Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel

Nature Structural and Molecular Biology

Volumn 19, Issue 12, 2012, Pages 1234-1241

  Bradatsch, Bettina ^a   Leidig, Christoph ^b   Granneman, Sander ^c   Gnädig, Marén ^a   Tollervey, David ^c   Böttcher, Bettina ^c,d   Beckmann, Roland ^b   Hurt, Ed ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARX1 PROTEIN; METHIONYL AMINOPEPTIDASE; PROTEIN; UNCLASSIFIED DRUG;

60S RIBOSOME SUBUNIT; ARTICLE; BIOGENESIS; CONTROLLED STUDY; CROSS LINKING; IMMUNOELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; RIBOSOME SUBUNIT; SACCHAROMYCES CEREVISIAE; STRUCTURAL HOMOLOGY;

BIOLOGICAL TRANSPORT; CELL NUCLEUS; CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; RIBOSOMES; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84870834419     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2438     Document Type: Article

References (60)

1. Kressler, D., Hurt, E. & Bassler, J. Driving ribosome assembly. Biochim. Biophys. Acta 1803, 673-683 (2010).
2. Karbstein, K. Inside the 40S ribosome assembly machinery. Curr. Opin. Chem. Biol. 15, 657-663 (2011).
3. Görlich, D. & Kutay, U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15, 607-660 (1999).
4. Zemp, I. & Kutay, U. Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 581, 2783-2793 (2007).
5. Spahn, C.M. et al. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA-ribosome and subunit-subunit interactions. Cell 107, 373-386 (2001).
6. Armache, J.P. et al. Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-A resolution. Proc. Natl. Acad. Sci. USA 107, 19748-19753 (2010).
7. Ben-Shem, A., Jenner, L., Yusupova, G. & Yusupov, M. Crystal structure of the eukaryotic ribosome. Science 330, 1203-1209 (2010).
8. Rabl, J., Leibundgut, M., Ataide, S.F., Haag, A. & Ban, N. Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 331, 730-736 (2011).
9. Klinge, S., Voigts-Hoffmann, F., Leibundgut, M., Arpagaus, S. & Ban, N. Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 334, 941-948 (2011).
10. Tschochner, H. & Hurt, E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13, 255-263 (2003).
11. Schäfer, T. et al. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441, 651-655 (2006).
12. Strunk, B.S. et al. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333, 1449-1453 (2011).
13. Nissan, T.A. et al. A pre-ribosome with a tadpole-like structure functions in ATP-dependent maturation of 60S subunits. Mol. Cell 15, 295-301 (2004).
14. Ulbrich, C. et al. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 138, 911-922 (2009).
15. Ho, J.H., Kallstrom, G. & Johnson, A.W. Nmd3p is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit. J. Cell Biol. 151, 1057-1066 (2000).
16. Gadal, O. et al. Nuclear export of 60s ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol. Cell. Biol. 21, 3405-3415 (2001).
17. Sengupta, J. et al. Characterization of the nuclear export adaptor protein Nmd3 in association with the 60S ribosomal subunit. J. Cell Biol. 189, 1079-1086 (2010).
18. Yao, W. et al. Nuclear export of ribosomal 60S subunits by the general mRNA export receptor Mex67-Mtr2. Mol. Cell 26, 51-62 (2007).
19. Yao, W., Lutzmann, M. & Hurt, E. A versatile interaction platform on the Mex67-Mtr2 receptor creates an overlap between mRNA and ribosome export. EMBO J. 27, 6-16 (2008).
20. Bradatsch, B. et al. Arx1 functions as an unorthodox nuclear export receptor for the 60S preribosomal subunit. Mol. Cell 27, 767-779 (2007).
21. Hung, N.J., Lo, K.Y., Patel, S.S., Helmke, K. & Johnson, A.W. Arx1 is a nuclear export receptor for the 60S ribosomal subunit in yeast. Mol. Biol. Cell 19, 735-744 (2008).
22. Yao, Y. et al. Ecm1 is a new pre-ribosomal factor involved in pre-60S particle export. RNA 16, 1007-1017 (2010).
23. Oeffinger, M., Dlakic, M. & Tollervey, D. A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev. 18, 196-209 (2004).
24. Hackmann, A., Gross, T., Baierlein, C. & Krebber, H. The mRNA export factor Npl3 mediates the nuclear export of large ribosomal subunits. EMBO Rep. 12, 1024-1031 (2011).
25. Lebreton, A. et al. A functional network involved in the recycling of nucleocytoplasmic pre-60S factors. J. Cell Biol. 173, 349-360 (2006).
26. Nissan, T.A., Bassler, J., Petfalski, E., Tollervey, D. & Hurt, E. 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J. 21, 5539-5547 (2002).
27. Ben-Shem, A. et al. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 334, 1524-1529 (2011).
28. Kowalinski, E. et al. The crystal structure of Ebp1 reveals a methionine aminopeptidase fold as binding platform for multiple interactions. FEBS Lett. 581, 4450-4454 (2007).
