Structure of EF-G-ribosome complex in a pretranslocation state

Nature Structural and Molecular Biology

Volumn 20, Issue 9, 2013, Pages 1077-1084

  Chen, Yun ^a   Feng, Shu ^a   Kumar, Veerendra ^a   Ero, Rya ^a   Gao, Yong Gui ^a,b  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR G; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE DERIVATIVE; PROTEIN S13; PROTEIN S19; RIBOSOME PROTEIN; RNA 23S; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; HYDROPHOBICITY; NONHUMAN; PRETRANSLOCATIONAL RIBOSOME; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RIBOSOME; RIBOSOME SUBUNIT; RNA HYBRIDIZATION; RNA STABILITY; STRUCTURE ANALYSIS; THERMUS THERMOPHILUS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GUANOSINE TRIPHOSPHATE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE ELONGATION FACTOR G; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RIBOSOMES; RNA, BACTERIAL; RNA, MESSENGER; RNA, TRANSFER; SEQUENCE HOMOLOGY, AMINO ACID; THERMUS THERMOPHILUS;

THERMUS THERMOPHILUS;

EID: 84883672314     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2645     Document Type: Article

References (50)

1. Moazed, D. & Noller, H.F. Intermediate states in the movement of transfer RNA in the ribosome. Nature 342, 142-148 (1989). (Pubitemid 19277015)
2. Frank, J. & Agrawal, R.K. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406, 318-322 (2000). (Pubitemid 30604411)
3. Rodnina, M.V., Savelsbergh, A., Katunin, V.I. & Wintermeyer, W. Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385, 37-41 (1997). (Pubitemid 27024544)
4. Connell, S.R. et al. Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol. Cell 25, 751-764 (2007). (Pubitemid 46341918)
5. Schuette, J.C. et al. GTPase activation of elongation factor EF-Tu by the ribosome during decoding. EMBO J. 28, 755-765 (2009).
6. Villa, E. et al. Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis. Proc. Natl. Acad. Sci. USA 106, 1063-1068 (2009).
7. Voorhees, R.M., Schmeing, T.M., Kelley, A.C. & Ramakrishnan, V. The mechanism for activation of GTP hydrolysis on the ribosome. Science 330, 835-838 (2010).
8. Liljas, A., Ehrenberg, M. & Aqvist, J. Comment on "The mechanism for activation of GTP hydrolysis on the ribosome". Science 333, 37 (2011).
9. Jin, H., Kelley, A.C. & Ramakrishnan, V. Crystal structure of the hybrid state of ribosome in complex with the guanosine triphosphatase release factor 3. Proc. Natl. Acad. Sci. USA 108, 15798-15803 (2011).
10. Zhou, J., Lancaster, L., Trakhanov, S. & Noller, H.F. Crystal structure of release factor RF3 trapped in the GTP state on a rotated conformation of the ribosome. RNA 18, 230-240 (2012).
11. Valle, M. et al. Locking and unlocking of ribosomal motions. Cell 114, 123-134 (2003). (Pubitemid 36859846)
12. Taylor, D.J. et al. Structures of modified eEF2 80S ribosome complexes reveal the role of GTP hydrolysis in translocation. EMBO J. 26, 2421-2431 (2007). (Pubitemid 46685859)
13. Selmer, M., Gao, Y.G., Weixlbaumer, A. & Ramakrishnan, V. Ribosome engineering to promote new crystal forms. Acta Crystallogr. D Biol. Crystallogr. 68, 578-583 (2012).
14. Gao, Y.G. et al. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326, 694-699 (2009).
15. Trabuco, L.G. et al. The role of L1 stalk-tRNA interaction in the ribosome elongation cycle. J. Mol. Biol. 402, 741-760 (2010).
16. Lill, R., Robertson, J.M. & Wintermeyer, W. Binding of the 3? terminus of tRNA to 23S rRNA in the ribosomal exit site actively promotes translocation. EMBO J. 8, 3933-3938 (1989). (Pubitemid 20016078)
17. Fei, J. et al. Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation. Proc. Natl. Acad. Sci. USA 106, 15702-15707 (2009).
18. Dorner, S., Brunelle, J.L., Sharma, D. & Green, R. The hybrid state of tRNA binding is an authentic translation elongation intermediate. Nat. Struct. Mol. Biol. 13, 234-241 (2006). (Pubitemid 43348509)
19. Ratje, A.H. et al. Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 468, 713-716 (2010).
20. Dunkle, J.A. et al. Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332, 981-984 (2011).
21. Ben-Shem, A. et al. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 334, 1524-1529 (2011).
22. Jenner, L., Demeshkina, N., Yusupova, G. & Yusupov, M. Structural rearrangements of the ribosome at the tRNA proofreading step. Nat. Struct. Mol. Biol. 17, 1072-1078 (2010).
