Non-coding RNAs: Multi-tasking molecules in the cell

International Journal of Molecular Sciences

Volumn 14, Issue 8, 2013, Pages 16010-16039

  Gomes, Anita Quintal ^a,b   Nolasco, Sofia ^a,c,d   Soares, Helena ^a,b,c  

^a INSTITUTO POLITÉCNICO DE LISBOA   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^d FACULDADE DE MEDICINA VETERINÁRIA   (Portugal)

Author keywords

Epigenetic regulation; Gene expression regulation; lncRNAs; miRNAs; piRNAs; siRNAs; sncRNAs

Indexed keywords

LONG UNTRANSLATED RNA; MICRORNA; PIWI INTERACTING RNA; SMALL INTERFERING RNA; UNTRANSLATED RNA;

BIOGENESIS; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELLULAR DISTRIBUTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; GENE SILENCING; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN RNA BINDING; REVIEW; RNA SYNTHESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; CELL DIFFERENTIATION; DROSOPHILA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; HUMANS; MICRORNAS; NEOPLASMS; RNA, CATALYTIC; RNA, LONG NONCODING; RNA, SMALL INTERFERING;

EID: 84881170401     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140816010     Document Type: Review

References (187)

1. Cech, T.R.; Zaug, A.J.; Grabowski, P.J. In vitro splicing of the ribosomal RNA precursor of Tetrahymena: Involvement of a guanosine nucleotide in the excision of the intervening sequence. Cell 1981, 27, 487-496.
2. Guerrier-Takada, C.; Gardiner, K.; Marsh, T.; Pace, N.; Altman, S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 1983, 35, 849-857.
3. Dworkin, J.P.; Lazcano, A.; Miller, S.L. The roads to and from the RNA world. J. Theor. Boil. 2003, 222, 127-134.
4. Lehman, N. RNA in evolution. Wiley Interdiscip. Rev. 2010, 1, 202-213.
5. Noller, H.F.; Hoffarth, V.; Zimniak, L. Unusual resistance of peptidyl transferase to protein extraction procedures. Science 1992, 256, 1416-1419.
6. Von Ahsen, U.; Noller, H.F. Identification of bases in 16S rRNA essential for tRNA binding at the 30S ribosomal P site. Science 1995, 267, 234-237.
7. Moazed, D.; Noller, H.F. Sites of interaction of the CCA end of peptidyl-tRNA with 23S rRNA. Proc. Natl. Acad. Sci.USA 1991, 88, 3725-3728.
8. Wassarman, D.A.; Steitz, J.A. Interactions of small nuclear RNA's with precursor messenger RNA during in vitro splicing. Science 1992, 257, 1918-1925.
9. Brennicke, A.; Marchfelder, A.; Binder, S. RNA editing. FEMS Microbial. Rev 1999, 23, 297-316.
10. Bachellerie, J.P.; Cavaille, J.; Huttenhofer, A. The expanding snoRNA world. Biochimie 2002, 84, 775-790.
11. Greider, C.W.; Blackburn, E.H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 1985, 43, 405-413.
12. Greider, C.W.; Blackburn, E.H. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 1989, 337, 331-337.
13. Qiao, F.; Cech, T.R. Triple-helix structure in telomerase RNA contributes to catalysis. Nat. Struct. Mol. Boil. 2008, 15, 634-640.
14. Birney, E.; Stamatoyannopoulos, J.A.; Dutta, A.; Guigo, R.; Gingeras, T.R.; Margulies, E.H.; Weng, Z.; Snyder, M.; Dermitzakis, E.T.; Thurman, R.E.; et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447, 799-816.
15. Mattick, J.S.; Makunin, I.V. Non-coding RNA. Hum. Mol. Genet. 2006, 15, R17-R29.
16. Moazed, D. Small RNAs in transcriptional gene silencing and genome defence. Nature 2009, 457, 413-420.
17. Eliceiri, G.L. Small nucleolar RNAs. Cell. Mol. Life Sci. 1999, 56, 22-31.
18. Mannoor, K.; Liao, J.; Jiang, F. Small nucleolar RNAs in cancer. Biochim. Biophys. Acta 2012, 1826, 121-128.
19. Lee, R.C.; Feinbaum, R.L.; Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75, 843-854.
20. Reinhart, B.J.; Slack, F.J.; Basson, M.; Pasquinelli, A.E.; Bettinger, J.C.; Rougvie, A.E.; Horvitz, H.R.; Ruvkun, G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403, 901-906.
21. Meister, G.; Tuschl, T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431, 343-349.
22. Jinek, M.; Doudna, J.A. A three-dimensional view of the molecular machinery of RNA interference. Nature 2009, 457, 405-412.
23. Michlewski, G.; Guil, S.; Semple, C.A.; Cáceres, J.F. Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol. Cell 2008, 7, 383-393.
