Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses

Genes and Development

Volumn 25, Issue 18, 2011, Pages 1915-1927

  Cabili, Moran ^a,b,c   Trapnell, Cole ^a,c   Goff, Loyal ^a,d   Koziol, Magdalena ^a,c   Tazon Vega, Barbara ^a,c   Regev, Aviv ^a,e   Rinn, John L ^a,c  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Massachusetts General Hospital   (United States)

^d Massachusetts Institute of Technology   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Lincrnas; Long noncoding rnas; Rna sequencing

Indexed keywords

UNTRANSLATED RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC CODE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR GENETICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; ORTHOLOGY; PRIORITY JOURNAL; RNA SEQUENCE; RNA TRANSCRIPTION;

ALTERNATIVE SPLICING; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENES, OVERLAPPING; HUMANS; MOLECULAR SEQUENCE ANNOTATION; RNA, UNTRANSLATED; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 80052978224     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.17446611     Document Type: Article

References (61)

1. Amaral PP, Clark MB, Gascoigne DK, Dinger ME, Mattick JS. 2010. lncRNAdb: a reference database for long noncoding RNAs. Nucleic Acids Res 39: D146-D151. doi: 10.1093/nar/ gkq1138.
2. Bertone P, Stolc V, Royce TE, Rozowsky JS, Urban AE, Zhu X, Rinn JL, Tongprasit W, Samanta M, Weissman S, et al. 2004. Global identification of human transcribed sequences with enome tiling arrays. Science 306: 2242-2246.
3. Birney E, Stamatoyannopoulos JA, Dutta A, Guigó R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
4. Bradley RK, Roberts A, Smoot M, Juvekar S, Do J, Dewey C, Holmes I, Pachter L. 2009. Fast statistical alignment. PLoS Comput Biol 5: e1000392. doi: 10.1371/journal.pcbi.1000392.
5. Brown CJ, Hendrich BD, Rupert JL, Lafreniere RG, Xing Y, Lawrence J, Willard HF. 1992. The human XIST gene: nalysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71: 527-542.
6. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, et al. 2005. The ranscriptional landscape of the mammalian genome. Science 09: 1559-1563.
7. Chodroff RA, Goodstadt L, Sirey TM, Oliver PL, Davies KE, Green ED, Molnar Z, Ponting CP. 2010. Long noncoding RNA genes: conservation of sequence and brain expression among diverse amniotes. Genome Biol 11: R72. doi: 10.1186/ b-2010-11-7-r72.
8. Cohen BA, Mitra RD, Hughes JD, Church GM. 2000. A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression. Nat Genet 26: 183-186.
9. ore LJ, Waterfall JJ, Lis JT. 2008. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322: 1845-1848.
10. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, Muller H, Ragoussis J,Wei CL, Natoli G. 2010. A large fraction f extragenic RNA pol II transcription sites overlap enhancers. LoS Biol 8: e1000384. doi: 10.1371/journal.pbio.1000384.
11. Ebisuya M, Yamamoto T, Nakajima M, Nishida E. 2008. Ripples from neighbouring transcription. Nat Cell Biol 10: 1106-1113.
12. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, et al. 2011. apping and analysis of chromatin state dynamics in nine uman cell types. Nature 473: 43-49.
13. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, et al. 2010. The Pfam protein families database. Nucleic Acids Res 38: 211-D222. doi: 10.1093/nar/gkp985.
14. Fuglede B, Topsoe F. 2004. Jensen-Shannon divergence and Hilbert space embedding. In Proceedings of the IEEE International Symposium on Information Theory, p. 31.doi: 10.1109/ ISIT.2004.1365067.
15. Garber M, Grabherr MG, Guttman M, Trapnell C. 2011. omputational methods for transcriptome annotation and uantification using RNA-seq. Nat Methods 8: 469-477.
16. Girard Al, Sachidanandam R, Hannon GJ, Carmell MA. 2006. A germline-specific class of small RNAs binds mammalian iwi proteins. Nature 442: 199-202.
17. Gudmundsson J, Sulem P, Gudbjartsson DF, Jonasson JG, Sigurdsson A, Bergthorsson JT, He H, Blondal T, Geller F, Jakobsdottir M, et al. 2009. Common variants on 9q22.33 and 14q13.3 predispose to thyroid cancer in European populations. Nat Genet 41: 460-464.
18. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, et al. 2009. Chromatin signature reveals over a thousand highly conserved arge non-coding RNAs in mammals. Nature 458: 23-227.
19. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, et al. 2010. Ab initio reconstruction of cell type-specific transcriptomes n mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28: 503-510.
20. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Yang X, et al. 2011. incRNAs act in the circuitry controlling pluripotency and ifferentiation. Nature (in press).
21. Harrow J, Denoeud F, Frankish A, Reymond A, Chen CK, Chrast J, Lagarde J, Gilbert JG, Storey R, Swarbreck D, et al. 2006. GENCODE: producing a reference annotation for ENCODE. enome Biol 7: S4. doi: 10.1186/gb-2006-7-s1-s4.
22. Heo JB, Sung S. 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76-79.
23. indorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA. 2009. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci 106: 9362-9367.
24. Hsu F, Kent WJ, Clawson H, Kuhn RM, Diekhans M, Haussler D. 2006. The UCSC known genes. Bioinformatics 22: 1036-1046.
25. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, et al. 2010. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142: 409-419.
