Structural insights into the interaction of the nuclear exosome helicase Mtr4 with the preribosomal protein Nop53

RNA

Volumn 23, Issue 12, 2017, Pages 1780-1787

  Falk, Sebastian ^a   Tants, Jan Niklas ^b,c   Basquin, Jerôme ^a   Thoms, Matthias ^d   Hurt, Ed ^d   Sattler, Michael ^b,c   Conti, Elena ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

DExH helicase; FRH; Ribosome biogenesis; RNA exosome

Indexed keywords

ARGININE; GUANIDINE; HELICASE; MTR4 PROTEIN; NOP53 PROTEIN; PROTEIN; RIBOSOME RNA; RNA; RNA 23S; UNCLASSIFIED DRUG; DEAD BOX PROTEIN; MTR4 PROTEIN, S CEREVISIAE; NOP53 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HYDROPHOBICITY; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA BINDING; SACCHAROMYCES CEREVISIAE; STATIC ELECTRICITY; STEREOCHEMISTRY; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; CELL NUCLEUS; CHEMISTRY; ENZYMOLOGY; EXOSOME; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN CONFORMATION; QUANTITATIVE STRUCTURE ACTIVITY RELATION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CELL NUCLEUS; CRYSTALLOGRAPHY, X-RAY; DEAD-BOX RNA HELICASES; EXOSOMES; NUCLEAR PROTEINS; PROTEIN CONFORMATION; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY;

EID: 85034067551     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.062901.117     Document Type: Article

