Xist Exon 7 Contributes to the Stable Localization of Xist RNA on the Inactive X-Chromosome

PLoS Genetics

Volumn 11, Issue 8, 2015, Pages

  Yamada, Norishige ^a,b   Hasegawa, Yuko ^c   Yue, Minghui ^a,b   Hamada, Tomofumi ^d   Nakagawa, Shinichi ^c   Ogawa, Yuya ^a,b  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c RIKEN   (Japan)

^d KAGOSHIMA UNIVERSITY HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN U; LONG UNTRANSLATED RNA; UNCLASSIFIED DRUG; X INACTIVE SPECIFIC TRANSCRIPT RNA; XIST NON-CODING RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; EXON; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE SILENCING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; RNA ANALYSIS; RNA STABILITY; STRUCTURE ACTIVITY RELATION; WILD TYPE; X CHROMOSOME INACTIVATION; XIST EXON 7; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; COCULTURE; EMBRYOID BODY; FEMALE; GENETICS; MALE; PHYSIOLOGY; RNA TRANSPORT; X CHROMOSOME;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYOID BODIES; EXONS; FEMALE; GENE EXPRESSION; GENE SILENCING; MALE; MICE; RNA TRANSPORT; RNA, LONG NONCODING; X CHROMOSOME; X CHROMOSOME INACTIVATION;

EID: 84940758356     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005430     Document Type: Article

References (67)

1. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, et al. (2005) The transcriptional landscape of the mammalian genome. Science 309: 1559–1563. 16141072
2. Mattick JS, Makunin IV, (2006) Non-coding RNA. Hum Mol Genet 15 Spec No 1: R17–29. 16651366
3. Mercer TR, Mattick JS, (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20: 300–307. doi: 10.1038/nsmb.2480 23463315
4. Rinn JL, Chang HY, (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81: 145–166. doi: 10.1146/annurev-biochem-051410-092902 22663078
5. Kitagawa M, Kitagawa K, Kotake Y, Niida H, Ohhata T, (2013) Cell cycle regulation by long non-coding RNAs. Cell Mol Life Sci 70: 4785–4794. doi: 10.1007/s00018-013-1423-0 23880895
6. Fatica A, Bozzoni I, (2014) Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15: 7–21. doi: 10.1038/nrg3606 24296535
7. Kornfeld JW, Bruning JC, (2014) Regulation of metabolism by long, non-coding RNAs. Front Genet 5: 57. doi: 10.3389/fgene.2014.00057 24723937
8. Cheetham SW, Gruhl F, Mattick JS, Dinger ME, (2013) Long noncoding RNAs and the genetics of cancer. Br J Cancer 108: 2419–2425. doi: 10.1038/bjc.2013.233 23660942
9. Gutschner T, Diederichs S, (2012) The hallmarks of cancer: a long non-coding RNA point of view. RNA Biol 9: 703–719. doi: 10.4161/rna.20481 22664915
10. Payer B, Lee JT, (2008) X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 42: 733–772. doi: 10.1146/annurev.genet.42.110807.091711 18729722
11. Maclary E, Hinten M, Harris C, Kalantry S, (2013) Long nonoding RNAs in the X-inactivation center. Chromosome Res 21: 601–614. doi: 10.1007/s10577-013-9396-2 24297756
12. Augui S, Nora EP, Heard E, (2011) Regulation of X-chromosome inactivation by the X-inactivation centre. Nat Rev Genet 12: 429–442. doi: 10.1038/nrg2987 21587299
13. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N, (1996) Requirement for Xist in X chromosome inactivation. Nature 379: 131–137. 8538762
14. Clemson CM, McNeil JA, Willard HF, Lawrence JB, (1996) XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol 132: 259–275. 8636206
15. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, et al. (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300: 131–135. 12649488
16. Silva J, Mak W, Zvetkova I, Appanah R, Nesterova TB, et al. (2003) Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev Cell 4: 481–495. 12689588
17. Csankovszki G, Nagy A, Jaenisch R, (2001) Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation. J Cell Biol 153: 773–784. 11352938
18. Brown CJ, Willard HF, (1994) The human X-inactivation centre is not required for maintenance of X-chromosome inactivation. Nature 368: 154–156. 8139659
19. 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. 10431231
20. Zhang LF, Huynh KD, Lee JT, (2007) Perinucleolar targeting of the inactive X during S phase: evidence for a role in the maintenance of silencing. Cell 129: 693–706. 17512404
21. Yildirim E, Kirby JE, Brown DE, Mercier FE, Sadreyev RI, et al. (2013) Xist RNA is a potent suppressor of hematologic cancer in mice. Cell 152: 727–742. doi: 10.1016/j.cell.2013.01.034 23415223
22. Sado T, Brockdorff N, (2013) Advances in understanding chromosome silencing by the long non-coding RNA Xist. Philos Trans R Soc Lond B Biol Sci 368: 20110325. doi: 10.1098/rstb.2011.0325 23166390
23. Wutz A, Rasmussen TP, Jaenisch R, (2002) Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 30: 167–174. 11780141
24. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT, (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750–756. doi: 10.1126/science.1163045 18974356
25. Davidovich C, Wang X, Cifuentes-Rojas C, Goodrich KJ, Gooding AR, et al. (2015) Toward a consensus on the binding specificity and promiscuity of PRC2 for RNA. Mol Cell 57: 552–558. doi: 10.1016/j.molcel.2014.12.017 25601759
26. Davidovich C, Zheng L, Goodrich KJ, Cech TR, (2013) Promiscuous RNA binding by Polycomb repressive complex 2. Nat Struct Mol Biol 20: 1250–1257. doi: 10.1038/nsmb.2679 24077223
27. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, et al. (2010) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 40: 939–953. doi: 10.1016/j.molcel.2010.12.011 21172659
28. Kaneko S, Son J, Shen SS, Reinberg D, Bonasio R, (2013) PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat Struct Mol Biol 20: 1258–1264. doi: 10.1038/nsmb.2700 24141703
29. Kanhere A, Viiri K, Araujo CC, Rasaiyaah J, Bouwman RD, et al. (2010) Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol Cell 38: 675–688. doi: 10.1016/j.molcel.2010.03.019 20542000
30. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, et al. (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 106: 11667–11672. doi: 10.1073/pnas.0904715106 19571010
31. Cifuentes-Rojas C, Hernandez AJ, Sarma K, Lee JT, (2014) Regulatory interactions between RNA and polycomb repressive complex 2. Mol Cell 55: 171–185. doi: 10.1016/j.molcel.2014.05.009 24882207
32. Beletskii A, Hong YK, Pehrson J, Egholm M, Strauss WM, (2001) PNA interference mapping demonstrates functional domains in the noncoding RNA Xist. Proc Natl Acad Sci U S A 98: 9215–9220. 11481485
33. Sarma K, Levasseur P, Aristarkhov A, Lee JT, (2010) Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proc Natl Acad Sci U S A 107: 22196–22201. doi: 10.1073/pnas.1009785107 21135235
34. Jeon Y, Lee JT, (2011) YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146: 119–133. doi: 10.1016/j.cell.2011.06.026 21729784
35. Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Tsutui K, et al. (2010) The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev Cell 19: 469–476. doi: 10.1016/j.devcel.2010.08.006 20833368
