Ukr.Biochem.J. 2014; Volume 86, Issue 2, Mar-Apr, pp. 5-15

doi: http://dx.doi.org/10.15407/ubj86.02.005

Long non-coding rnas – “tuning fork” in regulation of cell processes

V. V. Gordiyuk

Insitute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, Kyiv;
e-mail: vasilij_gordiyuk@yahoo.com

Most of RNA transcripts, instead of serving templates for protein synthesis, perform different functions such as control of embryogenesis, differentiation, imprinting, X-chromosome inactivation, immune response, and stress reactions. A large portion of these RNAs are denoted as long non-coding RNAs (lncRNAs) which function as signaling molecules, navigating systems and platforms for ribonucleic complexes assembly. They also participate in the organization of specific cellular domains. Moreover, they are able to bind regulatory proteins and micro-RNAs, and serve as precursors for small RNAs. It was shown that lncRNAs participate in transcription regulation; they are also involved in alternative splicing, RNA editing, traffic, translation and degradation of RNA. The three-dimensional structure of lncRNAs plays a crucial role in processes of chromatin remodeling and transcription regulation. In this review we discuss various aspects of lncRNAs functioning.

Keywords: , , , , , ,


References:

  1. www.gencodegenes.org/releases/15.html
  2. Clark MB, Amaral PP, Schlesinger FJ, Dinger ME, Taft RJ, Rinn JL, Ponting CP, Stadler PF, Morris KV, Morillon A, Rozowsky JS, Gerstein MB, Wahlestedt C, Hayashizaki Y, Carninci P, Gingeras TR, Mattick JS. The reality of pervasive transcription. PLoS Biol. 2011 Jul;9(7):e1000625; discussion e1001102. PubMed, PubMedCentral, CrossRef
  3. Beiter T, Reich E, Williams RW, Simon P. Antisense transcription: a critical look in both directions. Cell Mol Life Sci. 2009 Jan;66(1):94-112. Review. PubMed, CrossRef
  4. Gibb EA, Brown CJ, Lam WL. The functional role of long non-coding RNA in human carcinomas. Mol Cancer. 2011 Apr 13;10:38. Review. PubMed, PubMedCentral, CrossRef
  5. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermüller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science. 2007 Jun 8;316(5830):1484-8. PubMed, CrossRef
  6. Lee JT. Epigenetic regulation by long noncoding RNAs. Science. 2012 Dec 14;338(6113):1435-9. Review. PubMed, CrossRef
  7. Maruyama R, Suzuki H, Yamamoto E, Imai K, Shinomura Y. Emerging links between epigenetic alterations and dysregulation of noncoding RNAs in cancer. Tumour Biol. 2012 Apr;33(2):277-85. Review. PubMed, CrossRef
  8. Clark MB, Johnston RL, Inostroza-Ponta M, Fox AH, Fortini E, Moscato P, Dinger ME, Mattick JS. Genome-wide analysis of long noncoding RNA stability. Genome Res. 2012 May;22(5):885-98.  PubMed, CrossRef
  9. 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. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature. 2011 Apr 7;472(7341):120-4. PubMed, PubMedCentral, CrossRef
  10. Harrison PM, Zheng D, Zhang Z, Carriero N, Gerstein M. Transcribed processed pseudogenes in the human genome: an intermediate form of expressed retrosequence lacking protein-coding ability. Nucleic Acids Res. 2005 Apr 28;33(8):2374-83. PubMedPubMedCentral, CrossRef
  11. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, Suzuki H, Carninci P, Hayashizaki Y, Wells C, Frith M, Ravasi T, Pang KC, Hallinan J, Mattick J, Hume DA, Lipovich L, Batalov S, Engström PG, Mizuno Y, Faghihi MA, Sandelin A, Chalk AM, Mottagui-Tabar S, Liang Z, Lenhard B, Wahlestedt C. Antisense transcription in the mammalian transcriptome. Science. 2005 Sep 2;309(5740):1564-6. PubMed
