The RIDL hypothesis: Transposable elements as functional domains of long noncoding RNAs

RNA

Volumn 20, Issue 7, 2014, Pages 959-976

  Johnson, Rory ^a,b,c   Guigó, Roderic ^a,b,c  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c HOSPITAL DEL MAR   (Spain)

Author keywords

Evolution; Functional domain; Genome; LncRNA; Long noncoding rna; Repeat element; Transposable element; Transposon

Indexed keywords

DNA; LONG UNTRANSLATED RNA; NUCLEIC ACID; PROTEIN; RNA;

ARTICLE; CELLULAR DISTRIBUTION; CONSENSUS SEQUENCE; DNA BINDING; EXON; GENE; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC CONSERVATION; GENOME; GENOMICS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; RNA BINDING; TRANSPOSON;

EVOLUTION; FUNCTIONAL DOMAIN; GENOME; LNCRNA; LONG NONCODING RNA; REPEAT ELEMENT; TRANSPOSABLE ELEMENT; TRANSPOSON;

ANIMALS; BASE SEQUENCE; BINDING SITES; CHROMOSOME MAPPING; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; EXONS; FEMALE; GENE REGULATORY NETWORKS; HUMANS; PROTEINS; RNA, LONG NONCODING;

EID: 84902682913     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.044560.114     Document Type: Article

References (107)