23. Czworkowski, J., Wang, J., Steitz, T.A. & Moore, P.B. The crystal structure of elongation factor G complexed with GDP, at 2.7 A resolution. EMBO J. 13, 3661-3668 (1994).
24. Hansson, S., Singh, R., Gudkov, A.T., Liljas, A. & Logan, D.T. Structural insights into fusidic acid resistance and sensitivity in EF-G. J. Mol. Biol. 348, 939-949 (2005). (Pubitemid 40544393)
25. Hausner, T.P., Atmadja, J. & Nierhaus, K.H. Evidence that the G2661 region of 23S rRNA is located at the ribosomal binding sites of both elongation factors. Biochimie 69, 911-923 (1987).
26. Rambelli, F. et al. Effect of the antibiotic purpuromycin on cell-free protein-synthesizing systems. Biochem. J. 259, 307-310 (1989). (Pubitemid 19100530)
27. Clementi, N., Chirkova, A., Puffer, B., Micura, R. & Polacek, N. Atomic mutagenesis reveals A2660 of 23S ribosomal RNA as key to EF-G GTPase activation. Nat. Chem. Biol. 6, 344-351 (2010).
28. AEvarsson, A. et al. Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J. 13, 3669-3677 (1994).
29. Martemyanov, K.A. & Gudkov, A.T. Domain III of elongation factor G from Thermus thermophilus is essential for induction of GTP hydrolysis on the ribosome. J. Biol. Chem. 275, 35820-35824 (2000).
30. Savelsbergh, A. et al. An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation. Mol. Cell 11, 1517-1523 (2003). (Pubitemid 36776538)
31. Savelsbergh, A., Mohr, D., Kothe, U., Wintermeyer, W. & Rodnina, M.V. Control of phosphate release from elongation factor G by ribosomal protein L7/12. EMBO J. 24, 4316-4323 (2005). (Pubitemid 41828906)
32. Feng, S., Chen, Y. & Gao, Y.G. Crystal structure of 70S ribosome with both cognate tRNAs in the E and P sites representing an authentic elongation complex. PLoS ONE 8, e58829 (2013).
33. Munro, J.B., Altman, R.B., O'Connor, N. & Blanchard, S.C. Identification of two distinct hybrid state intermediates on the ribosome. Mol. Cell 25, 505-517 (2007). (Pubitemid 46274447)
34. Pan, D., Kirillov, S., Zhang, C.M., Hou, Y.M. & Cooperman, B.S. Rapid ribosomal translocation depends on the conserved 18-55 base pair in P-site transfer RNA. Nat. Struct. Mol. Biol. 13, 354-359 (2006). (Pubitemid 43873507)
35. Sprinzl, M. et al. Regulation of GTPases in the bacterial translation machinery. Biol. Chem. 381, 367-375 (2000). (Pubitemid 30453813)
36. Wallin, G., Kamerlin, S.C. & Aqvist, J. Energetics of activation of GTP hydrolysis on the ribosome. Nat. Commun. 4, 1733 (2013).
37. Schweins, T. et al. Substrate-assisted catalysis as a mechanism for GTP hydrolysis of p21ras and other GTP-binding proteins. Nat. Struct. Biol. 2, 36-44 (1995).
38. Cukras, A.R., Southworth, D.R., Brunelle, J.L., Culver, G.M. & Green, R. Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA:tRNA complex. Mol. Cell 12, 321-328 (2003). (Pubitemid 37238919)
39. Cukras, A.R. & Green, R. Multiple effects of S13 in modulating the strength of intersubunit interactions in the ribosome during translation. J. Mol. Biol. 349, 47-59 (2005). (Pubitemid 40616447)
40. Joseph, S. & Noller, H.F. EF-G-catalyzed translocation of anticodon stem-loop analogs of transfer RNA in the ribosome. EMBO J. 17, 3478-3483 (1998). (Pubitemid 28279520)
41. Agirrezabala, X. et al. Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol. Cell 32, 190-197 (2008).
42. Sengupta, J. et al. Visualization of the eEF2-80S ribosome transition-state complex by cryo-electron microscopy. J. Mol. Biol. 382, 179-187 (2008).
43. Tourigny, D.S., Fernandez, I.S., Kelley, A.C. & Ramakrishnan, V. Elongation factor G bound to the ribosome in an intermediate state of translocation. Science 340, 1235490 (2013).
44. Pulk, A. & Cate, J.H. Control of ribosomal subunit rotation by elongation factor G. Science 340, 1235970 (2013).
45. Zhou, J., Lancaster, L., Donohue, J.P. & Noller, H.F. Crystal structures of EF-G-ribosome complexes trapped in intermediate states of translocation. Science 340, 1236086 (2013).
46. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-200 (1993).
47. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007). (Pubitemid 47080256)
48. Brünger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
49. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
50. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).