Modular regulatory principles of large non-coding RNAs (original) (raw)

• Warner, J. R., Soeiro, R., Birnboim, H. C., Girard, M. & Darnell, J. E. Rapidly labeled HeLa cell nuclear RNA. I. Identification by zone sedimentation of a heterogeneous fraction separate from ribosomal precursor RNA. J. Mol. Biol. 19, 349–361 (1966).
  CAS PubMed Google Scholar
• Salditt-Georgieff, M., Harpold, M. M., Wilson, M. C. & Darnell, J. E., Jr. Large heterogeneous nuclear ribonucleic acid has three times as many 5′ caps as polyadenylic acid segments, and most caps do not enter polyribosomes. Mol. Cell. Biol. 1, 179–187 (1981). This paper demonstrates an abundant class of RNA species that do not enter polyribosomes.
  CAS PubMed PubMed Central Google Scholar
• Weinberg, R. A. & Penman, S. Small molecular weight monodisperse nuclear RNA. J. Mol. Biol. 38, 289–304 (1968).
  CAS PubMed Google Scholar
• Zieve, G. & Penman, S. Small RNA species of the HeLa cell: metabolism and subcellular localization. Cell 8, 19–31 (1976).
  CAS PubMed Google Scholar
• Gesteland, R. F., Cech, T. & Atkins, J. F. The RNA World : The Nature of Modern RNA Suggests a Prebiotic RNA World. 3rd edn (Cold Spring Harbor Laboratory Press, 2006).
  Google Scholar
• Eddy, S. R. Non-coding RNA genes and the modern RNA world. Nature Rev. Genet. 2, 919–929 (2001).
  CAS PubMed Google Scholar
• Pachnis, V., Brannan, C. I. & Tilghman, S. M. The structure and expression of a novel gene activated in early mouse embryogenesis. EMBO J. 7, 673–681 (1988).
  CAS PubMed PubMed Central Google Scholar
• Brannan, C. I., Dees, E. C., Ingram, R. S. & Tilghman, S. M. The product of the H19 gene may function as an RNA. Mol. Cell. Biol. 10, 28–36 (1990). This paper was the first report of a large ncRNA showing that the H19 transcript lacked conserved ORFs and did not make a protein product in vivo.
  CAS PubMed PubMed Central Google Scholar
• Brown, C. J. et al. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349, 38–44 (1991).
  ADS CAS PubMed Google Scholar
• Penny, G. D., Kay, G. F., Sheardown, S. A., Rastan, S. & Brockdorff, N. Requirement for Xist in X chromosome inactivation. Nature 379, 131–137 (1996).
  ADS CAS PubMed Google Scholar
• Sleutels, F., Zwart, R. & Barlow, D. P. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415, 810–813 (2002).
  ADS CAS PubMed Google Scholar
• Young, T. L., Matsuda, T. & Cepko, C. L. The noncoding RNA taurine upregulated gene 1 is required for differentiation of the murine retina. Curr. Biol. 15, 501–512 (2005).
  CAS PubMed Google Scholar
• Willingham, A. T. et al. A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 309, 1570–1573 (2005).
  ADS CAS PubMed Google Scholar
• Rinn, J. L. et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311–1323 (2007).
  CAS PubMed PubMed Central Google Scholar
• Carninci, P. et al. The transcriptional landscape of the mammalian genome. Science 309, 1559–1563 (2005). This paper describes the large-scale cDNA sequencing efforts in the mouse genome and reveals many thousands of non-coding transcripts.
  ADS CAS PubMed Google Scholar
• Birney, E. et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799–816 (2007).
  ADS CAS PubMed Google Scholar
• Bertone, P. et al. Global identification of human transcribed sequences with genome tiling arrays. Science 306, 2242–2246 (2004).
  ADS CAS PubMed Google Scholar
• Kapranov, P. et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316, 1484–1488 (2007).
  ADS CAS PubMed Google Scholar
• Rinn, J. L. et al. The transcriptional activity of human Chromosome 22. Genes Dev. 17, 529–540 (2003).
  CAS PubMed PubMed Central Google Scholar
• Kapranov, P. et al. Large-scale transcriptional activity in chromosomes 21 and 22. Science 296, 916–919 (2002).
  ADS CAS PubMed Google Scholar
• Ebisuya, M., Yamamoto, T., Nakajima, M. & Nishida, E. Ripples from neighbouring transcription. Nature Cell Biol. 10, 1106–1113 (2008).
  CAS PubMed Google Scholar
• Struhl, K. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nature Struct. Mol. Biol. 14, 103–105 (2007).
