Structure and semi-sequence-specific RNA binding of Nrd1

Nucleic Acids Research

Volumn 42, Issue 12, 2014, Pages 8024-8038

  Bacikova, Veronika ^a   Pasulka, Josef ^a   Kubicek, Karel ^a   Stefl, Richard ^a  

^a MASARYK UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDES AND PROTEINS; PROTEIN NRD1; RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ANISOTROPY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FLUORESCENCE ANALYSIS; IN VIVO STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA PROCESSING; RNA STRUCTURE; RNA TRANSCRIPTION; RNA TRANSLATION;

DIMERIZATION; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84903979434     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku446     Document Type: Article

References (68)

1. Richard, P., Manley, J.L. (2009) Transcription termination by nuclear RNA polymerases. Genes Dev., 23, 1247-1269.
2. Bentley, D. (2002) The mRNA assembly line: transcription and processing machines in the same factory. Curr. Opin. Cell Biol., 14, 336-342.
3. Steinmetz, E.J., Conrad, N.K., Brow, D.A., Corden, J.L. (2001) RNA-binding protein Nrd1 directs poly(A)-independent 3'-end formation of RNA polymerase II transcripts. Nature, 413, 327-331.
4. Arigo, J.T., Eyler, D.E., Carroll, K.L., Corden, J.L. (2006) Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell, 23, 841-851.
5. 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.
6. Vasiljeva, L., Buratowski, S. (2006) Nrd1 interacts with the nuclear exosome for 3' processing of RNA polymerase II transcripts. Mol. Cell, 21, 239-248.
7. Vanacova, S., Stefl, R. (2007) The exosome and RNA quality control in the nucleus. EMBO Rep., 8, 651-657.
8. Steinmetz, E.J., Brow, D.A. (1996) Repression of gene expression by an exogenous sequence element acting in concert with a heterogeneous nuclear ribonucleoprotein-like protein, Nrd1, and the putative helicase Sen1. Mol. Cell. Biol., 16, 6993-7003.
9. Steinmetz, E.J., Brow, D.A. (1998) Control of pre-mRNA accumulation by the essential yeast protein Nrd1 requires high-affinity transcript binding and a domain implicated in RNA polymerase II association. Proc. Natl. Acad. Sci. U.S.A., 95, 6699-6704.
10. Carroll, K.L., Pradhan, D.A., Granek, J.A., Clarke, N.D., Corden, J.L. (2004) Identification of cis elements directing termination of yeast nonpolyadenylated snoRNA transcripts. Mol. Cell. Biol., 24, 6241-6252.
11. Carroll, K.L., Ghirlando, R., Ames, J.M., Corden, J.L. (2007) Interaction of yeast RNA-binding proteins Nrd1 and Nab3 with RNA polymerase II terminator elements. RNA, 13, 361-373.
12. 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.
13. Porrua, O., Hobor, F., Boulay, J., Kubicek, K., D'Aubenton-Carafa, Y., Gudipati, R.K., Stefl, R., Libri, D. (2012) In vivo SELEX reveals novel sequence and structural determinants of Nrd1-Nab3-Sen1-dependent transcription termination. EMBO J., 31, 3935-3948.
14. Lunde, B.M., 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.
15. Vasiljeva, L., Kim, M., Terzi, N., Soares, L.M., Buratowski, S. (2008) Transcription termination and RNA degradation contribute to silencing of RNA polymerase II transcription within heterochromatin. Mol. Cell, 29, 313-323.
16. Jasnovidova, O., Stefl, R. (2013) The CTD code of RNA polymerase II: a structural view. Wiley Interdiscip. Rev. RNA, 4, 1-16.
17. Kubicek, K., Cerna, H., Holub, P., Pasulka, J., Hrossova, D., Loehr, F., Hofr, C., Vanacova, S., Stefl, R. (2012) Serine phosphorylation and proline isomerization in RNAP II CTD control recruitment of Nrd1. Genes Dev., 26, 1891-1896.
18. 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.
19. 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.
20. Wyers, F., Rougemaille, M., Badis, G., Rousselle, J.C., Dufour, M.E., Boulay, J., Regnault, B., Devaux, F., Namane, A., Seraphin, 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.
21. 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.
22. Jamonnak, N., Creamer, T.J., Darby, M.M., Schaughency, P., Wheelan, S.J., Corden, J.L. (2011) Yeast Nrd1, Nab3, and Sen1 transcriptome-wide binding maps suggest multiple roles in post-transcriptional RNA processing. RNA, 17, 2011-2025.
