The RNA polymerase 2 C-terminal domain-interacting domain of yeast Nrd1 contributes to the choice of termination pathway and couples to RNA processing by the nuclear exosome

Journal of Biological Chemistry

Volumn 288, Issue 51, 2013, Pages 36676-36690

  Heo, Dong Hyuk ^a   Yoo, Inhea ^b   Kong, Jiwon ^b   Lidschreiber, Michael ^c   Mayer, Andreas ^c   Choi, Byung Yi ^a   Hahn, Yoonsoo ^d   Cramer, Patrick ^c   Buratowski, Stephen ^e   Kim, Minkyu ^a,b  

^a Institute for Basic Science   (South Korea)

^b Seoul National University   (South Korea)

^c UNIVERSITY OF MUNICH   (Germany)

^d Chung Ang University   (South Korea)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; DIFFERENTIAL INTERACTION; RNA POLYMERASE; RNA PROCESSING; YEAST RNA;

RNA; YEAST;

PLANTS (BOTANY);

DIS3 PROTEIN; FUNGAL PROTEIN; MESSENGER RNA; NRD1 PROTEIN; PHOSPHOPROTEIN; PHOSPHORYLATED SERINE 5; RNA POLYMERASE II; RRP4 PROTEIN; RRP41 PROTEIN; RRP6 PROTEIN; RTT103 PROTEIN; SMALL NUCLEOLAR RNA; TRF4 PROTEIN; UNCLASSIFIED DRUG; ADH1 PROTEIN, S CEREVISIAE; ALCOHOL DEHYDROGENASE; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; NAB3 PROTEIN, S CEREVISIAE; NRD1 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; RNA BINDING PROTEIN; RRP6 PROTEIN, S CEREVISIAE; RTT103 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR;

ADH1 GENE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; EXOSOME; GENE; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN RNA BINDING; RNA CLEAVAGE; RNA DEGRADATION; RNA PROCESSING; RNA TRANSCRIPTION; SNORNA GENE; SNR13 GENE; SNR33 GENE; TRANSCRIPTION TERMINATION; YEAST; CELL NUCLEUS; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; C-TERMINAL DOMAIN; NRD1; SMALL NUCLEOLAR RNA (SNORNA);

ALCOHOL DEHYDROGENASE; BASE SEQUENCE; BINDING SITES; CELL NUCLEUS; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION TERMINATION, GENETIC;

C-TERMINAL DOMAIN; MRNA; NRD1; RNA POLYMERASE II; RNA PROCESSING; SMALL NUCLEOLAR RNA (SNORNA); TRANSCRIPTION TERMINATION;

EID: 84890905264     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.508267     Document Type: Article

References (56)

