1932

Abstract

Noncoding RNAs (ncRNAs) are remarkably powerful, flexible, and pervasive cellular regulators. The involvement of these molecules in virtually all aspects of eukaryotic chromatin function is notable. Long and short ncRNAs play broadly complementary roles in these processes. Short ncRNAs underlie a programmable system of chromatin modification that silences mobile elements, identifies boundaries, and initiates the formation of constitutive heterochromatin in yeast. In contrast, long noncoding RNAs (lncRNAs) enforce developmentally appropriate expression and switch gene expression programs. lncRNAs accomplish this through diverse mechanisms, but often by modulating the activity or localization of chromatin regulatory complexes. Both long and short ncRNAs play key roles in organization of complex genomes of higher eukaryotes, and their coordinated actions appear to underlie some of the more dramatic examples of epigenetic regulation. This review contrasts well-studied examples of chromatin regulation by RNA and introduces examples of coordination between these systems.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-112414-055205
2015-11-23
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/genet/49/1/annurev-genet-112414-055205.html?itemId=/content/journals/10.1146/annurev-genet-112414-055205&mimeType=html&fmt=ahah

Literature Cited

  1. Agrelo R, Souabni A, Novatchkova M, Haslinger C, Leeb M. 1.  et al. 2009. SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev. Cell 16:507–16 [Google Scholar]
  2. Akhtar A, Becker P. 2.  2000. Activation of transcription through histone H4 acetylation by MOF, and acetyltransferase essential for dosage compensation in Drosophila. Mol. Cell 5:367–75 [Google Scholar]
  3. Alekseyenko AA, Larschan E, Lai WR, Park PJ, Kuroda MI. 3.  2006. High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome. Genes Dev. 20:848–57 [Google Scholar]
  4. Alekseyenko AA, Peng S, Larschan E, Gorchakov AA, Lee OK. 4.  et al. 2008. A sequence motif within chromatin entry sites directs MSL establishment on the Drosophila X chromosome. Cell 134:599–609 [Google Scholar]
  5. Aravin A, Sachidanandam R, Girard A, Fejes-Toth K, Hannon G. 5.  2007. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316:744–47 [Google Scholar]
  6. Augui S, Filion G, Huart S, Nora E, Guggiari M. 6.  et al. 2007. Sensing X chromosome pairs before X inactivation via a novel X-pairing region of the Xic. Science 318:1632–36 [Google Scholar]
  7. Bantignies F, Roure V, Comet I, Leblanc B, Schuettengruber B. 7.  et al. 2011. Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 144:214–26 [Google Scholar]
  8. Barlow DP, Bartolomei MS. 8.  2014. Genomic imprinting in mammals. Cold Spring Harb. Perspect. Biol. 6:pii:a018382 [Google Scholar]
  9. Bender W, Fitzgerald DP. 9.  2002. Transcription activates repressed domains in the Drosophila bithorax complex. Development 129:4923–30 [Google Scholar]
  10. Bowman SK, Deaton AM, Domingues H, Wang PI, Sadreyev RI. 10.  et al. 2014. H3K27 modifications define segmental regulatory domains in the Drosophila bithorax complex. eLife 3:e02833 [Google Scholar]
  11. Brower-Toland B, Findley SD, Jiang L, Liu L, Yin H. 11.  et al. 2007. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev. 21:2300–11 [Google Scholar]
  12. Brown JD, Mitchell SE, O'Neill RJ. 12.  2012. Making a long story short: noncoding RNAs and chromosome change. Heredity 108:42–49 [Google Scholar]
  13. Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, Grewal SI. 13.  2005. Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat. Genet. 37:809–19 [Google Scholar]
  14. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH. 14.  et al. 2007. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12:503–14 [Google Scholar]
