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Biological and bioinformatical approaches to study crosstalk of long-non-coding RNAs and chromatin-modifying proteins

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Abstract

Long-non-coding RNA (lncRNA) regulates gene expression through transcriptional and epigenetic regulation as well as alternative splicing in the nucleus. In addition, regulation is achieved at the levels of mRNA translation, storage and degradation in the cytoplasm. During recent years, several studies have described the interaction of lncRNAs with enzymes that confer so-called epigenetic modifications, such as DNA methylation, histone modifications and chromatin structure or remodelling. LncRNA interaction with chromatin-modifying enzymes (CME) is an emerging field that confers another layer of complexity in transcriptional regulation. Given that CME–lncRNA interactions have been identified in many biological processes, ranging from development to disease, comprehensive understanding of underlying mechanisms is important to inspire basic and translational research in the future. In this review, we highlight recent findings to extend our understanding about the functional interdependencies between lncRNAs and CMEs that activate or repress gene expression. We focus on recent highlights of molecular and functional roles for CME–lncRNAs and provide an interdisciplinary overview of recent technical and methodological developments that have improved biological and bioinformatical approaches for detection and functional studies of CME–lncRNA interaction.

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References

  • Aguilera A, Garcia-Muse T (2012) R loops: from transcription byproducts to threats to genome stability. Mol Cell 46:115–124

    CAS  PubMed  Google Scholar 

  • Backofen R, Hess WR (2010) Computational prediction of sRNAs and their targets in bacteria. RNA Biol 7:33–42

    CAS  PubMed  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beckedorff FC, Ayupe AC, Crocci-Souza R, Amaral MS, Nakaya HI, Soltys DT, Menck CFM, Reis EM, Verjovski-Almeida S (2013) The intronic long noncoding RNA ANRASSF1 recruits PRC2 to the RASSF1A promoter, reducing the expression of RASSF1A and increasing cell proliferation. PLoS Genet 9:e1003705

    CAS  PubMed Central  PubMed  Google Scholar 

  • Benetti R, Gonzalo S, Jaco I, Muñoz P, Gonzalez S, Schoeftner S, Murchison E, Andl T, Chen T, Klatt P, Li E, Serrano M, Millar S, Hannon G, Blasco MA (2008) A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nature structural &#38. Mol Biol 15:268–279

    CAS  Google Scholar 

  • Bertani S, Sauer S, Bolotin E, Sauer F (2011) The noncoding RNA Mistral activates Hoxa6 and Hoxa7 expression and stem cell differentiation by recruiting MLL1 to chromatin. Mol Cell 43:1040–1046

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bond AM, Vangompel MJW, Sametsky EA, Clark MF, Savage JC, Disterhoft JF, Kohtz JD (2009) Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. Nat Neurosci 12:1020–1027

    CAS  PubMed Central  PubMed  Google Scholar 

  • Braconi C, Huang N, Patel T (2010) MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology (Baltimore, Md) 51:881–890

    CAS  Google Scholar 

  • Brockdorff N (2011) Chromosome silencing mechanisms in X-chromosome inactivation: unknown unknowns. Development 138:5057–5065

    CAS  PubMed  Google Scholar 

  • Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, Eddy SR, Gardner PP, Bateman A (2013) Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 41:D226–D232

    CAS  PubMed Central  PubMed  Google Scholar 

  • Busch A, Richter AS, Backofen R (2008) IntaRNA: efficient prediction of bacterial sRNA targets incorporating target site accessibility and seed regions. Bioinformatics 24:2849–2856

    CAS  PubMed Central  PubMed  Google Scholar 

  • Buske FA, Bauer DC, Mattick JS, Bailey TL (2012) Triplexator: detecting nucleic acid triple helices in genomic and transcriptomic data. Genome Res 22:1372–1381

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cao Q, Wang X, Zhao M, Yang R, Malik R, Qiao Y, Poliakov A, Yocum AK, Li Y, Chen W, Cao X, Jiang X, Dahiya A, Harris C, Feng FY, Kalantry S, Qin ZS, Dhanasekaran SM, Chinnaiyan AM (2014) The central role of EED in the orchestration of polycomb group complexes. Nat Commun 5:3127