1. Birse, C. E., Minvielle-Sebastia, L., Lee, B. A., Keller, W., and Proudfoot, N. J. (1998) Coupling termination of transcription to messenger RNA maturation in yeast. Science 280, 298-301
2. Proudfoot, N. (2004) New perspectives on connecting messenger RNA 3' end formation to transcription. Curr. Opin. Cell Biol. 16, 272-278
3. Buratowski, S. (2005) Connections between mRNA 3' end processing and transcription termination. Curr. Opin. Cell Biol. 17, 257-261
4. Cho, E. J., Kobor, M. S., Kim, M., Greenblatt, J., and Buratowski, S. (2001) Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser-2 of theRNA polymerase 2 C- terminal domain. Genes Dev. 15, 3319-3329
5. Komarnitsky, P., Cho, E. J., and Buratowski, S. (2000) Different phosphorylated forms of RNA polymerase 2 and associated mRNA processing factors during transcription. Genes Dev. 14, 2452-2460
6. Cho, E. J., Takagi, T., Moore, C. R., and Buratowski, S. (1997) mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase 2 carboxy-terminal domain. Genes Dev. 11, 3319-3326
7. Kim, M., Ahn, S. H., Krogan, N. J., Greenblatt, J. F., and Buratowski, S. (2004) Transitions in RNA polymerase 2 elongation complexes at the 3' ends of genes. EMBO J. 23, 354-364
8. Ahn, S. H., Kim, M., and Buratowski, S. (2004) Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3' end processing. Mol. Cell 13, 67-76
9. Buratowski, S. (2003) The CTD code. Nat. Struct. Biol. 10, 679-680
10. Egloff, S., Dienstbier, M., and Murphy, S. (2012) Updating the RNA polymerase CTD code. Adding gene-specific layers. Trends Genet. 28, 333-341
11. Egloff, S., O'Reilly, D., Chapman, R. D., Taylor, A., Tanzhaus, K., Pitts, L., Eick, D., and Murphy, S. (2007) Serine-7 of the RNA polymerase 2 CTD is specifically required for snRNA gene expression. Science 318, 1777-1779
12. Hsin, J. P., Sheth, A., and Manley, J. L. (2011) RNAP 2 CTD phosphorylated on threonine-4 is required for histone mRNA 3' end processing. Science 334, 683-686
13. Hintermair, C., Heidemann, M., Koch, F., Descostes, N., Gut, M., Gut, I., Fenouil, R., Ferrier, P., Flatley, A., Kremmer, E., Chapman, R. D., Andrau, J. C., and Eick, D. (2012) Threonine-4 of mammalian RNA polymerase 2 CTD is targeted by Polo-like kinase 3 and required for transcriptional elongation. EMBO J. 31, 2784-2797
14. Mayer, A., Heidemann, M., Lidschreiber, M., Schreieck, A., Sun, M., Hintermair, C., Kremmer, E., Eick, D., and Cramer, P. (2012) CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase 2. Science 336, 1723-1725
15. Kim, M., Vasiljeva, L., Rando, O. J., Zhelkovsky, A., Moore, C., and Buratowski, S. (2006) Distinct pathways for snoRNA and mRNA termination. Mol. Cell 24, 723-734
16. Kim, M., Krogan, N. J., Vasiljeva, L., Rando, O. J., Nedea, E., Greenblatt, J. F., and Buratowski, S. (2004) The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase 2. Nature 432, 517-522
17. West, S., Gromak, N., and Proudfoot, N. J. (2004) Human 5'→33' exonuclease Xrn2 promotes transcription termination at co-transcriptional cleavage sites. Nature 432, 522-525
18. Kiss, T. (2002) Small nucleolar RNAs. An abundant group of noncoding RNAs with diverse cellular functions. Cell 109, 145-148
19. Thiebaut, M., Kisseleva-Romanova, E., Rougemaille, M., Boulay, J., and 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
20. Steinmetz, E. J., Conrad, N. K., Brow, D. A., and Corden, J. L. (2001) RNA-binding protein Nrd1 directs poly(A)-independent 3'-end formation of RNA polymerase 2 transcripts. Nature 413, 327-331
