Xist and Tsix Transcription Dynamics Is Regulated by the X-to-Autosome Ratio and Semistable Transcriptional States

REFERENCES

• Borsani G, Tonlorenzi R, Simmler MC, Dandolo L, Arnaud D, Capra V, Grompe M, Pizzuti A, Muzny D, Lawrence C, Willard HF, Avner P, Ballabio A. 1991. Characterization of a murine gene expressed from the inactive X chromosome. Nature 351:325–329. http://dx.doi.org/10.1038/351325a0.
   PubMed Web of Science ®Google Scholar
• Brockdorff N, Ashworth A, Kay GF, Cooper P, Smith S, McCabe VM, Norris DP, Penny GD, Patel D, Rastan S. 1991. Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 351:329–331. http://dx.doi.org/10.1038/351329a0.
   PubMed Web of Science ®Google Scholar
• Dixon-McDougall T, Brown C. 2016. The making of a Barr body: the mosaic of factors that eXIST on the mammalian inactive X chromosome. Biochem Cell Biol 94:56–70. http://dx.doi.org/10.1139/bcb-2015-0016.
   PubMedGoogle Scholar
• Moindrot B, Brockdorff N. 24 January 2016. RNA binding proteins implicated in Xist-mediated chromosome silencing. Semin Cell Dev Biol http://dx.doi.org/10.1016/j.semcdb.2016.01.029.
   Google 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
• 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
• 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, 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
• 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
• Ma Z, Swigut T, Valouev A, Rada-Iglesias A, Wysocka J. 2011. Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat Struct Mol Biol 18:120–127. http://dx.doi.org/10.1038/nsmb.2000.
   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
• Payer B, Rosenberg M, Yamaji M, Yabuta Y, Koyanagi-Aoi M, Hayashi K, Yamanaka S, Saitou M, Lee JT. 2013. Tsix RNA and the germline factor, PRDM14, link X reactivation and stem cell reprogramming. Mol Cell 52:805–818. http://dx.doi.org/10.1016/j.molcel.2013.10.023.
   PubMed Web of Science ®Google Scholar
• Donohoe ME, Zhang LF, Xu N, Shi Y, Lee JT. 2007. Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Mol Cell 25:43–56. http://dx.doi.org/10.1016/j.molcel.2006.11.017.
   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
• 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
• 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
• 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
• Gontan C, Achame EM, Demmers J, Barakat TS, Rentmeester E, van Ijcken 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
• Makhlouf M, Ouimette JF, Oldfield A, Navarro P, Neuillet D, Rougeulle C. 2014. A prominent and conserved role for YY1 in Xist transcriptional activation. Nat Commun 5:4878. http://dx.doi.org/10.1038/ncomms5878.
   PubMed Web of Science ®Google Scholar
• Shin J, Wallingford MC, Gallant J, Marcho C, Jiao B, Byron M, Bossenz M, Lawrence JB, Jones SN, Mager J, Bach I. 2014. RLIM is dispensable for X-chromosome inactivation in the mouse embryonic epiblast. Nature 511:86–89. http://dx.doi.org/10.1038/nature13286.
   PubMedGoogle 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
• 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
• Barakat TS, Loos F, van Staveren S, Myronova E, Ghazvini M, Grootegoed JA, Gribnau J. 2014. The trans-activator RNF12 and cis-acting elements effectuate X chromosome inactivation independent of X-pairing. Mol Cell 53:965–978. http://dx.doi.org/10.1016/j.molcel.2014.02.006.
   PubMedGoogle Scholar
• Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–380. http://dx.doi.org/10.1038/nature11082.
   PubMed Web of Science ®Google Scholar
• Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, Gribnau J, Barillot E, Bluthgen N, Dekker J, Heard E. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–385. http://dx.doi.org/10.1038/nature11049.