  15. Castel SE, Martienssen RA. 15.  2013. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 14:100–12 [Google Scholar]
  16. Castro-Diaz N, Ecco G, Coluccio A, Kapopoulou A, Yazdanpanah B. 16.  et al. 2014. Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev. 28:1397–409 [Google Scholar]
  17. Cernilogar FM, Burroughs AM, Lanzuolo C, Breiling A, Imhof A, Orlando V. 17.  2013. RNA-interference components are dispensable for transcriptional silencing of the Drosophila bithorax-complex. PLOS ONE 8:e65740 [Google Scholar]
  18. Chen ES, Zhang K, Nicolas E, Cam HP, Zofall M, Grewal SI. 18.  2008. Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451:734–37 [Google Scholar]
  19. Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N. 19.  et al. 2010. LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141:956–69 [Google Scholar]
  20. Chu C, Zhang QC, Teixeira da Rocha S, Flynn RA, Bharadwaj M. 20.  et al. 2015. Systematic discovery of Xist RNA binding proteins. Cell 161:404–16 [Google Scholar]
  21. Ciaudo C, Jay F, Okamoto I, Chen CJ, Sarazin A. 21.  et al. 2013. RNAi-dependent and independent control of LINE1 accumulation and mobility in mouse embryonic stem cells. PLOS Genet. 9:e1003791 [Google Scholar]
  22. Cifuentes-Rojas C, Hernandez AJ, Sarma K, Lee JT. 22.  2014. Regulatory interactions between RNA and Polycomb repressive complex 2. Mol. Cell 55:171–85 [Google Scholar]
  23. Clemson C, McNeil J, Willard H, Lawrence J. 23.  1996. Xist RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell Biol. 132:259–75 [Google Scholar]
  24. Clemson CM, Hall LL, Byron M, McNeil J, Lawrence JB. 24.  2006. The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced nongenic sequences. PNAS 103:7688–93 [Google Scholar]
  25. Cohen AL, Jia S. 25.  2014. Noncoding RNAs and the borders of heterochromatin. Wiley Interdiscip. Rev. RNA 5:835–47 [Google Scholar]
  26. Costanzi C, Pehrson J. 26.  1998. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393:599–601 [Google Scholar]
  27. Csankovszki G, Nagy A, Jaenisch R. 27.  2001. Synergism of Xist RNA, DNA methylation and histone hypoacetylation in maintaining X chromosome inactivation. J. Cell Biol. 153:773–83 [Google Scholar]
  28. Davidovich C, Zheng L, Goodrich KJ, Cech TR. 28.  2013. Promiscuous RNA binding by Polycomb repressive complex 2. Nat. Struct. Mol. Biol. 20:1250–57 [Google Scholar]
  29. Deng X, Berletch JB, Nguyen DK, Disteche CM. 29.  2014. X chromosome regulation: diverse patterns in development, tissues and disease. Nat. Rev. Genet. 15:367–78 [Google Scholar]
  30. Deng X, Meller VH. 30.  2006. roX RNAs are required for increased expression of X-linked genes in Drosophila melanogaster males. Genetics 174:1859–66 [Google Scholar]
  31. Donley N, Smith L, Thayer MJ. 31.  2015. ASAR15, a cis-acting locus that controls chromosome-wide replication timing and stability of human chromosome 15. PLOS Genet 11:e1004923 [Google Scholar]
  32. Dunn K, Zhao H, Davie J. 32.  2003. The insulator binding protein CTCF associates with the nuclear matrix. Exp. Cell Res. 288:218–23 [Google Scholar]
  33. Elisaphenko EA, Kolesnikov NN, Shevchenko AI, Rogozin IB, Nesterova TB. 33.  et al. 2008. A dual origin of the Xist gene from a protein-coding gene and a set of transposable elements. PLOS ONE 3:e2521 [Google Scholar]
  34. Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K. 34.  et al. 2013. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341:6147 [Google Scholar]
  35. Ferrari F, Alekseyenko AA, Park PJ, Kuroda MI. 35.  2014. Transcriptional control of a whole chromosome: emerging models for dosage compensation. Nat. Struct. Mol. Biol. 21:118–25 [Google Scholar]
  36. Fischle W, Wang Y, Jacobs S, Kim Y, Allis CD, Khorasanizadeh S. 36.  2003. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17:1870–81 [Google Scholar]
