Regulation of the mammalian elongation cycle by subunit rolling: A eukaryotic-specific ribosome rearrangement

Cell

Volumn 158, Issue 1, 2014, Pages 121-131

  Budkevich, Tatyana V ^a,b,c   Giesebrecht, Jan ^a   Behrmann, Elmar ^a   Loerke, Justus ^a   Ramrath, David J F ^a   Mielke, Thorsten ^a,b   Ismer, Jochen ^a   Hildebrand, Peter W ^a   Tung, Chang Shung ^d   Nierhaus, Knud H ^a,b   Sanbonmatsu, Karissa Y ^d,e   Spahn, Christian M T ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c INSTITUTE OF MOLECULAR BIOLOGY AND GENETICS   (Ukraine)

^d LOS ALAMOS NATIONAL LABORATORY   (United States)

^e NEW MEXICO CONSORTIUM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 2; ELONGATION FACTOR TU; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE DERIVATIVE; MESSENGER RNA; PROTEIN; PROTEIN GMPPNP; RIBOSOME PROTEIN; RIBOSOME RNA; TRANSFER RNA; UNCLASSIFIED DRUG; VALINE TRANSFER RNA;

ALPHA HELIX; ARTICLE; CODON; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; RIBOSOME; RNA CONFORMATION; ROTATION;

AMINO ACID SEQUENCE; ANIMALS; ANTICODON; CODON; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; HUMANS; MAMMALS; MOLECULAR SEQUENCE DATA; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; RABBITS; RIBOSOMES; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; TETRAHYMENA THERMOPHILA;

EID: 84903950561     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.04.044     Document Type: Article

References (62)