1. Amaral PP, Clark MB, Gascoigne DK, Dinger ME, Mattick JS. 2011. lncRNAdb: a reference database for long noncoding RNAs. Nucleic Acids Res 39: D146-D151.
2. Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, De Sapio F, Brennan PM, Rizzu P, Smith S, Fell M, et al. 2011. Somatic retrotransposition alters the genetic landscape of the human brain. Nature 479: 534-537.
3. Baker D, Sali A. 2001. Protein structure prediction and structural genomics. Science 294: 93-96. (Pubitemid 32952955)
4. Beletskii A, Hong YK, Pehrson J, Egholm M, Strauss WM. 2001. PNA interference mapping demonstrates functional domains in the non-coding RNA Xist. Proc Natl Acad Sci 98: 9215-9220. (Pubitemid 32743896)
5. Bellucci M, Agostini F, Masin M, Tartaglia GG. 2011. Predicting protein associations with long noncoding RNAs. Nat Methods 8: 444-445.
6. Blackwell BJ, Lopez MF, Wang J, Krastins B, Sarracino D, Tollervey JR, Dobke M, Jordan IK, Lunyak VV. 2012. Protein interactions with piALU RNA indicates putative participation of retroRNA in the cell cycle, DNA repair and chromatin assembly. Mob Genet Elements 2: 26-35.
7. Bourque G, Leong B, Vega VB, Chen X, Lee YL, Srinivasan KG, Chew JL, Ruan Y, Wei CL, Ng HH, et al. 2008. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 18: 1752-1762.
8. Bowen NJ, Jordan IK. 2007. Exaptation of protein coding sequences from transposable elements. Genome Dyn 3: 147-162.
9. Britten RJ, Davidson EH. 1971. Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q Rev Biol 46: 111-138.
10. Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HF. 1991. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349: 38-44. (Pubitemid 21912005)
11. Buljan M, Frankish A, Bateman A. 2010. Quantifying the mechanisms of domain gain in animal proteins. Genome Biol 11: R74.
12. 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.
13. Carpenter S, Aiello D, Atianand MK, Ricci EP, Gandhi P, Hall LL, Byron M, Monks B, Henry-Bezy M, Lawrence JB, et al. 2013. A long noncoding RNA mediates both activation and repression of immune response genes. Science 341: 789-792.
14. Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, Pesce E, Ferrer I, Collavin L, Santoro C, et al. 2012. Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491: 454-457.
15. Cartault F, Munier P, Benko E, Desguerre I, Hanein S, Boddaert N, Bandiera S, Vellayoudom J, Krejbich-Trotot P, Bintner M, et al. 2012. Mutation in a primate-conserved retrotransposon reveals a noncoding RNA as a mediator of infantile encephalopathy. Proc Natl Acad Sci 109: 4980-4985.
16. 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.
17. Chueh AC, Northrop EL, Brettingham-Moore KH, Choo KH, Wong LH. 2009. LINE retrotransposon RNA is an essential structural and functional epigenetic component of a core neocentromeric chromatin. PLoS Genet 5: e1000354.
18. Clark MB, Johnston RL, Inostroza-Ponta M, Fox AH, Fortini E, Moscato P, Dinger ME, Mattick JS. 2012. Genome-wide analysis of long noncoding RNA stability. Genome Res 22: 885-898.
19. Cordaux R, Batzer MA. 2009. The impact of retrotransposons on human genome evolution. Nat Rev Genet 10: 691-703.
20. da Rocha ST, Boeva V, Escamilla-Del-Arenal M, Ancelin K, Granier C, Matias NR, Sanulli S, Chow J, Schulz E, Picard C, et al. 2014. Jarid2 is implicated in the initial Xist-induced targeting of PRC2 to the inactive X chromosome. Mol Cell 53: 301-316.
21. de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD. 2011. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7: e1002384.
22. de Souza FS, Franchini LF, Rubinstein M. 2013. Exaptation of transposable elements into novel cis-regulatory elements: Is the evidence always strong? Mol Biol Evol 30: 1239 -1251.
23. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, et al. 2012. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22: 1775-1789.
24. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. 2012. Landscape of transcription in human cells. Nature 489: 101-108.
25. Duszczyk MM, Wutz A, Rybin V, Sattler M. 2011. The Xist RNA A-repeat comprises a novel AUCG tetraloop fold and a platform for multimerization. RNA 17: 1973-1982.
26. Elisaphenko EA, Kolesnikov NN, Shevchenko AI, Rogozin IB, Nesterova TB, Brockdorff N, Zakian SM. 2008. A dual origin of the Xist gene from a protein-coding gene and a set of transposable elements. PLoS One 3: e2521.
27. Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K, Surka C, Kadri S, Xing J, Goren A, Lander ES, et al. 2013. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341: 1237973.
28. Faghihi MA, Modarresi F, Khalil AM, Wood DE, Sahagan BG, Morgan TE, Finch CE, St Laurent G III, Kenny PJ, Wahlestedt C. 2008. Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of β-secretase. Nat Med 14: 723-730.
29. Faulkner GJ, Kimura Y, Daub CO, Wani S, Plessy C, Irvine KM, Schroder K, Cloonan N, Steptoe AL, Lassmann T, et al. 2009. The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41: 563-571.
30. Ferreira PG, Jares P, Rico D, Gomez-Lopez G, Martinez-Trillos A, Villamor N, Ecker S, Gonzalez-Perez A, Knowles DG, Monlong J, et al. 2014. Transcriptome characterization by RNA sequencing identifies a major molecular and clinical subdivision in chronic lymphocytic leukemia. Genome Res 24: 212-226.
31. V600E remodels the melanocyte transcriptome and induces BANCR to regulate melanoma cell migration. Genome Res 22: 1006-1014.
32. Gifford WD, Pfaff SL, Macfarlan TS. 2013. Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol 23: 218-226.
33. Giordano J, Ge Y, Gelfand Y, Abrusan G, Benson G, Warburton PE. 2007. Evolutionary history of mammalian transposons determined by genome-wide defragmentation. PLoS Comput Biol 3: e137.