    PubMed  Google Scholar 

  • Chavali V, Tyagi SC, Mishra PK (2012) MicroRNA-133a regulates DNA methylation in diabetic cardiomyocytes. Biochem Biophys Res Commun 425:668–672

    CAS  PubMed  Google Scholar 

  • Chen G, Wang Z, Wang D, Qiu C, Liu M, Chen X, Zhang Q, Yan G, Cui Q (2013) LncRNADisease: a database for long-non-coding RNA-associated diseases. Nucleic Acids Res 41:D983–D986

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chisholm KM, Wan Y, Li R, Montgomery KD, Chang HY, West RB (2012) Detection of long non-coding RNA in archival tissue: correlation with polycomb protein expression in primary and metastatic breast carcinoma. PLoS ONE 7:e47998

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chu C, Qu K, Zhong FL, Artandi SE, Chang HY (2011) Genomic maps of long noncoding RNA occupancy reveal principles of RNA–chromatin interactions. Mol Cell 44:667–678

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clamp M, Fry B, Kamal M, Xie X, Cuff J, Lin MF, Kellis M, Lindblad-Toh K, Lander ES (2007) Distinguishing protein-coding and noncoding genes in the human genome. Proc Natl Acad Sci USA 104:19428–19433

    CAS  PubMed Central  PubMed  Google Scholar 

  • Congrains A, Kamide K, Ohishi M, Rakugi H (2013) ANRIL: Molecular Mechanisms and Implications in Human Health. Int J Mol Sci 14:1278–1292

    CAS  PubMed Central  PubMed  Google Scholar 

  • Corcoran DL, Georgiev S, Mukherjee N, Gottwein E, Skalsky RL, Keene JD, Ohler U (2011) PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data. Genome Biol 12:R79

    CAS  PubMed Central  PubMed  Google Scholar 

  • Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigo R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dharap A, Pokrzywa C, Vemuganti R (2013) Increased binding of stroke-induced long non-coding RNAs to the transcriptional corepressors Sin3A and coREST. ASN Neuro 5:283–289

    CAS  PubMed  Google Scholar 

  • Di Ruscio A, Ebralidze AK, Benoukraf T, Amabile G, Goff LA, Terragni J, Figueroa ME, De Figueiredo Pontes LL, Alberich-Jorda M, Zhang P, Wu M, D’Alò F, Melnick A, Leone G, Ebralidze KK, Pradhan S, Rinn JL, Tenen DG (2013) DNMT1-interacting RNAs block gene-specific DNA methylation. Nature 1–10

  • Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, Sunkin SM, Crowe ML, Grimmond SM, Perkins AC, Mattick JS (2008) Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 18:1433–1445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Drolet M (2006) Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 59:723–730

    CAS  PubMed  Google Scholar 

  • Drolet M, Broccoli S, Rallu F, Hraiky C, Fortin C, Masse E, Baaklini I (2003) The problem of hypernegative supercoiling and R-loop formation in transcription. Front Biosci J Virtual Libr 8:d210–d221

    CAS  Google Scholar 

  • Eggenhofer F, Tafer H, Stadler PF, Hofacker IL (2011) RNApredator: fast accessibility-based prediction of sRNA targets. Nucleic Acids Res 39:W149–W154

    CAS  PubMed Central  PubMed  Google Scholar 

  • Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in Drosophila. Genome Biol 5:R1

    PubMed Central  PubMed  Google Scholar 

  • Erhard F, Zimmer R (2010) Classification of ncRNAs using position and size information in deep sequencing data. Bioinformatics 26:i426–i432

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez-Cymering C, Volinia S, Guler G, Morrison CD, Chan KK, Marcucci G, Calin GA, Huebner K, Croce CM (2007) MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA 104:15805–15810

    CAS  PubMed Central  PubMed  Google Scholar 

  • Faghihi MA, Modarresi F, Khalil AM, Wood DE, Sahagan BG, Morgan TE, Finch CE, St Laurent G 3rd, Kenny PJ, Wahlestedt C (2008) Expression of a noncoding RNA is elevated in Alzheimer’s disease and drives rapid feed–forward regulation of beta-secretase. Nat Med 14:723–730

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fasold M, Langenberger D, Binder H, Stadler PF, Hoffmann S (2011) DARIO: a ncRNA detection and analysis tool for next-generation sequencing experiments. Nucleic Acids Res 39:W112–W117