23. Creamer, T.J., Darby, M.M., Jamonnak, N., Schaughency, P., Hao, H., Wheelan, S.J., Corden, J.L. (2011) Transcriptome-wide binding sites for components of the Saccharomyces cerevisiae non-poly(A) termination pathway: Nrd1, Nab3, and Sen1. PLoS Genet., 7, e1002329.
24. Lepore, N., L., L.D. (2011) A functional interface at the rDNA connects rRNA synthesis, pre-rRNA processing and nucleolar surveillance in budding yeast. PLoS ONE, 6, e24962.
25. Honorine, R., Mosrin-Huaman, C., Hervouet-Coste, N., Libri, D., Rahmouni, A.R. (2011) Nuclear mRNA quality control in yeast is mediated by Nrd1 co-transcriptional recruitment, as revealed by the targeting of Rho-induced aberrant transcripts. Nucleic Acids Res., 39, 2809-2820.
26. Jenks, M.H., O'Rourke, T.W., Reines, D. (2008) Properties of an intergenic terminator and start site switch that regulate IMD2 transcription in yeast. Mol. Cell. Biol., 28, 3883-3893.
27. Ciais, D., Bohnsack, M.T., Tollervey, D. (2008) The mRNA encoding the yeast ARE-binding protein Cth2 is generated by a novel 3' processing. Nucleic Acids Res., 36, 3075-3084.
28. Noel, J.F., Larose, S., Abou Elela, S., Wellinger, R.J. (2012) Budding yeast telomerase RNA transcription termination is dictated by the Nrd1/Nab3 non-coding RNA termination pathway. Nucleic Acids Res., 40, 5625-5636.
29. Gardner, K.H., Kay, L.E. (1998) The use of 2H, 13C, 15N multidimensional NMR to study the structure and dynamics of proteins. Annu. Rev. Biophys. Biomol. Struct., 27, 357-406.
30. Goto, N.K., Gardner, K.H., Mueller, G.A., Willis, R.C., Kay, L.E. (1999) A robust and cost-effective method for the production of Val, Leu, Ile (delta 1) methyl-protonated 15N-, 13C-, 2H-labeled proteins. J. Biomol. NMR, 13, 369-374.
31. Tugarinov, V., Kanelis, V., Kay, L.E. (2006) Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat. Protoc., 1, 749-754.
32. Sattler, M., Schleucher, J., Griesinger, C. (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Magn. Reson. Spectrosc., 34, 93-158.
33. Tugarinov, V., Kay, L.E., Ibraghimov, I., Orekhov, V.Y. (2005) High-resolution four-dimensional 1H-13C NOE spectroscopy using methyl-TROSY, sparse data acquisition, and multidimensional decomposition. J. Am. Chem. Soc., 127, 2767-2775.
34. Montelione, G.T., Lyons, B.A., Emerson, S.D., Tashiro, M. (1992) An efficient triple resonance experiment using C-13 isotropic mixing for determining sequence-specific resonance assignments of isotopically-enriched proteins. J. Am. Chem. Soc., 114, 10974-10975.
35. Kay, L.E., Xu, G.Y., Singer, A.U., Muhandiram, D.R., Forman-Kay, J.D. (1993) A gradient-enhanced HCCH TOCSY experiment for recording side-chain H-1 and C-13 correlations in H2O samples of proteins. J. Magn. Reson. B, 101, 333-337.
36. Morris, M.J., Wingate, K.L., Silwal, J., Leeper, T.C., Basu, S. (2012) The porphyrin TmPyP4 unfolds the extremely stable G-quadruplex in MT3-MMP mRNA and alleviates its repressive effect to enhance translation in eukaryotic cells. Nucleic Acids Res., 40, 4137-4145.
37. Korzhnev, D.M., Billeter, M., Arseniev, A.S., Orekhov, V.Y. (2001) NMR studies of Brownian tumbling and internal motions in proteins. Prog. Nucl. Magn. Reson. Spectrosc., 38, 197-266.
38. Guntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol., 278, 353-378.
39. Herrmann, T., Guntert, P., Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 319, 209-227.
40. Case, D.A., Darden, T.A., Cheatham, T.E III, Simmerling, C.L., Wang, J., Duke, R.E., Luo, R., Walker Ross, C., Zhang, W., Merz, K.M. et al. (2012) AMBER 12. University of California, San Francisco, CA.
41. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins, 65, 712-725.
42. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K.M., Ferguson, D.M., Spellmeyer, D.C., Fox, T., Caldwell, J.W., Kollman, P.A. (1995) A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J. Am. Chem. Soc., 117, 5179-5197.
43. Stefl, R., Oberstrass, F.C., Hood, J.L., Jourdan, M., Zimmermann, M., Skrisovska, L., Maris, C., Peng, L., Hofr, C., Emeson, R.B. et al. (2010) The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove. Cell, 143, 225-237.
44. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R., Thornton, J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486.
45. Vriend, G. (1990) What If-a molecular modeling and drug design program. J. Mol. Graph., 8, 52-56.
