Visualization of two transfer RNAs trapped in transit during elongation factor G-mediated translocation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 52, 2013, Pages 20964-20969

  Ramrath, David J F ^a,d   Lancaster, Laura ^b   Sprink, Thiemo ^a   Mielke, Thorsten ^a,c   Loerke, Justus ^a   Noller, Harry F ^b   Spahn, Christian M T ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d ETH ZURICH   (Switzerland)

Author keywords

Chimeric hybrid state; Fusidic acid; Ratcheting; Ribosome dynamics; Translocation mechanism

Indexed keywords

ELONGATION FACTOR G; MESSENGER RNA; TRANSFER RNA;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; EXTRACELLULAR MATRIX; HYDROLYSIS; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; RIBOSOME;

EID: 84891369006     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1320387110     Document Type: Article

References (43)

1. Yusupov MM, et al. (2001) Crystal structure of the ribosome at 5.5 A resolution. Science 292(5518): 883-896.
2. Moazed D, Noller HF (1989) Intermediate states in the movement of transfer RNA in the ribosome. Nature 342(6246): 142-148.
3. Blanchard SC, Kim HD, Gonzalez RL, Jr., Puglisi JD, Chu S (2004) tRNA dynamics on the ribosome during translation. Proc Natl Acad Sci USA 101(35): 12893-12898.
4. Munro JB, Altman RB, O'Connor N, Blanchard SC (2007) Identification of two distinct hybrid state intermediates on the ribosome. Mol Cell 25(4): 505-517.
5. Frank J, Agrawal RK (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406(6793): 318-322.
6. Ratje AH, et al. (2010) Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 468(7324): 713-716.
7. Ermolenko DN, Noller HF (2011) mRNA translocation occurs during the second step of ribosomal intersubunit rotation. Nat Struct Mol Biol 18(4): 457-462.
8. Spahn CM, et al. (2004) Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J 23(5): 1008-1019.
9. Guo Z, Noller HF (2012) Rotation of the head of the 30S ribosomal subunit during mRNA translocation. Proc Natl Acad Sci USA 109(50): 20391-20394.
10. Zhou J, Lancaster L, Donohue JP, Noller HF (2013) Crystal structures of EF-G-ribosome complexes trapped in intermediate states of translocation. Science 340(6140): 1236086.
11. Pulk A, Cate JH (2013) Control of ribosomal subunit rotation by elongation factor G. Science 340(6140):1235970.
12. Tourigny DS, Fernández IS, Kelley AC, Ramakrishnan V (2013) Elongation factor G bound to the ribosome in an intermediate state of translocation. Science 340(6140): 1235490.
13. Chen Y, Feng S, Kumar V, Ero R, Gao YG (2013) Structure of EF-G-ribosome complex in a pretranslocation state. Nat Struct Mol Biol 20(9): 1077-1084.
14. Agirrezabala X, et al. (2008) Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol Cell 32(2): 190-197.
15. Julián P, et al. (2008) Structure of ratcheted ribosomes with tRNAs in hybrid states. Proc Natl Acad Sci USA 105(44): 16924-16927.
16. Fischer N, Konevega AL, Wintermeyer W, Rodnina MV, Stark H (2010) Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 466(7304): 329-333.
17. Budkevich T, et al. (2011) Structure and dynamics of the mammalian ribosomal pretranslocation complex. Mol Cell 44(2): 214-224.
18. Agirrezabala X, et al. (2012) Structural characterization of mRNA-tRNA translocation intermediates. Proc Natl Acad Sci USA 109(16): 6094-6099.
19. Schuwirth BS, et al. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science 310(5749): 827-834.
20. Valle M, et al. (2003) Locking and unlocking of ribosomal motions. Cell 114(1): 123-134.
21. Connell SR, et al. (2007) Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol Cell 25(5): 751-764.
22. Gao YG, et al. (2009) The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326(5953): 694-699.
23. Loerke J, Giesebrecht J, Spahn CM (2010) Multiparticle cryo-EM of ribosomes. Methods Enzymol 483: 161-177.
24. Wang L, Altman RB, Blanchard SC (2011) Insights into the molecular determinants of EF-G catalyzed translocation. RNA 17(12): 2189-2200.
25. Spiegel PC, Ermolenko DN, Noller HF (2007) Elongation factor G stabilizes the hybridstate conformation of the 70S ribosome. RNA 13(9): 1473-1482.
26. Savelsbergh A, et al. (2003) An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation. Mol Cell 11(6): 1517-1523.
27. Matassova AB, Rodnina MV, Wintermeyer W (2001) Elongation factor G-induced structural change in helix 34 of 16S rRNA related to translocation on the ribosome. RNA 7(12): 1879-1885.
28. Taylor DJ, et al. (2007) Structures of modified eEF2 80S ribosome complexes reveal the role of GTP hydrolysis in translocation. EMBO J 26(9): 2421-2431.
29. Khade PK, Joseph S (2011) Messenger RNA interactions in the decoding center control the rate of translocation. Nat Struct Mol Biol 18(11): 1300-1302.
30. Peske F, Savelsbergh A, Katunin VI, Rodnina MV, Wintermeyer W (2004) Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J Mol Biol 343(5): 1183-1194.
31. Stanley RE, Blaha G, Grodzicki RL, Strickler MD, Steitz TA (2010) The structures of the anti-tuberculosis antibiotics viomycin and capreomycin bound to the 70S ribosome. Nat Struct Mol Biol 17(3): 289-293.
32. Ogle JM, Murphy FV, Tarry MJ, Ramakrishnan V (2002) Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111(5): 721-732.
33. Pan D, Kirillov SV, Cooperman BS (2007) Kinetically competent intermediates in the translocation step of protein synthesis. Mol Cell 25(4): 519-529.
34. Nguyen B, Ticu C, Wilson KS (2010) Intramolecular movements in EF-G, trapped at different stages in its GTP hydrolytic cycle, probed by FRET. J Mol Biol 397(5): 1245-1260.
35. Weisser M, Voigts-Hoffmann F, Rabl J, Leibundgut M, Ban N (2013) The crystal structure of the eukaryotic 40S ribosomal subunit in complex with eIF1 and eIF1A. Nat Struct Mol Biol 20(8): 1015-1017.
36. Jenner LB, Demeshkina N, Yusupova G, Yusupov M (2010) Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nat Struct Mol Biol 17(5): 555-560.
37. Feng S, Chen Y, Gao YG (2013) Crystal structure of 70S ribosome with both cognate tRNAs in the E and P sites representing an authentic elongation complex. PLoS ONE 8(3):e58829.
38. Hohsaka T, Taira H, Fukushima M, Sisido M (2001) Effect of single base insertion into anticodon loop of frameshift suppressor tRNA. Nucleic Acids Res Suppl (1): 189-190.
39. Pande S, Vimaladithan A, Zhao H, Farabaugh PJ (1995) Pulling the ribosome out of frame by +1 at a programmed frameshift site by cognate binding of aminoacyl-tRNA. Mol Cell Biol 15(1): 298-304.
40. Dunham CM, et al. (2007) Structures of tRNAs with an expanded anticodon loop in the decoding center of the 30S ribosomal subunit. RNA 13(6): 817-823.
41. Joseph S, Noller HF (1998) EF-G-catalyzed translocation of anticodon stem-loop analogs of transfer RNA in the ribosome. EMBO J 17(12): 3478-3483.
42. Frank J, et al. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116(1): 190-199.
43. Schmeing TM, et al. (2009) The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326(5953): 688-694.