Insertion of the Biogenesis Factor Rei1 Probes the Ribosomal Tunnel during 60S Maturation

Cell

Volumn 164, Issue 1-2, 2016, Pages 91-102

  Greber, Basil Johannes ^a,d   Gerhardy, Stefan ^a   Leitner, Alexander ^a   Leibundgut, Marc ^a   Salem, Michèle ^b   Boehringer, Daniel ^a   Leulliot, Nicolas ^b   Aebersold, Ruedi ^a,c   Panse, Vikram Govind ^a   Ban, Nenad ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALB1 PROTEIN; ARX1 PROTEIN; NUCLEOPORIN; PEPTIDYLTRANSFERASE; REI1 PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ALB1 PROTEIN, S CEREVISIAE; ARX1 PROTEIN, S CEREVISIAE; FUNGAL PROTEIN; REI1 PROTEIN, S CEREVISIAE; RIBOSOME PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL MATURATION; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; CYTOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RIBOSOME SUBUNIT; SACCHAROMYCES CEREVISIAE; AMINO ACID SEQUENCE; CHAETOMIUM; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; GENETICS; HUMAN; LARGE RIBOSOMAL SUBUNIT; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; CHAETOMIUM; CRYOELECTRON MICROSCOPY; FUNGAL PROTEINS; HUMANS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, LARGE, EUKARYOTIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EID: 84954271442     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.11.027     Document Type: Article

References (55)