References (51)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecu-lar structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. 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.
3. Allmang C, Mitchell P, Petfalski E, Tollervey D. 2000. Degradation of ri-bosomal RNA precursors by the exosome. Nucleic Acids Res 28: 1684-1691.
4. Araki Y, Takahashi S, Kobayashi T, Kajiho H, Hoshino S, Katada T. 2001. Ski7p G protein interacts with the exosome and the Ski complex for 3′-to-5′ mRNA decay in yeast. EMBO J 20: 4684-4693.
5. Bernstein KA, Gallagher JEG, Mitchell BM, Granneman S, Baserga SJ. 2004. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell 3: 1619-1626.
6. Briggs MW. 1998. Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J Biol Chem 273: 13255-13263.
7. Brown JT, Bai X, Johnson AW. 2000. The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6: 449-457.
8. Butler JS, Mitchell P. 2011. Rrp6, rrp47 and cofactors of the nuclear exo-some. Adv Exp Med Biol 702: 91-104.
9. Chlebowski A, Lubas M, Jensen TH, Dziembowski A. 2013. RNA decay machines: the exosome. Biochim Biophys Acta 1829: 552-560.
10. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
11. Falk S, Weir JR, Hentschel J, Reichelt P, Bonneau F, Conti E. 2014. The molecular architecture of the TRAMP complex reveals the organization and interplay of its two catalytic activities. Mol Cell 55: 856-867.
12. Graille M, Séraphin B. 2012. Surveillance pathways rescuing eukaryotic ribosomes lost in translation. Nat Rev Mol Cell Biol 13: 727-735.
13. Granato DC, Gonzales FA, Luz JS, Cassiola F, Machado-Santelli GM, Oliveira CC. 2005. Nop53p, an essential nucleolar protein that interacts with Nop17p and Nip7p, is required for pre-rRNA processing in Saccharomyces cerevisiae. FEBS J 272: 4450-4463.
14. Granato DC, Machado-Santelli GM, Oliveira CC. 2008. Nop53p interacts with 5.8S rRNA co-transcriptionally, and regulates processing of pre-rRNA by the exosome. FEBS J 275: 4164-4178.
15. Halbach F, Rode M, Conti E. 2012. The crystal structure of S. cerevisiae Ski2, a DExH helicase associated with the cytoplasmic functions of the exosome. RNA 18: 124-134.
16. Halbach F, Reichelt P, Rode M, Conti E. 2013. The yeast ski complex: crystal structure and RNA channeling to the exosome complex. Cell 154: 814-826.
17. Henras AK, Plisson-Chastang C, O'Donohue MF, Chakraborty A, Gleizes PE. 2015. An overview of pre-ribosomal RNA processing in eukaryotes. Wiley Interdiscip Rev RNA 6: 225-242.
18. Jackson RN, Klauer AA, Hintze BJ, Robinson H, van Hoof A, Johnson SJ. 2010. The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing. EMBO J 29: 2205-2216.
19. Johnson SJ, Jackson RN. 2013. Ski2-like RNA helicase structures: common themes and complex assemblies. RNA Biol 10: 33-43.
20. Kabsch W. 2010. Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr D Biol Crystallogr 66: 133-144.
21. Kilchert C, Wittmann S, Vasiljeva L. 2016. The regulation and functions of the nuclear RNA exosome complex. Nat Rev Mol Cell Biol 17: 227-239.
22. Klauer AA, van Hoof A. 2012. Genetic interactions suggest multiple distinct roles of the arch and core helicase domains of Mtr4 in Rrp6 and exosome function. Nucleic Acids Res 41: 533-541.
23. Kowalinski E, Kögel A, Ebert J, Reichelt P, Stegmann E, Habermann B, Conti E. 2016. Structure of a cytoplasmic 11-subunit RNA exosome complex. Mol Cell 63: 125-134.
24. Kyrpides NC, Woese CR, Ouzounis CA. 1996. KOW: a novel motif linking a bacterial transcription factor with ribosomal proteins. Trends Biochem Sci 21: 425-426.
25. Met turnover in Saccharomyces cerevisiae and Mtr4p enzymatic activities in vitro. PLoS One 11: e0148090.
26. Makino DL, Baumgärtner M, Conti E. 2013a. Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495: 70-75.
27. Makino DL, Halbach F, Conti E. 2013b. The RNA exosome and protea-some: common principles of degradation control. Nat Rev Mol Cell Biol 14: 654-660.
28. Makino DL, Schuch B, Stegmann E, Baumgärtner M, Basquin C, Conti E. 2015. RNA degradation paths in a 12-subunit nuclear exo-some complex. Nature 524: 54-58.
29. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
30. 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.
31. Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E. 2002. 60S pre-ri-bosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J 21: 5539-5547.
32. Ozgur S, Buchwald G, Falk S, Chakrabarti S, Prabu JR, Conti E. 2015. The conformational plasticity of eukaryotic RNA-dependent ATPases. FEBS J 282: 850-863.
33. 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.
34. Schaeffer D, Clark A, Klauer AA, Tsanova B, van Hoof A. 2011. Functions of the cytoplasmic exosome. Adv Exp Med Biol 702: 79-90.
35. Schilders G, Raijmakers R, Raats JMH, Pruijn GJM. 2005. MPP6 is an exosome-associated RNA-binding protein involved in 5.8S rRNA maturation. Nucleic Acids Res 33: 6795-6804.
36. Schilders G, Egberts WV, Raijmakers R, Pruijn GJM. 2007. C1D is a major autoantibody target in patients with the polymyositis-sclero-derma overlap syndrome. Arthritis Rheum 56: 2449-2454.
37. Schmidt C, Kowalinski E, Shanmuganathan V, Defenouillère Q, Braunger K, Heuer A, Pech M, Namane A, Berninghausen O, Fromont-Racine M, et al. 2016. The cryo-EM structure of a ribo-some-Ski2-Ski3-Ski8 helicase complex. Science 354: 1431-1433.
38. Schuch B, Feigenbutz M, Makino DL, Falk S, Basquin C, Mitchell P, Conti E. 2014. The exosome-binding factors Rrp6 and Rrp47 form a composite surface for recruiting the Mtr4 helicase. EMBO J 33: 2828-2846.
39. Shi M, Collett M, Loros JJ, Dunlap JC. 2010. FRQ-interacting RNA heli-case mediates negative and positive feedback in the Neurospora cir-cadian clock. Genetics 184: 351-361.
40. Shoemaker CJ, Green R. 2012. Translation drives mRNA quality control. Nat Struct Mol Biol 19: 594-601.
41. Sloan KE, Schneider C, Watkins NJ. 2012. Comparison of the yeast and human nuclear exosome complexes. Biochem Soc Trans 40: 850-855.
42. Thoms M, Thomson E, Bassler J, Gnädig M, Griesel S, Hurt E. 2015. The exosome is recruited to RNA substrates through specific adaptor proteins. Cell 162: 1029-1038.
43. Thomson E, Tollervey D. 2005. Nop53p is required for late 60S ribo-some subunit maturation and nuclear export in yeast. RNA 11: 1215-1224.
44. Thomson E, Tollervey D. 2010. The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol Cell Biol 30: 976-984.
45. Thomson E, Ferreira-Cerca S, Hurt E. 2013. Eukaryotic ribosome biogenesis at a glance. J Cell Sci 126: 4815-4821.
46. Turowski TW, Tollervey D. 2015. Cotranscriptional events in eukaryotic ribosome synthesis. Wiley Interdiscip Rev RNA 6: 129-139.
47. Wasmuth EV, Januszyk K, Lima CD. 2014. Structure of an Rrp6-RNA exosome complex bound to poly(A) RNA. Nature 511: 435-439.
48. Weir JR, Bonneau F, Hentschel J, Conti E. 2010. Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance. Proc Natl Acad Sci 107: 12139-12144.
49. Wu S, Tutuncuoglu B, Yan K, Brown H, Zhang Y, TanD, Gamalinda M, Yuan Y, Li Z, Jakovljevic J, et al. 2016. Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes. Nature 534: 133-137.
50. Zinder JC, Lima CD. 2017. Targeting RNA for processing or destruction by the eukaryotic RNA exosome and its cofactors. Genes Dev 31: 88-100.
51. Zinder JC, Wasmuth EV, Lima CD. 2016. Nuclear RNA exosome at 3.1 Å reveals substrate specificities, RNA paths, and allosteric inhibition of Rrp44/Dis3. Mol Cell 64: 734-745.