1. G.R. Andersen, L. Pedersen, L. Valente, I. Chatterjee, T.G. Kinzy, M. Kjeldgaard, and J. Nyborg Structural basis for nucleotide exchange and competition with tRNA in the yeast elongation factor complex eEF1A:eEF1Balpha Mol. Cell 6 2000 1261 1266
2. C.B. Andersen, T. Becker, M. Blau, M. Anand, M. Halic, B. Balar, T. Mielke, T. Boesen, J.S. Pedersen, and C.M. Spahn et al. Structure of eEF3 and the mechanism of transfer RNA release from the E-site Nature 443 2006 663 668
3. A.M. Anger, J.P. Armache, O. Berninghausen, M. Habeck, M. Subklewe, D.N. Wilson, and R. Beckmann Structures of the human and Drosophila 80S ribosome Nature 497 2013 80 85
4. N. Ban, R. Beckmann, J.H. Cate, J.D. Dinman, F. Dragon, S.R. Ellis, D.L. Lafontaine, L. Lindahl, A. Liljas, and J.M. Lipton et al. A new system for naming ribosomal proteins Curr. Opin. Struct. Biol. 24 2014 165 169
5. 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
6. U. Bommer, N. Burkhardt, R. Junemann, C.M.T. Spahn, F. Triana-Alonso, and K.H. Nierhaus Ribosomes and polysomes J. Graham, D. Rickwood, Subcellular Fractionation: A practical Approach 1997 IRL Press Washington, DC 271 301
7. T.V. Budkevich, A.V. El'skaya, and K.H. Nierhaus Features of 80S mammalian ribosome and its subunits Nucleic Acids Res. 36 2008 4736 4744
8. T. Budkevich, J. Giesebrecht, R.B. Altman, J.B. Munro, T. Mielke, K.H. Nierhaus, S.C. Blanchard, and C.M. Spahn Structure and dynamics of the mammalian ribosomal pretranslocation complex Mol. Cell 44 2011 214 224
9. S.R. Connell, C. Takemoto, D.N. Wilson, H. Wang, K. Murayama, T. Terada, M. Shirouzu, M. Rost, M. Schüler, and J. Giesebrecht et al. Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors Mol. Cell 25 2007 751 764
10. S.R. Connell, M. Topf, Y. Qin, D.N. Wilson, T. Mielke, P. Fucini, K.H. Nierhaus, and C.M. Spahn A new tRNA intermediate revealed on the ribosome during EF4-mediated back-translocation Nat. Struct. Mol. Biol. 15 2008 910 915
11. C.E. Fagan, J.A. Dunkle, T. Maehigashi, M.N. Dang, A. Devaraj, S.J. Miles, D. Qin, K. Fredrick, and C.M. Dunham Reorganization of an intersubunit bridge induced by disparate 16S ribosomal ambiguity mutations mimics an EF-Tu-bound state Proc. Natl. Acad. Sci. USA 110 2013 9716 9721
12. J. Frank, and C.M. Spahn The ribosome and the mechanism of protein synthesis Rep. Prog. Phys. 69 2006 1383 1417
13. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199
14. P. Geggier, R. Dave, M.B. Feldman, D.S. Terry, R.B. Altman, J.B. Munro, and S.C. Blanchard Conformational sampling of aminoacyl-tRNA during selection on the bacterial ribosome J. Mol. Biol. 399 2010 576 595
15. M. Hohn, G. Tang, G. Goodyear, P.R. Baldwin, Z. Huang, P.A. Penczek, C. Yang, R.M. Glaeser, P.D. Adams, and S.J. Ludtke SPARX, a new environment for Cryo-EM image processing J. Struct. Biol. 157 2007 47 55
16. N.T. Ingolia, L.F. Lareau, and J.S. Weissman Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes Cell 147 2011 789 802
17. M.P. Jacobson, R.A. Friesner, Z. Xiang, and B. Honig On the role of the crystal environment in determining protein side-chain conformations J. Mol. Biol. 320 2002 597 608
18. M.P. Jacobson, D.L. Pincus, C.S. Rapp, T.J. Day, B. Honig, D.E. Shaw, and R.A. Friesner A hierarchical approach to all-atom protein loop prediction Proteins 55 2004 351 367
19. L.B. Jenner, N. Demeshkina, G. Yusupova, and M. Yusupov Structural aspects of messenger RNA reading frame maintenance by the ribosome Nat. Struct. Mol. Biol. 17 2010 555 560
20. 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
21. K. Kobayashi, K. Saito, R. Ishitani, K. Ito, and O. Nureki Structural basis for translation termination by archaeal RF1 and GTP-bound EF1α complex Nucleic Acids Res. 40 2012 9319 9328
22. J. Loerke, J. Giesebrecht, and C.M. Spahn Multiparticle cryo-EM of ribosomes Methods Enzymol. 483 2010 161 177
23. S. Melnikov, A. Ben-Shem, N. Garreau de Loubresse, L. Jenner, G. Yusupova, and M. Yusupov One core, two shells: bacterial and eukaryotic ribosomes Nat. Struct. Mol. Biol. 19 2012 560 567
24. J.B. Munro, K.Y. Sanbonmatsu, C.M. Spahn, and S.C. Blanchard Navigating the ribosome's metastable energy landscape Trends Biochem. Sci. 34 2009 390 400
25. J.M. Ogle, F.V. Murphy, M.J. Tarry, and V. Ramakrishnan Selection of tRNA by the ribosome requires a transition from an open to a closed form Cell 111 2002 721 732
26. P.A. Penczek, C. Yang, J. Frank, and C.M. Spahn Estimation of variance in single-particle reconstruction using the bootstrap technique J. Struct. Biol. 154 2006 168 183
27. 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
28. A.H. Ratje, J. Loerke, A. Mikolajka, M. Brünner, P.W. Hildebrand, A.L. Starosta, A. Dönhöfer, S.R. Connell, P. Fucini, and T. Mielke et al. Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites Nature 468 2010 713 716
29. M.V. Rodnina, and W. Wintermeyer Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms Annu. Rev. Biochem. 70 2001 415 435
30. K.Y. Sanbonmatsu, S. Joseph, and C.S. Tung Simulating movement of tRNA into the ribosome during decoding Proc. Natl. Acad. Sci. USA 102 2005 15854 15859
31. S. Schilling-Bartetzko, A. Bartetzko, and K.H. Nierhaus Kinetic and thermodynamic parameters for tRNA binding to the ribosome and for the translocation reaction J. Biol. Chem. 267 1992 4703 4712