1. M. Altvater, Y. Chang, A. Melnik, L. Occhipinti, S. Schütz, U. Rothenbusch, P. Picotti, and V.G. Panse Targeted proteomics reveals compositional dynamics of 60S pre-ribosomes after nuclear export Mol. Syst. Biol. 8 2012 628
2. M. Altvater, S. Schütz, Y. Chang, and V.G. Panse Dissecting ribosome assembly and transport in budding yeast Methods Cell Biol. 122 2014 437 461
3. J. Bassler, I. Klein, C. Schmidt, M. Kallas, E. Thomson, M.A. Wagner, B. Bradatsch, G. Rechberger, H. Strohmaier, E. Hurt, and H. Bergler The conserved Bud20 zinc finger protein is a new component of the ribosomal 60S subunit export machinery Mol. Cell. Biol. 32 2012 4898 4912
4. A. Ben-Shem, N. Garreau de Loubresse, S. Melnikov, L. Jenner, G. Yusupova, and M. Yusupov The structure of the eukaryotic ribosome at 3.0 Å resolution Science 334 2011 1524 1529
5. B. Bradatsch, J. Katahira, E. Kowalinski, G. Bange, W. Yao, T. Sekimoto, V. Baumgärtel, G. Boese, J. Bassler, K. Wild, and et al. Arx1 functions as an unorthodox nuclear export receptor for the 60S preribosomal subunit Mol. Cell 27 2007 767 779
6. B. Bradatsch, C. Leidig, S. Granneman, M. Gnädig, D. Tollervey, B. Böttcher, R. Beckmann, and E. Hurt Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel Nat. Struct. Mol. Biol. 19 2012 1234 1241
7. C. Bussiere, Y. Hashem, S. Arora, J. Frank, and A.W. Johnson Integrity of the P-site is probed during maturation of the 60S ribosomal subunit J. Cell Biol. 197 2012 747 759
8. E. Demoinet, A. Jacquier, G. Lutfalla, and M. Fromont-Racine The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae RNA 13 2007 1570 1581
9. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
10. A.J. Finch, C. Hilcenko, N. Basse, L.F. Drynan, B. Goyenechea, T.F. Menne, A. González Fernández, P. Simpson, C.S. D'Santos, M.J. Arends, and et al. Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman-Diamond syndrome Genes Dev. 25 2011 917 929
11. S. Gerhardy, A.M. Menet, C. Peña, J.J. Petkowski, and V.G. Panse Assembly and nuclear export of pre-ribosomal particles in budding yeast Chromosoma 123 2014 327 344
12. C. Giglione, A. Boularot, and T. Meinnel Protein N-terminal methionine excision Cell. Mol. Life Sci. 61 2004 1455 1474
13. B.J. Greber, D. Boehringer, C. Montellese, and N. Ban Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit Nat. Struct. Mol. Biol. 19 2012 1228 1233
14. B.J. Greber, D. Boehringer, M. Leibundgut, P. Bieri, A. Leitner, N. Schmitz, R. Aebersold, and N. Ban The complete structure of the large subunit of the mammalian mitochondrial ribosome Nature 515 2014 283 286
15. B.J. Greber, D. Boehringer, A. Leitner, P. Bieri, F. Voigts-Hoffmann, J.P. Erzberger, M. Leibundgut, R. Aebersold, and N. Ban Architecture of the large subunit of the mammalian mitochondrial ribosome Nature 505 2014 515 519
16. J.H. Ho, G. Kallstrom, and A.W. Johnson Nmd3p is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit J. Cell Biol. 151 2000 1057 1066
17. N.-J. Hung, and A.W. Johnson Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae Mol. Cell. Biol. 26 2006 3718 3727
18. N.-J. Hung, K.-Y. Lo, S.S. Patel, K. Helmke, and A.W. Johnson Arx1 is a nuclear export receptor for the 60S ribosomal subunit in yeast Mol. Biol. Cell 19 2008 735 744
19. M. Iwase, and A. Toh-e Ybr267w is a new cytoplasmic protein belonging to the mitotic signaling network of Saccharomyces cerevisiae Cell Struct. Funct. 29 2004 1 15
20. T.A. Jones, J.Y. Zou, S.W. Cowan, and M. Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. A 47 1991 110 119
21. K. Karbstein Quality control mechanisms during ribosome maturation Trends Cell Biol. 23 2013 242 250
22. L.A. Kaschner, R. Sharma, O.K. Shrestha, A.E. Meyer, and E.A. Craig A conserved domain important for association of eukaryotic J-protein co-chaperones Jjj1 and Zuo1 with the ribosome Biochim. Biophys. Acta 1853 2015 1035 1045
23. S. Kemmler, L. Occhipinti, M. Veisu, and V.G. Panse Yvh1 is required for a late maturation step in the 60S biogenesis pathway J. Cell Biol. 186 2009 863 880
24. S. Klinge, F. Voigts-Hoffmann, M. Leibundgut, S. Arpagaus, and N. Ban Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6 Science 334 2011 941 948
25. S. Klinge, F. Voigts-Hoffmann, M. Leibundgut, and N. Ban Atomic structures of the eukaryotic ribosome Trends Biochem. Sci. 37 2012 189 198
26. E. Kowalinski, G. Bange, B. Bradatsch, E. Hurt, K. Wild, and I. Sinning The crystal structure of Ebp1 reveals a methionine aminopeptidase fold as binding platform for multiple interactions FEBS Lett. 581 2007 4450 4454
27. G. Kramer, D. Boehringer, N. Ban, and B. Bukau The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins Nat. Struct. Mol. Biol. 16 2009 589 597
28. A. Lebreton, C. Saveanu, L. Decourty, J.-C. Rain, A. Jacquier, and M. Fromont-Racine A functional network involved in the recycling of nucleocytoplasmic pre-60S factors J. Cell Biol. 173 2006 349 360
