RNA-RNA interactions enable specific targeting of noncoding RNAs to nascent pre-mRNAs and chromatin sites

Cell

Volumn 159, Issue 1, 2014, Pages 188-199

  Engreitz, Jesse M ^a   Sirokman, Klara ^a   McDonel, Patrick ^a   Shishkin, Alexander A ^b   Surka, Christine ^b   Russell, Pamela ^b   Grossman, Sharon R ^a   Chow, Amy Y ^b   Guttman, Mitchell ^b   Lander, Eric S ^a,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b California Institute of Technology   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; MESSENGER RNA PRECURSOR; RNA BINDING PROTEIN; SMALL NUCLEAR RNA; UNTRANSLATED RNA; CROSS LINKING REAGENT; LONG UNTRANSLATED RNA; MALAT1 LONG NON-CODING RNA, MOUSE; MESSENGER RNA; RNA SPLICING; U1 SMALL NUCLEAR RNA;

ARTICLE; CHROMATIN; CONTROLLED STUDY; CROSS LINKING; GENE TARGETING; INTERACTIONS WITH RNA; INTRON; RNA PROCESSING; RNA PURIFICATION; RNA RNA HYBRIDIZATION; RNA SPLICING; RNA TRANSCRIPTION; SPLICEOSOME; ANIMAL; CHEMISTRY; GENETIC PROCEDURES; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE;

ANIMALS; BASE SEQUENCE; CROSS-LINKING REAGENTS; GENETIC TECHNIQUES; MICE; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; RNA SPLICE SITES; RNA, LONG NONCODING; RNA, MESSENGER; RNA, SMALL NUCLEAR; RNA, UNTRANSLATED;

EID: 84907536806     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.08.018     Document Type: Article

References (59)

