. Coordinate regulation of DNA methylation and H3K27me3 in mouse embryonic stem cells. PLoS One 8:e53880. http://dx.doi.org/10.1371/journal.pone.0053880.
   PubMed Web of Science ®Google 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
• Joshi AA, Struhl K. 2005. Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol Cell 20:971–978. http://dx.doi.org/10.1016/j.molcel.2005.11.021.
   PubMed Web of Science ®Google Scholar
• Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ. 2005. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123:593–605. http://dx.doi.org/10.1016/j.cell.2005.10.025.
   PubMed Web of Science ®Google Scholar
• Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560. http://dx.doi.org/10.1038/nature06008.
   PubMed Web of Science ®Google Scholar
• Nimura K, Ura K, Shiratori H, Ikawa M, Okabe M, Schwartz RJ, Kaneda Y. 2009. A histone H3 lysine 36 trimethyltransferase links Nkx2-5 to Wolf-Hirschhorn syndrome. Nature 460:287–291. http://dx.doi.org/10.1038/nature08086.
   PubMed Web of Science ®Google Scholar
• Wagner EJ, Carpenter PB. 2012. Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol 13:115–126. http://dx.doi.org/10.1038/nrm3274.
   PubMed Web of Science ®Google Scholar
• Lewis PW, Muller MM, Koletsky MS, Cordero F, Lin S, Banaszynski LA, Garcia BA, Muir TW, Becher OJ, Allis CD. 2013. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340:857–861. http://dx.doi.org/10.1126/science.1232245.
   PubMed Web of Science ®Google Scholar
• Nesterova TB, Senner CE, Schneider J, Alcayna-Stevens T, Tattermusch A, Hemberger M, Brockdorff N. 2011. Pluripotency factor binding and Tsix expression act synergistically to repress Xist in undifferentiated embryonic stem cells. Epigenetics Chromatin 4:17. http://dx.doi.org/10.1186/1756-8935-4-17.
   PubMed Web of Science ®Google Scholar
• Sun S, Fukue Y, Nolen L, Sadreyev R, Lee JT. 2010. Characterization of Xpr (Xpct) reveals instability but no effects on X-chromosome pairing or Xist expression. Transcription 1:46–56. http://dx.doi.org/10.4161/trns.1.1.12401.
   PubMedGoogle Scholar