  37. Gao Z, Liu HL, Daxinger L, Pontes O, He X. 37.  et al. 2010. An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465:106–9 [Google Scholar]
  38. Gerasimova T, Byrd K, Corces V. 38.  2000. A chromatin insulator determines the nuclear localization of DNA. Mol. Cell 6:1025–35 [Google Scholar]
  39. Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S. 39.  et al. 2013. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell 152:743–54 [Google Scholar]
  40. Grimaud C, Bantignies F, Pal-Bhadra M, Ghana P, Bhadra U, Cavalli G. 40.  2006. RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 124:957–71 [Google Scholar]
  41. Grimaud C, Becker PB. 41.  2009. The dosage compensation complex shapes the conformation of the X chromosome in Drosophila. Genes Dev. 23:2490–95 [Google Scholar]
  42. Grote P, Wittler L, Hendrix D, Koch F, Wahrisch S. 42.  et al. 2013. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev. Cell 24:206–14 [Google Scholar]
  43. Gu T, Elgin SC. 43.  2013. Maternal depletion of Piwi, a component of the RNAi system, impacts heterochromatin formation in Drosophila. PLOS Genet. 9:e1003780 [Google Scholar]
  44. Gummalla M, Maeda RK, Castro Alvarez JJ, Gyurkovics H, Singari S. 44.  et al. 2012. abd-A regulation by the iab-8 noncoding RNA. PLOS Genet. 8:e1002720 [Google Scholar]
  45. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK. 45.  et al. 2011. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–300 [Google Scholar]
  46. Hall LL, Carone DM, Gomez AV, Kolpa HJ, Byron M. 46.  et al. 2014. Stable CoT-1 repeat RNA is abundant and is associated with euchromatic interphase chromosomes. Cell 156:907–19 [Google Scholar]
  47. Hall LL, Lawrence JB. 47.  2010. XIST RNA and architecture of the inactive X chromosome: implications for the repeat genome. Cold Spring Harb. Symp. Quant. Biol. 75:345–56 [Google Scholar]
  48. Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Tsutui K, Nakagawa S. 48.  2010. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell 19:469–76 [Google Scholar]
  49. Heard E, Clerc P, Avner P. 49.  1997. X chromosome inactivation in mammals. Annu. Rev. Genet. 31:571–610 [Google Scholar]
  50. Heo JB, Sung S. 50.  2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79 [Google Scholar]
  51. Herzog VA, Lempradl A, Trupke J, Okulski H, Altmutter C. 51.  et al. 2014. A strand-specific switch in noncoding transcription switches the function of a Polycomb/Trithorax response element. Nat. Genet. 46:973–81 [Google Scholar]
  52. Hochedlinger K, Plath K. 52.  2009. Epigenetic reprogramming and induced pluripotency. Development 136:509–23 [Google Scholar]
  53. Holoch D, Moazed D. 53.  2015. RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 16:71–84 [Google Scholar]
  54. Ilik IA, Quinn JJ, Georgiev P, Tavares-Cadete F, Maticzka D. 54.  et al. 2013. Tandem stem-loops in roX RNAs act together to mediate X chromosome dosage compensation in Drosophila. Mol. Cell 51:156–73 [Google Scholar]
  55. Ishizu H, Siomi H, Siomi MC. 55.  2012. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 26:2361–73 [Google Scholar]
  56. Ito H, Kakutani T. 56.  2014. Control of transposable elements in Arabidopsis thaliana. Chromosome Res. 22:217–23 [Google Scholar]
  57. Jeon Y, Lee JT. 57.  2011. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146:119–33 [Google Scholar]
  58. Kalantry S, Magnuson T. 58.  2006. The Polycomb group protein EED is dispensable for the initiation of random X chromosome inactivation. PLOS Genet. 2:5e66 [Google Scholar]
  59. Kaneko S, Son J, Shen SS, Reinberg D, Bonasio R. 59.  2013. PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat. Struct. Mol. Biol. 20:1258–64 [Google Scholar]