34. Glazko GV, Zybailov BL, Rogozin IB. 2012. Computational prediction of polycomb-associated long non-coding RNAs. PLoS One 7: e44878.
35. Gong C, Maquat LE. 2011. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature 470: 284-288.
36. Goodier JL, Mandal PK, Zhang L, Kazazian HH Jr. 2010. Discrete subcellular partitioning of human retrotransposon RNAs despite a common mechanism of genome insertion. Hum Mol Genet 19: 1712-1725.
37. Goodier JL, Cheung LE, Kazazian HH Jr. 2013. Mapping the LINE1 ORF1 protein interactome reveals associated inhibitors of human retrotransposition. Nucleic Acids Res 41: 7401-7419.
38. Graur D, Zheng Y, Price N, Azevedo RB, Zufall RA, Elhaik E. 2013. On the immortality of television sets: "function" in the human genome according to the evolution-free gospel of ENCODE. Genome Biol Evol 5: 578-590.
39. Grote P, Herrmann BG. 2013. The long non-coding RNA Fendrr links epigenetic control mechanisms to gene regulatory networks in mammalian embryogenesis. RNA Biol 10: 1579-1585.
40. Grote P, Wittler L, Hendrix D, Koch F, Wahrisch S, Beisaw A, Macura K, Bläss G, Kellis M, Werber M, et al. 2013. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell 24: 206-214.
41. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, et al. 2010. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464: 1071-1076.
42. Guttman M, Rinn JL. 2012. Modular regulatory principles of large non-coding RNAs. Nature 482: 339-346.
43. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, et al. 2011. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477: 295-300.
44. Hangauer MJ, Vaughn IW, McManus MT. 2013. Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet 9: e1003569.
45. He S, Gu W, Li Y, Zhu H. 2013. ANRIL/CDKN2B-AS shows two-stage clade-specific evolution and becomes conserved after transposon insertions in simians. BMC Evol Biol 13: 247.
46. Holdt LM, Hoffmann S, Sass K, Langenberger D, Scholz M, Krohn K, Finstermeier K, Stahringer A, Wilfert W, Beutner F, et al. 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.
47. Huda A, Bowen NJ, Conley AB, Jordan IK. 2011a. Epigenetic regulation of transposable element derived human gene promoters. Gene 475: 39-48.
48. Huda A, Tyagi E, Mariño-Ramírez L, Bowen NJ, Jjingo D, Jordan IK. 2011b. Prediction of transposable element derived enhancers using chromatin modification profiles. PLoS One 6: e27513.
49. Huntley S, Baggott DM, Hamilton AT, Tran-Gyamfi M, Yang S, Kim J, Gordon L, Branscomb E, Stubbs L. 2006. A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res 16: 669-677.
50. Jeon Y, Lee JT. 2011. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146: 119-133.
51. Johnson R, Gamblin RJ, Ooi L, Bruce AW, Donaldson IJ, Westhead DR, Wood IC, Jackson RM, Buckley NJ. 2006. Identification of the REST regulon reveals extensive transposable element-mediated binding site duplication. Nucleic Acids Res 34: 3862-3877. (Pubitemid 44391002)
52. Johnson R, Teh CH, Jia H, Vanisri RR, Pandey T, Lu ZH, Buckley NJ, Stanton LW, Lipovich L. 2009. Regulation of neural macroRNAs by the transcriptional repressor REST. RNA 15: 85-96.
53. Kaneko H, Dridi S, Tarallo V, Gelfand BD, Fowler BJ, Cho WG, Kleinman ME, Ponicsan SL, Hauswirth WW, Chiodo VA, et al. 2011. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 471: 325-330.
54. Kapusta A, Kronenberg Z, Lynch VJ, Zhuo X, Ramsay L, Bourque G, Yandell M, Feschotte C. 2013. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet 9: e1003470.
55. Kelley D, Rinn J. 2012. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol 13: R107.
56. 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.
57. Kim YK, Furic L, Parisien M, Major F, DesGroseillers L, Maquat LE. 2007. Staufen1 regulates diverse classes of mammalian transcripts. EMBO J 26: 2670-2681. (Pubitemid 46884281)
58. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP. 2010. Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal 3: ra8.
59. Koonin EV, Wolf YI, Karev GP. 2002. The structure of the protein universe and genome evolution. Nature 420: 218-223. (Pubitemid 35340133)
60. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921. (Pubitemid 32165345)
61. Li W, Jin Y, Prazak L, Hammell M, Dubnau J. 2012. Transposable elements in TDP-43-mediated neurodegenerative disorders. PLoS One 7: e44099.
62. Lipovich L, Dachet F, Cai J, Bagla S, Balan K, Jia H, Loeb JA. 2012. Activity-dependent human brain coding/noncoding gene regulatory networks. Genetics 192: 1133-1148.
63. Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH, Garber M, Curran M, Onder T, Agarwal S, et al. 2010. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 42: 1113-1117.
64. Lowe CB, Bejerano G, Haussler D. 2007. Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc Natl Acad Sci 104: 8005- 8010.
65. Maamar H, Cabili MN, Rinn J, Raj A. 2013. linc-HOXA1 is a noncoding RNA that represses Hoxa1 transcription in cis. Genes Dev 27: 1260-1271.
66. Maenner S, Blaud M, Fouillen L, Savoye A, Marchand V, Dubois A, Sanglier-Cianférani S, Van Dorsselaer A, Clerc P, Avner P, et al. 2010. 2-D structure of the A region of Xist RNA and its implication for PRC2 association. PLoS Biol 8: e1000276.
67. Mariner PD, Walters RD, Espinoza CA, Drullinger LF, Wagner SD, Kugel JF, Goodrich JA. 2008. Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol Cell 29: 499-509. (Pubitemid 351282533)
68. Marsh JA, Teichmann SA. 2010. How do proteins gain new domains? Genome Biol 11: 126.
69. Mattick JS. 2009. Deconstructing the dogma: a new view of the evolution and genetic programming of complex organisms. Ann N Y Acad Sci 1178: 29-46.