    CAS  PubMed Central  PubMed  Google Scholar 

  • Findeiss S, Langenberger D, Stadler PF, Hoffmann S (2011) Traces of post-transcriptional RNA modifications in deep sequencing data. Biol Chem 392:305–313

    CAS  PubMed  Google Scholar 

  • Foat BC, Morozov AV, Bussemaker HJ (2006) Statistical mechanical modeling of genome-wide transcription factor occupancy data by MatrixREDUCE. Bioinformatics 22:e141–e149

    CAS  PubMed  Google Scholar 

  • Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92–105

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fujita N, Watanabe S, Ichimura T, Tsuruzoe S, Shinkai Y, Tachibana M, Chiba T, Nakao M (2003) Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1–HP1 heterochromatic complex for DNA methylation-based transcriptional repression. J Biol Chem 278:24132–24138

    CAS  PubMed  Google Scholar 

  • Gan J, Shaw G, Tropea JE, Waugh DS, Court DL, Ji X (2008) A stepwise model for double-stranded RNA processing by ribonuclease III. Mol Microbiol 67:143–154

    CAS  PubMed  Google Scholar 

  • Gao Z, Zhang J, Bonasio R, Strino F, Sawai A, Parisi F, Kluger Y, Reinberg D (2012) PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol Cell 45:344–356

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garber M, Grabherr MG, Guttman M, Trapnell C (2011) Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods 8:469–477

    CAS  PubMed  Google Scholar 

  • Gilbert, C, Svejstrup, JQ (2006) RNA immunoprecipitation for determining RNA–protein associations in vivo. Current protocols in molecular biology / edited by Frederick M Ausubel [et al.] Chapter 27: Unit 27 24

  • Ginno PA, Lott PL, Christensen HC, Korf I, Chedin F (2012) R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol Cell 45:814–825

    CAS  PubMed Central  PubMed  Google Scholar 

  • Glazko GV, Zybailov BL, Rogozin IB (2012) Computational prediction of polycomb-associated long non-coding RNAs. PLoS ONE 7:e44878

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gong C, Maquat LE (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature 470:284–288

    CAS  PubMed Central  PubMed  Google Scholar 

  • Granneman S, Kudla G, Petfalski E, Tollervey D (2009) Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs. Proc Natl Acad Sci USA 106:9613–9618

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grote P, Wittler L, Hendrix D, Koch F, Währisch S, Beisaw A, Macura K, Bläss G, Kellis M, Werber M, Herrmann BG (2013) The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell 24:206–214

    CAS  PubMed  Google Scholar 

  • Gupta SK, Kosti I, Plaut G, Pivko A, Tkacz ID, Cohen-Chalamish S, Biswas DK, Wachtel C, Waldman Ben-Asher H, Carmi S, Glaser F, Mandel-Gutfreund Y, Michaeli S (2013) The hnRNP F/H homologue of Trypanosoma brucei is differentially expressed in the two life cycle stages of the parasite and regulates splicing and mRNA stability. Nucleic Acids Res 41:6577–6594

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S, Chang HY (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464:1071–1076

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458:223–227

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander ES, Regev A (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28:503–510

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–300

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guttman M, Russell P, Ingolia NT, Weissman JS, Lander ES (2013) Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154:240–251

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haag JR, Pikaard CS (2011) Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol 12:483–492

    CAS  PubMed  Google Scholar 

  • Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141:129–141

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388

    CAS  PubMed  Google Scholar 

  • Hargreaves DC, Crabtree GR (2011) ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res 21:396–420

    CAS  PubMed Central  PubMed  Google Scholar 

  • He W, Cai Q, Sun F, Zhong G, Wang P, Liu H, Luo J, Yu H, Huang J, Lin T (2013) linc-UBC1 physically associates with polycomb repressive complex 2 (PRC2) and acts as a negative prognostic factor for lymph node metastasis and survival in bladder cancer. Biochim Biophys Acta 1832:1528–1537

    CAS  PubMed  Google Scholar 

  • Helwak A, Kudla G, Dudnakova T, Tollervey D (2013) Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153:654–665