  60. Kassis JA, Brown JL. 60.  2013. Polycomb group response elements in Drosophila and vertebrates. Adv. Genet. 81:83–118 [Google Scholar]
  61. Keene JD, Komisarow JM, Friedersdorf MB. 61.  2006. RIP-Chip: the isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts. Nat. Protoc. 1:302–7 [Google Scholar]
  62. Kelley R, Meller VH, Gordadze P, Roman G, Davis R, Kuroda M. 62.  1999. Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin. Cell 98:513–22 [Google Scholar]
  63. Kennison J. 63.  1995. The Polycomb and Trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu. Rev. Genet. 29:289–303 [Google Scholar]
  64. Kennison J, Tamkun J. 64.  1988. Dosage-dependent modifiers of Polycomb and Antennapedia mutations of Drosophila. PNAS 85:8136–40 [Google Scholar]
  65. Kim DH, Villeneuve LM, Morris KV, Rossi JJ. 65.  2006. Argonaute-1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat. Struct. Mol. Biol. 13:793–97 [Google Scholar]
  66. Kyrchanova O, Georgiev P. 66.  2014. Chromatin insulators and long-distance interactions in Drosophila. FEBS Lett. 588:8–14 [Google Scholar]
  67. Latos PA, Pauler FM, Koerner MV, Senergin HB, Hudson QJ. 67.  et al. 2012. Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing. Science 338:1469–72 [Google Scholar]
  68. Lempradl A, Ringrose L. 68.  2008. How does noncoding transcription regulate Hox genes?. BioEssays 30:110–21 [Google Scholar]
  69. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE. 69.  et al. 2013. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 27:390–99 [Google Scholar]
  70. Li L, Liu B, Wapinski OL, Tsai MC, Qu K. 70.  et al. 2013. Targeted disruption of Hotair leads to homeotic transformation and gene derepression. Cell Rep. 5:3–12 [Google Scholar]
  71. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C. 71.  2010. Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:94–97 [Google Scholar]
  72. Luteijn MJ, Ketting RF. 72.  2013. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat. Rev. Genet. 14:523–34 [Google Scholar]
  73. Lyon M. 73.  1998. X-chromosome inactivation. Curr. Biol. 9:R235–37 [Google Scholar]
  74. Maclary E, Hinten M, Harris C, Kalantry S. 74.  2013. Long noncoding RNAs in the X-inactivation center. Chromosome Res. 21:601–14 [Google Scholar]
  75. Maenner S, Muller M, Frohlich J, Langer D, Becker PB. 75.  2013. ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Mol. Cell 51:174–84 [Google Scholar]
  76. Mansour AA, Gafni O, Weinberger L, Zviran A, Ayyash M. 76.  et al. 2012. The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming. Nature 488:409–13 [Google Scholar]
  77. Margueron R, Justin N, Ohno K, Sharpe ML, Son J. 77.  et al. 2009. Role of the Polycomb protein EED in the propagation of repressive histone marks. Nature 461:762–67 [Google Scholar]
  78. Matzat LH, Dale RK, Lei EP. 78.  2013. Messenger RNA is a functional component of a chromatin insulator complex. EMBO Rep. 14:916–22 [Google Scholar]
  79. Matzke MA, Mosher RA. 79.  2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15:394–408 [Google Scholar]
  80. McGinnis W, Krumlauf R. 80.  1992. Homeobox genes and axial patterning. Cell 68:283–302 [Google Scholar]
  81. McHugh CA, Chen C-K, Chow A, Surka CF, Tran C. 81.  et al. 2015. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521:232–36 [Google Scholar]
  82. Meller VH, Rattner B. 82.  2002. The roX genes encode redundant male specific lethal transcripts required for targeting of the MSL complex. EMBO J. 21:1084–91 [Google Scholar]
  83. Menon DU, Coarfa C, Xiao W, Gunaratne PH, Meller VH. 83.  2014. siRNAs from an X-linked satellite repeat promote X-chromosome recognition in Drosophila melanogaster. PNAS 111:16460–65 [Google Scholar]