24. Zeng, Y.; Cullen, B.R. Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res. 2004, 32, 4776-4785.
25. Berezikov, E.; Chung, W.J.; Willis, J.; Cuppen, E.; Lai, E.C. Mammalian mirtron genes. Mol. Cell 2007, 28, 328-336.
26. Farazi, T.A.; Juranek, S.A.; Tuschl, T. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 2008, 135, 1201-1214.
27. Forstemann, K.; Horwich, M.D.; Wee, L.; Tomari, Y.; Zamore, P.D. Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 2007, 130, 287-297.
28. Tomari, Y.; Du, T.; Zamore, P.D. Sorting of Drosophila small silencing RNAs. Cell 2007, 130, 299-308.
29. Ameres, S.L.; Horwich, M.D.; Hung, J.H.; Xu, J.; Ghildiyal, M.; Weng, Z.; Zamore, P.D. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010, 328, 1534-1539.
30. Heo, I.; Ha, M.; Lim, J.; Yoon, M.J.; Park, J.E.; Kwon, S.C.; Chang, H.; Kim, V.N. Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs. Cell 2012, 151, 521-532.
31. Khvorova, A.; Reynolds, A.; Jayasena, S.D. Functional siRNAs and miRNAs exhibit strand bias. Cell 2003, 115, 209-216.
32. Siomi, H.; Siomi, M.C. On the road to reading the RNA-interference code. Nature 2009, 457, 396-404.
33. Fukunaga, R.; Han, B.W.; Hung, J.H.; Xu, J.; Weng, Z.; Zamore, P.D. Dicer partner proteins tune the length of mature miRNAs in flies and mammals. Cell 2012, 151, 533-546.
34. Lee, H.Y.; Doudna, J.A. TRBP alters human precursor microRNA processing in vitro. RNA 2012, 18, 2012-2019.
35. Grewal, S.I.; Elgin, S.C. Transcription and RNA interference in the formation of heterochromatin. Nature 2007, 447, 399-406.
36. Verdel, A.; Jia, S.; Gerber, S.; Sugiyama, T.; Gygi, S.; Grewal, S.I.; Moazed, D. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 2004, 303, 672-676.
37. Creamer, K.M.; Partridge, J.F. RITS-connecting transcription, RNA interference, and heterochromatin assembly in fission yeast. Wiley Interdiscip. Rev. 2011, 2, 632-646.
38. Aravin, A.A.; Lagos-Quintana, M.; Yalcin, A.; Zavolan, M.; Marks, D.; Snyder, B.; Gaasterland, T.; Meyer, J.; Tuschl, T. The small RNA profile during Drosophila melanogaster development. Dev. cell 2003, 5, 337-350.
39. Lau, N.C.; Seto, A.G.; Kim, J.; Kuramochi-Miyagawa, S.; Nakano, T.; Bartel, D.P.; Kingston, R.E. Characterization of the piRNA complex from rat testes. Science 2006, 313, 363-367.
40. Aravin, A.A.; Hannon, G.J.; Brennecke, J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007, 318, 761-764.
41. Brennecke, J.; Aravin, A.A.; Stark, A.; Dus, M.; Kellis, M.; Sachidanandam, R.; Hannon, G.J., Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128, 1089-1103.
42. Houwing, S.; Kamminga, L.M.; Berezikov, E.; Cronembold, D.; Girard, A.; van den Elst, H.; Filippov, D.V.; Blaser, H.; Raz, E.; Moens, C.B.; et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 2007, 129, 69-82.
43. Robine, N.; Lau, N.C.; Balla, S.; Jin, Z.; Okamura, K.; Kuramochi-Miyagawa, S.; Blower, M.D.; Lai, E.C. A broadly conserved pathway generates 3' UTR-directed primary piRNAs. Curr. Biol. 2009, 19, 2066-2076.
44. Khurana, J.S.; Theurkauf, W. piRNAs, transposon silencing, and Drosophila germline development. J. Cell Biol. 2010, 191, 905-913.
45. Chen, Y.; Pane, A.; Schupbach, T. Cutoff and aubergine mutations result in retrotransposon upregulation and checkpoint activation in Drosophila. Curr. Biol. 2007, 17, 637-642.
46. Khurana, J.S.; Xu, J.; Weng, Z.; Theurkauf, W.E. Distinct functions for the Drosophila piRNA pathway in genome maintenance and telomere protection. PLoS Genet. 2010, 6, e1001246.
47. Gunawardane, L.S.; Saito, K.; Nishida, K.M.; Miyoshi, K.; Kawamura, Y.; Nagami, T.; Siomi, H.; Siomi, M.C. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 2007, 315, 1587-1590.
48. Ishizu, H.; Siomi, H.; Siomi, M.C. Biology of PIWI-interacting RNAs: New insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012, 26, 2361-2373.
49. Yan, B.X.; Ma, J.X. Promoter-associated RNAs and promoter-targeted RNAs. Cell. Mol. Life Sci. 2012, 69, 2833-2842.
50. Rouget, C.; Papin, C.; Boureux, A.; Meunier, A.C.; Franco, B.; Robine, N.; Lai, E.C.; Pelisson, A.; Simonelig, M. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 2010, 467, 1128-1132.