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79

    CAS  PubMed  Google Scholar 

  • Heyne S, Costa F, Rose D, Backofen R (2012) GraphClust: alignment-free structural clustering of local RNA secondary structures. Bioinformatics 28:i224–i232

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hiller M, Pudimat R, Busch A, Backofen R (2006) Using RNA secondary structures to guide sequence motif finding towards single-stranded regions. Nucleic Acids Res 34:e117

    PubMed Central  PubMed  Google Scholar 

  • Hiller M, Zhang Z, Backofen R, Stamm S (2007) Pre-mRNA secondary structures influence exon recognition. PLoS Genet 3:e204

    PubMed Central  PubMed  Google Scholar 

  • Holdt LM, Hoffmann S, Sass K, Langenberger D, Scholz M, Krohn K, Finstermeier K, Stahringer A, Wilfert W, Beutner F, Gielen S, Schuler G, Gäbel G, Bergert H, Bechmann I, Stadler PF, Thiery J, Teupser D (2013) Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet 9:e1003588

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hon GC, Hawkins RD, Ren B (2009) Predictive chromatin signatures in the mammalian genome. Hum Mol Genet 18:R195–R201

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huertas P, Aguilera A (2003) Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12:711–721

    CAS  PubMed  Google Scholar 

  • Idogawa, M, Ohashi, T, Sasaki, Y, Maruyama, R, Kashima, L, Suzuki, H, Tokino, T (2014) Identification and analysis of large intergenic non-coding RNAs regulated by p53 family members through a genome-wide analysis of p53-binding sites. Hum Mol Genetics (in press)

  • Ilik IA, Quinn JJ, Georgiev P, Tavares-Cadete F, Maticzka D, Toscano S, Wan Y, Spitale RC, Luscombe N, Backofen R, Chang HY, Akhtar A (2013) Tandem Stem-Loops in roX RNAs Act Together to Mediate X Chromosome Dosage Compensation in Drosophila. Mol Cell 51:156–173

    CAS  PubMed  Google Scholar 

  • Ilott NE, Ponting CP (2013) Predicting long non-coding RNAs using RNA sequencing. Methods 63:50–59

    CAS  PubMed  Google Scholar 

  • Jeffery L, Nakielny S (2004) Components of the DNA methylation system of chromatin control are RNA-binding proteins. J Biol Chem 279:49479–49487

    CAS  PubMed  Google Scholar 

  • Ji W, Yang L, Yuan J, Yang L, Zhang M, Qi D, Duan X, Xuan A, Zhang W, Lu J, Zhuang Z, Zeng G (2013) MicroRNA-152 targets DNA methyltransferase 1 in NiS-transformed cells via a feedback mechanism. Carcinogenesis 34:446–453

    CAS  PubMed  Google Scholar 

  • Jiang L, Mu J, Zhang Q, Ni T, Srinivasan P, Rayavara K, Yang W, Turner L, Lavstsen T, Theander TG, Peng W, Wei G, Jing Q, Wakabayashi Y, Bansal A, Luo Y, Ribeiro JMC, Scherf A, Aravind L, Zhu J, Zhao K, Miller LH (2013) PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 499:223–227

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kaneko S, Bonasio R, Saldaña-Meyer R, Yoshida T, Son J, Nishino K, Umezawa A, Reinberg D (2013) Interactions between JARID2 and Noncoding RNAs Regulate PRC2 Recruitment to Chromatin. Mol Cell 1–11

  • Kanhere A, Viiri K, Araújo CC, Rasaiyaah J, Bouwman RD, Whyte WA, Pereira CF, Brookes E, Walker K, Bell GW, Pombo A, Fisher AG, Young RA, Jenner RG (2010) Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol Cell 38:675–688

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kazan H, Ray D, Chan ET, Hughes TR, Morris Q (2010) RNAcontext: a new method for learning the sequence and structure binding preferences of RNA-binding proteins. PLoS Comput Biol 6:e1000832

    PubMed Central  PubMed  Google Scholar 

  • Keller C, Kulasegaran-Shylini R, Shimada Y, Hotz H-R, Bühler M (2013) Noncoding RNAs prevent spreading of a repressive histone mark. Nature Structural &#38. Mol Biol 20:994–1000

    CAS  Google Scholar 

  • Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39:1278–1284

    CAS  PubMed  Google Scholar 

  • Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, Rinn JL (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci USA 106:11667–11672