  84. Menon DU, Meller VH. 84.  2012. A role for siRNA in X-chromosome dosage compensation in Drosophila melanogaster. Genetics 191:1023–28 [Google Scholar]
  85. Mills AA. 85.  2010. Throwing the cancer switch: reciprocal roles of Polycomb and Trithorax proteins. Nat. Rev. Cancer 10:669–82 [Google Scholar]
  86. Min J, Zhang Y, Xu R-M. 86.  2002. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys27. Genes Dev. 17:1823–28 [Google Scholar]
  87. Minajigi A, Froberg JE, Wei C, Sunwoo H, Kesner B. 87.  et al. 2015. A comprehensive Xist interactome reveals cohesion repulsion and an RNA-directed chromosome conformation. Science 349:282 [Google Scholar]
  88. Moazed D. 88.  2009. Small RNAs in transcriptional gene silencing and genome defence. Nature 457:413–20 [Google Scholar]
  89. Mohammad F, Mondal T, Guseva N, Pandey G K, Kanduri C. 89.  2010. Kcnq10t1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1. Development 137:2493–99 [Google Scholar]
  90. Motamedi MR, Verdel A, Colmenares SU, Gerber SA, Gygi SP, Moazed D. 90.  2004. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119:789–802 [Google Scholar]
  91. Muntean AG, Hess JL. 91.  2012. The pathogenesis of mixed-lineage leukemia. Annu. Rev. Pathol. 7:283–301 [Google Scholar]
  92. Nagano T, Mitchell J, Sanz L, Pauler F, Ferguson-Smith A. 92.  et al. 2008. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322:1717–20 [Google Scholar]
  93. Noma K, Allis CD, Grewal S. 93.  2001. Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293:1150–55 [Google Scholar]
  94. Obier N, Lin Q, Cauchy P, Hornich V, Zenke M. 94.  et al. 2014. Polycomb protein EED is required for silencing of pluripotency genes upon ESC differentiation. Stem Cell Rev. 11:50–61 [Google Scholar]
  95. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L. 95.  et al. 2008. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol. Cell 32:232–46 [Google Scholar]
  96. Panning B, Dausman J, Jaenisch R. 96.  1997. X chromosome inactivation is mediated by Xist RNA stabilization. Cell 90:907–16 [Google Scholar]
  97. Pease B, Borges AC, Bender W. 97.  2013. Noncoding RNAs of the Ultrabithorax domain of the Drosophila bithorax complex. Genetics 195:1253–64 [Google Scholar]
  98. Penny G, Kay G, Sheardown S, Rastan S, Brockdorff N. 98.  1996. Requirement for Xist in X chromosome inactivation. Nature 397:131–37 [Google Scholar]
  99. Pikaard CS, Haag JR, Pontes OM, Blevins T, Cocklin R. 99.  2012. A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation. Cold Spring Harb. Symp. Quant. Biol. 77:205–12 [Google Scholar]
  100. Plath K, Talbot D, Hamer KM, Otte AP, Yang TP. 100.  et al. 2004. Developmentally regulated alterations in Polycomb repressive complex 1 proteins on the inactive X chromosome. J. Cell Biol. 167:1025–35 [Google Scholar]
  101. Pullirsch D, Hartel R, Kishimoto H, Leeb M, Steiner G, Wutz A. 101.  2010. The Trithorax group protein Ash2l and Saf-A are recruited to the inactive X chromosome at the onset of stable X inactivation. Development 137:935–43 [Google Scholar]
  102. Quinn JJ, Ilik IA, Qu K, Georgiev P, Chu C. 102.  et al. 2014. Revealing long noncoding RNA architecture and functions using domain-specific chromatin isolation by RNA purification. Nat. Biotechnol. 32:933–40 [Google Scholar]
  103. Rasmussen T, Mastrangelo M-A, Eden A, Pehrson J, Jaenisch R. 103.  2000. Dynamic relocalization of macroH2A1 from centrosomes to inactive X chromosomes during X inactivation. J. Cell Biol. 150:1189–98 [Google Scholar]
  104. Rastan S, Brown S. 104.  1990. The search for the mouse X chromosome inactivation center. Genet. Res. 56:99–106 [Google Scholar]
  105. Reis EM, Verjovski-Almeida S. 105.  2012. Perspectives of long non-coding RNAs in cancer diagnostics. Front. Genet. 3:32 [Google Scholar]