51. Lee, E.J.; Banerjee, S.; Zhou, H.; Jammalamadaka, A.; Arcila, M.; Manjunath, B.S.; Kosik, K.S. Identification of piRNAs in the central nervous system. RNA 2011, 17, 1090-1099.
52. Rajasethupathy, P.; Antonov, I.; Sheridan, R.; Frey, S.; Sander, C.; Tuschl, T.; Kandel, E.R. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 2012, 149, 693-707.
53. Sienski, G.; Donertas, D.; Brennecke, J. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 2012, 151, 964-980.
54. Watanabe, T.; Tomizawa, S.; Mitsuya, K.; Totoki, Y.; Yamamoto, Y.; Kuramochi-Miyagawa, S.; Iida, N.; Hoki, Y.; Murphy, P.J.; Toyoda, A.; et al. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 2011, 332, 848-852.
55. Gangaraju, V.K.; Yin, H.; Weiner, M.M.; Wang, J.; Huang, X.A.; Lin, H. Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nat. genet. 2011, 43, 153-158.
56. Rutherford, S.L.; Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 1998, 396, 336-342.
57. Specchia, V.; Piacentini, L.; Tritto, P.; Fanti, L.; D'Alessandro, R.; Palumbo, G.; Pimpinelli, S.; Bozzetti, M.P. Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 2010, 463, 662-665.
58. Kim, V.N. Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev. 2006, 20, 1993-1997.
59. Siddiqi, S.; Matushansky, I. Piwis and piwi-interacting RNAs in the epigenetics of cancer. J. Cell. Biochem. 2012, 113, 373-380.
60. Siddiqi, S.; Terry, M.; Matushansky, I. Hiwi mediated tumorigenesis is associated with DNA hypermethylation. PLoS One 2012, 7, e33711.
61. Prescott, D.M., The DNA of ciliated protozoa. Microbiol. Rev. 1994, 58, 233-267.
62. Chalker, D.L. Dynamic nuclear reorganization during genome remodeling of Tetrahymena. Biochim. Biophys. Acta 2008, 1783, 2130-2136.
63. Duharcourt, S.; Lepere, G.; Meyer, E. Developmental genome rearrangements in ciliates: A natural genomic subtraction mediated by non-coding transcripts. Trends Genet. 2009, 25, 344-350.
64. Lee, J.T. Epigenetic regulation by long noncoding RNAs. Science 2012, 338, 1435-1439.
65. Pink, R.C.; Wicks, K.; Caley, D.P.; Punch, E.K.; Jacobs, L.; Carter, D.R. Pseudogenes: Pseudo-functional or key regulators in health and disease? RNA 2011, 17, 792-798.
66. Rackham, O.; Shearwood, A.M.; Mercer, T.R.; Davies, S.M.; Mattick, J.S.; Filipovska, A. Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA 2011, 17, 2085-2093.
67. Carninci, P.; Kasukawa, T.; Katayama, S.; Gough, J.; Frith, M.C.; Maeda, N.; Oyama, R.; Ravasi, T.; Lenhard, B.; Wells, C.; et al. The transcriptional landscape of the mammalian genome. Science 2005, 309, 1559-1563.
68. Kapranov, P.; Cheng, J.; Dike, S.; Nix, D.A.; Duttagupta, R.; Willingham, A.T.; Stadler, P.F.; Hertel, J.; Hackermuller, J.; Hofacker, I.L.; et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 2007, 316, 1484-1488.
69. Magistri, M.; Faghihi, M.A.; St Laurent, G., 3rd; Wahlestedt, C. Regulation of chromatin structure by long noncoding RNAs: Focus on natural antisense transcripts. Trends Genet. 2012, 28, 389-396.
70. Guttman, M.; Amit, I.; Garber, M.; French, C.; Lin, M.F.; Feldser, D.; Huarte, M.; Zuk, O.; Carey, B.W.; Cassady, J.P.; et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458, 223-227.
71. Orom, U.A.; Derrien, T.; Beringer, M.; Gumireddy, K.; Gardini, A.; Bussotti, G.; Lai, F.; Zytnicki, M.; Notredame, C.; Huang, Q.; et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 2010, 143, 46-58.
72. Kim, T.K.; Hemberg, M.; Gray, J.M.; Costa, A.M.; Bear, D.M.; Wu, J.; Harmin, D.A.; Laptewicz, M.; Barbara-Haley, K.; Kuersten, S.; et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465, 182-187.
73. Katayama, S.; Tomaru, Y.; Kasukawa, T.; Waki, K.; Nakanishi, M.; Nakamura, M.; Nishida, H.; Yap, C.C.; Suzuki, M.; Kawai, J.; et al. Antisense transcription in the mammalian transcriptome. Science 2005, 309, 1564-1566.
74. Korneev, S.A.; Korneeva, E.I.; Lagarkova, M.A.; Kiselev, S.L.; Critchley, G.; O'Shea, M. Novel noncoding antisense RNA transcribed from human anti-NOS2A locus is differentially regulated during neuronal differentiation of embryonic stem cells. RNA 2008, 14, 2030-2037.