  12. Hung T, Wang Y, Lin MF, Koegel AK, Kotake Y, Grant GD, Horlings HM, Shah N, Umbricht C, Wang P, Wang Y, Kong B, Langerød A, Børresen-Dale AL, Kim SK, van de Vijver M, Sukumar S, Whitfield ML, Kellis M, Xiong Y, Wong DJ, Chang HY. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet. 2011 Jun 5;43(7):621-9. PubMed, PubMedCentral, CrossRef
  13. Suo G, Han J, Wang X, Zhang J, Zhao Y, Zhao Y, Dai J. Oct4 pseudogenes are transcribed in cancers. Biochem Biophys Res Commun. 2005 Dec 2;337(4):1047-51. PubMed, CrossRef
  14. Matouk I, Raveh E, Ohana P, Lail RA, Gershtain E, Gilon M, De Groot N, Czerniak A, Hochberg A. The increasing complexity of the oncofetal h19 gene locus: functional dissection and therapeutic intervention. Int J Mol Sci. 2013 Feb 21;14(2):4298-316. PubMed, PubMedCentral, CrossRef
  15. Lee JT. The X as model for RNA’s niche in epigenomic regulation. Cold Spring Harb Perspect Biol. 2010 Sep;2(9):a003749. Review. PubMed, PubMedCentral, CrossRef
  16. Kapusta A, Kronenberg Z, Lynch VJ, Zhuo X, Ramsay L, Bourque G, Yandell M, Feschotte C. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 2013 Apr;9(4):e1003470. PubMed, PubMedCentral, CrossRef
  17. Niland CN, Merry CR, Khalil AM. Emerging Roles for Long Non-Coding RNAs in Cancer and Neurological Disorders. Front Genet. 2012 Feb 27;3:25. eCollection 2012. PubMed, PubMedCentral, CrossRef
  18. Ingolia NT, Lareau LF, Weissman JS. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell. 2011 Nov 11;147(4):789-802. PubMed, PubMedCentral, CrossRef
  19. Gong C, Maquat LE. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature. 2011 Feb 10;470(7333):284-8. PubMed, PubMedCentral, CrossRef
  20. Novikova IV, Hennelly SP, Sanbonmatsu KY. Sizing up long non-coding RNAs: do lncRNAs have secondary and tertiary structure? Bioarchitecture. 2012 Nov-Dec;2(6):189-99. Review. PubMed, PubMedCentral, CrossRef
  21. Redon S, Reichenbach P, Lingner J. The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res. 2010 Sep;38(17):5797-806. PubMed, PubMedCentral, CrossRef
  22. Sampl S, Pramhas S, Stern C, Preusser M, Marosi C, Holzmann K. Expression of telomeres in astrocytoma WHO grade 2 to 4: TERRA level correlates with telomere length, telomerase activity, and advanced clinical grade. Transl Oncol. 2012 Feb;5(1):56-65. PubMed, PubMedCentral, CrossRef
  23. Feuerhahn S, Iglesias N, Panza A, Porro A, Lingner J. TERRA biogenesis, turnover and implications for function. FEBS Lett. 2010 Sep 10;584(17):3812-8. Review. PubMed, CrossRef
  24. Guttman M, Rinn JL. Modular regulatory principles of large non-coding RNAs. Nature. 2012 Feb 15;482(7385):339-46. Review. PubMed, PubMedCentral, CrossRef
  25. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81:145-66. Review. PubMed, PubMedCentral, CrossRef
  26. Louro R, El-Jundi T, Nakaya HI, Reis EM, Verjovski-Almeida S. Conserved tissue expression signatures of intronic noncoding RNAs transcribed from human and mouse loci. Genomics. 2008 Jul;92(1):18-25. PubMed, CrossRef
  27. Guil S, Soler M, Portela A, Carrère J, Fonalleras E, Gómez A, Villanueva A, Esteller M. Intronic RNAs mediate EZH2 regulation of epigenetic targets. Nat Struct Mol Biol. 2012 Jun 3;19(7):664-70. PubMed, CrossRef
  28. Lee C, Kikyo N. Strategies to identify long noncoding RNAs involved in gene regulation. Cell Biosci. 2012 Nov 6;2(1):37. PubMed, PubMedCentral, CrossRef
  29. Yap KL, Li S, Muñoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell. 2010 Jun 11;38(5):662-74. PubMed, PubMedCentral, CrossRef
  30. Kotake Y, Nakagawa T, Kitagawa K, Suzuki S, Liu N, Kitagawa M, Xiong Y. Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene. 2011 Apr 21;30(16):1956-62. PubMed, PubMedCentral, CrossRef
  31. Zhu Y, Rowley MJ, Böhmdorfer G, Wierzbicki AT. A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol Cell. 2013 Jan 24;49(2):298-309. PubMed, PubMedCentral, CrossRef