1. A.E. Almada, X. Wu, A.J. Kriz, C.B. Burge, and P.A. Sharp Promoter directionality is controlled by U1 snRNP and polyadenylation signals Nature 499 2013 360 363
2. M.-L. Änkö, M. Müller-McNicoll, H. Brandl, T. Curk, C. Gorup, I. Henry, J. Ule, and K.M. Neugebauer The RNA-binding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes Genome Biol. 13 2012 R17
3. D. Bernard, K.V. Prasanth, V. Tripathi, S. Colasse, T. Nakamura, Z. Xuan, M.Q. Zhang, F. Sedel, L. Jourdren, and F. Coulpier A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression EMBO J. 29 2010 3082 3093
4. M.N. Cabili, C. Trapnell, L. Goff, M. Koziol, B. Tazon-Vega, A. Regev, and J.L. Rinn Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses Genes Dev. 25 2011 1915 1927
5. J.P. Calvet, and T. Pederson Heterogeneous nuclear RNA double-stranded regions probed in living HeLa cells by crosslinking with the psoralen derivative aminomethyltrioxsalen Proc. Natl. Acad. Sci. USA 76 1979 755 759
6. P. Carninci, T. Kasukawa, S. Katayama, J. Gough, M.C. Frith, N. Maeda, R. Oyama, T. Ravasi, B. Lenhard, C. Wells FANTOM Consortium RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group) The transcriptional landscape of the mammalian genome Science 309 2005 1559 1563
7. C. Chu, K. Qu, F.L. Zhong, S.E. Artandi, and H.Y. Chang Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions Mol. Cell 44 2011 667 678
8. G.D. Cimino, H.B. Gamper, S.T. Isaacs, and J.E. Hearst Psoralens as photoactive probes of nucleic acid structure and function: organic chemistry, photochemistry, and biochemistry Annu. Rev. Biochem. 54 1985 1151 1193
9. C.K. Damgaard, S. Kahns, S. Lykke-Andersen, A.L. Nielsen, T.H. Jensen, and J. Kjems A 5′ splice site enhances the recruitment of basal transcription initiation factors in vivo Mol. Cell 29 2008 271 278
10. T. Derrien, R. Johnson, G. Bussotti, A. Tanzer, S. Djebali, H. Tilgner, G. Guernec, D. Martin, A. Merkel, and D.G. Knowles The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression Genome Res. 22 2012 1775 1789
11. C. Dieterich, and P.F. Stadler Computational biology of RNA interactions Wiley Interdiscip. Rev. RNA 4 2013 107 120
12. M. Eißmann, T. Gutschner, M. Hämmerle, S. Günther, M. Caudron-Herger, M. Groß, P. Schirmacher, K. Rippe, T. Braun, M. Zörnig, and S. Diederichs Loss of the abundant nuclear non-coding RNA MALAT1 is compatible with life and development RNA Biol. 9 2012 1076 1087
13. J.M. Engreitz, A. Pandya-Jones, P. McDonel, A. Shishkin, K. Sirokman, C. Surka, S. Kadri, J. Xing, A. Goren, and E.S. Lander The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome Science 341 2013 1237973
14. P. Grote, L. Wittler, D. Hendrix, F. Koch, S. Währisch, A. Beisaw, K. Macura, G. Bläss, M. Kellis, M. Werber, and B.G. Herrmann The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse Dev. Cell 24 2013 206 214
15. T. Gutschner, M. Hämmerle, and S. Diederichs MALAT1 - a paradigm for long noncoding RNA function in cancer J. Mol. Med. 91 2013 791 801
16. M. Guttman, I. Amit, M. Garber, C. French, M.F. Lin, D. Feldser, M. Huarte, O. Zuk, B.W. Carey, and J.P. Cassady Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals Nature 458 2009 223 227
17. M. Guttman, M. Garber, J.Z. Levin, J. Donaghey, J. Robinson, X. Adiconis, L. Fan, M.J. Koziol, A. Gnirke, and C. Nusbaum Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs Nat. Biotechnol. 28 2010 503 510
18. M. Guttman, J. Donaghey, B.W. Carey, M. Garber, J.K. Grenier, G. Munson, G. Young, A.B. Lucas, R. Ach, and L. Bruhn lincRNAs act in the circuitry controlling pluripotency and differentiation Nature 477 2011 295 300
19. A. Helwak, G. Kudla, T. Dudnakova, and D. Tollervey Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding Cell 153 2013 654 665
20. J.N. Hutchinson, A.W. Ensminger, C.M. Clemson, C.R. Lynch, J.B. Lawrence, and A. Chess A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains BMC Genomics 8 2007 39
21. D. Kaida, M.G. Berg, I. Younis, M. Kasim, L.N. Singh, L. Wan, and G. Dreyfuss U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation Nature 468 2010 664 668
22. M. Kretz, Z. Siprashvili, C. Chu, D.E. Webster, A. Zehnder, K. Qu, C.S. Lee, R.J. Flockhart, A.F. Groff, and J. Chow Control of somatic tissue differentiation by the long non-coding RNA TINCR Nature 493 2013 231 235
23. G. Kudla, S. Granneman, D. Hahn, J.D. Beggs, and D. Tollervey Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast Proc. Natl. Acad. Sci. USA 108 2011 10010 10015
24. K.Y. Kwek, S. Murphy, A. Furger, B. Thomas, W. O'Gorman, H. Kimura, N.J. Proudfoot, and A. Akoulitchev U1 snRNA associates with TFIIH and regulates transcriptional initiation Nat. Struct. Biol. 9 2002 800 805
25. L.F. Lareau, M. Inada, R.E. Green, J.C. Wengrod, and S.E. Brenner Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements Nature 446 2007 926 929
26. M.R. Lerner, J.A. Boyle, S.M. Mount, S.L. Wolin, and J.A. Steitz Are snRNPs involved in splicing? Nature 283 1980 220 224
27. R. Miyagawa, K. Tano, R. Mizuno, Y. Nakamura, K. Ijiri, R. Rakwal, J. Shibato, Y. Masuo, A. Mayeda, T. Hirose, and N. Akimitsu Identification of cis- and trans-acting factors involved in the localization of MALAT-1 noncoding RNA to nuclear speckles RNA 18 2012 738 751
28. S.M. Mount, I. Pettersson, M. Hinterberger, A. Karmas, and J.A. Steitz The U1 small nuclear RNA-protein complex selectively binds a 5′ splice site in vitro Cell 33 1983 509 518