    CAS  PubMed Central  PubMed  Google Scholar 

  • Konig J, Zarnack K, Rot G, Curk T, Kayikci M, Zupan B, Turner DJ, Luscombe NM, Ule J (2010) iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 17:909–915

    PubMed Central  PubMed  Google Scholar 

  • Kotake Y, Nakagawa T, Kitagawa K, Suzuki S, Liu N, Kitagawa M, Xiong Y (2011) Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 30:1956–1962

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lai F, Orom UA, Cesaroni M, Beringer M, Taatjes DJ, Blobel GA, Shiekhattar R (2013) Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature 494:497–501

    CAS  PubMed  Google Scholar 

  • Lall S, Grun D, Krek A, Chen K, Wang YL, Dewey CN, Sood P, Colombo T, Bray N, Macmenamin P, Kao HL, Gunsalus KC, Pachter L, Piano F, Rajewsky N (2006) A genome-wide map of conserved microRNA targets in C. elegans. Curr Biol 16:460–471

    CAS  PubMed  Google Scholar 

  • Lange SJ, Alkhnbashi OS, Rose D, Will S, Backofen R (2013) CRISPRmap: an automated classification of repeat conservation in prokaryotic adaptive immune systems. Nucleic Acids Res 41:8034–8044

    CAS  PubMed Central  PubMed  Google Scholar 

  • Langenberger D, Pundhir S, Ekstrom CT, Stadler PF, Hoffmann S, Gorodkin J (2012) DeepBlockAlign: a tool for aligning RNA-seq profiles of read block patterns. Bioinformatics 28:17–24

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lefevre P, Witham J, Lacroix CE, Cockerill PN, Bonifer C (2008) The LPS-induced transcriptional upregulation of the chicken lysozyme locus involves CTCF eviction and noncoding RNA transcription. Mol Cell 32:129–139

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leibovich L, Paz I, Yakhini Z, Mandel-Gutfreund Y (2013) DRIMust: a web server for discovering rank imbalanced motifs using suffix trees. Nucleic Acids Res 41:W174–W179

    PubMed Central  PubMed  Google Scholar 

  • Leung YY, Ryvkin P, Ungar LH, Gregory BD, Wang LS (2013) CoRAL: predicting non-coding RNAs from small RNA-sequencing data. Nucleic Acids Res 41:e137

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li, LC (2013) Chromatin remodeling by the small RNA machinery in mammalian cells. Epigenetics 9 (in press)

  • Liao Q, Liu C, Yuan X, Kang S, Miao R, Xiao H, Zhao G, Luo H, Bu D, Zhao H, Skogerbo G, Wu Z, Zhao Y (2011a) Large-scale prediction of long non-coding RNA functions in a coding-non-coding gene co-expression network. Nucleic Acids Res 39:3864–3878

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liao Q, Xiao H, Bu D, Xie C, Miao R, Luo H, Zhao G, Yu K, Zhao H, Skogerbo G, Chen R, Wu Z, Liu C, Zhao Y (2011b) ncFANs: a web server for functional annotation of long non-coding RNAs. Nucleic Acids Res 39:W118–W124

    CAS  PubMed Central  PubMed  Google Scholar 

  • Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, Darnell JC, Darnell RB (2008) HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456:464–469

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lorenz R, Hofacker IL, Bernhart SH (2012) Folding RNA/DNA hybrid duplexes. Bioinformatics 28:2530–2531

    CAS  PubMed  Google Scholar 

  • Luo M, Li Z, Wang W, Zeng Y, Liu Z, Qiu J (2013) Long non-coding RNA H19 increases bladder cancer metastasis by associating with EZH2 and inhibiting E-cadherin expression. Cancer Lett 333:213–221

    CAS  PubMed  Google Scholar 

  • Malik S, Roeder RG (2010) The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet 11:761–772

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marina DB, Shankar S, Natarajan P, Finn KJ, Madhani HD (2013) A conserved ncRNA-binding protein recruits silencing factors to heterochromatin through an RNAi-independent mechanism. Genes Dev 27:1851–1856

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, Buchman S, Chen CY, Chou A, Ienasescu H, Lim J, Shyr C, Tan G, Zhou M, Lenhard B, Sandelin A, Wasserman WW (2014) JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res 42:D142–D147