26. Hung T, Wang Y, Lin MF, Koegel AK, Kotake Y, Grant GD, Horlings HM, Shah N, Umbricht C, Wang P, et al. 2011. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet 43: 621-629.
27. Hurst LD, Pal C, Lercher MJ. 2004. The evolutionary dynamics of eukaryotic gene order. Nat Rev Genet 5: 299-310.
28. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218-223.
29. Kanhere A, Viiri K, Araujo CC, Rasaiyaah J, Bouwman RD, Whyte WA, Pereira CF, Brookes E, Walker K, Bell GW, et al. 2010. Short RNAs are transcribed from repressed polycomb arget genes and interact with polycomb repressive complex-. Mol Cell 38: 675-688.
30. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, et al. 2007. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316: 1484-1488.
31. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at CSC. Genome Res 12: 996-1006.
32. Kent WJ, Baertsch R, Hinrichs A, Miller W, Haussler D. 2003. Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc Natl Acad Sci 100: 11484-11489.
33. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, et al. 2009. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci 106: 11667-11672.
34. Kim T-K, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. 2010. Widespread transcription at neuronal activityregulated enhancers. Nature 465: 182-187.
35. Kondo T, Plaza S, Zanet J, Benrabah E, Valenti P, Hashimoto Y, Kobayashi S, Payre F, Kageyama Y. 2010. Small peptides switch the transcriptional activity of Shavenbaby during rosophila embryogenesis. Science 329: 336-339.
36. Koziol MJ, Rinn JL. 2010. RNA traffic control of chromatin complexes. Curr Opin Genet Dev 20: 142-148.
37. Leighton PA, Ingram RS, Eggenschwiler J, Efstratiadis A, Tilghman SM. 1995. Disruption of imprinting caused by deletion of the 19 gene region in mice. Nature 375: 34-39.
38. Lin MF, Jungreis I, Kellis M. 2011. PhyloCSF: a comparative genomics method to distinguish protein coding and noncoding regions. Bioinformatics 27: i275-i282. doi: 10.1093/ioinformatics/btr209.
39. Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH, arber M, Curran M, Onder T, Agarwal S, et al. 2010. Large intergenic non-coding RNA-RoR modulates reprogramming f human induced pluripotent stem cells. Nat Genet 42: 113-1117.
40. Mercer TR, Dinger ME, Mattick JS. 2009. Long non-coding RNAs: insights into functions. Nat Rev Genet 10: 155-159.
41. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods 5: 621-628.
42. 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.
43. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, ussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, et al. 2010. Long noncoding RNAs with enhancer-like function in human cells. Cell 143: 46-58.
44. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C. 2008. Kcnq1ot1 antisense noncoding RNA mediates lineagespecific transcriptional silencing through chromatin-level regulation. Mol Cell 32: 232-246.
45. Ponjavic J, Ponting CP, Lunter G. 2007. Functionality or transcriptional noise? Evidence for selection within long oncoding RNAs. Genome Res 17: 556-565.
46. Ponjavic J, Oliver PL, Lunter G, Ponting CP. 2009. Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet: e1000617. doi: 10.1371/journal.pgen.1000617.
47. Ponting CP, Oliver PL, Reik W. 2009. Evolution and functions of ong noncoding RNAs. Cell 136: 629-641.
48. Preker P, Nielsen J, Kammler S, Lykke-Andersen Sr, Christensen S, Mapendano CK, Schierup MH, Jensen TH. 2008. RNA exosome depletion reveals transcription upstream of active human promoters. Science 322: 1851-1854.
49. Pruitt K, Tatusova T, Maglott D. 2002. The reference sequence (RefSeq) project. In The NCBI handbook (ed. J McEntyre, J Ostell), chapter 18. National Center for Biotechnology Information, ethesda, MD. http://www.ncbi.nlm.nih.gov/books/NBK21091.
50. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2010. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
51. Ravasi T, Suzuki H, Pang KC, Katayama S, Furuno M, Okunishi R, Fukuda S, Ru K, Frith MC, Gongora MM, et al. 2006. xperimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. enome Res 16: 11-19.
52. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, oodnough LH, Helms JA, Farnham PJ, Segal E, et al. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
53. Schwartz S, Kent WJ, Smit A, Zhang Z, Baertsch R, Hardison C, Haussler D, Miller W. 2003. Human-mouse alignments ith BLASTZ. Genome Res 13: 103-107.
54. Seila AC, Calabrese JM, Levine SS, Yeo GW, Rahl PB, Flynn RA, Young RA, Sharp PA. 2008. Divergent transcription from active promoters. Science 322: 1849-1851.
55. 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 ranscripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
56. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, et al. 2011. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120-124.
57. Young TL, Matsuda T, Cepko CL. 2005. The noncoding RNA taurine upregulated gene 1 is required for differentiation of the murine retina. Curr Biol 15: 501-512.
58. Zentner GE, Tesar PJ, Scacheri PC. 2011. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res 21: 1273-1283.
59. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT. 2008. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750-756.
60. 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.
61. Zhu J, Sanborn JZ, Diekhans M, Lowe CB, Pringle TH, Haussler D. 2007. Comparative genomics search for losses of longestablished genes on the human lineage. PLoS Comput Biol 3: e247. doi: 10.1371/journal.pcbi.0030247.