36. Pullirsch D, Hartel R, Kishimoto H, Leeb M, Steiner G, et al. (2010) The Trithorax group protein Ash2l and Saf-A are recruited to the inactive X chromosome at the onset of stable X inactivation. Development 137: 935–943. doi: 10.1242/dev.035956 20150277
37. Romig H, Fackelmayer FO, Renz A, Ramsperger U, Richter A, (1992) Characterization of SAF-A, a novel nuclear DNA binding protein from HeLa cells with high affinity for nuclear matrix/scaffold attachment DNA elements. EMBO J 11: 3431–3440. 1324173
38. Kiledjian M, Dreyfuss G, (1992) Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J 11: 2655–2664. 1628625
39. Tsutsui K, Tsutsui K, Okada S, Watarai S, Seki S, et al. (1993) Identification and characterization of a nuclear scaffold protein that binds the matrix attachment region DNA. J Biol Chem 268: 12886–12894. 8509422
40. Kim MK, Nikodem VM, (1999) hnRNP U inhibits carboxy-terminal domain phosphorylation by TFIIH and represses RNA polymerase II elongation. Mol Cell Biol 19: 6833–6844. 10490622
41. Kukalev A, Nord Y, Palmberg C, Bergman T, Percipalle P, (2005) Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat Struct Mol Biol 12: 238–244. 15711563
42. Fu D, Collins K, (2007) Purification of human telomerase complexes identifies factors involved in telomerase biogenesis and telomere length regulation. Mol Cell 28: 773–785. 18082603
43. Hacisuleyman E, Goff LA, Trapnell C, Williams A, Henao-Mejia J, et al. (2014) Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat Struct Mol Biol 21: 198–206. doi: 10.1038/nsmb.2764 24463464
44. Kipp M, Gohring F, Ostendorp T, van Drunen CM, van Driel R, et al. (2000) SAF-Box, a conserved protein domain that specifically recognizes scaffold attachment region DNA. Mol Cell Biol 20: 7480–7489. 11003645
45. Helbig R, Fackelmayer FO, (2003) Scaffold attachment factor A (SAF-A) is concentrated in inactive X chromosome territories through its RGG domain. Chromosoma 112: 173–182. 14608463
46. Yen ZC, Meyer IM, Karalic S, Brown CJ, (2007) A cross-species comparison of X-chromosome inactivation in Eutheria. Genomics 90: 453–463. 17728098
47. Lee JT, Lu N, (1999) Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99: 47–57. 10520993
48. Ogawa Y, Sun BK, Lee JT, (2008) Intersection of the RNA interference and X-inactivation pathways. Science 320: 1336–1341. doi: 10.1126/science.1157676 18535243
49. 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. 16507360
50. Chow JC, Hall LL, Baldry SE, Thorogood NP, Lawrence JB, et al. (2007) Inducible XIST-dependent X-chromosome inactivation in human somatic cells is reversible. Proc Natl Acad Sci U S A 104: 10104–10109. 17537922
51. Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, et al. (1992) The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 71: 515–526. 1423610
52. Xiao R, Tang P, Yang B, Huang J, Zhou Y, et al. (2012) Nuclear matrix factor hnRNP U/SAF-A exerts a global control of alternative splicing by regulating U2 snRNP maturation. Mol Cell 45: 656–668. doi: 10.1016/j.molcel.2012.01.009 22325991
53. Fackelmayer FO, Dahm K, Renz A, Ramsperger U, Richter A, (1994) Nucleic-acid-binding properties of hnRNP-U/SAF-A, a nuclear-matrix protein which binds DNA and RNA in vivo and in vitro. Eur J Biochem 221: 749–757. 8174554
54. Koziol MJ, Rinn JL, (2010) RNA traffic control of chromatin complexes. Curr Opin Genet Dev 20: 142–148. doi: 10.1016/j.gde.2010.03.003 20362426
55. Wang KC, Chang HY, (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43: 904–914. doi: 10.1016/j.molcel.2011.08.018 21925379
56. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, et al. (2010) A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142: 409–419. doi: 10.1016/j.cell.2010.06.040 20673990
57. Carpenter S, Aiello D, Atianand MK, Ricci EP, Gandhi P, et al. (2013) A long noncoding RNA mediates both activation and repression of immune response genes. Science 341: 789–792. doi: 10.1126/science.1240925 23907535
58. Li Z, Chao TC, Chang KY, Lin N, Patil VS, et al. (2014) The long noncoding RNA THRIL regulates TNFalpha expression through its interaction with hnRNPL. Proc Natl Acad Sci U S A 111: 1002–1007. doi: 10.1073/pnas.1313768111 24371310
59. Martin GR, Evans MJ, (1975) Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci U S A 72: 1441–1445. 1055416
60. Lee EC, Yu D, Martinez de Velasco J, Tessarollo L, Swing DA, et al. (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73: 56–65. 11352566
61. Erwin JA, del Rosario B, Payer B, Lee JT, (2012) An ex vivo model for imprinting: mutually exclusive binding of Cdx2 and Oct4 as a switch for imprinted and random X-inactivation. Genetics 192: 857–868. doi: 10.1534/genetics.112.144121 22942124
62. Ogawa Y, Lee JT, (2003) Xite, X-inactivation intergenic transcription elements that regulate the probability of choice. Mol Cell 11: 731–743. 12667455
63. Yang Y, Seed B, (2003) Site-specific gene targeting in mouse embryonic stem cells with intact bacterial artificial chromosomes. Nat Biotechnol 21: 447–451. 12627171
64. 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. 11481444
65. Yue M, Charles Richard JL, Yamada N, Ogawa A, Ogawa Y, (2014) Quick fluorescent in situ hybridization protocol for Xist RNA combined with immunofluorescence of histone modification in X-chromosome inactivation. J Vis Exp: e52053. doi: 10.3791/52053 25489864
66. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, et al. (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8: 2281–2308. doi: 10.1038/nprot.2013.143 24157548
67. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, et al. (2013) Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155: 1479–1491. doi: 10.1016/j.cell.2013.12.001 24360272