  32. 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. RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell. 2012 Feb 17;148(4):664-78. PubMed, PubMedCentral, CrossRef
  33. Maenner S, Blaud M, Fouillen L, Savoye A, Marchand V, Dubois A, Sanglier-Cianférani S, Van Dorsselaer A, Clerc P, Avner P, Visvikis A, Branlant C. 2-D structure of the A region of Xist RNA and its implication for PRC2 association. PLoS Biol. 2010 Jan;8(1):e1000276. PubMed, PubMedCentral, CrossRef
  34. Jeon Y, Lee JT. YY1 tethers Xist RNA to the inactive X nucleation center. Cell. 2011 Jul 8;146(1):119-33. PubMed, PubMedCentral, CrossRef
  35. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 2007 Jun 29;129(7):1311-23. PubMed, PubMedCentral
  36. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY. Long noncoding RNA as modular scaffold of histone modification complexes. Science. 2010 Aug 6;329(5992):689-93. PubMed, PubMedCentral, CrossRef
  37. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT. Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell. 2010 Dec 22;40(6):939-53. PubMed, PubMedCentral, CrossRef
  38. Mohammad F, Mondal T, Guseva N, Pandey GK, Kanduri C. Kcnq1ot1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1. Development. 2010 Aug 1;137(15):2493-9. PubMed, CrossRef
  39. Schmitz KM, 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. 2010 Oct 15;24(20):2264-9. PubMed, PubMedCentral, CrossRef
  40. Balik V, Srovnal J, Sulla I, Kalita O, Foltanova T, Vaverka M, Hrabalek L, Hajduch M. MEG3: a novel long noncoding potentially tumour-suppressing RNA in meningiomas. J Neurooncol. 2013 Mar;112(1):1-8. Review. PubMed, CrossRef
  41. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP. Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal. 2010 Feb 2;3(107):ra8. PubMed, PubMedCentral, CrossRef
  42. Bhan A, Hussain I, Ansari KI, Kasiri S, Bashyal A, Mandal SS. Antisense transcript long noncoding RNA (lncRNA) HOTAIR is transcriptionally induced by estradiol. J Mol Biol. 2013 Oct 9;425(19):3707-22. PubMed, PubMedCentral, CrossRef
  43. Xu B, Gerin I, Miao H, Vu-Phan D, Johnson CN, Xu R, Chen XW, Cawthorn WP, MacDougald OA, Koenig RJ. Multiple roles for the non-coding RNA SRA in regulation of adipogenesis and insulin sensitivity. PLoS One. 2010 Dec 2;5(12):e14199. PubMed, PubMedCentral, CrossRef
  44. Ulveling D, Francastel C, Hubé F. When one is better than two: RNA with dual functions. Biochimie. 2011 Apr;93(4):633-44. Review. PubMed, CrossRef
  45. Lin CY, Huang TY, Shih HC, Yuan CH, Chen LJ, Tsai HS, Pan CH, Chiang HM, Liu HL, Su WC, Wu KT, Chao CH, Huang NE, Yang KD, Hsieh HM, Tsai LC, Linacre A, Yu YJ, Lin YY, Chu PC, Lee JC. The strategies to DVI challenges in Typhoon Morakot. Int J Legal Med. 2011 Sep;125(5):637-41. PubMed, CrossRef
  46. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, Markenscoff-Papadimitriou E, Kuhl D, Bito H, Worley PF, Kreiman G, Greenberg ME. Widespread transcription at neuronal activity-regulated enhancers. Nature. 2010 May 13;465(7295):182-7. PubMed, PubMedCentral, CrossRef
  47. Hudson RS, Yi M, Volfovsky N, Prueitt RL, Esposito D, Volinia S, Liu CG, Schetter AJ, Van Roosbroeck K, Stephens RM, Calin GA, Croce CM, Ambs S. Transcription signatures encoded by ultraconserved genomic regions in human prostate cancer. Mol Cancer. 2013 Feb 14;12:13.  PubMed, PubMedCentral, CrossRef
  48. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA, Blencowe BJ, Prasanth SG, Prasanth KV. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell. 2010 Sep 24;39(6):925-38. PubMed, PubMedCentral, CrossRef