29. C. Leidig, G. Bange, J. Kopp, S. Amlacher, A. Aravind, S. Wickles, G. Witte, E. Hurt, R. Beckmann, and I. Sinning Structural characterization of a eukaryotic chaperone - the ribosome-associated complex Nat. Struct. Mol. Biol. 20 2013 23 28
30. C. Leidig, M. Thoms, I. Holdermann, B. Bradatsch, O. Berninghausen, G. Bange, I. Sinning, E. Hurt, and R. Beckmann 60S ribosome biogenesis requires rotation of the 5S ribonucleoprotein particle Nat. Commun. 5 2014 3491
31. X. Li, P. Mooney, S. Zheng, C.R. Booth, M.B. Braunfeld, S. Gubbens, D.A. Agard, and Y. Cheng Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM Nat. Methods 10 2013 584 590
32. K.-Y. Lo, Z. Li, F. Wang, E.M. Marcotte, and A.W. Johnson Ribosome stalk assembly requires the dual-specificity phosphatase Yvh1 for the exchange of Mrt4 with P0 J. Cell Biol. 186 2009 849 862
33. K.-Y. Lo, Z. Li, C. Bussiere, S. Bresson, E.M. Marcotte, and A.W. Johnson Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit Mol. Cell 39 2010 196 208
34. S.J. Ludtke, P.R. Baldwin, and W. Chiu EMAN: semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128 1999 82 97
35. T.F. Menne, B. Goyenechea, N. Sánchez-Puig, C.C. Wong, L.M. Tonkin, P.J. Ancliff, R.L. Brost, M. Costanzo, C. Boone, and A.J. Warren The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast Nat. Genet. 39 2007 486 495
36. J. Merl, S. Jakob, K. Ridinger, T. Hierlmeier, R. Deutzmann, P. Milkereit, and H. Tschochner Analysis of ribosome biogenesis factor-modules in yeast cells depleted from pre-ribosomes Nucleic Acids Res. 38 2010 3068 3080
37. A.E. Meyer, N.-J. Hung, P. Yang, A.W. Johnson, and E.A. Craig The specialized cytosolic J-protein, Jjj1, functions in 60S ribosomal subunit biogenesis Proc. Natl. Acad. Sci. USA 104 2007 1558 1563
38. A.E. Meyer, L.A. Hoover, and E.A. Craig The cytosolic J-protein, Jjj1, and Rei1 function in the removal of the pre-60 S subunit factor Arx1 J. Biol. Chem. 285 2010 961 968
39. J.A. Mindell, and N. Grigorieff Accurate determination of local defocus and specimen tilt in electron microscopy J. Struct. Biol. 142 2003 334 347
40. V.G. Panse, and A.W. Johnson Maturation of eukaryotic ribosomes: acquisition of functionality Trends Biochem. Sci. 35 2010 260 266
41. K.M. Parnell, and B.L. Bass Functional redundancy of yeast proteins Reh1 and Rei1 in cytoplasmic 60S subunit maturation Mol. Cell. Biol. 29 2009 4014 4023
42. B. Pertschy, C. Saveanu, G. Zisser, A. Lebreton, M. Tengg, A. Jacquier, E. Liebminger, B. Nobis, L. Kappel, I. van der Klei, and et al. Cytoplasmic recycling of 60S preribosomal factors depends on the AAA protein Drg1 Mol. Cell. Biol. 27 2007 6581 6592
43. J. Rabl, M. Leibundgut, S.F. Ataide, A. Haag, and N. Ban Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1 Science 331 2011 730 736
44. U. Raue, S. Oellerer, and S. Rospert Association of protein biogenesis factors at the yeast ribosomal tunnel exit is affected by the translational status and nascent polypeptide sequence J. Biol. Chem. 282 2007 7809 7816
45. G. Rigaut, A. Shevchenko, B. Rutz, M. Wilm, M. Mann, and B. Séraphin A generic protein purification method for protein complex characterization and proteome exploration Nat. Biotechnol. 17 1999 1030 1032
46. P.B. Rosenthal, and R. Henderson Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy J. Mol. Biol. 333 2003 721 745
47. S.H.W. Scheres RELION: implementation of a Bayesian approach to cryo-EM structure determination J. Struct. Biol. 180 2012 519 530
48. S.H.W. Scheres, and S. Chen Prevention of overfitting in cryo-EM structure determination Nat. Methods 9 2012 853 854
49. P. Stelter, F.M. Huber, R. Kunze, D. Flemming, A. Hoelz, and E. Hurt Coordinated Ribosomal L4 Protein Assembly into the Pre-Ribosome Is Regulated by Its Eukaryote-Specific Extension Mol. Cell 58 2015 854 862
50. W.F. Tivol, A. Briegel, and G.J. Jensen An improved cryogen for plunge freezing Microsc. Microanal. 14 2008 375 379
51. V. van Noort, B. Bradatsch, M. Arumugam, S. Amlacher, G. Bange, C. Creevey, S. Falk, D.R. Mende, I. Sinning, E. Hurt, and P. Bork Consistent mutational paths predict eukaryotic thermostability BMC Evol. Biol. 13 2013 7
52. T. Walzthoeni, A. Leitner, F. Stengel, and R. Aebersold Mass spectrometry supported determination of protein complex structure Curr. Opin. Struct. Biol. 23 2013 252 260
53. W. Yao, D. Roser, A. Köhler, B. Bradatsch, J. Bassler, and E. Hurt Nuclear export of ribosomal 60S subunits by the general mRNA export receptor Mex67-Mtr2 Mol. Cell 26 2007 51 62
54. Y. Yao, E. Demoinet, C. Saveanu, P. Lenormand, A. Jacquier, and M. Fromont-Racine Ecm1 is a new pre-ribosomal factor involved in pre-60S particle export RNA 16 2010 1007 1017
55. Y. Zhang, C. Ma, Y. Yuan, J. Zhu, N. Li, C. Chen, S. Wu, L. Yu, J. Lei, and N. Gao Structural basis for interaction of a cotranslational chaperone with the eukaryotic ribosome Nat. Struct. Mol. Biol. 21 2014 1042 1046