  CAS Google Scholar
• Guttman, M. et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477, 295–300 (2011).
  ADS CAS PubMed PubMed Central Google Scholar
• Orom, U. A. et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 143, 46–58 (2010).
  CAS PubMed PubMed Central Google Scholar
• Guttman, M. et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223–227 (2009). This paper applied a chromatin signature to identify lincRNAs and used a guilt-by-association approach to classify their likely functions in diverse biological processes.
  ADS CAS PubMed PubMed Central Google Scholar
• Huarte, M. et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409–419 (2010).
  CAS PubMed PubMed Central Google Scholar
• Hung, T. et al. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nature Genet. 43, 621–629 (2011).
  CAS PubMed Google Scholar
• Wang, K. C. et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120–124 (2011).
  ADS CAS PubMed PubMed Central Google Scholar
• Wilusz, J. E., Freier, S. M. & Spector, D. L. 3′ end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 135, 919–932 (2008).
  CAS PubMed PubMed Central Google Scholar
• Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621–628 (2008).
  CAS PubMed Google Scholar
• Guttman, M. et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nature Biotechnol. 28, 503–510 (2010).
  CAS Google Scholar
• Cabili, M. N. et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 25, 1915–1927 (2011).
  CAS PubMed PubMed Central Google Scholar
• Mercer, T. R., Dinger, M. E., Sunkin, S. M., Mehler, M. F. & Mattick, J. S. Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl Acad. Sci. USA 105, 716–721 (2008).
  ADS CAS PubMed PubMed Central Google Scholar
• De Santa, F. et al. A large fraction of extragenic RNA Pol II transcription sites overlap enhancers. PLoS Biol. 8, e1000384 (2010).
  PubMed PubMed Central Google Scholar
• Kim, T. K. et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182–187 (2010).
  ADS CAS PubMed PubMed Central Google Scholar
• Ravasi, T. et al. Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. Genome Res. 16, 11–19 (2006).
  CAS PubMed PubMed Central Google Scholar
• Ponjavic, J., Ponting, C. P. & Lunter, G. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res. 17, 556–565 (2007).
  CAS PubMed PubMed Central Google Scholar
• Taft, R. J. et al. Tiny RNAs associated with transcription start sites in animals. Nature Genet. 41, 572–578 (2009).
  CAS PubMed Google Scholar
• Seila, A. C. et al. Divergent transcription from active promoters. Science 322, 1849–1851 (2008).
  ADS CAS PubMed PubMed Central Google Scholar
• Kouzarides, T. Chromatin modifications and their function. Cell 128, 693–705 (2007).
  CAS PubMed Google Scholar
• Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823–837 (2007).
  CAS PubMed Google Scholar
• Visel, A. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854–858 (2009).
  ADS CAS PubMed PubMed Central Google Scholar
• Heintzman, N. D. et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108–112 (2009).
  ADS CAS PubMed PubMed Central Google Scholar
• Mikkelsen, T. S. et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553–560 (2007).
  ADS CAS PubMed PubMed Central Google Scholar
• Khalil, A. M. et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl Acad. Sci. USA 106, 11667–11672 (2009).
  ADS CAS PubMed PubMed Central Google Scholar
• Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43–49 (2011).
  ADS CAS PubMed PubMed Central Google Scholar
• Loewer, S. et al. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nature Genet. 42, 1113–1117 (2010).
  CAS PubMed Google Scholar
• Dinger, M. E., Pang, K. C., Mercer, T. R. & Mattick, J. S. Differentiating protein-coding and noncoding RNA: challenges and ambiguities. PLoS Comput. Biol. 4, e1000176 (2008).
  ADS PubMed PubMed Central Google Scholar
• Brockdorff, N. et al. 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 (1992).
  CAS PubMed Google Scholar
• Lin, M. F., Deoras, A. N., Rasmussen, M. D. & Kellis, M. Performance and scalability of discriminative metrics for comparative gene identification in 12 Drosophila genomes. PLoS Comput. Biol. 4, e1000067 (2008).
  ADS MathSciNet PubMed PubMed Central Google Scholar
• Lin, M. F., Jungreis, I. & Kellis, M. PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics 27, i275–i282 (2011).
  CAS PubMed PubMed Central Google Scholar
• Finn, R. D. et al. The Pfam protein families database. Nucleic Acids Res. 38, D211–D222 (2010).
  CAS PubMed Google Scholar
• Ingolia, N. T., Lareau, L. F. & Weissman, J. S. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789–802 (2011).