29. Monie, T.P. et al. Structural insights into the transcriptional and translational roles of Ebp1. EMBO J. 26, 3936-3944 (2007).
30. Gartmann, M. et al. Mechanism of eIF6-mediated inhibition of ribosomal subunit joining. J. Biol. Chem. 285, 14848-14851 (2010).
31. Groft, C.M., Beckmann, R., Sali, A. & Burley, S.K. Crystal structures of ribosome anti-association factor IF6. Nat. Struct. Biol. 7, 1156-1164 (2000).
32. Lebreton, A., Saveanu, C., Decourty, L., Jacquier, A. & Fromont-Racine, M. Nsa2 is an unstable, conserved factor required for the maturation of 27 SB pre-rRNAs. J. Biol. Chem. 281, 27099-27108 (2006).
33. Granneman, S., Petfalski, E. & Tollervey, D. A cluster of ribosome synthesis factors regulate pre-rRNA folding and 5.8S rRNA maturation by the Rat1 exonuclease. EMBO J. 30, 4006-4019 (2011).
34. Granneman, S., Petfalski, E., Swiatkowska, A. & Tollervey, D. Cracking pre-40S ribosomal subunit structure by systematic analyses of RNA-protein cross-linking. EMBO J. 29, 2026-2036 (2010).
35. Granneman, S., Kudla, G., Petfalski, E. & Tollervey, D. Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs. Proc. Natl. Acad. Sci. USA 106, 9613-9618 (2009).
36. Beckmann, R. et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372 (2001).
37. Sweeney, R., Chen, L. & Yao, M.C. An rRNA variable region has an evolutionarily conserved essential role despite sequence divergence. Mol. Cell. Biol. 14, 4203-4215 (1994).
38. Wilson, D.N. & Nierhaus, K.H. Ribosomal proteins in the spotlight. Crit. Rev. Biochem. Mol. Biol. 40, 243-267 (2005).
39. Kemmler, S., Occhipinti, L., Veisu, M. & Panse, V.G. Yvh1 is required for a late maturation step in the 60S biogenesis pathway. J. Cell Biol. 186, 863-880 (2009).
40. Lo, K.Y., Li, Z., Wang, F., Marcotte, E.M. & Johnson, A.W. Ribosome stalk assembly requires the dual-specificity phosphatase Yvh1 for the exchange of Mrt4 with P0. J. Cell Biol. 186, 849-862 (2009).
41. Kruiswijk, T., Planta, R.J. & Krop, J.M. The course of the assembly of ribosomal subunits in yeast. Biochim. Biophys. Acta 517, 378-389 (1978).
42. Bassler, J., Kallas, M. & Hurt, E. The NUG1 GTPase reveals an N-terminal RNA-binding domain that is essential for association with 60 S pre-ribosomal particles. J. Biol. Chem. 281, 24737-24744 (2006).
43. Hung, N.J. & Johnson, A.W. Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae. Mol. Cell. Biol. 26, 3718-3727 (2006).
44. Hedges, J., West, M. & Johnson, A.W. Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J. 24, 567-579 (2005).
45. Strunk, B.S., Novak, M.N., Young, C.L. & Karbstein, K. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150, 111-121 (2012).
46. Thomson, E. & Tollervey, D. The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol. Cell. Biol. 30, 976-984 (2010).
47. Becker, T. et al. Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326, 1369-1373 (2009).
48. DeLano, W.L. The PyMOL Molecular Graphics System. http://www.pymol.org/ (2002).
49. Puig, O. et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24, 218-229 (2001).
50. Longtine, M.S. et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961 (1998).
51. Ludtke, S.J., Baldwin, P.R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
52. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R. & Schatz, M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24 (1996).
53. Radermacher, M., Wagenknecht, T., Verschoor, A. & Frank, J. Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli. J. Microsc. 146, 113-136 (1987).
54. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (1996).
55. Pettersen, E.F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
56. Wagenknecht, T., Grassucci, R. & Frank, J. Electron microscopy and computer image averaging of ice-embedded large ribosomal subunits from Escherichia coli. J. Mol. Biol. 199, 137-147 (1988).
57. Penczek, P.A., Frank, J. & Spahn, C.M. A method of focused classification, based on the bootstrap 3D variance analysis, and its application to EF-G-dependent translocation. J. Struct. Biol. 154, 184-194 (2006).
58. Ho, J.H., Kallstrom, G. & Johnson, A.W. Nascent 60S ribosomal subunits enter the free pool bound by Nmd3p. RNA 6, 1625-1634 (2000).
59. Santos-Rosa, H. et al. Nuclear mRNA export requires complex formation between Mex67p and Mtr2p at the nuclear pores. Mol. Cell. Biol. 18, 6826-6838 (1998).
60. Vilardell, J. & Warner, J.R. Ribosomal protein L32 of Saccharomyces cerevisiae influences both the splicing of its own transcript and the processing of rRNA. Mol. Cell. Biol. 17, 1959-1965 (1997).