21. Ursic, D., Chinchilla, K., Finkel, J. S., and Culbertson, M. R. (2004) Multiple protein/protein and protein/RNA interactions suggest roles for yeast DNA/RNA helicase Sen1p in transcription, transcription-coupled DNArepair and RNA processing. Nucleic Acids Res. 32, 2441-2452
22. Vasiljeva, L., Kim, M., Mutschler, H., Buratowski, S., and Meinhart, A. (2008) The Nrd1- Nab3-Sen1 termination complex interacts with the Ser- 5-phosphorylated RNA polymerase 2 C-terminal domain. Nat. Struct. Mol. Biol. 15, 795-804
23. Vasiljeva, L., and Buratowski, S. (2006) Nrd1 interacts with the nuclear exosome for 3' processing of RNA polymerase 2 transcripts. Mol. Cell 21, 239-248
24. Butler, J. S. (2002) The yin and yang of the exosome. Trends Cell Biol. 12, 90-96
25. Liu, Q., Greimann, J. C., and Lima, C. D. (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127, 1223-1237
26. Lykke-Andersen, S., Brodersen, D. E., and Jensen, T. H. (2009) Origins and activities of the eukaryotic exosome. J. Cell Sci. 122, 1487-1494
27. Houseley, J., and Tollervey, D. (2009) The many pathways of RNA degradation. Cell 136, 763-776
28. Vanácová, S., Wolf, J., Martin, G., Blank, D., Dettwiler, S., Friedlein, A., Langen, H., Keith, G., and Keller, W. (2005) A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3, e189
29. Wyers, F., Rougemaille, M., Badis, G., Rousselle, J. C., Dufour, M. E., Boulay, J., Régnault, B., Devaux, F., Namane, A., Séraphin, B., Libri, D., and Jacquier, A. (2005) Cryptic pol 2 transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121, 725-737
30. Steinmetz, E. J., Warren, C. L., Kuehner, J. N., Panbehi, B., Ansari, A. Z., and Brow, D. A. (2006) Genome-wide distribution of yeast RNA polymerase 2 and its control by Sen1 helicase. Mol. Cell 24, 735-746
31. Gudipati, R. K., Villa, T., Boulay, J., and Libri, D. (2008) Phosphorylation of the RNA polymerase 2 C-terminal domain dictates transcription termination choice. Nat. Struct. Mol. Biol. 15, 786-794
32. Kubicek, K., Cerna, H., Holub, P., Pasulka, J., Hrossova, D., Loehr, F., Hofr, C., Vanacova, S., and Stefl, R. (2012) Serine phosphorylation and praline isomerization in RNAP 2 CTD control recruitment of Nrd1. Genes Dev. 26, 1891-1896
33. Storici, F., and Resnick, M. A. (2006) The delitto perfetto approach to in vivo site- directed mutagenesis and chromosome rearrangements with synthetic oligonucleotides in yeast. Methods Enzymol. 409, 329-345
34. Sung, M. K., Ha, C. W., and Huh, W. K. (2008)Avector system for efficient and economical switching of C-terminal epitope tags in Saccharomyces cerevisiae. Yeast 25, 301-311
35. O'Geen, H., Nicolet, C. M., Blahnik, K., Green, R., and Farnham, P. J. (2006) Comparison of sample preparation methods for ChIP-chip assays. Bio Techniques 41, 577-580
36. David, L., Huber, W., Granovskaia, M., Toedling, J., Palm, C. J., Bofkin, L., Jones, T., Davis, R. W., and Steinmetz, L. M. (2006) A high-resolution map of transcription in the yeast genome. Proc. Natl. Acad. Sci. U.S.A. 103, 5320-5325
37. Mayer, A., Lidschreiber, M., Siebert, M., Leike, K., Söding, J., and Cramer, P. (2010) Uniform transitions of the general RNA polymerase 2 transcription complex. Nat. Struct. Mol. Biol. 17, 1272-1278
38. Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M., and Snyder, M. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320, 1344-1349
39. Dengl, S., Mayer, A., Sun, M., and Cramer, P. (2009) Structure and in vivo requirement of the yeast Spt6 SH2 domain. J. Mol. Biol. 389, 211-225