  49. Hutchinson JN, Ensminger AW, Clemson CM, Lynch CR, Lawrence JB, Chess A. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genomics. 2007 Feb 1;8:39. PubMed, PubMedCentral
  50. Bernard D, Prasanth KV, Tripathi V, Colasse S, Nakamura T, Xuan Z, Zhang MQ, Sedel F, Jourdren L, Coulpier F, Triller A, Spector DL, Bessis A. A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J. 2010 Sep 15;29(18):3082-93. PubMed, PubMedCentral, CrossRef
  51. Morrissy AS, Griffith M, Marra MA. Extensive relationship between antisense transcription and alternative splicing in the human genome. Genome Res. 2011 Aug;21(8):1203-12. PubMed, PubMedCentral, CrossRef
  52. Zhang X, Rice K, Wang Y, Chen W, Zhong Y, Nakayama Y, Zhou Y, Klibanski A. Maternally expressed gene 3 (MEG3) noncoding ribonucleic acid: isoform structure, expression, and functions. Endocrinology. 2010 Mar;151(3):939-47. PubMed, PubMedCentral, CrossRef
  53. Nagano T, Fraser P. No-nonsense functions for long noncoding RNAs. Cell. 2011 Apr 15;145(2):178-81. Review. PubMed, CrossRef
  54. Mao YS, Sunwoo H, Zhang B, Spector DL. Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs. Nat Cell Biol. 2011 Jan;13(1):95-101. Epub 2010 Dec 19. PubMed, PubMedCentral, CrossRef
  55. Naganuma T, Hirose T. Paraspeckle formation during the biogenesis of long non-coding RNAs. RNA Biol. 2013 Mar;10(3):456-61. Review. PubMed, PubMedCentral, CrossRef
  56. Chen LL, Carmichael GG. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. Mol Cell. 2009 Aug 28;35(4):467-78. PubMed, PubMedCentral, CrossRef
  57. Sie CP, Kuchka M. RNA editing adds flavor to complexity. Biochemistry (Mosc). 2011 Aug;76(8):869-81. Review. PubMed, CrossRef
  58. Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Tsutui K, Nakagawa S. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev Cell. 2010 Sep 14;19(3):469-76. PubMed, CrossRef
  59. Ip JY, Nakagawa S. Long non-coding RNAs in nuclear bodies. Dev Growth Differ. 2012 Jan;54(1):44-54. Review. PubMed, CrossRef
  60. Hagan JP, O’Neill BL, Stewart CL, Kozlov SV, Croce CM. At least ten genes define the imprinted Dlk1-Dio3 cluster on mouse chromosome 12qF1. PLoS One. 2009;4(2):e4352. PubMed, PubMedCentral, CrossRef
  61. Wilusz JE, Freier SM, Spector DL. 3′ end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell. 2008 Nov 28;135(5):919-32. PubMed, PubMedCentral, CrossRef
  62. Redfern AD, Colley SM, Beveridge DJ, Ikeda N, Epis MR, Li X, Foulds CE, Stuart LM, Barker A, Russell VJ, Ramsay K, Kobelke SJ, Li X, Hatchell EC, Payne C, Giles KM, Messineo A, Gatignol A, Lanz RB, O’Malley BW, Leedman PJ. RNA-induced silencing complex (RISC) Proteins PACT, TRBP, and Dicer are SRA binding nuclear receptor coregulators. Proc Natl Acad Sci USA. 2013 Apr 16;110(16):6536-41. PubMed, PubMedCentral, CrossRef
  63. Xing L, Kieff E. Epstein-Barr virus BHRF1 micro- and stable RNAs during latency III and after induction of replication. J Virol. 2007 Sep;81(18):9967-75. PubMed, PubMedCentral, CrossRef
  64. Cai X, Cullen BR. The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA. 2007 Mar;13(3):313-6. PubMed, PubMedCentral
  65. Keniry A, Oxley D, Monnier P, Kyba M, Dandolo L, Smits G, Reik W. The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nat Cell Biol. 2012 Jun 10;14(7):659-65. PubMed, PubMedCentral, CrossRef
  66. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature. 2008 May 22;453(7194):534-8. PubMed, PubMedCentral, CrossRef
  67. Mourtada-Maarabouni M, Pickard MR, Hedge VL, Farzaneh F, Williams GT. GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene. 2009 Jan 15;28(2):195-208. PubMed, CrossRef
  68. da Rocha ST, Edwards CA, Ito M, Ogata T, Ferguson-Smith AC. Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet. 2008 Jun;24(6):306-16. Review. PubMed, CrossRef