75. Lavorgna, G.; Dahary, D.; Lehner, B.; Sorek, R.; Sanderson, C.M.; Casari, G. In search of antisense. Trends Biochem. Sci. 2004, 29, 88-94.
76. Werner, A.; Carlile, M.; Swan, D. What do natural antisense transcripts regulate? RNA Biol. 2009, 6, 43-48.
77. He, Y.; Vogelstein, B.; Velculescu, V.E.; Papadopoulos, N.; Kinzler, K.W. The antisense transcriptomes of human cells. Science 2008, 322, 1855-1857.
78. Ravasi, T.; Suzuki, H.; Pang, K.C.; Katayama, S.; Furuno, M.; Okunishi, R.; Fukuda, S.; Ru, K.; Frith, M.C.; Gongora, M.M.; et al. Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. Genome Res. 2006, 16, 11-19.
79. Clemson, C.M.; Hutchinson, J.N.; Sara, S.A.; Ensminger, A.W.; Fox, A.H.; Chess, A.; Lawrence, J.B. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell 2009, 33, 717-726.
80. 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 2008, 322, 750-756.
81. Cai, X.; Cullen, B.R. The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 2007, 13, 313-316.
82. Hung, T.; Chang, H.Y. Long noncoding RNA in genome regulation: Prospects and mechanisms. RNA Biol. 2010, 7, 582-585.
83. Mohammad, F.; Mondal, T.; Guseva, N.; Pandey, G.K.; Kanduri, C. Kcnq1ot1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1. Development 2010, 137, 2493-2499.
84. Tsai, M.C.; Manor, O.; Wan, Y.; Mosammaparast, N.; Wang, J.K.; Lan, F.; Shi, Y.; Segal, E.; Chang, H.Y. Long noncoding RNA as modular scaffold of histone modification complexes. Science 2010, 329, 689-693.
85. Swiezewski, S.; Liu, F.; Magusin, A.; Dean, C. Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature 2009, 462, 799-802.
86. Heo, J.B.; Sung, S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 2011, 331, 76-79.
87. Hung, T.; Wang, Y.; Lin, M.F.; Koegel, A.K.; Kotake, Y.; Grant, G.D.; Horlings, H.M.; Shah, N.; Umbricht, C.; Wang, P.; et al. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat. Genet. 2011, 43, 621-629.
88. 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 2011, 43, 1040-1046.
89. Khalil, A.M.; Guttman, M.; Huarte, M.; Garber, M.; Raj, A.; Rivea Morales, D.; Thomas, K.; Presser, A.; Bernstein, B.E.; van Oudenaarden, A.; et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. USA 2009, 106, 11667-11672.
90. Dinger, M.E.; Amaral, P.P.; Mercer, T.R.; Pang, K.C.; Bruce, S.J.; Gardiner, B.B.; Askarian-Amiri, M.E.; Ru, K.; Solda, G.; Simons, C.; et al. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 2008, 18, 1433-1445.
91. Cabili, M.N.; Trapnell, C.; Goff, L.; Koziol, M.; Tazon-Vega, B.; Regev, A.; Rinn, J.L. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011, 25, 1915-1927.
92. Mercer, T.R.; Mattick, J.S. Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 2013, 20, 300-307.
93. Su, W.Y.; Xiong, H.; Fang, J.Y. Natural antisense transcripts regulate gene expression in an epigenetic manner. Biochem. Biophys. Res. Commun. 2010, 396, 177-181.
94. Imamura, T.; Yamamoto, S.; Ohgane, J.; Hattori, N.; Tanaka, S.; Shiota, K. Non-coding RNA directed DNA demethylation of Sphk1 CpG island. Biochem. Biophys. Res. Commun. 2004, 322, 593-600.
95. Berretta, J.; Pinskaya, M.; Morillon, A. A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes Dev. 2008, 22, 615-626.
96. 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 2007, 445, 666-670.
97. Morris, K.V.; Chan, S.W.; Jacobsen, S.E.; Looney, D.J. Small interfering RNA-induced transcriptional gene silencing in human cells. Science 2004, 305, 1289-1292.
98. Napoli, S.; Pastori, C.; Magistri, M.; Carbone, G.M.; Catapano, C.V. Promoter-specific transcriptional interference and c-myc gene silencing by siRNAs in human cells. EMBO J. 2009, 28, 1708-1719.
99. Hawkins, P.G.; Santoso, S.; Adams, C.; Anest, V.; Morris, K.V. Promoter targeted small RNAs induce long-term transcriptional gene silencing in human cells. Nucleic Acids Res. 2009, 37, 2984-2995.
100. Place, R.F.; Li, L.C.; Pookot, D.; Noonan, E.J.; Dahiya, R. microRNA-373 induces expression of genes with complementary promoter sequences. Proc. Natl. Acad. Sci. USA 2008, 105, 1608-1613.
