In vivo SELEX reveals novel sequence and structural determinants of Nrd1-Nab3-Sen1-dependent transcription termination

EMBO Journal

Volumn 31, Issue 19, 2012, Pages 3935-3948

  Porrua, Odil ^a   Hobor, Fruzsina ^b   Boulay, Jocelyne ^a   Kubicek, Karel ^b   D'Aubenton Carafa, Yves ^a   Gudipati, Rajani Kanth ^a,c   Stefl, Richard ^b   Libri, Domenico ^a  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

^b MASARYK UNIVERSITY   (Czech Republic)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

cryptic unstable transcripts; hidden transcription; Nrd1p Nab3p Sen1p complex; transcription termination; transcriptional insulators

Indexed keywords

MESSENGER RNA; NRD1 NAB3 SEN1 COMPLEX; PEPTIDES AND PROTEINS; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; COMBINATORIAL CHEMISTRY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MOTIF; TRANSCRIPTION TERMINATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; DNA HELICASES; GENE EXPRESSION REGULATION, FUNGAL; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; RNA HELICASES; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SELEX APTAMER TECHNIQUE; TRANSCRIPTION TERMINATION, GENETIC;

EID: 84867036854     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.237     Document Type: Article

References (46)

1. Arigo JT, Carroll KL, Ames JM, Corden JL (2006a) Regulation of yeast NRD1 expression by premature transcription termination. Mol Cell 21: 641-651
2. Arigo JT, Eyler DE, Carroll KL, Corden JL (2006b) Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol Cell 23: 841-851
3. Carroll KL, Ghirlando R, Ames JM, Corden JL (2007) Interaction of yeast RNA-binding proteins Nrd1 and Nab3 with RNA polymerase II terminator elements. RNA 13: 361-373
4. Carroll KL, Pradhan DA, Granek JA, Clarke ND, Corden JL (2004) Identification of cis elements directing termination of yeast nonpolyadenylated snoRNA transcripts. Mol Cell Biol 24: 6241-6252
5. Chlebowski A, Tomecki R, Lopez ME, Seraphin B, Dziembowski A (2011) Catalytic properties of the eukaryotic exosome. Adv Exp Med Biol 702: 63-78
6. Creamer TJ, Darby MM, Jamonnak N, Schaughency P, Hao H, Wheelan SJ, Corden JL (2011) Transcriptome-wide binding sites for components of the Saccharomyces cerevisiae non-poly(A) termination pathway: Nrd1, Nab3, and Sen1. PLoS Genet 7: e1002329
7. Davis CA, Ares Jr M (2006) Accumulation of unstable promoterassociated transcripts upon loss of the nuclear exosome subunit Rrp6p in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 103: 3262-3267
8. Egecioglu DE, Henras AK, Chanfreau GF (2006) Contributions of Trf4p-and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12: 26-32
9. Fatica A, Morlando M, Bozzoni I (2000) Yeast snoRNA accumulation relies on a cleavage-dependent/polyadenylation-independent 30-processing apparatus. EMBO J 19: 6218-6229
10. Gross S, Moore CL (2001) Rna15 interaction with the A-rich yeast polyadenylation signal is an essential step in mRNA 30-end formation. Mol Cell Biol 21: 8045-8055
11. Gudipati RK, Villa T, Boulay J, Libri D (2008) Phosphorylation of RNA polymerase CTD dictates transcription termination choice. Nat Struct Mol Biol 15: 786-794
12. Heyduk T, Lee JC (1990) Application of fluorescence energy transfer and polarization to monitor Escherichia coli cAMP receptor protein and lac promoter interaction. Proc Natl Acad Sci USA 87: 1744-1748
13. Hobor F, Pergoli R, Kubicek K, Hrossova D, Bacikova V, Zimmermann M, Pasulka J, Hofr C, Vanacova S, Stefl R (2011) Recognition of transcription termination signal by the nuclear polyadenylated RNA-binding (NAB) 3 protein. J Biol Chem 286: 3645-3657
14. Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO (2008) Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol 6: e255
15. Houalla R, Devaux F, Fatica A, Kufel J, Barrass D, Torchet C, Tollervey D (2006) Microarray detection of novel nuclear RNA substrates for the exosome. Yeast 23: 439-454
16. Jacquier A (2009) The complex eukaryotic transcriptome: unexpected pervasive transcription and novel small RNAs. Nat Rev Genet 10: 833-844
17. Jenks MH, Reines D (2005) Dissection of the molecular basis of mycophenolate resistance in Saccharomyces cerevisiae. Yeast 22: 1181-1190
18. Johnson JM, Edwards S, Shoemaker D, Schadt EE (2005) Dark matter in the genome: evidence of widespread transcription detected by microarray tiling experiments. Trends Genet 21: 93-102