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maticzka D, Lange SJ, Costa F, Backofen R (2014) GraphProt: modeling binding preferences of RNA-binding proteins. Genome Biol 15:R17

    PubMed  Google Scholar 

  • Maxwell SS, Pelka GJ, Tam PP, El-Osta A (2013) Chromatin context and ncRNA highlight targets of MeCP2 in brain. RNA Biol 10:1741–1759

    CAS  PubMed  Google Scholar 

  • Mercer TR, Mattick JS (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20:300–307

    CAS  PubMed  Google Scholar 

  • Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci USA 105:716–721

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meyer F, Kurtz S, Backofen R, Will S, Beckstette M (2011) Structator: fast index-based search for RNA sequence-structure patterns. BMC Bioinforma 12:214

    CAS  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Milek M, Wyler E, Landthaler M (2012) Transcriptome-wide analysis of protein–RNA interactions using high-throughput sequencing. Semin Cell Dev Biol 23:206–212

    CAS  PubMed  Google Scholar 

  • Mohammad F, Mondal T, Guseva N, Pandey GK, Kanduri C (2010) Kcnq1ot1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1. Development 137:2493–2499

    CAS  PubMed  Google Scholar 

  • Mohammad F, Pandey GK, Mondal T, Enroth S, Redrup L, Gyllensten U, Kanduri C (2012) Long noncoding RNA-mediated maintenance of DNA methylation and transcriptional gene silencing. Development 139:2792–2803

    CAS  PubMed  Google Scholar 

  • Mondal T, Rasmussen M, Pandey GK, Isaksson A, Kanduri C (2010) Characterization of the RNA content of chromatin. Genome Res 20:899–907

    CAS  PubMed Central  PubMed  Google Scholar 

  • Monnier P, Martinet C, Pontis J, Stancheva I, Ait-Si-Ali S, Dandolo L (2013) H19 lncRNA controls gene expression of the Imprinted Gene Network by recruiting MBD1. Proc Natl Acad Sci USA 110:20693–20698

    CAS  PubMed  Google Scholar 

  • Morey L, Aloia L, Cozzuto L, Benitah SA, Di Croce L (2013) RYBP and Cbx7 define specific biological functions of polycomb complexes in mouse embryonic stem cells. Cell Rep 3:60–69

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Nikolajewa S, Pudimat R, Hiller M, Platzer M, Backofen R (2007) BioBayesNet: a web server for feature extraction and Bayesian network modeling of biological sequence data. Nucleic Acids Res 35:W688–W693

    PubMed Central  PubMed  Google Scholar 

  • Ogawa Y, Sun BK, Lee JT (2008) Intersection of the RNA interference and X-inactivation pathways. Science 320:1336–1341

    CAS  PubMed Central  PubMed  Google Scholar 

  • Oliveira CS, Saraiva NZ, Cruz MHC, Mazeti B, Oliveira LZ, Lopes FL, Garcia JM (2013) HDAC inhibition decreases XIST expression on female IVP bovine blastocysts. Reproduction (Cambridge, England) 145:9–17

    CAS  Google Scholar 

  • Panning B, Jaenisch R (1996) DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes Dev 10:1991–2002

    CAS  PubMed  Google Scholar 

  • Parker BJ, Moltke I, Roth A, Washietl S, Wen J, Kellis M, Breaker R, Pedersen JS (2011) New families of human regulatory RNA structures identified by comparative analysis of vertebrate genomes. Genome Res 21:1929–1943

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pasquinelli AE (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13:271–282

    CAS  PubMed  Google Scholar 

  • Phillips JE, Corces VG (2009) CTCF: master weaver of the genome. Cell 137:1194–1211

    PubMed Central  PubMed  Google Scholar 

  • Pullirsch D, Härtel R, Kishimoto H, Leeb M, Steiner G, Wutz A (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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ramos AD, Diaz A, Nellore A, Delgado RN, Park KY, Gonzales-Roybal G, Oldham MC, Song JS, Lim DA (2013) Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell Stem Cell 12:616–628

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rapicavoli NA, Poth EM, Zhu H, Blackshaw S (2011) The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity. Neural Dev 6:32