101. Li, L.C.; Okino, S.T.; Zhao, H.; Pookot, D.; Place, R.F.; Urakami, S.; Enokida, H.; Dahiya, R. Small dsRNAs induce transcriptional activation in human cells. Proc. Natl. Acad. Sci. USA 2006, 103, 17337-17342.
102. Janowski, B.A.; Younger, S.T.; Hardy, D.B.; Ram, R.; Huffman, K.E.; Corey, D.R. Activating gene expression in mammalian cells with promoter-targeted duplex RNAs. Nat. Chem. Biol. 2007, 3, 166-173.
103. Natoli, G.; Andrau, J.C. Noncoding transcription at enhancers: General principles and functional models. Annu. Rev. Genet. 2012, 46, 1-19.
104. Orom, U.A.; Shiekhattar, R. Long non-coding RNAs and enhancers. Curr. Opin. Genet. Dev. 2011, 21, 194-198.
105. Panganiban, G.; Rubenstein, J.L. Developmental functions of the Distal-less/Dlx homeobox genes. Development 2002, 129, 4371-4386.
106. Wang, X.; Arai, S.; Song, X.; Reichart, D.; Du, K.; Pascual, G.; Tempst, P.; Rosenfeld, M.G.; Glass, C.K.; Kurokawa, R. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 2008, 454, 126-130.
107. Goodrich, J.A.; Kugel, J.F. Non-coding-RNA regulators of RNA polymerase II transcription. Nat. Rev. 2006, 7, 612-616.
108. Hastings, M.L.; Ingle, H.A.; Lazar, M.A.; Munroe, S.H. Post-transcriptional regulation of thyroid hormone receptor expression by cis-acting sequences and a naturally occurring antisense RNA. J. Boil. Chem. 2000, 275, 11507-11513.
109. Yin, Q.F.; Yang, L.; Zhang, Y.; Xiang, J.F.; Wu, Y.W.; Carmichael, G.G.; Chen, L.L. Long noncoding RNAs with snoRNA ends. Mol. Cell 2012, 48, 219-230.
110. Gong, C.; Maquat, L.E. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3' UTRs via Alu elements. Nature 2011, 470, 284-288.
111. Kretz, M.; Siprashvili, Z.; Chu, C.; Webster, D.E.; Zehnder, A.; Qu, K.; Lee, C.S.; Flockhart, R.J.; Groff; A.F.; Chow, J.; et al. Control of somatic tissue differentiation by the long non-coding RNA TINCR. Nature 2013, 493, 231-235.
112. Faghihi, M.A.; Modarresi, F.; Khalil, A.M.; Wood, D.E.; Sahagan, B.G.; Morgan, T.E.; Finch, C.E.; St Laurent, G., 3rd; Kenny, P.J.; Wahlestedt, C. Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat. Med. 2008, 14, 723-730.
113. Ebralidze, A.K.; Guibal, F.C.; Steidl, U.; Zhang, P.; Lee, S.; Bartholdy, B.; Jorda, M.A.; Petkova, V.; Rosenbauer, F.; Huang, G.; et al. PU.1 expression is modulated by the balance of functional sense and antisense RNAs regulated by a shared cis-regulatory element. Genes Dev. 2008, 22, 2085-2092.
114. Carrieri, C.; Cimatti, L.; Biagioli, M.; Beugnet, A.; Zucchelli, S.; Fedele, S.; Pesce, E.; Ferrer, I.; Collavin, L.; Santoro, C.; et al. Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 2012, 491, 454-457.
115. Willingham, A.T.; Orth, A.P.; Batalov, S.; Peters, E.C.; Wen, B.G.; Aza-Blanc, P.; Hogenesch, J.B.; Schultz, P.G. A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 2005, 309, 1570-1573.
116. Guo, X.; Zhang, Z.; Gerstein, M.B.; Zheng, D. Small RNAs originated from pseudogenes: cis- or trans-acting? PLoS Comput. Biol. 2009, 5, e1000449.
117. Tam, O.H.; Aravin, A.A.; Stein, P.; Girard, A.; Murchison, E.P.; Cheloufi, S.; Hodges, E.; Anger, M.; Sachidanandam, R.; Schultz, R.M.; et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453, 534-538.
118. Watanabe, T.; Totoki, Y.; Toyoda, A.; Kaneda, M.; Kuramochi-Miyagawa, S.; Obata, Y.; Chiba, H.; Kohara, Y.; Kono, T.; Nakano, T.; et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008, 453, 539-543.
119. Mighell, A.J.; Smith, N.R.; Robinson, P.A.; Markham, A.F. Vertebrate pseudogenes. FEBS Lett. 2000, 468, 109-114.
120. Zhang, Z.D.; Frankish, A.; Hunt, T.; Harrow, J.; Gerstein, M. Identification and analysis of unitary pseudogenes: Historic and contemporary gene losses in humans and other primates. Genome Biol. 2010, 11, R26.
121. Maestre, J.; Tchenio, T.; Dhellin, O.; Heidmann, T. mRNA retroposition in human cells: Processed pseudogene formation. EMBO J. 1995, 14, 6333-6338.