46. Koradi, R., Billeter, M., Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph., 14, 51-55, 29-32.
47. Letunic, I., Doerks, T., Bork, P. (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res., 40, D302-D305.
48. Akerud, T., Thulin, E., Van Etten, R.L., Akke, M. (2002) Intramolecular dynamics of low molecular weight protein tyrosine phosphatase in monomer-dimer equilibrium studied by NMR: a model for changes in dynamics upon target binding. J. Mol. Biol., 322, 137-152.
49. Guntert, P., Mumenthaler, C., Wuthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol., 273, 283-298.
50. Maris, C., Dominguez, C., Allain, F.H. (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J., 272, 2118-2131.
51. Stefl, R., Skrisovska, L., Allain, F.H. (2005) RNA sequence- and shape-dependent recognition by proteins in the ribonucleoprotein particle. EMBO Rep., 6, 33-38.
52. Swanson, M.S., Nakagawa, T.Y., LeVan, K., Dreyfuss, G. (1987) Primary structure of human nuclear ribonucleoprotein particle C proteins: conservation of sequence and domain structures in heterogeneous nuclear RNA, mRNA, and pre-rRNA-binding proteins. Mol. Cell. Biol., 7, 1731-1739.
53. Adam, S.A., Nakagawa, T., Swanson, M.S., Woodruff, T.K., Dreyfuss, G. (1986) mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol. Cell. Biol., 6, 2932-2943.
54. Dreyfuss, G., Swanson, M.S., Pinol-Roma, S. (1988) Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation. Trends Biochem. Sci., 13, 86-91.
55. Handa, N., Nureki, O., Kurimoto, K., Kim, I., Sakamoto, H., Shimura, Y., Muto, Y., Yokoyama, S. (1999) Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature, 398, 579-585.
56. Clery, A., Blatter, M., Allain, F.H. (2008) RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol., 18, 290-298.
57. Daubner, G.M., Clery, A., Allain, F.H. (2013) RRM-RNA recognition: NMR or crystallography. . ., new findings. Curr. Opin. Struct. Biol., 23, 100-108.
58. Barraud, P., Allain, F.H. (2013) Solution structure of the two RNA recognition motifs of hnRNP A1 using segmental isotope labeling: how the relative orientation between RRMs influences the nucleic acid binding topology. J. Biomol. NMR, 55, 119-138.
59. Teplova, M., Yuan, Y.R., Phan, A.T., Malinina, L., Ilin, S., Teplov, A., Patel, D.J. (2006) Structural basis for recognition and sequestration of UUU(OH) 3' termini of nascent RNA polymerase III transcripts by La, a rheumatic disease autoantigen. Mol. Cell, 21, 75-85.
60. Huang, Y., Bayfield, M.A., Intine, R.V., Marala, R.J. (2006) Separate RNA-binding surfaces on the multifunctional La protein mediate distinguishable activities in tRNA. Nat. Struct. Mol. Biol., 13, 611-618.
61. Oberstrass, F.C., Auweter, S.D., Erat, M., Hargous, Y., Henning, A., Wenter, P., Reymond, L., Amir-Ahmady, B., Pitsch, S., Black, D.L. et al. (2005) Structure of PTB bound to RNA: specific binding and implications for splicing regulation. Science, 309, 2054-2057.
62. Sickmier, E.A., Frato, K.E., Shen, H., Paranawithana, S.R., Green, M.R., Klelkopf, C.L. (2006) Structural basis for polypyrimidine tract recognition by the essential pre-mRNA splicing factor U2AF65. Mol. Cell, 23, 49-59.
63. Deka, P., Rajan, P.K., Perez-Canadillas, J.M., Varani, G. (2005) Protein and RNA dynamics play key roles in determining the specific recognition of GU-rich polyadenylation regulatory elements by human Cstf-64 protein. J. Mol. Biol., 347, 719-733.
64. Perez-Canadillas, J.M., Varani, G. (2003) Recognition of GU-rich polyadenylation regulatory elements by human CstF-64 protein. EMBO J., 22, 2821-2830.
65. Schulz, D., Schwalb, B., Kiesel, A., Baejen, C., Torkler, P., Gagneur, J., Soeding, J., Cramer, P. (2013) Transcriptome surveillance by selective termination of noncoding RNA synthesis. Cell, 155, 1075-1087.
66. Dominguez, C., Fisette, J.F., Chabot, B., Allain, F.H. (2010) Structural basis of G-tract recognition and encaging by hnRNP F quasi-RRMs. Nat. Struct. Mol. Biol., 17, 853-861.
67. Samatanga, B., Dominguez, C., Jelesarov, I., Allain, F.H. (2013) The high kinetic stability of a G-quadruplex limits hnRNP F qRRM3 binding to G-tract RNA. Nucleic Acids Res., 41, 2505-2516.
68. Neil, H., Malabat, C., D'Aubenton-Carafa, Y., Xu, Z., Steinmetz, L.M., Jacquier, A. (2009) Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature, 457, 1038-1042.