Crystal structures of EF-G - Ribosome complexes trapped in intermediate states of translocation

Science

Volumn 340, Issue 6140, 2013, Pages

  Zhou, Jie ^a   Lancaster, Laura ^a   Donohue, John Paul ^a   Noller, Harry F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR G; FUSIDIC ACID; GUANOSINE TRIPHOSPHATE DERIVATIVE; MESSENGER RNA; RNA 16S; TRANSFER RNA; VIOMYCIN; DRUG DERIVATIVE; GDPNP COMPOUND; GUANOSINE TRIPHOSPHATE;

CRYSTAL STRUCTURE; MOLECULAR ANALYSIS; RNA;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLIZATION; GEOMETRY; HYDROLYSIS; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RIBOSOME; THERMUS THERMOPHILUS; CHEMISTRY; ENZYMOLOGY; LARGE RIBOSOMAL SUBUNIT; PROTEIN CONFORMATION; PROTEIN SYNTHESIS; X RAY CRYSTALLOGRAPHY;

THERMUS;

CRYSTALLOGRAPHY, X-RAY; FUSIDIC ACID; GUANOSINE TRIPHOSPHATE; PEPTIDE ELONGATION FACTOR G; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RNA, MESSENGER; RNA, TRANSFER; THERMUS THERMOPHILUS;

MLCS; MLOWN;

EID: 84879625362     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1236086     Document Type: Article

References (45)

