Nuclear stability and transcriptional directionality separate functionally distinct RNA species

Nature Communications

Volumn 5, Issue , 2014, Pages

  Andersson, Robin ^a   Refsing Andersen, Peter ^b,g   Valen, Eivind ^c,d   Core, Leighton J ^e,f   Bornholdt, Jette ^a   Boyd, Mette ^a   Heick Jensen, Torben ^b,h   Sandelin, Albin ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Centre for MRNP Biogenesis and Metabolism   (Denmark)

^c UNIVERSITY OF BERGEN   (Norway)

^d HARVARD UNIVERSITY   (United States)

^e Department of Obstetrics Gynecology   (United States)

^f UNIVERSITY OF CONNECTICUT   (United States)

^g Institute of Molecular Biotechnology Austrian Academy of Sciences ^*  (United States)

^h ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CAPPED RNA; DEOXYRIBONUCLEASE; LONG UNTRANSLATED RNA; RNA; UNTRANSLATED RNA;

BIOCHEMISTRY; GENOME; MAMMAL; PROTEIN; RNA;

ARTICLE; CONTROLLED STUDY; EXOSOME; FEMALE; HUMAN; HUMAN CELL; RNA STABILITY; RNA TRANSCRIPTION; SENSITIVITY ANALYSIS; TRANSCRIPTION INITIATION; CLASSIFICATION; GENETIC TRANSCRIPTION; GENETICS; HELA CELL LINE; PHYSIOLOGY; PROMOTER REGION;

MAMMALIA;

EXOSOMES; HELA CELLS; HUMANS; PROMOTER REGIONS, GENETIC; RNA; RNA STABILITY; RNA, UNTRANSLATED; TRANSCRIPTION INITIATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84920954858     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6336     Document Type: Article

References (48)

1. 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).
2. Djebali, S. et al. Landscape of transcription in human cells. Nature 489, 101-108 (2012).
3. Kapranov, P. et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316, 1484-1488 (2007).
4. The FANTOM Consortium. The transcriptional landscape of the mammalian genome. Science 309, 1559-1563 (2005).
5. Derrien, T. et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 22, 1775-1789 (2012).
6. Rinn, J. L. & Chang, H. Y. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81, 145-166 (2011).
7. Ulitsky, I. & Bartel, D. P. lincRNAs: genomics, evolution, and mechanisms. Cell 154, 26-46 (2013).
8. Lam, M. T. Y., Li, W., Rosenfeld, M. G. & Glass, C. K. Enhancer RNAs and regulated transcriptional programs. Trends Biochem. Sci. 39, 170-182 (2014).
9. Jensen, T. H., Jacquier, A. & Libri, D. Dealing with pervasive transcription. Mol. Cell 52, 473-484 (2013).
10. Cech, T. R. & Steitz, J. A. The noncoding RNA revolution-trashing old Rules to forge new ones. Cell 157, 77-94 (2014).
11. Preker, P. et al. RNA exosome depletion reveals transcription upstream of active human promoters. Science 322, 1851-1854 (2008).
12. Almada, A. E., Wu, X., Kriz, A. J., Burge, C. B. & Sharp, P. A. Promoter directionality is controlled by U1 snRNP and polyadenylation signals. Nature 499, 360-363 (2013).
13. Ntini, E. et al. Polyadenylation site-induced decay of upstream transcripts enforces promoter directionality. Nat. Struct. Mol. Biol. 20, 923-928 (2013).
14. Sigova, A. A. et al. Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc. Natl Acad. Sci. USA 110, 2876-2881 (2013).
15. Kim, T.-K. et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182-187 (2010).
16. De Santa, F. et al. A large fraction of extragenic RNA Pol II transcription sites overlap enhancers. PLoS Biol. 8, e1000384 (2010).
17. Core, L. J., Waterfall, J. J. & Lis, J. T. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322, 1845-1848 (2008).
18. Seila, A. C. et al. Divergent transcription from active promoters. Science 322, 1849-1851 (2008).
19. Andersson, R. et al. An atlas of active enhancers across human cell types and tissues. Nature 507, 455-461 (2014).
20. Schmid, M. & Jensen, T. H. Transcription-associated quality control of mRNP. Biochim. Biophys. Acta 1829, 158-168 (2013).
21. Takahashi, H., Lassmann, T., Murata, M. & Carninci, P. 50 end-centered expression profiling using cap-analysis gene expression and next-generation sequencing. Nat. Protoc. 7, 542-561 (2012).
22. Thurman, R. E. et al. The accessible chromatin landscape of the human genome. Nature 489, 75-82 (2012).
23. Fejes-Toth, K. et al. Post-transcriptional processing generates a diversity of 50-modified long and short RNAs. Nature 457, 1028-1032 (2009).
24. Wang, J. et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 22, 1798-1812 (2012).
25. Mathelier, A. et al. JASPAR 2014: an extensively expanded and updated openaccess database of transcription factor binding profiles. Nucleic Acids Res. 42, D142-D147 (2013).
26. Core, L. J. et al. Defining the status of RNA polymerase at promoters. Cell Rep. 2, 1025-1035 (2012).
27. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
28. Trapnell, C. et al. Differential gene and transcript expression analysis of RNAseq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).
29. Andersen, P. R. et al. The human cap-binding complex is functionally connected to the nuclear RNA exosome. Nat. Struct. Mol. Biol. 20, 1367-1376 (2013).
30. 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).
31. Kaida, D. et al. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468, 664-668 (2010).
32. Cooper, G. M. et al. Distribution and intensity of constraint in mammalian genomic sequence. Genome Res. 15, 901-913 (2005).
33. Taylor, M. S. et al. Rapidly evolving human promoter regions. Nature Genet. 40, 1262-1264 (2008).
34. Marques, A. C. et al. Chromatin signatures at transcriptional start sites separate two equally populated yet distinct classes of intergenic long noncoding RNAs. Genome Biol. 14, R131 (2013).
35. The FANTOM Consortium and the RIKEN PMI and CLST(DGT). A promoter level mammalian expression atlas. Nature 507, 462-470 (2014).
36. Kiss, T. & Filipowicz, W. Exonucleolytic processing of small nucleolar RNAs from pre-mRNA introns. Genes Dev. 9, 1411-1424 (1995).
37. Koch, F. et al. Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters. Nat. Struct.Mol. Biol. 18, 956-963 (2011).
38. Kowalczyk, M. S. et al. Intragenic enhancers act as alternative promoters. Mol. Cell 45, 447-458 (2012).
39. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
40. Marstrand, T. T. et al. Asap: a framework for over-representation statistics for transcription factor binding sites. PLoS ONE 3, e1623 (2008).
41. Kim, H. & Park, H. Sparse non-negative matrix factorizations via alternating non-negativity-constrained least squares for microarray data analysis. Bioinformatics 23, 1495-1502 (2007).
42. Hoffman, M. M. et al. Unsupervised pattern discovery in human chromatin structure through genomic segmentation. Nat. Methods 9, 473-476 (2012).
43. Ernst, J. & Kellis, M. ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9, 215-216 (2012).
44. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
45. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2012).
46. Ramsköld, D., Wang, E. T., Burge, C. B. & Sandberg, R. An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput. Biol. 5, e1000598 (2009).
47. 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).
48. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010).