  CAS PubMed PubMed Central Google Scholar
• Galindo, M. I., Pueyo, J. I., Fouix, S., Bishop, S. A. & Couso, J. P. Peptides encoded by short ORFs control development and define a new eukaryotic gene family. PLoS Biol. 5, e106 (2007). This paper demonstrates the existence of functional small peptides within a presumed 'non-coding' transcript through ORF conservation, in vivo protein identification and functional analysis.
  PubMed PubMed Central Google Scholar
• Kondo, T. et al. Small peptides switch the transcriptional activity of Shavenbaby during Drosophila embryogenesis. Science 329, 336–339 (2010).
  ADS CAS PubMed Google Scholar
• Jiao, Y. & Meyerowitz, E. M. Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol. Syst. Biol. 6, 419 (2010).
  PubMed PubMed Central Google Scholar
• Li, Y. M. et al. The H19 transcript is associated with polysomes and may regulate IGF2 expression in trans. J. Biol. Chem. 273, 28247–28252 (1998).
  CAS PubMed Google Scholar
• Cai, X. & Cullen, B. R. The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13, 313–316 (2007).
  CAS PubMed PubMed Central Google Scholar
• Yang, L. et al. ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 147, 773–788 (2011).
  CAS PubMed PubMed Central Google Scholar
• Clamp, M. et al. Distinguishing protein-coding and noncoding genes in the human genome. Proc. Natl Acad. Sci. USA 104, 19428–19433 (2007).
  ADS CAS PubMed PubMed Central Google Scholar
• Kastenmayer, J. P. et al. Functional genomics of genes with small open reading frames (sORFs) in S. cerevisiae. Genome Res. 16, 365–373 (2006).
  CAS PubMed PubMed Central Google Scholar
• Hanada, K., Zhang, X., Borevitz, J. O., Li, W. H. & Shiu, S. H. A large number of novel coding small open reading frames in the intergenic regions of the Arabidopsis thaliana genome are transcribed and/or under purifying selection. Genome Res 17, 632–640 (2007).
  CAS PubMed PubMed Central Google Scholar
• Mattick, J. S. The genetic signatures of noncoding RNAs. PLoS Genet. 5, e1000459 (2009).
  PubMed PubMed Central Google Scholar
• Tsai, M. C. et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689–693 (2010). This paper identified multiple protein-interaction domains within HOTAIR that together allowed it to carry out its function, which demonstrated that a large ncRNA can act as a molecular scaffold.
  ADS CAS PubMed PubMed Central Google Scholar
• Gupta, R. A. et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464, 1071–1076 (2010).
  ADS CAS PubMed PubMed Central Google Scholar
• Zappulla, D. C. & Cech, T. R. Yeast telomerase RNA: a flexible scaffold for protein subunits. Proc. Natl Acad. Sci. USA 101, 10024–10029 (2004). This paper demonstrated that telomerase RNA can bridge proteins by showing that protein interaction domains can be swapped and spacer regions deleted with minimal impact on the function of the RNA.
  ADS CAS PubMed PubMed Central Google Scholar
• Korostelev, A. & Noller, H. F. The ribosome in focus: new structures bring new insights. Trends Biochem. Sci. 32, 434–441 (2007).
  CAS PubMed Google Scholar
• Ivanova, N. et al. Dissecting self-renewal in stem cells with RNA interference. Nature 442, 533–538 (2006).
  ADS CAS PubMed Google Scholar
• Martens, J. A., Laprade, L. & Winston, F. Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature 429, 571–574 (2004).
  ADS CAS PubMed Google Scholar
• Schmitt, S., Prestel, M. & Paro, R. Intergenic transcription through a Polycomb group response element counteracts silencing. Genes Dev. 19, 697–708 (2005).
  CAS PubMed PubMed Central Google Scholar
• Lee, J. T. Lessons from X-chromosome inactivation: long ncRNA as guides and tethers to the epigenome. Genes Dev. 23, 1831–1842 (2009).
  CAS PubMed PubMed Central Google Scholar
• Ponjavic, J., Oliver, P. L., Lunter, G. & Ponting, C. P. Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet. 5, e1000617 (2009).
  PubMed PubMed Central Google Scholar
• Tian, D., Sun, S. & Lee, J. T. The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143, 390–403 (2010).
  CAS PubMed PubMed Central Google Scholar
• Koerner, M. V., Pauler, F. M., Huang, R. & Barlow, D. P. The function of non-coding RNAs in genomic imprinting. Development 136, 1771–1783 (2009).
  CAS PubMed Google Scholar
• Pandey, R. R. et al. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol. Cell 32, 232–246 (2008).