32. T.M. Schmeing, R.M. Voorhees, A.C. Kelley, Y.G. Gao, F.V. Murphy 4th, J.R. Weir, and V. Ramakrishnan The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA Science 326 2009 688 694
33. J.C. Schuette, F.V. Murphy 4th, A.C. Kelley, J.R. Weir, J. Giesebrecht, S.R. Connell, J. Loerke, T. Mielke, W. Zhang, and P.A. Penczek et al. GTPase activation of elongation factor EF-Tu by the ribosome during decoding EMBO J. 28 2009 755 765
34. C.M. Spahn, E. Jan, A. Mulder, R.A. Grassucci, P. Sarnow, and J. Frank Cryo-EM visualization of a viral internal ribosome entry site bound to human ribosomes: the IRES functions as an RNA-based translation factor Cell 118 2004 465 475
35. C.M. Spahn, M.G. Gomez-Lorenzo, R.A. Grassucci, R. Jørgensen, G.R. Andersen, R. Beckmann, P.A. Penczek, J.P. Ballesta, and J. Frank Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation EMBO J. 23 2004 1008 1019
36. J.A. Steitz Nucleotide sequences of the ribosomal binding sites of bacteriophage R17 RNA Cold Spring Harb. Symp. Quant. Biol. 34 1969 621 630
37. C.S. Tung, and K.Y. Sanbonmatsu Atomic model of the Thermus thermophilus 70S ribosome developed in silico Biophys. J. 87 2004 2714 2722
38. E. Villa, J. Sengupta, L.G. Trabuco, J. LeBarron, W.T. Baxter, T.R. Shaikh, R.A. Grassucci, P. Nissen, M. Ehrenberg, K. Schulten, and J. Frank Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis Proc. Natl. Acad. Sci. USA 106 2009 1063 1068
39. R.M. Voorhees, and V. Ramakrishnan Structural basis of the translational elongation cycle Annu. Rev. Biochem. 82 2013 203 236
40. R.M. Voorhees, T.M. Schmeing, A.C. Kelley, and V. Ramakrishnan The mechanism for activation of GTP hydrolysis on the ribosome Science 330 2010 835 838
41. D.N. Wilson The A-Z of bacterial translation inhibitors Crit. Rev. Biochem. Mol. Biol. 44 2009 393 433
42. R. Apweiler, A. Bairoch, C.H. Wu, W.C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H. Huang, R. Lopez, and M. Magrane et al. UniProt: the Universal Protein knowledgebase Nucleic Acids Res. 32 Database issue 2004 D115 D119
43. A. Ben-Shem, L. Jenner, G. Yusupova, and M. Yusupov Crystal structure of the eukaryotic ribosome Science 330 2010 1203 1209
44. A.T. Brunger Version 1.2 of the Crystallography and NMR system Nat. Protoc. 2 2007 2728 2733
45. E. Cayama, A. Yépez, F. Rotondo, E. Bandeira, A.C. Ferreras, and F.J. Triana-Alonso New chromatographic and biochemical strategies for quick preparative isolation of tRNA Nucleic Acids Res. 28 2000 E64
46. J.Z. Chen, and N. Grigorieff SIGNATURE: a single-particle selection system for molecular electron microscopy J. Struct. Biol. 157 2007 168 173
47. A.V. El'skaya, G.V. Ovcharenko, S.S. Palchevskii, Z.M. Petrushenko, F.J. Triana-Alonso, and K.H. Nierhaus Three tRNA binding sites in rabbit liver ribosomes and role of the intrinsic ATPase in 80S ribosomes from higher eukaryotes Biochemistry 36 1997 10492 10497
48. P.W. Hildebrand, A. Goede, R.A. Bauer, B. Gruening, J. Ismer, E. Michalsky, and R. Preissner SuperLooper - a prediction server for the modeling of loops in globular and membrane proteins Nucleic Acids Res. 37 Web Server issue 2009 W571 W574
49. K.S. Keating, and A.M. Pyle RCrane: semi-automated RNA model building Acta Crystallogr. D Biol. Crystallogr. 68 2012 985 995
50. W.M. Kemper, and W.C. Merrick Preparation of protein synthesis elongation factors from rabbit reticulocytes Methods Enzymol. 60 1979 638 648
51. M. Kjeldgaard, J. Nyborg, and B.F. Clark The GTP binding motif: variations on a theme FASEB J. 10 1996 1347 1368
52. L. Nilsson, and O. Nygård Reduced puromycin sensitivity of translocated polysomes after the addition of elongation factor 2 and non-hydrolysable GTP analogues FEBS Lett. 309 1992 89 91
53. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
54. M.H. Rhodin, and J.D. Dinman A flexible loop in yeast ribosomal protein L11 coordinates P-site tRNA binding Nucleic Acids Res. 38 2010 8377 8389
55. V.F. Shalak, T.V. Budkevich, B.S. Negrutskił, and A.V. El'skaia A fast and effective method for purification of elongation factor 1 alpha from rabbit liver Ukr. Biokhim. Zh. 69 1997 104 109
56. S. Shoji, S.E. Walker, and K. Fredrick Reverse translocation of tRNA in the ribosome Mol. Cell 24 2006 931 942
57. F. Sievers, A. Wilm, D. Dineen, T.J. Gibson, K. Karplus, W. Li, R. Lopez, H. McWilliam, M. Remmert, and J. Söding et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega Mol. Syst. Biol. 7 2011 539
58. C.M. Spahn, R. Beckmann, N. Eswar, P.A. Penczek, A. Sali, G. Blobel, and J. Frank Structure of the 80S ribosome from Saccharomyces cerevisiae - tRNA-ribosome and subunit-subunit interactions Cell 107 2001 373 386
59. F.J. Triana-Alonso, M. Dabrowski, J. Wadzack, and K.H. Nierhaus Self-coded 3′-extension of run-off transcripts produces aberrant products during in vitro transcription with T7 RNA polymerase J. Biol. Chem. 270 1995 6298 6307
60. C.S. Tung, S. Joseph, and K.Y. Sanbonmatsu All-atom homology model of the Escherichia coli 30S ribosomal subunit Nat. Struct. Biol. 9 2002 750 755
61. A.M. Waterhouse, J.B. Procter, D.M. Martin, M. Clamp, and G.J. Barton Jalview Version 2 - a multiple sequence alignment editor and analysis workbench Bioinformatics 25 2009 1189 1191
62. P.C. Whitford, A. Ahmed, Y.A. Yu, S.P. Hennelly, F. Tama, C.M.T. Spahn, J.N. Onuchic, and K.Y. Sanbonmatsu Excited states of ribosome translocation revealed through integrative molecular modeling Proc. Natl. Acad. Sci. USA 108 2011 18943 18948