122. D'Errico, I.; Gadaleta, G.; Saccone, C. Pseudogenes in metazoa: Origin and features. Briefings Funct. Genomics Proteomics 2004, 3, 157-167.
123. Werner, A.; Schmutzler, G.; Carlile, M.; Miles, C.G.; Peters, H. Expression profiling of antisense transcripts on DNA arrays. Physiol. Genomics 2007, 28, 294-300.
124. Fanarraga, M.L.; Parraga, M.; Aloria, K.; del Mazo, J.; Avila, J.; Zabala, J.C. Regulated expression of p14 (cofactor A) during spermatogenesis. Cell Motil. Cytoskeleton 1999, 43, 243-254.
125. Pavlicek, A.; Gentles, A.J.; Paces, J.; Paces, V.; Jurka, J. Retroposition of processed pseudogenes: The impact of RNA stability and translational control. Trends Genet. 2006, 22, 69-73.
126. Borsani, O.; Zhu, J.; Verslues, P.E.; Sunkar, R.; Zhu, J.K. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 2005, 123, 1279-1291.
127. Okada, Y.; Tashiro, C.; Numata, K.; Watanabe, K.; Nakaoka, H.; Yamamoto, N.; Okubo, K.; Ikeda, R.; Saito, R.; Kanai, A.; et al. Comparative expression analysis uncovers novel features of endogenous antisense transcription. Hum. Mol. Genet. 2008, 17, 1631-1640.
128. Okamoto, I.; Arnaud, D.; le Baccon, P.; Otte, A.P.; Disteche, C.M.; Avner, P.; Heard, E. Evidence for de novo imprinted X-chromosome inactivation independent of meiotic inactivation in mice. Nature 2005, 438, 369-373.
129. 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. 2005, 15, 501-512.
130. Ginger, M.R.; Shore, A.N.; Contreras, A.; Rijnkels, M.; Miller, J.; Gonzalez-Rimbau, M.F.; Rosen, J.M. A noncoding RNA is a potential marker of cell fate during mammary gland development. Proc. Natl. Acad. Sci. USA 2006, 103, 5781-5786.
131. Rinn, J.L.; Kertesz, M.; Wang, J.K.; Squazzo, S.L.; Xu, X.; Brugmann, S.A.; Goodnough, L.H.; Helms, J.A.; Farnham, P.J.; Segal, E.; et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129, 1311-1323.
132. Loewer, S.; Cabili, M.N.; Guttman, M.; Loh, Y.H.; Thomas, K.; Park, I.H.; Garber, M.; Curran, M.; Onder, T.; Agarwal, S.; et al. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat. Genet. 2010, 42, 1113-1117.
133. Kierszenbaum, A.L.; Tres, L.L. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch. Histol. Cytol. 2004, 67, 271-284.
134. Nolasco, S.; Bellido, J.; Goncalves, J.; Tavares, A.; Zabala, J.C.; Soares, H. The expression of tubulin cofactor A (TBCA) is regulated by a noncoding antisense Tbca RNA during testis maturation. PLoS One 2012, 7, e42536.
135. Bartel, D.P. microRNAs: Target recognition and regulatory functions. Cell 2009, 136, 215-233.
136. Lim, L.P.; Lau, N.C.; Garrett-Engele, P.; Grimson, A.; Schelter, J.M.; Castle, J.; Bartel, D.P.; Linsley, P.S.; Johnson, J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433, 769-773.
137. Jing, Q.; Huang, S.; Guth, S.; Zarubin, T.; Motoyama, A.; Chen, J.; di Padova, F.; Lin, S.C.; Gram, H.; Han, J. Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 2005, 120, 623-634.
138. Behm-Ansmant, I.; Rehwinkel, J.; Doerks, T.; Stark, A.; Bork, P.; Izaurralde, E. mRNA degradation by miRNAs and GW182 requires both CCR4: NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 2006, 20, 1885-1898.
139. Llave, C.; Xie, Z.; Kasschau, K.D.; Carrington, J.C. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 2002, 297, 2053-2056.
140. Kim, D.H.; Saetrom, P.; Snove, O., Jr.; Rossi, J.J. microRNA-directed transcriptional gene silencing in mammalian cells. Proc. Natl. Acad. Sci. USA 2008, 105, 16230-16235.
141. Liu, J.; Valencia-Sanchez, M.A.; Hannon, G.J.; Parker, R. microRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 2005, 7, 719-723.
142. Pillai, R.S.; Bhattacharyya, S.N.; Artus, C.G.; Zoller, T.; Cougot, N.; Basyuk, E.; Bertrand, E.; Filipowicz, W. Inhibition of translational initiation by Let-7 microRNA in human cells. Science 2005, 309, 1573-1576.
143. Humphreys, D.T.; Westman, B.J.; Martin, D.I.; Preiss, T. microRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc. Natl. Acad. Sci. USA 2005, 102, 16961-16966.