   PubMed Web of Science ®Google Scholar
• Anguera MC, Ma W, Clift D, Namekawa S, Kelleher RJ, III, Lee JT. 2011. Tsx produces a long noncoding RNA and has general functions in the germline, stem cells, and brain. PLoS Genet 7:e1002248. http://dx.doi.org/10.1371/journal.pgen.1002248.
   PubMed Web of Science ®Google Scholar
• Ogawa Y, Lee JT. 2003. Xite, X-inactivation intergenic transcription elements that regulate the probability of choice. Mol Cell 11:731–743. http://dx.doi.org/10.1016/S1097-2765(03)00063-7.
   PubMed Web of Science ®Google Scholar
• Schulz EG, Meisig J, Nakamura T, Okamoto I, Sieber A, Picard C, Borensztein M, Saitou M, Bluthgen N, Heard E. 2014. The two active X chromosomes in female ESCs block exit from the pluripotent state by modulating the ESC signaling network. Cell Stem Cell 14:203–216. http://dx.doi.org/10.1016/j.stem.2013.11.022.
   PubMed Web of Science ®Google Scholar
• Barakat TS, Rentmeester E, Sleutels F, Grootegoed JA, Gribnau J. 2011. Precise BAC targeting of genetically polymorphic mouse ES cells. Nucleic Acids Res 39:e121. http://dx.doi.org/10.1093/nar/gkr550.
   PubMedGoogle Scholar
• Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R. 1997. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev 11:156–166. http://dx.doi.org/10.1101/gad.11.2.156.
   PubMed Web of Science ®Google Scholar
• Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N. 1996. Requirement for Xist in X chromosome inactivation. Nature 379:131–137. http://dx.doi.org/10.1038/379131a0.
   PubMed Web of Science ®Google Scholar
• Stavropoulos N, Lu N, Lee JT. 2001. A functional role for Tsix transcription in blocking Xist RNA accumulation but not in X-chromosome choice. Proc Natl Acad Sci U S A 98:10232–10237. http://dx.doi.org/10.1073/pnas.171243598.
   PubMed Web of Science ®Google Scholar
• Csankovszki G, Panning B, Bates B, Pehrson JR, Jaenisch R. 1999. Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat Genet 22:323–324. http://dx.doi.org/10.1038/11887.
   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
• Masui O, Bonnet I, Le Baccon P, Brito I, Pollex T, Murphy N, Hupe P, Barillot E, Belmont AS, Heard E. 2011. Live-cell chromosome dynamics and outcome of X chromosome pairing events during ES cell differentiation. Cell 145:447–458. http://dx.doi.org/10.1016/j.cell.2011.03.032.
   PubMed Web of Science ®Google Scholar
• Mlynarczyk-Evans S, Royce-Tolland M, Alexander MK, Andersen AA, Kalantry S, Gribnau J, Panning B. 2006. X chromosomes alternate between two states prior to random X-inactivation. PLoS Biol 4:e159. http://dx.doi.org/10.1371/journal.pbio.0040159.
   PubMedGoogle Scholar
• Giorgetti L, Galupa R, Nora EP, Piolot T, Lam F, Dekker J, Tiana G, Heard E. 2014. Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell 157:950–963. http://dx.doi.org/10.1016/j.cell.2014.03.025.
   PubMed Web of Science ®Google Scholar
• Habibi E, Brinkman AB, Arand J, Kroeze LI, Kerstens HH, Matarese F, Lepikhov K, Gut M, Brun-Heath I, Hubner NC, Benedetti R, Altucci L, Jansen JH, Walter J, Gut IG, Marks H, Stunnenberg HG. 2013. Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells. Cell Stem Cell 13:360–369. http://dx.doi.org/10.1016/j.stem.2013.06.002.
   PubMed Web of Science ®Google Scholar
• Navarro P, Moffat M, Mullin NP, Chambers I. 2011. The X-inactivation trans-activator Rnf12 is negatively regulated by pluripotency factors in embryonic stem cells. Hum Genet 130:255–264. http://dx.doi.org/10.1007/s00439-011-0998-5.
   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