  106. Rinn JL, Bondre C, Gladstone HB, Brown PO, Chang HY. 106.  2006. Anatomic demarcation by positional variation in fibroblast gene expression programs. PLOS Genet. 2:e119 [Google Scholar]
  107. Rinn JL, Chang HY. 107.  2012. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81:145–66 [Google Scholar]
  108. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X. 108.  et al. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–23 [Google Scholar]
  109. Rosa S, De Lucia F, Mylne JS, Zhu D, Ohmido N. 109.  et al. 2013. Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization. Genes Dev. 27:1845–50 [Google Scholar]
  110. Rozhkov NV, Hammell M, Hannon GJ. 110.  2013. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev. 27:400–12 [Google Scholar]
  111. Ryba T, Hiratani I, Lu J, Itoh M, Kulik M. 111.  et al. 2010. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 20:761–70 [Google Scholar]
  112. Savva YA, Jepson JE, Chang YJ, Whitaker R, Jones BC. 112.  et al. 2013. RNA editing regulates transposon-mediated heterochromatic gene silencing. Nat. Commun. 4:2745 [Google Scholar]
  113. Schalch T, Job G, Noffsinger VJ, Shanker S, Kuscu C. 113.  et al. 2009. High-affinity binding of Chp1 chromodomain to K9 methylated histone H3 is required to establish centromeric heterochromatin. Mol. Cell 34:36–46 [Google Scholar]
  114. Schmitt S, Prestel M, Paro R. 114.  2005. Intergenic transcription through a Polycomb group response element counteracts silencing. Genes Dev. 19:697–708 [Google Scholar]
  115. Schubert T, Pusch MC, Diermeier S, Benes V, Kremmer E. 115.  et al. 2012. Df31 protein and snoRNAs maintain accessible higher-order structures of chromatin. Mol. Cell 48:434–44 [Google Scholar]
  116. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. 116.  2007. Genome regulation by Polycomb and Trithorax proteins. Cell 128:735–45 [Google Scholar]
  117. Schuettengruber B, Martinez AM, Iovino N, Cavalli G. 117.  2011. Trithorax group proteins: switching genes on and keeping them active. Nat. Rev. Mol. Cell Biol. 12:799–814 [Google Scholar]
  118. Schwartz YB, Pirrotta V. 118.  2013. A new world of Polycombs: unexpected partnerships and emerging functions. Nat. Rev. Genet. 14:853–64 [Google Scholar]
  119. Sentmanat M, Elgin S. 119.  2012. Ectopic assembly of heterochromatin in Drosophila melanogaster triggered by transposable elements. PNAS 109:14104–9 [Google Scholar]
  120. Sheardown S, Duthie S, Johnston C, Newall A, Formstone E. 120.  et al. 1997. Stabilization of Xist RNA mediates initiation of X chromosome inactivation. Cell 91:99–107 [Google Scholar]
  121. Simon MD, Pinter SF, Fang R, Sarma K, Rutenberg-Schoenberg M. 121.  et al. 2013. High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature 504:465–69 [Google Scholar]
  122. Slotkin RK, Martienssen R. 122.  2007. Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8:272–85 [Google Scholar]
  123. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD. 123.  et al. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–72 [Google Scholar]
  124. Smith E, Pannuti A, Gu W, Steurnagel A, Cook R. 124.  et al. 2000. The Drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol. Cell. Biol. 20:312–18 [Google Scholar]
  125. Smith ER, Lee MG, Winter B, Droz NM, Eissenberg JC. 125.  et al. 2008. Drosophila UTX is a histone H3 Lys27 demethylase that colocalizes with the elongating form of RNA polymerase II. Mol. Cell. Biol. 28:1041–46 [Google Scholar]
  126. Song J, Irwin J, Dean C. 126.  2013. Remembering the prolonged cold of winter. Curr. Biol. 23:R807–11 [Google Scholar]
  127. Soruco MM, Chery J, Bishop EP, Siggers T, Tolstorukov MY. 127.  et al. 2013. The CLAMP protein links the MSL complex to the X chromosome during Drosophila dosage compensation. Genes Dev. 27:1551–56 [Google Scholar]