  CAS PubMed Google Scholar
• Bertani, S., Sauer, S., Bolotin, E. & Sauer, F. The noncoding RNA Mistral activates Hoxa6 and Hoxa7 expression and stem cell differentiation by recruiting MLL1 to chromatin. Mol. Cell 43, 1040–1046 (2011).
  CAS PubMed PubMed Central Google Scholar
• Feng, J. et al. The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev. 20, 1470–1484 (2006).
  CAS PubMed PubMed Central Google Scholar
• Koziol, M. J. & Rinn, J. L. RNA traffic control of chromatin complexes. Curr. Opin. Genet. Dev. 20, 142–148 (2010).
  CAS PubMed PubMed Central Google Scholar
• Maison, C. et al. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nature Genet. 30, 329–334 (2002).
  PubMed Google Scholar
• Bernstein, E. et al. Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol. Cell. Biol. 26, 2560–2569 (2006).
  CAS PubMed PubMed Central Google Scholar
• Wutz, A., Rasmussen, T. P. & Jaenisch, R. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nature Genet. 30, 167–174 (2002). This paper reported the generation of deletion mutants across the Xist locus and identified the discrete domains responsible for the silencing and localization roles of the RNA.
  CAS PubMed Google Scholar
• Chu, C., Qu, K., Zhong, F. L., Artandi, S. E. & Chang, H. Y. Genomic maps of long noncoding RNA occupancy reveal principles of RNA–chromatin interactions. Mol. Cell 44, 667–678 (2011).
  CAS PubMed PubMed Central Google Scholar
• Simon, M. D. et al. The genomic binding-sites of a non-coding RNA. Proc. Natl Acad. Sci. USA 108, 20497–20502 (2011).
  ADS CAS PubMed PubMed Central Google Scholar
• Zhao, J., Sun, B. K., Erwin, J. A., Song, J. J. & Lee, J. T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322, 750–756 (2008).
  ADS CAS PubMed PubMed Central Google Scholar
• Plath, K., Mlynarczyk-Evans, S., Nusinow, D. A. & Panning, B. Xist RNA and the mechanism of X chromosome inactivation. Annu. Rev. Genet. 36, 233–278 (2002).
  CAS PubMed Google Scholar
• Nagano, T. et al. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322, 1717–1720 (2008).
  ADS CAS PubMed Google Scholar
• Zhao, J. et al. Genome-wide identification of Polycomb-associated RNAs by RIP-seq. Mol. Cell 40, 939–953 (2010).
  CAS PubMed PubMed Central Google Scholar
• Kaneko, S. et al. Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev. 24, 2615–2620 (2010).
  CAS PubMed PubMed Central Google Scholar
• Wang, X. et al. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454, 126–130 (2008).
  ADS CAS PubMed PubMed Central Google Scholar
• Kino, T., Hurt, D. E., Ichijo, T., Nader, N. & Chrousos, G. P. Noncoding RNA Gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci. Signal 3, ra8 (2010).
  PubMed PubMed Central Google Scholar
• Salmena, L., Poliseno, L., Tay, Y., Kats, L. & Pandolfi, P. P. A ceRNA hypothesis: the Rosetta stone of a hidden RNA language? Cell 146, 353–358 (2011).
  CAS PubMed PubMed Central Google Scholar
• Cesana, M. et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147, 358–369 (2011).
  CAS PubMed PubMed Central Google Scholar
• Greider, C. W. & Blackburn, E. H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43, 405–413 (1985).
  CAS PubMed Google Scholar
• Feng, J. et al. The RNA component of human telomerase. Science 269, 1236–1241 (1995).
  ADS CAS PubMed Google Scholar
• Lingner, J. et al. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276, 561–567 (1997).
  CAS PubMed Google Scholar
• Jeon, Y. & Lee, J. T. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146, 119–133 (2011).
  CAS PubMed PubMed Central Google Scholar
• Hasegawa, Y., Brockdorff, N., Kawano, S., Tsutui, K. & Nakagawa, S. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell 19, 469–476 (2010).
  CAS PubMed Google Scholar
• Schmitz, K. M., Mayer, C., Postepska, A. & Grummt, I. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 24, 2264–2269 (2010).
  CAS PubMed PubMed Central Google Scholar
• Martianov, I., Ramadass, A., Serra Barros, A., Chow, N. & Akoulitchev, A. Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445, 666–670 (2007).
  CAS PubMed Google Scholar
• Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233 (2009).
  CAS PubMed PubMed Central Google Scholar