DIS3 shapes the RNA polymerase II transcriptome in humans by degrading a variety of unwanted transcripts

Genome Research

Volumn 25, Issue 11, 2015, Pages 1622-1633

  Szczepińska, Teresa ^a,b   Kalisiak, Katarzyna ^a,b   Tomecki, Rafal ^a,b   Labno, Anna ^a,b   Borowski, Lukasz S ^a,b   Kulinski, Tomasz M ^a,b   Adamska, Dorota ^a,b   Kosinska, Joanna ^c   Dziembowski, Andrzej ^a,b  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^b UNIVERSITY OF WARSAW   (Poland)

^c MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

DIS3 PROTEIN; EXORIBONUCLEASE; RNA POLYMERASE II; SMALL NUCLEOLAR RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; UNTRANSLATED RNA; DIS3 PROTEIN, HUMAN; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; LONG UNTRANSLATED RNA; MESSENGER RNA; MUTANT PROTEIN; NEAT1 LONG NON-CODING RNA, HUMAN;

ARTICLE; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; DOWN REGULATION; ENHANCER REGION; ENZYME ACTIVE SITE; EXOSOME; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC TRANSFECTION; HOMEOSTASIS; HUMAN GENOME; IMMUNOPRECIPITATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; REGULATORY MECHANISM; RNA DEGRADATION; STEADY STATE; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS; UPREGULATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; SEQUENCE ANALYSIS;

EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MUTANT PROTEINS; RNA POLYMERASE II; RNA, LONG NONCODING; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84946549518     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.189597.115     Document Type: Article

References (71)

1. Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D. 1999. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18: 5399-5410.
2. Almada AE, Wu X, Kriz AJ, Burge CB, Sharp PA. 2013. Promoter directionality is controlled by U1 snRNP and polyadenylation signals. Nature 499: 360-363.
3. Andersen PK, Lykke-Andersen S, Jensen TH. 2012. Promoter-proximal polyadenylation sites reduce transcription activity. Genes Dev 26: 2169-2179.
4. Andersen PR, Domanski M, Kristiansen MS, Storvall H, Ntini E, Verheggen C, Schein A, Bunkenborg J, Poser I, Hallais M, et al. 2013. The human cap-binding complex is functionally connected to the nuclear RNA exosome. Nat Struct Mol Biol 20: 1367-1376.
5. Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, Chen Y, Zhao X, Schmidl C, Suzuki T, et al. 2014. An atlas of active enhancers across human cell types and tissues. Nature 507: 455-461.
6. Basu U, Meng FL, Keim C, Grinstein V, Pefanis E, Eccleston J, Zhang T, Myers D, Wasserman CR, Wesemann DR, et al. 2011. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell 144: 353-363.
7. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57: 289-300.
8. Berg MG, Singh LN, Younis I, Liu Q, Pinto AM, Kaida D, Zhang Z, Cho S, Sherrill-Mix S, Wan L, et al. 2012. U1 snRNP determines mRNA length and regulates isoform expression. Cell 150: 53-64.
9. Bresson SM, Conrad NK. 2013. The human nuclear poly(A)-binding protein promotes RNA hyperadenylation and decay. PLoS Genet 9: e1003893.
10. Chang HM, Triboulet R, Thornton JE, Gregory RI. 2013. A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 497: 244-248.
11. Chapman MA, Lawrence MS, Keats JJ, Cibulskis K, Sougnez C, Schinzel AC, Harview CL, Brunet JP, Ahmann GJ, Adli M, et al. 2011. Initial genome sequencing and analysis of multiple myeloma. Nature 471: 467-472.
12. Chlebowski A, Tomecki R, López MEG, Séraphin B, Dziembowski A. 2010. Catalytic properties of the eukaryotic exosome. Adv Exp Med Biol 702: 63-78.
13. Chlebowski A, Lubas M, Jensen TH, Dziembowski A. 2013. RNA decay machines: the exosome. Biochim Biophys Acta 1829: 552-560.
14. Clark MB, Amaral PP, Schlesinger FJ, Dinger ME, Taft RJ, Rinn JL, Ponting CP, Stadler PF, Morris KV, Morillon A, et al. 2011. The reality of pervasive transcription. PLoS Biol 9: e1000625; discussion e1001102.
15. Dziembowski A, Lorentzen E, Conti E, Séraphin B. 2007. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14: 15-22.
16. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
17. Euskirchen GM, Rozowsky JS, Wei CL, Lee WH, Zhang ZD, Hartman S, Emanuelsson O, Stolc V, Weissman S, Gerstein MB, et al. 2007. Mapping of transcription factor binding regions in mammalian cells by ChIP: comparison of array- and sequencing-based technologies. Genome Res 17: 898-909.
18. Fox AH, Lamond AI. 2010. Paraspeckles. Cold Spring Harb Perspect Biol 2: a000687.
19. Grant GR, Farkas MH, Pizarro AD, Lahens NF, Schug J, Brunk BP, Stoeckert CJ, Hogenesch JB, Pierce EA. 2011. Comparative analysis of RNA-Seq alignment algorithms and the RNA-Seq unified mapper (RUM). Bioinformatics 27: 2518-2528.
20. Gudipati RK, Xu Z, Lebreton A, Séraphin B, Steinmetz LM, Jacquier A, Libri D. 2012. Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell 48: 409-421.
21. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp AC, Munschauer M, et al. 2010. PAR-CliP-a method to identify transcriptome-wide the binding sites of RNA binding proteins. J Vis Exp JoVE doi: 10.3791/2034.
22. Hallais M, Pontvianne F, Andersen PR, Clerici M, Lener D, Benbahouche Nel H, Gostan T, Vandermoere F, Robert M-C, Cusack S, et al. 2013. CBC- ARS2 stimulates 3'-end maturation of multiple RNA families and favors cap-proximal processing. Nat Struct Mol Biol 20: 1358-1366.
23. Imamura K, Imamachi N, Akizuki G, Kumakura M, Kawaguchi A, Nagata K, Kato A, Kawaguchi Y, Sato H, Yoneda M, et al. 2014. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol Cell 53: 393-406.
24. Jensen TH, Jacquier A, Libri D. 2013. Dealing with pervasive transcription. Mol Cell 52: 473-484.
25. Kaida D, Berg MG, Younis I, Kasim M, Singh LN, Wan L, Dreyfuss G. 2010. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468: 664-668.
26. Kent WJ, SugnetCW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12: 996-1006.
27. LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, Tollervey D. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713-724.
28. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
29. Lebreton A, Tomecki R, Dziembowski A, Séraphin B. 2008. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456: 993-996.
30. Lemay JF, Larochelle M, Marguerat S, Atkinson S, Bähler J, Bachand F. 2014. The RNA exosome promotes transcription termination of backtracked RNA polymerase II. Nat Struct Mol Biol 21: 919-926.
31. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
32. Liu Q, Greimann JC, Lima CD. 2006. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127: 1223-1237.
33. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550.
34. Lubas M, Christensen MS, Kristiansen MS, Domanski M, Falkenby LG, Lykke-Andersen S, Andersen JS, Dziembowski A, Jensen TH. 2011. Interaction profiling identifies the human nuclear exosome targeting complex. Mol Cell 43: 624-637.
35. Lubas M, Damgaard CK, Tomecki R, Cysewski D, Jensen TH, Dziembowski A. 2013. Exonuclease hDIS3L2 specifies an exosome-independent 3'-5' degradation pathway of human cytoplasmic mRNA. EMBO J 32: 1855-1868.
36. Lubas M, Andersen PR, Schein A, Dziembowski A, Kudla G, Jensen TH. 2015. The human nuclear exosome targeting complex is loaded onto newly synthesized RNA to direct early ribonucleolysis. Cell Rep 10: 178-192.
37. Lykke-Andersen S, Tomecki R, Jensen TH, Dziembowski A. 2011. The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol 8: 61-66.
38. Makino DL, Baumgärtner M, Conti E. 2013. Crystal structure of an RNAbound 11-subunit eukaryotic exosome complex. Nature 495: 70-75.
39. Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.J 17: 10-12.
40. Melo CA, Drost J, Wijchers PJ, van de Werken H, de Wit E, Oude Vrielink JA, Elkon R, Melo SA, Léveillé N, Kalluri R, et al. 2013. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol Cell 49: 524-535.
41. Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D. 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3'→5' exoribonucleases. Cell 91: 457-466.
42. Naganuma T, Nakagawa S, Tanigawa A, Sasaki YF, Goshima N, Hirose T. 2012. Alternative 3'-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J 31: 4020-4034.
43. Ntini E, Järvelin AI, Bornholdt J, Chen Y, Boyd M, Jørgensen M, Andersson R, Hoof I, Schein A, Andersen PR, et al. 2013. Polyadenylation site-induced decay of upstream transcripts enforces promoter directionality. Nat Struct Mol Biol 20: 923-928.
44. Pefanis E, Wang J, Rothschild G, Lim J, Chao J, Rabadan R, Economides AN, Basu U. 2014. Noncoding RNA transcription targets AID to divergently transcribed loci in B cells. Nature 514: 389-393.
45. Preker P, Nielsen J, Kammler S, Lykke-Andersen S, Christensen MS, Mapendano CK, Schierup MH, Jensen TH. 2008. RNA exosome depletion reveals transcription upstream of active human promoters. Science 322: 1851-1854.
46. Preker P, Almvig K, Christensen MS, Valen E, Mapendano CK, Sandelin A, Jensen TH. 2011. PROMoter uPstream Transcripts share characteristics with mRNAs and are produced upstream of all three major types of mammalian promoters. Nucleic Acids Res 39: 7179-7193.
47. Preti M, O'Donohue MF, Montel-Lehry N, Bortolin-Cavaillé ML, Choesmel V, Gleizes PE. 2013. Gradual processing of the ITS1 from the nucleolus to the cytoplasm during synthesis of the human 18S rRNA. Nucleic Acids Res 41: 4709-4723.
48. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
49. Schaeffer D, Tsanova B, Barbas A, Reis FP, Dastidar EG, Sanchez-Rotunno M, Arraiano CM, van Hoof A. 2009. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16: 56-62.
50. Schaukowitch K, Joo JY, Liu X, Watts JK, Martinez C, Kim TK. 2014. Enhancer RNA facilitates NELF release from immediate early genes. Mol Cell 56: 29-42.
51. Schneider C, Tollervey D. 2013. Threading the barrel of the RNA exosome. Trends Biochem Sci 38: 485-493.
52. Schneider C, Leung E, Brown J, Tollervey D. 2009. The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37: 1127-1140.
53. Schneider C, Kudla G, Wlotzka W, Tuck A, Tollervey D. 2012. Transcriptome- wide analysis of exosome targets. Mol Cell 48: 422-433.
54. Sloan KE, Mattijssen S, Lebaron S, Tollervey D, Pruijn GJ, Watkins NJ. 2013. Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J Cell Biol 200: 577-588.
55. Staals RHJ, Bronkhorst AW, Schilders G, Slomovic S, Schuster G, Heck AJR, Raijmakers R, Pruijn GJ. 2010. Dis3-like 1: a novel exoribonuclease associated with the human exosome. EMBO J 29: 2358-2367.
56. Thomson E, Tollervey D. 2010. The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol Cell Biol 30: 976-984.
57. Tomecki R, Kristiansen MS, Lykke-Andersen S, Chlebowski A, Larsen KM, Szczesny RJ, Drazkowska K, Pastula A, Andersen JS, Stepien PP, et al. 2010. The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J 29: 2342-2357.
58. Tomecki R, Drazkowska K, Kucinski I, Stodus K, Szczesny RJ, Gruchota J, Owczarek EP, Kalisiak K, Dziembowski A. 2014. Multiple myeloma-associated hDIS3 mutations cause perturbations in cellular RNA metabolism and suggest hDIS3 PIN domain as a potential drug target. Nucleic Acids Res 42: 1270-1290.
59. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
60. Tudek A, Porrua O, Kabzinski T, Lidschreiber M, Kubicek K, Fortova A, Lacroute F, Vanacova S, Cramer P, Stefl R, et al. 2014. Molecular basis for coordinating transcription termination with noncoding RNA degradation. Mol Cell 55: 467-481.
61. Ustianenko D, Hrossova D, Potesil D, Chalupnikova K, Hrazdilova K, Pachernik J, Cetkovska K, Uldrijan S, Zdrahal Z, Vanacova S. 2013. Mammalian DIS3L2 exoribonuclease targets the uridylated precursors of let-7 miRNAs. RNA 19: 1632-1638.
62. van Bakel H, Nislow C, Blencowe BJ, Hughes TR. 2010. Most "dark matter" transcripts are associated with known genes. PLoS Biol 8: e1000371.
63. Vanácová S, Wolf J, Martin G, Blank D, Dettwiler S, Friedlein A, Langen H, Keith G, Keller W. 2005. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol 3: e189.
64. Vasiljeva L, Kim M, Terzi N, Soares LM, Buratowski S. 2008. Transcription termination and RNA degradation contribute to silencing of RNA polymerase II transcription within heterochromatin. Mol Cell 29: 313-323.
65. Walker BA, Wardell CP, Melchor L, Hulkki S, Potter NE, Johnson DC, Fenwick K, Kozarewa I, Gonzalez D, Lord CJ, et al. 2012. Intraclonal heterogeneity and distinct molecular mechanisms characterize the development of t(4;14) and t(11;14) myeloma. Blood 120: 1077-1086.
66. Wasmuth EV, Januszyk K, Lima CD. 2014. Structure of an Rrp6-RNA exosome complex bound to poly(A) RNA. Nature 511: 435-439.
67. Weißbach S, Langer C, Puppe B, Nedeva T, Bach E, Kull M, Bargou R, Einsele H, Rosenwald A, Knop S, et al. 2014. The molecular spectrum and clinical impact of DIS3 mutations in multiple myeloma. Br J Haematol 169: 57-70.
68. Wilusz JE, Freier SM, Spector DL. 2008. 3' end processing of a long nuclearretained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 135: 919-932.
69. Wilusz JE, JnBaptiste CK, Lu LY, Kuhn CD, Joshua-Tor L, Sharp PA. 2012. A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly (A) tails. Genes Dev 26: 2392-2407.
70. Wlotzka W, Kudla G, Granneman S, TollerveyD. 2011. The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J 30: 1790-1803.
71. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, Régnault B, Devaux F, Namane A, Séraphin B, et al. 2005. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.