  69. Poliseno L, Haimovic A, Christos PJ, Vega Y Saenz de Miera EC, Shapiro R, Pavlick A, Berman RS, Darvishian F, Osman I. Deletion of PTENP1 pseudogene in human melanoma. J Invest Dermatol. 2011 Dec;131(12):2497-500. PubMed, CrossRef
  70. Muro EM, Mah N, Andrade-Navarro MA. Functional evidence of post-transcriptional regulation by pseudogenes. Biochimie. 2011 Nov;93(11):1916-21. Review. PubMed, CrossRef
  71. Faghihi MA, Zhang M, Huang J, Modarresi F, Van der Brug MP, Nalls MA, Cookson MR, St-Laurent G 3rd, Wahlestedt C. Evidence for natural antisense transcript-mediated inhibition of microRNA function. Genome Biol. 2010;11(5):R56. PubMed, PubMedCentral, CrossRef
  72. Wang J, Liu X, Wu H, Ni P,  Gu Z, Qiao Y, Chen N, Sun F, Fan Q. CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res. 2010 Sep; 38(16): 5366-5383. PubMed, PubMedCentral, CrossRef
  73. Chiefari E, Iiritano S, Paonessa F, Le Pera I, Arcidiacono B, Filocamo M, Foti D, Liebhaber SA, Brunetti A. Pseudogene-mediated posttranscriptional silencing of HMGA1 can result in insulin resistance and type 2 diabetes. Nat Commun. 2010 Jul 27;1:40. PubMed, CrossRef
  74. Yoon JH, Abdelmohsen K, Srikantan S, Yang X, Martindale JL, De S, Huarte M, Zhan M, Becker KG, Gorospe M. LincRNA-p21 suppresses target mRNA translation. Mol Cell. 2012 Aug 24;47(4):648-55. PubMed, PubMedCentral, CrossRef
  75. Korneev SA, Kemenes I, Bettini NL, Kemenes G, Staras K, Benjamin PR, O’Shea M. Axonal trafficking of an antisense RNA transcribed from a pseudogene is regulated by classical conditioning. Sci Rep. 2013;3:1027. PubMed, PubMedCentral, CrossRef
  76. Ebralidze AK, Guibal FC, Steidl U, Zhang P, Lee S, Bartholdy B, Jorda MA, Petkova V, Rosenbauer F, Huang G, Dayaram T, Klupp J, O’Brien KB, Will B, Hoogenkamp M, Borden KL, Bonifer C, Tenen DG. PU.1 expression is modulated by the balance of functional sense and antisense RNAs regulated by a shared cis-regulatory element. Genes Dev. 2008 Aug 1;22(15):2085-92. PubMed, PubMedCentral, CrossRef
  77. Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 2009 Jul 1;23(13):1494-504. Review. PubMed, PubMedCentral, CrossRef
  78. Ding DQ, Okamasa K, Yamane M, Tsutsumi C, Haraguchi T, Yamamoto M, Hiraoka Y. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis. Science. 2012 May 11;336(6082):732-6. PubMed, CrossRef
  79. Shamovsky I, Nudler E. Isolation and characterization of the heat shock RNA 1. Methods Mol Biol. 2009;540:265-79. PubMed, PubMedCentral, CrossRef
  80. Mariner PD, Walters RD, Espinoza CA, Drullinger LF, Wagner SD, Kugel JF, Goodrich JA. Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol Cell. 2008 Feb 29;29(4):499-509. PubMed, CrossRef
  81. Batista PJ, Chang HY. Cytotopic localization by long noncoding RNAs. Curr Opin Cell Biol. 2013 Apr;25(2):195-9. Review. PubMed, PubMedCentral, CrossRef
  82. Nakagawa S, Naganuma T, Shioi G, Hirose T. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J Cell Biol. 2011 Apr 4;193(1):31-9. PubMed, PubMedCentral, CrossRef
  83. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, Lander ES, Jacks T, Rinn JL. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell. 2010 Aug 6;142(3):409-19. PubMed, PubMedCentral, CrossRef
  84. Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK, Kurokawa R. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature. 2008 Jul 3;454(7200):126-30.  PubMed, PubMedCentral, CrossRef
  85. Song X, Wang X, Arai S, Kurokawa R. Promoter-associated noncoding RNA from the CCND1 promoter. Methods Mol Biol. 2012;809:609-22. PubMed, CrossRef