1. D. Moazed, H. F. Noller, Intermediate states in the movement of transfer RNA in the ribosome. Nature 342, 142 (1989). doi: 10.1038/342142a0; pmid: 2682263
2. S. Dorner, J. L. Brunelle, D. Sharma, R. Green, The hybrid state of tRNA binding is an authentic translation elongation intermediate. Nat. Struct. Mol. Biol. 13, 234 (2006). doi: 10.1038/nsmb1060; pmid: 16501572
3. P. V. Cornish, D. N. Ermolenko, H. F. Noller, T. Ha, Spontaneous intersubunit rotation in single ribosomes. Mol. Cell 30, 578 (2008). doi: 10.1016/j.molcel.2008.05.004; pmid: 18538656
4. X. Agirrezabala et al., Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol. Cell 32, 190 (2008). doi: 10.1016/j.molcel.2008.10.001; pmid: 18951087
5. P. C. Spiegel, D. N. Ermolenko, H. F. Noller, Elongation factor G stabilizes the hybrid-state conformation of the 70S ribosome. RNA 13, 1473 (2007). doi: 10.1261/rna.601507; pmid: 17630323
6. J. A. Dunkle et al., Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332, 981 (2011). doi: 10.1126/science.1202692; pmid: 21596992
7. M. V. Rodnina, W. Wintermeyer, The ribosome as a molecular machine: The mechanism of tRNA-mRNA movement in translocation. Biochem. Soc. Trans. 39, 658 (2011). doi: 10.1042/BST0390658; pmid: 21428957
8. A. H. Ratje et al., Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 468, 713 (2010). doi: 10.1038/nature09547; pmid: 21124459
9. Z. Guo, H. F. Noller, Rotation of the head of the 30S ribosomal subunit during mRNA translocation. Proc. Natl. Acad. Sci. U.S.A. 109, 20391 (2012). doi: 10.1073/pnas.1218999109; pmid: 23188795
10. M. A. Borovinskaya, S. Shoji, J. M. Holton, K. Fredrick, J. H. Cate, A steric block in translation caused by the antibiotic spectinomycin. ACS Chem. Biol. 2, 545 (2007). doi: 10.1021/cb700100n; pmid: 17696316
11. D. J. Taylor et al., Structures of modified eEF2 80S ribosome complexes reveal the role of GTP hydrolysis in translocation. EMBO J. 26, 2421 (2007). doi: 10.1038/sj.emboj.7601677; pmid: 17446867
12. J. Frank, R. K. Agrawal, A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406, 318 (2000). doi: 10.1038/35018597; pmid: 10917535
13. H. Gao, M. Valle, M. Ehrenberg, J. Frank, Dynamics of EF-G interaction with the ribosome explored by classification of a heterogeneous cryo-EM dataset. J. Struct. Biol. 147, 283 (2004). doi: 10.1016/j.jsb.2004.02.008; pmid: 15450297
14. H. Stark, M. V. Rodnina, H. J. Wieden, M. van Heel, W. Wintermeyer, Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100, 301 (2000). doi: 10.1016/S0092-8674(00)80666-2; pmid: 10676812
15. Y. G. Gao et al., The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326, 694 (2009). doi: 10.1126/science.1179709; pmid: 19833919
16. J. W. Bodley, F. J. Zieve, L. Lin, S. T. Zieve, Formation of the ribosome-G factor-GDP complex in the presence of fusidic acid. Biochem. Biophys. Res. Commun. 37, 437 (1969). doi: 10.1016/0006-291X(69)90934-6; pmid: 4900137
17. L. B. Jenner, N. Demeshkina, G. Yusupova, M. Yusupov, Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nat. Struct. Mol. Biol. 17, 555 (2010). doi: 10.1038/nsmb.1790; pmid: 20400952
18. J. Zhou, L. Lancaster, S. Trakhanov, H. F. Noller, Crystal structure of release factor RF3 trapped in the GTP state on a rotated conformation of the ribosome. RNA 18, 230 (2012). doi: 10.1261/rna.031187.111; pmid: 22187675
19. A. Korostelev, S. Trakhanov, M. Laurberg, H. F. Noller, Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126, 1065 (2006). doi: 10.1016/j.cell.2006.08.032; pmid: 16962654
20. M. Selmer et al., Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 1935 (2006). http://www.ncbi.nlm.nih.gov/entrez/query.fcgi? cmd=Retrieve&db=PubMed&list-uids=16959973&dopt=Abstractdoi: 10.1126/science.1131127; pmid: 16959973
21. B. S. Schuwirth et al., Structures of the bacterial ribosome at 3.5 A resolution. Science 310, 827 (2005). doi: 10.1126/science.1117230; pmid: 16272117
22. T. M. Schmeing et al., The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326, 688 (2009). http://www.ncbi.nlm.nih.gov/ entrez/query.fcgi?cmd=Retrieve&db=PubMed&list-uids=19833920&dopt= Abstract doi: 10.1126/science.1179700; pmid: 19833920
23. J. C. Schuette et al., GTPase activation of elongation factor EF-Tu by the ribosome during decoding. EMBO J. 28, 755 (2009). doi: 10.1038/emboj.2009. 26; pmid: 19229291
24. A. Korostelev et al., Crystal structure of a translation termination complex formed with release factor RF2. Proc. Natl. Acad. Sci. U.S.A. 105, 19684 (2008). doi: 10.1073/pnas.0810953105; pmid: 19064930
25. H. R. Bourne, D. A. Sanders, F. McCormick, The GTPase superfamily: Conserved structure and molecular mechanism. Nature 349, 117 (1991). doi: 10.1038/349117a0; pmid: 1898771
26. R. M. Voorhees, T. M. Schmeing, A. C. Kelley, V. Ramakrishnan, The mechanism for activation of GTP hydrolysis on the ribosome. Science 330, 835 (2010). doi: 10.1126/science.1194460; pmid: 21051640
27. M. Laurberg et al., Structure of a mutant EF-G reveals domain III and possibly the fusidic acid binding site. J. Mol. Biol. 303, 593 (2000). doi: 10.1006/jmbi.2000.4168; pmid: 11054294
28. S. R. Connell et al., Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol. Cell 25, 751 (2007). doi: 10.1016/j.molcel.2007.01.027; pmid: 17349960
29. D. Mohr, W. Wintermeyer, M. V. Rodnina, GTPase activation of elongation factors Tu and G on the ribosome. Biochemistry 41, 12520 (2002). doi: 10.1021/bi026301y; pmid: 12369843
30. M. Helgstrand et al., The ribosomal stalk binds to translation factors IF2, EF-Tu, EF-G and RF3 via a conserved region of the L12 C-terminal domain. J. Mol. Biol. 365, 468 (2007). doi: 10.1016/j.jmb.2006.10.025; pmid: 17070545
31. H. Noji, R. Yasuda, M. Yoshida, K. Kinosita Jr., Direct observation of the rotation of F1-ATPase. Nature 386, 299 (1997). doi: 10.1038/386299a0; pmid: 9069291
32. C. Woese, Molecular mechanics of translation: A reciprocating ratchet mechanism. Nature 226, 817 (1970). doi: 10.1038/226817a0; pmid: 5444622
33. J. Frank, Intermediate states during mRNA-tRNA translocation. Curr. Opin. Struct. Biol. 22, 778 (2012). doi: 10.1016/j.sbi.2012.08.001; pmid: 22906732
34. P. Julián et al., Structure of ratcheted ribosomes with tRNAs in hybrid states. Proc. Natl. Acad. Sci. U.S.A. 105, 16924 (2008). doi: 10.1073/pnas.0809587105; pmid: 18971332
35. A. Korostelev, H. F. Noller, Analysis of structural dynamics in the ribosome by TLS crystallographic refinement. J. Mol. Biol. 373, 1058 (2007). doi: 10.1016/j.jmb.2007.08.054; pmid: 17897673
36. H. Jin, A. C. Kelley, V. Ramakrishnan, Crystal structure of the hybrid state of ribosome in complex with the guanosine triphosphatase release factor 3. Proc. Natl. Acad. Sci. U.S.A. 108, 15798 (2011). doi: 10.1073/pnas.1112185108; pmid: 21903932
37. T. A. Kunkel, K. Bebenek, J. McClary, Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204, 125 (1991). doi: 10.1016/0076-6879(91)04008-C; pmid: 1943776
38. I. Lasa, J. R. Castón, L. A. Fernández-Herrero, M. A. de Pedro, J. Berenguer, Insertional mutagenesis in the extreme thermophilic eubacteria Thermus thermophilus HB8. Mol. Microbiol. 6, 1555 (1992). doi: 10.1111/j.1365-2958.1992.tb00877.x; pmid: 1625584
39. W. Kabsch, Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795 (1993). doi: 10.1107/S0021889893005588
40. P. Evans, Scaling and assessment of data quality. Acta Crystallogr. D 62, 72 (2006). doi: 10.1107/S0907444905036693; pmid: 16369096
41. A. J. McCoy et al., Phaser crystallographic software. J. Appl. Cryst. 40, 658 (2007). doi: 10.1107/S0021889807021206
42. P. D. Adams et al., PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213 (2010). doi: 10.1107/S0907444909052925; pmid: 20124702
43. A. T. Brünger et al., Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905 (1998). doi: 10.1107/S0907444998003254; pmid: 9757107
44. T. A. Jones, J. Y. Zou, S. W. Cowan, M. Kjeldgaard, Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110 (1991). doi: 10.1107/ S0108767390010224; pmid: 2025413
45. P. Emsley, K. Cowtan, Coot: Model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126 (2004). doi: 10.1107/S0907444904019158; pmid: 15572765