  128. Splinter E, de Laat W. 128.  2011. The complex transcription regulatory landscape of our genome: control in three dimensions. EMBO J. 30:4345–55 [Google Scholar]
  129. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P. 129.  et al. 2006. CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev. 20:2349–54 [Google Scholar]
  130. Straub T, Gilfillan G, Maier V, Becker P. 130.  2005. The Drosophila MSL complex activates the transcription of target genes. Genes Dev. 19:2284–88 [Google Scholar]
  131. Swiezewski S, Liu F, Magusin A, Dean C. 131.  2009. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–802 [Google Scholar]
  132. Tang YA, Huntley D, Montana G, Cerase A, Nesterova TB, Brockdorff N. 132.  2010. Efficiency of Xist-mediated silencing on autosomes is linked to chromosomal domain organisation. Epigenet. Chromatin 3:10 [Google Scholar]
  133. Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V. 133.  et al. 2009. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136:3131–41 [Google Scholar]
  134. Tolhuis B, de Wit E, Muijrers I, Teunissen H, Talhout W. 134.  et al. 2006. Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat. Genet. 38:694–99 [Google Scholar]
  135. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK. 135.  et al. 2010. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329:689–93 [Google Scholar]
  136. Vallot C, Huret C, Lesecque Y, Resch A, Oudrhiri N. 136.  et al. 2013. XACT, a long noncoding transcript coating the active X chromosome in human pluripotent cells. Nat. Genet. 45:239–41 [Google Scholar]
  137. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P. 137.  et al. 2004. Role of histone H2A ubiquitination in Polycomb silencing. Nature 431:873–78 [Google Scholar]
  138. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R. 138.  et al. 2011. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472:120–24 [Google Scholar]
  139. Wilkinson FH, Park K, Atchison ML. 139.  2006. Polycomb recruitment to DNA in vivo by the YY1 REPO domain. PNAS 103:19296–301 [Google Scholar]
  140. Wutz A. 140.  2011. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat. Rev. Genet. 12:542–53 [Google Scholar]
  141. Xu C, Bian C, Yang W, Galka M, Ouyang H. 141.  et al. 2010. Binding of different histone marks differentially regulates the activity and specificity of Polycomb repressive complex 2 (PRC2). PNAS 107:19266–71 [Google Scholar]
  142. Yamanaka S, Siomi M, Siomi H. 142.  2014. piRNA clusters and open chromatin structure. Mobile DNA 5:22 [Google Scholar]
  143. Yang L, Lin C, Liu W, Zhang J, Ohgi KA. 143.  et al. 2011. ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 147:773–88 [Google Scholar]
  144. Yang YW, Flynn RA, Chen Y, Qu K, Wan B. 144.  et al. 2014. Essential role of lncRNA binding for WDR5 maintenance of active chromatin and embryonic stem cell pluripotency. eLife 3:e02046 [Google Scholar]
  145. Yap KL, Li S, Muñoz-Cabello AM, Raguz S, Zeng L. 145.  et al. 2010. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by Polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 38:662–74 [Google Scholar]
  146. Yusufzai T, Tagami H, Nakatani Y, Felsenfeld G. 146.  2004. CTCF tethers an insulator to subnuclear sites, suggesting shared mechanisms across species. Mol. Cell 13:291–98 [Google Scholar]
  147. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ. 147.  et al. 2010. Genome-wide identification of Polycomb-associated RNAs by RIP-seq. Mol. Cell 40:939–53 [Google Scholar]
  148. Zhao J, Sun B, Erwin J, Song J-J, Lee J. 148.  2008. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322:750–56 [Google Scholar]
/content/journals/10.1146/annurev-genet-112414-055205
Loading
/content/journals/10.1146/annurev-genet-112414-055205
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error