  86. Peng X, Gralinski L, Armour CD, Ferris MT, Thomas MJ, Proll S, Bradel-Tretheway BG, Korth MJ, Castle JC, Biery MC, Bouzek HK, Haynor DR, Frieman MB, Heise M, Raymond CK, Baric RS, Katze MG. Unique signatures of long noncoding RNA expression in response to virus infection and altered innate immune signaling. MBio. 2010 Oct 26;1(5). pii: e00206-10. PubMed, PubMedCentral, CrossRef
  87. Tycowski KT, Shu MD, Borah S, Shi M, Steitz JA. Conservation of a triple-helix-forming RNA stability element in noncoding and genomic RNAs of diverse viruses. Cell Rep. 2012 Jul 26;2(1):26-32. PubMed, PubMedCentral, CrossRef
  88. Herquel B, Ouararhni K, Martianov I, Le Gras S, Ye T, Keime C, Lerouge T, Jost B, Cammas F, Losson R, Davidson I. Trim24-repressed VL30 retrotransposons regulate gene expression by producing noncoding RNA. Nat Struct Mol Biol. 2013 Mar;20(3):339-46. PubMed, CrossRef
  89. Zhang Q, Chen CY, Yedavalli VS, Jeang KT. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio. 2013 Jan 29;4(1):e00596-12. PubMed, PubMedCentral, CrossRef
  90. Sharma S, Findlay GM, Bandukwala HS, Oberdoerffer S, Baust B, Li Z, Schmidt V, Hogan PG, Sacks DB, Rao A. Dephosphorylation of the nuclear factor of activated T cells (NFAT) transcription factor is regulated by an RNA-protein scaffold complex. Proc Natl Acad Sci USA. 2011 Jul 12;108(28):11381-6. PubMed, PubMedCentral, CrossRef
  91. Sigova AA, Mullen AC, Molinie B, Gupta S, Orlando DA, Guenther MG, Almada AE, Lin C, Sharp PA, Giallourakis CC, Young RA. Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc Natl Acad Sci USA. 2013 Feb 19;110(8):2876-81. PubMed, PubMedCentral, CrossRef
  92. Sheik Mohamed J, Gaughwin PM, Lim B, Robson P, Lipovich L. Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA. 2010 Feb;16(2):324-37. PubMed, PubMedCentral, CrossRef
  93. Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH, Garber M, Curran M, Onder T, Agarwal S, Manos PD, Datta S, Lander ES, Schlaeger TM, Daley GQ, Rinn JL. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet. 2010 Dec;42(12):1113-7.  PubMed, PubMedCentral, CrossRef
  94. Ghosal S, Das S, Chakrabarti J. Long noncoding RNAs: new players in the molecular mechanism for maintenance and differentiation of pluripotent stem cells. Stem Cells Dev. 2013 Aug 15;22(16):2240-53.  Review.PubMed, PubMedCentral, CrossRef
  95. Hawkins PG, Morris KV. Transcriptional regulation of Oct4 by a long non-coding RNA antisense to Oct4-pseudogene 5. Transcription. 2010 Nov;1(3):165-175. PubMed, PubMedCentral
  96. Zhao S, Yuan Q, Hao H, Guo Y, Liu S, Zhang Y, Wang J, Liu H, Wang F, Liu K, Ling EA, Hao A. Expression of OCT4 pseudogenes in human tumours: lessons from glioma and breast carcinoma. J Pathol. 2011 Apr;223(5):672-82.  PubMed, CrossRef
  97. 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. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature. 2011 Aug 28;477(7364):295-300. PubMed, PubMedCentral, CrossRef
  98. Ng SY, Johnson R, Stanton LW. Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J. 2012 Feb 1;31(3):522-33.  PubMed, PubMedCentral, CrossRef
  99. Wu SC, Kallin EM, Zhang Y. Role of H3K27 methylation in the regulation of lncRNA expression. Cell Res. 2010 Oct;20(10):1109-16. PubMed, PubMedCentral, CrossRef
  100. Maass PG, Rump A, Schulz H, Stricker S, Schulze L, Platzer K, Aydin A, Tinschert S, Goldring MB, Luft FC, Bähring S. A misplaced lncRNA causes brachydactyly in humans. J Clin Invest. 2012 Nov;122(11):3990-4002.  PubMed, PubMedCentral, CrossRef
  101. Bright AT, Winzeler EA. Noncoding RNA, antigenic variation, and the virulence genes of Plasmodium falciparum. BMC Biol. 2011 Jul 19;9:50. PubMedPubMedCentral, CrossRef
  102. Tautz D, Domazet-Lošo T. The evolutionary origin of orphan genes. Nat Rev Genet. 2011 Aug 31;12(10):692-702. Review. PubMed, CrossRef

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