70. Muotri AR, Chu VT, Marchetto MC, Deng W, Moran JV, Gage FH. 2005. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435: 903-910. (Pubitemid 40896309)
71. Muppirala UK, Honavar VG, Dobbs D. 2011. Predicting RNA-protein interactions using only sequence information. BMC Bioinformatics 12: 489.
72. Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, Zeller U, Baker JC, Grutzner F, Kaessmann H. 2014. The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505: 635-640.
73. Negishi M, Wongpalee SP, Sarkar S, Park J, Lee KY, Shibata Y, Reon BJ, Abounader R, Suzuki Y, Sugano S, et al. 2014. A new lncRNA, APTR, associates with and represses the CDKN1A/p21 promoter by recruiting polycomb proteins. PLoS One 9: e95216.
74. Ng SY, Johnson R, Stanton LW. 2012. Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J 31: 522-533.
75. Novikova IV, Hennelly SP, Sanbonmatsu KY. 2012. Structural architecture of the human long non-coding RNA, steroid receptor RNA activator. Nucleic Acids Res 40: 5034-5051.
76. Peaston AE, Evsikov AV, Graber JH, de Vries WN, Holbrook AE, Solter D, Knowles BB. 2004. Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev Cell 7: 597-606. (Pubitemid 39341844)
77. Pedersen JS, Bejerano G, Siepel A, Rosenbloom K, Lindblad-Toh K, Lander ES, Kent J, Miller W, Haussler D. 2006. Identification and classification of conserved RNA secondary structures in the human genome. PLoS Comput Biol 2: e33.
78. Piriyapongsa J, Jordan IK. 2007. A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS One 2: e203.
79. Pollard KS, Salama SR, Lambert N, Lambot MA, Coppens S, Pedersen JS, Katzman S, King B, Onodera C, Siepel A, et al. 2006. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443: 167-172. (Pubitemid 44387600)
80. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A. 2010. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20: 110-121.
81. Ponjavic J, Ponting CP, Lunter G. 2007. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 17: 556-565. (Pubitemid 46715505)
82. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough 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. (Pubitemid 46962090)
83. Rowe HM, Trono D. 2011. Dynamic control of endogenous retroviruses during development. Virology 411: 273-287.
84. Santoni FA, Guerra J, Luban J. 2012. HERV-H RNA is abundant in human embryonic stem cells and a precise marker for pluripotency. Retrovirology 9: 111.
85. Schad E, Kalmar L, Tompa P. 2013. Exon-phase symmetry and intrinsic structural disorder promote modular evolution in the human genome. Nucleic Acids Res 41: 4409-4422.
86. Sela N, Mersch B, Hotz-Wagenblatt A, Ast G. 2010. Characteristics of transposable element exonization within human and mouse. PLoS One 5: e10907.
87. Shukla R, Upton KR, Muñoz-Lopez M, Gerhardt DJ, Fisher ME, Nguyen T, Brennan PM, Baillie JK, Collino A, Ghisletti S, et al. 2013. Endogenous retrotransposition activates oncogenic pathways in hepatocellular carcinoma. Cell 153: 101-111.
88. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050. (Pubitemid 41126859)
89. Simon MD, Wang CI, Kharchenko PV, West JA, Chapman BA, Alekseyenko AA, Borowsky ML, Kuroda MI, Kingston RE. 2011. The genomic binding sites of a noncoding RNA. Proc Natl Acad Sci 108: 20497-20502.
90. Smith MA, Gesell T, Stadler PF, Mattick JS. 2013. Widespread purifying selection on RNA structure in mammals. Nucleic Acids Res 41: 8220-8236.
91. Spengler RM, Oakley CK, Davidson BL. 2014. Functional microRNAs and target sites are created by lineage-specific transposition. Hum Mol Genet 23: 1783-1793.
92. Tsai MC, 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.
93. 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. (Pubitemid 37421026)
94. van Bakel H, Nislow C, Blencowe BJ, Hughes TR. 2010. Most "dark matter" transcripts are associated with known genes. PLoS Biol 8: e1000371.
95. Wang Z, Willard HF, Mukherjee S, Furey TS. 2006. Evidence of influence of genomic DNA sequence on human X chromosome inactivation. PLoS Comput Biol 2: e113.
96. 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 non-coding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120-124.
97. Wang J, Gong C, Maquat LE. 2013a. Control of myogenesis by rodent SINE-containing lncRNAs. Genes Dev 27: 793-804.
98. Wang Y, Chen X, Liu ZP, Huang Q, Xu D, Zhang XS, Chen R, Chen L. 2013b. De novo prediction of RNA-protein interactions from sequence information. Mol Biosyst 9: 133-142.
99. Washietl S, Hofacker IL, Stadler PF. 2005. Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci 102: 2454-2459. (Pubitemid 40279397)
100. Washietl S, Kellis M, Garber M. 2014. Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res 24: 616-628.
101. Wutz A, Rasmussen TP, Jaenisch R. 2002. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 30: 167-174.
102. Yakovchuk P, Goodrich JA, Kugel JF. 2009. B2 RNA and Alu RNA repress transcription by disrupting contacts between RNA polymerase II and promoter DNA within assembled complexes. Proc Natl Acad Sci 106: 5569-5574.
103. Yang JH, Li JH, Shao P, Zhou H, Chen YQ, Qu LH. 2011. starBase: a database for exploring microRNA-mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data. Nucleic Acids Res 39: D202-D209.
104. York B, O'Malley BW. 2010. Steroid receptor coactivator (SRC) family: masters of systems biology. J Biol Chem 285: 38743-38750.
105. 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. (Pubitemid 40413388)
106. 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.
107. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415. (Pubitemid 37442169)