29. S. Nakagawa, J.Y. Ip, G. Shioi, V. Tripathi, X. Zong, T. Hirose, and K.V. Prasanth Malat1 is not an essential component of nuclear speckles in mice RNA 18 2012 1487 1499
30. J.Z. Ni, L. Grate, J.P. Donohue, C. Preston, N. Nobida, G. O'Brien, L. Shiue, T.A. Clark, J.E. Blume, and M. Ares Jr. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay Genes Dev. 21 2007 708 718
31. W. O'Gorman, B. Thomas, K.Y. Kwek, A. Furger, and A. Akoulitchev Analysis of U1 small nuclear RNA interaction with cyclin H J. Biol. Chem. 280 2005 36920 36925
32. S. Pandit, Y. Zhou, L. Shiue, G. Coutinho-Mansfield, H. Li, J. Qiu, J. Huang, G.W. Yeo, M. Ares Jr., and X.-D. Fu Genome-wide analysis reveals SR protein cooperation and competition in regulated splicing Mol. Cell 50 2013 223 235
33. P.B. Rahl, C.Y. Lin, A.C. Seila, R.A. Flynn, S. McCuine, C.B. Burge, P.A. Sharp, and R.A. Young c-Myc regulates transcriptional pause release Cell 141 2010 432 445
34. A.L. Saltzman, Y.K. Kim, Q. Pan, M.M. Fagnani, L.E. Maquat, and B.J. Blencowe Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay Mol. Cell. Biol. 28 2008 4320 4330
35. J.R. Sanford, X. Wang, M. Mort, N. Vanduyn, D.N. Cooper, S.D. Mooney, H.J. Edenberg, and Y. Liu Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts Genome Res. 19 2009 381 394
36. M. Sauvageau, L.A. Goff, S. Lodato, B. Bonev, A.F. Groff, C. Gerhardinger, D.B. Sanchez-Gomez, E. Hacisuleyman, E. Li, and M. Spence Multiple knockout mouse models reveal lincRNAs are required for life and brain development eLife 2 2013 e01749
37. M.D. Simon, C.I. Wang, P.V. Kharchenko, J.A. West, B.A. Chapman, A.A. Alekseyenko, M.L. Borowsky, M.I. Kuroda, and R.E. Kingston The genomic binding sites of a noncoding RNA Proc. Natl. Acad. Sci. USA 108 2011 20497 20502
38. M.M.L. Soruco, J. Chery, E.P. Bishop, T. Siggers, M.Y. Tolstorukov, A.R. Leydon, A.U. Sugden, K. Goebel, J. Feng, and P. Xia The CLAMP protein links the MSL complex to the X chromosome during Drosophila dosage compensation Genes Dev. 27 2013 1551 1556
39. D.L. Spector, and A.I. Lamond Nuclear speckles Cold Spring Harb. Perspect. Biol. 3 2011 a000646-a000646
40. J.R. Tollervey, T. Curk, B. Rogelj, M. Briese, M. Cereda, M. Kayikci, J. König, T. Hortobágyi, A.L. Nishimura, and V. Zupunski Characterizing the RNA targets and position-dependent splicing regulation by TDP-43 Nat. Neurosci. 14 2011 452 458
41. V. Tripathi, J.D. Ellis, Z. Shen, D.Y. Song, Q. Pan, A.T. Watt, S.M. Freier, C.F. Bennett, A. Sharma, and P.A. Bubulya The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation Mol. Cell 39 2010 925 938
42. V. Tripathi, D.Y. Song, X. Zong, S.P. Shevtsov, S. Hearn, X.-D. Fu, M. Dundr, and K.V. Prasanth SRSF1 regulates the assembly of pre-mRNA processing factors in nuclear speckles Mol. Biol. Cell 23 2012 3694 3706
43. V. Tripathi, Z. Shen, A. Chakraborty, S. Giri, S.M. Freier, X. Wu, Y. Zhang, M. Gorospe, S.G. Prasanth, A. Lal, and K.V. Prasanth Long noncoding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB PLoS Genet. 9 2013 e1003368
44. Z. Wang, M. Kayikci, M. Briese, K. Zarnack, N.M. Luscombe, G. Rot, B. Zupan, T. Curk, and J. Ule iCLIP predicts the dual splicing effects of TIA-RNA interactions PLoS Biol. 8 2010 e1000530
45. B. Zhang, G. Arun, Y.S. Mao, Z. Lazar, G. Hung, G. Bhattacharjee, X. Xiao, C.J. Booth, J. Wu, C. Zhang, and D.L. Spector The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult Cell Reports 2 2012 111 123
46. Y. Zhuang, and A.M. Weiner A compensatory base change in U1 snRNA suppresses a 5′ splice site mutation Cell 46 1986 827 835
47. T.S. Alioto U12DB: a database of orthologous U12-type spliceosomal introns Nucleic Acids Res. 35 2007 D110 D115
48. M. Beltrame, and D. Tollervey Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA EMBO J. 11 1992 1531 1542
49. D.M. Bhatt, A. Pandya-Jones, A.-J. Tong, I. Barozzi, M.M. Lissner, G. Natoli, D.L. Black, and S.T. Smale Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions Cell 150 2012 279 290
50. A.V. Borovjagin, and S.A. Gerbi Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction RNA 10 2004 942 953
51. L.J. Core, J.J. Waterfall, and J.T. Lis Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters Science 322 2008 1845 1848
52. E. Fayet-Lebaron, V. Atzorn, Y. Henry, and T. Kiss 18S rRNA processing requires base pairings of snR30 H/ACA snoRNA to eukaryote-specific 18S sequences EMBO J. 28 2009 1260 1270
53. C. Guthrie, and B. Patterson Spliceosomal snRNAs Annu. Rev. Genet. 22 1988 387 419
54. W. Huang, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57
55. J.M. Hughes Functional base-pairing interaction between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit RNA J. Mol. Biol. 259 1996 645 654
56. M. Marz, A. Donath, N. Verstraete, V.T. Nguyen, P.F. Stadler, and O. Bensaude Evolution of 7SK RNA and its protein partners in metazoa Mol. Biol. Evol. 26 2009 2821 2830
57. R.L. Maser, and J.P. Calvet U3 small nuclear RNA can be psoralen-cross-linked in vivo to the 5′ external transcribed spacer of pre-ribosomal-RNA Proc. Natl. Acad. Sci. USA 86 1989 6523 6527
58. A. Pandya-Jones, and D.L. Black Co-transcriptional splicing of constitutive and alternative exons RNA 15 2009 1896 1908
59. I.L. Stroke, and A.M. Weiner The 5′ end of U3 snRNA can be crosslinked in vivo to the external transcribed spacer of rat ribosomal RNA precursors J. Mol. Biol. 210 1989 497 512