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ringrose L, Paro R (2007) Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134:223–232

    CAS  PubMed  Google Scholar 

  • Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81:145–166

    CAS  PubMed  Google Scholar 

  • Sanford JR, Wang X, Mort M, Vanduyn N, Cooper DN, Mooney SD, Edenberg HJ, Liu Y (2009) Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res 19:381–394

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sarraf SA, Stancheva I (2004) Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol Cell 15:595–605

    CAS  PubMed  Google Scholar 

  • Schmitz KM, Mayer C, Postepska A, Grummt I (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev 24:2264–2269

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schoeftner S, Sengupta AK, Kubicek S, Mechtler K, Spahn L, Koseki H, Jenuwein T, Wutz A (2006) Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J 25:3110–3122

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schor IE, Llères D, Risso GJ, Pawellek A, Ule J, Lamond AI, Kornblihtt AR (2012) Perturbation of chromatin structure globally affects localization and recruitment of splicing factors. PLoS ONE 7:e48084

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stoltenburg R, Reinemann C, Strehlitz B (2007) SELEX– a (r)evolutionary method to generate high-affinity nucleic acid ligands. Biomol Eng 24:381–403

    CAS  PubMed  Google Scholar 

  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102:15545–15550

    CAS  PubMed Central  PubMed  Google 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

    CAS  PubMed  Google Scholar 

  • Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C (2013a) R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340:619–621

    CAS  PubMed  Google Scholar 

  • Sun S, Del Rosario BC, Szanto A, Ogawa Y, Jeon Y, Lee JT (2013b) Jpx RNA activates Xist by evicting CTCF. Cell 153:1537–1551

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sun L, Luo H, Bu D, Zhao G, Yu K, Zhang C, Liu Y, Chen R, Zhao Y (2013c) Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res 41:e166

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tavares L, Dimitrova E, Oxley D, Webster J, Poot R, Demmers J, Bezstarosti K, Taylor S, Ura H, Koide H, Wutz A, Vidal M, Elderkin S, Brockdorff N (2012) RYBP–PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 148:664–678

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tenenbaum SA, Carson CC, Lager PJ, Keene JD (2000) Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc Natl Acad Sci USA 97:14085–14090

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, Gottesman S, Storz G (2006) Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res 34:2791–2802

    CAS  PubMed Central  PubMed  Google Scholar 

  • Torarinsson E, Havgaard JH, Gorodkin J (2007) Multiple structural alignment and clustering of RNA sequences. Bioinformatics 23:926–932

    CAS  PubMed  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsai M-C, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329:689–693

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tseng HH, Weinberg Z, Gore J, Breaker RR, Ruzzo WL (2009) Finding non-coding RNAs through genome-scale clustering. J Bioinforma Comput Biol 7:373–388

    CAS  Google Scholar 

  • Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB (2003) CLIP identifies Nova-regulated RNA networks in the brain. Science 302:1212–1215

    CAS  PubMed  Google Scholar 

  • Uren PJ, Bahrami-Samani E, Burns SC, Qiao M, Karginov FV, Hodges E, Hannon GJ, Sanford JR, Penalva LO, Smith AD (2012) Site identification in high-throughput RNA–protein interaction data. Bioinformatics 28:3013–3020

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vogel T, Stoykova A, Gruss P (2006) Differential expression of polycomb repression complex 1 (PRC1) members in the developing mouse brain reveals multiple complexes. Dev Dyn 235:2574–2585

    CAS  PubMed  Google Scholar 

  • Wan G, Hu X, Liu Y, Han C, Sood AK, Calin GA, Zhang X, Lu X (2013) A novel non-coding RNA lncRNA–JADE connects DNA damage signalling to histone H4 acetylation. EMBO J 32:2833–2847

    CAS  PubMed  Google Scholar 

  • Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43:904–914

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, Wysocka J, Lei M, Dekker J, Helms JA, Chang HY (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472:120–124

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang X, Lu Z, Gomez A, Hon GC, Yue Y, Han D, Fu Y, Parisien M, Dai Q, Jia G, Ren B, Pan T, He C (2014) N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 505:117–120