40. Marquardt, S., Hazelbaker, D. Z., and Buratowski, S. (2011) Distinct RNA degradation pathways and 3' extensions of yeast non-coding RNA species. Transcription 2, 145-154
41. Lunde, B. M., Reichow, S. L., Kim, M., Suh, H., Leeper, T. C., Yang, F., Mutschler, H., Buratowski, S., Meinhart, A., and Varani, G. (2010) Cooperative interaction of transcription termination factors with the RNA polymerase 2 C-terminal domain. Nat. Struct. Mol. Biol. 17, 1195-1201
42. Xu, Z., Wei, W., Gagneur, J., Perocchi, F., Clauder-Münster, S., Camblong, J., Guffanti, E., Stutz, F., Huber, W., and Steinmetz, L. M. (2009) Bidirectional promoters generate pervasive transcription in yeast. Nature 457, 1033-1037
43. Kim, M., Suh, H., Cho, E. J., and Buratowski, S. (2009) Phosphorylation of the yeast pb1 C-terminal domain at serines 2, 5, and 7. J. Biol. Chem. 284, 26421-26426
44. Meinhart, A., and Cramer, P. (2004) Recognition of RNA polymerase II carboxy-terminal domain by 3'-RNA-processing factors. Nature 430, 223-226
45. Becker, R., Loll, B., and Meinhart, A. (2008) Snapshots of the RNA processing factor CAF8 bound to different phosphorylated forms of the carboxyl-terminal domain of RNA polymerase 2. J. Biol. Chem. 283, 22659-22669
46. Chinchilla, K., Rodriguez-Molina, J. B., Ursic, D., Finkel, J. S., Ansari, A. Z., and Culbertson, M. R. (2012) Interactions of Sen1, Nrd1, and Nab3 with multiple phosphorylated forms of the Rpb1 C-terminal domain in Saccharomyces cerevisiae. Eukaryot. Cell 11, 417-429
47. Arigo, J. T., Carroll, K. L., Ames, J. M., and Corden, J. L. (2006) Regulation of yeast NRD1 expression by premature transcription termination. Mol. Cell 21, 641-651
48. Mandart, E., and Parker, R. (1995) Effects of mutations in the Saccharomyces cerevisiae RNA14, RNA15, and PAP1 genes on polyadenylation in vivo. Mol. Cell. Biol. 15, 6979-6986
49. Vo, L. T., Minet, M., Schmitter, J. M., Lacroute, F., and Wyers, F. (2001) Mpe1, a zinc knuckle protein, is an essential component of yeast cleavage and polyadenylation factor required for the cleavage and polyadenylation of mRNA. Mol. Cell. Biol. 21, 8346-8356
50. Carroll, K. L., Pradhan, D. A., Granek, J. A., Clarke, N. D., and Corden, J. L. (2004) Identification of cis elements directing termination of yeast nonpolyadenylated snoRNA transcripts. Mol. Cell. Biol. 24, 6241-6252
51. Carroll, K. L., Ghirlando, R., Ames, J. M., and Corden, J. L. (2007) Interaction of yeast RNA-binding proteins Nrd1 and Nab3 with RNA polymerase 2 terminator elements. RNA 13, 361-373
52. Heidmann, S., Schindewolf, C., Stumpf, G., and Domdey, H. (1994) Flexibility and interchangeability of polyadenylation signals in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 4633-4642
53. Porrua, O., Hobor, F., Boulay, J., Kubicek, K., D'Aubenton-Carafa, Y., Gudipati, R. K., Stefl, R., and Libri, D. (2012) In vivo SELEX reveals novel sequence and structural determinants of Nrd1-Nab3-Sen1-dependent transcription termination. EMBO J. 31, 3935-3948
54. Kim, H., Erickson, B., Luo, W., Seward, D., Graber, J. H., Pollock, D. D., Megee, P. C., and Bentley, D. L. (2010) Gene-specific RNA polymerase 2 phosphorylation and the CTD code. Nat. Struct. Mol. Biol. 17, 1279 -1286
55. Bataille, A. R., Jeronimo, C., Jacques, P. É., Laramée, L., Fortin, M. È., Forest, A., Bergeron, M., Hanes, S. D., and Robert, F. (2012) A universal RNA polymerase 2 CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Mol. Cell. 45, 158-170
56. Rondón, A. G., Mischo, H. E., Kawauchi, J., and Proudfoot, N. J. (2009) Fail-safe transcriptional termination for protein-coding genes in S. cerevisiae. Mol. Cell. 36, 88-98