144. Kiriakidou, M.; Tan, G.S.; Lamprinaki, S.; de Planell-Saguer, M.; Nelson, P.T.; Mourelatos, Z. An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell 2007, 129, 1141-1151.
145. Eulalio, A.; Huntzinger, E.; Izaurralde, E. GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat. Struct. Mol. Biol. 2008, 15, 346-353.
146. Wang, B.; Yanez, A.; Novina, C.D. microRNA-repressed mRNAs contain 40S but not 60S components. Proc. Natl. Acad. Sci. USA 2008, 105, 5343-5348.
147. Thermann, R.; Hentze, M.W. Drosophila miR2 induces pseudo-polysomes and inhibits translation initiation. Nature 2007, 447, 875-878.
148. Maroney, P.A.; Yu, Y.; Fisher, J.; Nilsen, T.W. Evidence that microRNAs are associated with translating messenger RNAs in human cells. Nat. Struct. Mol. Biol. 2006, 13, 1102-1107.
149. Petersen, C.P.; Bordeleau, M.E.; Pelletier, J.; Sharp, P.A. Short RNAs repress translation after initiation in mammalian cells. Mol. Cell 2006, 21, 533-542.
150. Lytle, J.R.; Yario, T.A.; Steitz, J.A. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR. Proc. Natl. Acad. Sci. USA 2007, 104, 9667-9672.
151. Vasudevan, S.; Steitz, J.A. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 2007, 128, 1105-1118.
152. Orom, U.A.; Nielsen, F.C.; Lund, A.H. microRNA-10a binds the 5' UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell 2008, 30, 460-471.
153. Lee, S.; Vasudevan, S. Post-transcriptional stimulation of gene expression by microRNAs. Adv. Exper. Med. Biol. 2013, 768, 97-126.
154. Bernstein, E.; Kim, S.Y.; Carmell, M.A.; Murchison, E.P.; Alcorn, H.; Li, M.Z.; Mills, A.A.; Elledge, S.J.; Anderson, K.V.; Hannon, G.J. Dicer is essential for mouse development. Nat. Genet. 2003, 35, 215-217.
155. Leonardo, T.R.; Schultheisz, H.L.; Loring, J.F.; Laurent, L.C. The functions of microRNAs in pluripotency and reprogramming. Nat. Cell Biol. 2012, 14, 1114-1121.
156. Giraldez, A.J.; Cinalli, R.M.; Glasner, M.E.; Enright, A.J.; Thomson, J.M.; Baskerville, S.; Hammond, S.M.; Bartel, D.P.; Schier, A.F. microRNAs regulate brain morphogenesis in zebrafish. Science 2005, 308, 833-838.
157. Stark, K.L.; Xu, B.; Bagchi, A.; Lai, W.S.; Liu, H.; Hsu, R.; Wan, X.; Pavlidis, P.; Mills, A.A.; Karayiorgou, M.; et al. Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nat. Genet. 2008, 40, 751-760.
158. Cobb, B.S.; Nesterova, T.B.; Thompson, E.; Hertweck, A.; O'Connor, E.; Godwin, J.; Wilson, C.B.; Brockdorff, N.; Fisher, A.G.; Smale, S.T.; et al. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J. Exp. Med. 2005, 201, 1367-1373.
159. Muljo, S.A.; Ansel, K.M.; Kanellopoulou, C.; Livingston, D.M.; Rao, A.; Rajewsky, K. Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 2005, 202, 261-269.
160. Edbauer, D.; Neilson, J.R.; Foster, K.A.; Wang, C.F.; Seeburg, D.P.; Batterton, M.N.; Tada, T.; Dolan, B.M.; Sharp, P.A.; Sheng, M. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 2010, 65, 373-384.
161. Monticelli, S.; Ansel, K.M.; Xiao, C.; Socci, N.D.; Krichevsky, A.M.; Thai, T.H.; Rajewsky, N.; Marks, D.S.; Sander, C.; Rajewsky, K.; et al. microRNA profiling of the murine hematopoietic system. Genome Biol. 2005, 6, R71.
162. Rodriguez, A.; Vigorito, E.; Clare, S.; Warren, M.V.; Couttet, P.; Soond, D.R.; van Dongen, S.; Grocock, R.J.; Das, P.P.; Miska, E.A.; et al. Requirement of bic/microRNA-155 for normal immune function. Science 2007, 316, 608-611.
163. Boldin, M.P.; Taganov, K.D.; Rao, D.S.; Yang, L.; Zhao, J.L.; Kalwani, M.; Garcia-Flores, Y.; Luong, M.; Devrekanli, A.; Xu, J.; et al. miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J. Exp. Med. 2011, 208, 1189-1201.
164. Steiner, D.F.; Thomas, M.F.; Hu, J.K.; Yang, Z.; Babiarz, J.E.; Allen, C.D.; Matloubian, M.; Blelloch, R.; Ansel, K.M. microRNA-29 regulates T-box transcription factors and interferon-gamma production in helper T cells. Immunity 2011, 35, 169-181.