    PubMed  Google Scholar 

  • Warnecke PM, Biniszkiewicz D, Jaenisch R, Frommer M, Clark SJ (1998) Sequence-specific methylation of the mouse H19 gene in embryonic cells deficient in the Dnmt-1 gene. Dev Genet 22:111–121

    CAS  PubMed  Google Scholar 

  • Washietl S, Findeiss S, Muller SA, Kalkhof S, von Bergen M, Hofacker IL, Stadler PF, Goldman N (2011) RNAcode: robust discrimination of coding and noncoding regions in comparative sequence data. RNA 17:578–594

    CAS  PubMed Central  PubMed  Google Scholar 

  • Will S, Reiche K, Hofacker IL, Stadler PF, Backofen R (2007) Inferring noncoding RNA families and classes by means of genome-scale structure-based clustering. PLoS Comput Biol 3:e65

    PubMed Central  PubMed  Google Scholar 

  • Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J (2013) Comparative genomics boosts target prediction for bacterial small RNAs. Proc Natl Acad Sci USA 110:E3487–E3496

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu X, Johansen JV, Helin K (2013a) Fbxl10/Kdm2b recruits polycomb repressive complex 1 to CpG islands and regulates H2A ubiquitylation. Mol Cell 49:1134–1146

    CAS  PubMed  Google Scholar 

  • Wu L, Murat P, Matak-Vinkovic D, Murrell A, Balasubramanian S (2013b) Binding Interactions between Long Noncoding RNA HOTAIR and PRC2 Proteins. Biochemistry 52:9519–9527

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xie C, Yuan J, Li H, Li M, Zhao G, Bu D, Zhu W, Wu W, Chen R, Zhao Y (2014) NONCODEv4: exploring the world of long non-coding RNA genes. Nucleic Acids Res 42:D98–D103

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang F, Huo X, Yuan S, Zhang L, Zhou W, Wang F, Sun S (2013a) Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cell 49:1083–1096

    CAS  PubMed  Google Scholar 

  • Yang JH, Li JH, Jiang S, Zhou H, Qu LH (2013b) ChIPBase: a database for decoding the transcriptional regulation of long non-coding RNA and microRNA genes from ChIP-Seq data. Nucleic Acids Res 41:D177–D187

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang L, Lin C, Jin C, Yang JC, Tanasa B, Li W, Merkurjev D, Ohgi KA, Meng D, Zhang J, Evans CP, Rosenfeld MG (2013c) lncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs. Nature 500:598–602

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoon JH, Abdelmohsen K, Gorospe M (2013) Posttranscriptional gene regulation by long noncoding RNA. J Mol Biol 425:3723–3730

    CAS  PubMed  Google Scholar 

  • Yap KL, Li S, Muñoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou M-M (2010) Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38:662–674

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoon JH, Abdelmohsen K, Srikantan S, Yang X, Martindale JL, De S, Huarte M, Zhan M, Becker KG, Gorospe M (2012) LincRNA-p21 suppresses target mRNA translation. Mol Cell 47:648–655

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zambelli F, Pesole G, Pavesi G (2013) PscanChIP: Finding over-represented transcription factor-binding site motifs and their correlations in sequences from ChIP-Seq experiments. Nucleic Acids Res 41:W535–W543

    PubMed Central  PubMed  Google Scholar 

  • Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137

    PubMed Central  PubMed  Google Scholar 

  • Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT (2010) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 40:939–953

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu L, Xu P-C (2013) Downregulated LncRNA–ANCR promotes osteoblast differentiation by targeting EZH2 and regulating Runx2 expression. Biochem Biophys Res Commun 432:612–617

    CAS  PubMed  Google Scholar 

  • Zhu Y, Rowley MJ, Böhmdorfer G, Wierzbicki AT (2013) A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol Cell 49:298–309

    CAS  PubMed Central  PubMed  Google Scholar 

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  1. Institute of Computer Science, Albert-Ludwigs-University, Freiburg, Germany

    Rolf Backofen

  2. Institute of Anatomy and Cell Biology, Albert-Ludwigs-University, Freiburg, Germany

    Tanja Vogel

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Backofen, R., Vogel, T. Biological and bioinformatical approaches to study crosstalk of long-non-coding RNAs and chromatin-modifying proteins. Cell Tissue Res 356, 507–526 (2014). https://doi.org/10.1007/s00441-014-1885-x

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