19. Kessler MM, Henry MF, Shen E, Zhao J, Gross S, Silver PA, Moore CL (1997) Hrp1, a sequence-specific RNA-binding protein that shuttles between the nucleus and the cytoplasm, is required for mRNA 30-end formation in yeast. Genes Dev 11: 2545-2556
20. KimM, Vasiljeva L, Rando OJ, Zhelkovsky A, Moore C, Buratowski S (2006) Distinct pathways for snoRNA and mRNA termination. Mol Cell 24: 723-734
21. Kopcewicz KA, O'Rourke TW, Reines D (2007) Metabolic regulation of IMD2 transcription and an unusual DNA element that generates short transcripts. Mol Cell Biol 27: 2821-2829
22. Kuehner JN, Brow DA (2008) Regulation of a eukaryotic gene by GTP-dependent start site selection and transcription attenuation. Mol Cell 31: 201-211
23. Kuehner JN, Pearson EL, Moore C (2011) Unravelling the means to an end: RNA polymerase II transcription termination. Nat Rev Mol Cell Biol 12: 283-294
24. 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
25. Lebreton A, Seraphin B (2008) Exosome-mediated quality control: substrate recruitment and molecular activity. Biochim Biophys Acta 1779: 558-565
26. Lunde BM, Horner M, Meinhart A (2011) Structural insights into cis element recognition of non-polyadenylated RNAs by the Nab3-RRM. Nucleic Acids Res 39: 337-346
27. Mandel CR, Bai Y, Tong L (2008) Protein factors in pre-mRNA 30-end processing. Cell Mol Life Sci 65: 1099-1122
28. Mayer A, Lidschreiber M, Siebert M, Leike K, Soding J, Cramer P (2011) Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol 17: 1272-1278
29. Millevoi S, Vagner S (2011) Molecular mechanisms of eukaryotic pre-mRNA 30 end processing regulation. Nucleic Acids Res 38: 2757-2774
30. Neil H, Malabat C, d'Aubenton-Carafa Y, Xu Z, Steinmetz LM, Jacquier A (2009) Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457: 1038-1042
31. Peters JM, Vangeloff AD, Landick R (2011) Bacterial transcription terminators: the RNA 30-end chronicles. J Mol Biol 412: 793-813
32. Proudfoot NJ (2011) Ending the message: poly(A) signals then and now. Genes Dev 25: 1770-1782
33. Schmid M, Jensen TH (2008) The exosome: a multipurpose RNAdecay machine. Trends Biochem Sci 33: 501-510
34. Schneider TD, Stormo GD, Gold L, Ehrenfeucht A (1986) Information content of binding sites on nucleotide sequences. J Mol Biol 188: 415-431
35. Steinmetz EJ, Conrad NK, Brow DA, Corden JL (2001) RNA-binding protein Nrd1 directs poly(A)-independent 30-end formation of RNA polymerase II transcripts. Nature 413: 327-331
36. Steinmetz EJ, Ng SB, Cloute JP, Brow DA (2006) cis-and trans-Acting determinants of transcription termination by yeast RNA polymerase II. Mol Cell Biol 26: 2688-2696
37. Thiebaut M, Colin J, Neil H, Jacquier A, Seraphin B, Lacroute F, Libri D (2008) Futile cycle of transcription initiation and termination modulates the response to nucleotide shortage in S. cerevisiae. Mol Cell 31: 671-682
38. Thiebaut M, Kisseleva-Romanova E, Rougemaille M, Boulay J, Libri D (2006) Transcription termination and nuclear degradation of cryptic unstable transcripts: a role for the nrd1-nab3 pathway in genome surveillance. Mol Cell 23: 853-864
39. Tietjen JR, Zhang DW, Rodriguez-Molina JB, White BE, Akhtar MS, Heidemann M, Li X, Chapman RD, Shokat K, Keles S, Eick D, Ansari AZ (2011) Chemical-genomic dissection of the CTD code. Nat Struct Mol Biol 17: 1154-1161
40. Valentini SR, Weiss VH, Silver PA (1999) Arginine methylation and binding of Hrp1p to the efficiency element for mRNA 30-end formation. RNA 5: 272-280
41. van Helden J (2003) Regulatory sequence analysis tools. Nucleic Acids Res 31: 3593-3596
42. Vanacova 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
43. Vasiljeva L, Kim M, Mutschler H, Buratowski S, Meinhart A (2008) The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain. Nat Struct Mol Biol 15: 795-804
44. Wlotzka W, Kudla G, Granneman S, Tollervey D (2011) The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J 30: 1790-1803
45. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, Regnault B, Devaux F, Namane A, Seraphin B, Libri D, Jacquier A (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737
46. Xu Z, WeiW, Gagneur J, Perocchi F, Clauder-Munster S, Camblong J, Guffanti E, Stutz F, Huber W, Steinmetz LM (2009) Bidirectional promoters generate pervasive transcription in yeast. Nature 457: 1033-1037