165. Cheetham, S.W.; Gruhl, F.; Mattick, J.S.; Dinger, M.E. Long noncoding RNAs and the genetics of cancer. Br. J. Cancer 2013, 108, 2419-2425.
166. Munker, R.; Calin, G.A. microRNA profiling in cancer. Clin. Sci. 2011, 121, 141-158.
167. Faraoni, I.; Antonetti, F.R.; Cardone, J.; Bonmassar, E. miR-155 gene: A typical multifunctional microRNA. Biochim. Biophys. Acta 2009, 1792, 497-505.
168. Chan, J.A.; Krichevsky, A.M.; Kosik, K.S. microRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005, 65, 6029-6033.
169. Volinia, S.; Calin, G.A.; Liu, C.G.; Ambs, S.; Cimmino, A.; Petrocca, F.; Visone, R.; Iorio, M.; Roldo, C.; Ferracin, M.; et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. USA 2006, 103, 2257-2261.
170. Xiao, C.; Srinivasan, L.; Calado, D.P.; Patterson, H.C.; Zhang, B.; Wang, J.; Henderson, J.M.; Kutok, J.L.; Rajewsky, K. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat. Immunol. 2008, 9, 405-414.
171. Concepcion, C.P.; Bonetti, C.; Ventura, A. The microRNA-17-92 family of microRNA clusters in development and disease. Cancer J. 2012, 18, 262-267.
172. Tripathi, V.; Ellis, J.D.; Shen, Z.; Song, D.Y.; Pan, Q.; Watt, A.T.; Freier, S.M.; Bennett, C.F.; Sharma, A.; Bubulya, P.A.; et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol. Cell 2010, 39, 925-938.
173. Gutschner, T.; Hammerle, M.; Eissmann, M.; Hsu, J.; Kim, Y.; Hung, G.; Revenko, A.; Arun, G.; Stentrup, M.; Gross, M.; et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 2013, 73, 1180-1189.
174. Drakaki, A.; Iliopoulos, D. microRNA gene networks in oncogenesis. Curr. Genomics 2009, 10, 35-41.
175. Dalmay, T.; Edwards, D.R. microRNAs and the hallmarks of cancer. Oncogene 2006, 25, 6170-6175.
176. Gutschner, T.; Diederichs, S. The hallmarks of cancer: A long non-coding RNA point of view. RNA Biol. 2012, 9, 703-719.
177. He, L.; He, X.; Lim, L.P.; de Stanchina, E.; Xuan, Z.; Liang, Y.; Xue, W.; Zender, L.; Magnus, J.; Ridzon, D.; et al. A microRNA component of the p53 tumour suppressor network. Nature 2007, 447, 1130-1134.
178. Concepcion, C.P.; Han, Y.C.; Mu, P.; Bonetti, C.; Yao, E.; D'Andrea, A.; Vidigal, J.A.; Maughan, W.P.; Ogrodowski, P.; Ventura, A. Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet. 2012, 8, e1002797.
179. Huarte, M.; Guttman, M.; Feldser, D.; Garber, M.; Koziol, M.J.; Kenzelmann-Broz, D.; Khalil, A.M.; Zuk, O.; Amit, I.; Rabani, M.; et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010, 142, 409-419.
180. 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, 38, 5797-5806.
181. Packer, A.N.; Xing, Y.; Harper, S.Q.; Jones, L.; Davidson, B.L. The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. J. Neurosci. 2008, 28, 14341-14346.
182. Cogswell, J.P.; Ward, J.; Taylor, I.A.; Waters, M.; Shi, Y.; Cannon, B.; Kelnar, K.; Kemppainen, J.; Brown, D.; Chen, C.; et al. Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimer's Disease 2008, 14, 27-41.
183. Kim, J.; Inoue, K.; Ishii, J.; Vanti, W.B.; Voronov, S.V.; Murchison, E.; Hannon, G.; Abeliovich, A. A microRNA feedback circuit in midbrain dopamine neurons. Science 2007, 317, 1220-1224.
184. Contreras, J.; Rao, D.S. microRNAs in inflammation and immune responses. Leukemia 2012, 26, 404-413.
185. Cabianca, D.S.; Casa, V.; Bodega, B.; Xynos, A.; Ginelli, E.; Tanaka, Y.; Gabellini, D. A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 2012, 149, 819-831.
186. Szafranski, P.; Dharmadhikari, A.V.; Brosens, E.; Gurha, P.; Kolodziejska, K.E.; Zhishuo, O.; Dittwald, P.; Majewski, T.; Mohan, K.N.; Chen, B.; et al. Small noncoding differentially methylated copy-number variants, including lncRNA genes, cause a lethal lung developmental disorder. Genome Res. 2013, 23, 23-33.
187. Van Dijk, M.; Thulluru, H.K.; Mulders, J.; Michel, O.J.; Poutsma, A.; Windhorst, S.; Kleiverda, G.; Sie, D.; Lachmeijer, A.M.; Oudejans, C.B. HELLP babies link a novel lincRNA to the trophoblast cell cycle. J. Clin. Invest. 2012, 122, 4003-4011.