Destabilization of the P site codon-anticodon helix results from movement of tRNA into the P/E hybrid state within the ribosome

Molecular Cell

Volumn 20, Issue 4, 2005, Pages 613-622

  McGarry, Kevin G ^a   Walker, Sarah E ^a   Wang, Huanyu ^a   Fredrick, Kurt ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNESIUM CHLORIDE; MESSENGER RNA; PEPTIDE; TRANSFER RNA;

ACYLATION; ANTICODON; ARTICLE; CODON; COMPLEX FORMATION; DNA FLANKING REGION; GENETIC STABILITY; HYBRID; MUTAGENESIS; OPEN READING FRAME; RIBOSOME; RNA BINDING; RNA STABILITY; RNA STRUCTURE; RNA TRANSLATION; RNA TRANSPORT;

ANTICODON; BINDING SITES; CODON; ESCHERICHIA COLI PROTEINS; MAGNESIUM CHLORIDE; MUTATION; NUCLEIC ACID CONFORMATION; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PEPTIDES; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; RIBOSOMAL PROTEINS; RIBOSOMES; RNA STABILITY; RNA, MESSENGER; RNA, RIBOSOMAL; RNA, TRANSFER; RNA, TRANSFER, AMINO ACYL; TRANSFER RNA AMINOACYLATION;

EID: 27944445035     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2005.10.007     Document Type: Article

References (43)

1. R.K. Agrawal, P. Penczek, R.A. Grassucci, N. Burkhardt, K.H. Nierhaus, and J. Frank Effect of buffer conditions on the position of tRNA on the 70S ribosome as visualized by cryoelectron microscopy J. Biol. Chem. 274 1999 8723 8729
2. R.K. Agrawal, M.R. Sharma, M.C. Kiel, G. Hirokawa, T.M. Booth, C.M.T. Spahn, R.A. Grassucci, A. Kaji, and J. Frank Visualization of ribosome-recycling factor on the Escherichia coli 70S ribosome: functional implications Proc. Natl. Acad. Sci. USA 101 2004 8900 8905
3. P.F. Agris Decoding the genome: a modified view Nucleic Acids Res. 32 2004 223 238
4. S.C. Blanchard, H.D. Kim, R.J. Gonzalez, J.D. Puglisi, and S. Chu tRNA dynamics on the ribosome during translation Proc. Natl. Acad. Sci. USA 101 2004 12893 12898
5. M. Ehrenberg, N. Bilgin, and C.G. Kurland Design and use of a fast and accurate in vitro translation system G. Spedding Ribosomes and Protein Synthesis- A Practical Approach 1990 IRL Press Oxford 101 129
6. R.P. Fahlman, and O.C. Uhlenbeck Contribution of the esterified amino acid to the binding of aminoacylated tRNAs to the ribosomal P- and A-sites Biochemistry 43 2004 7575 7583
7. J. Feinberg, and S. Joseph Identification of molecular interactions between P site tRNA and the ribosome essential for translocation Proc. Natl. Acad. Sci. USA 98 2001 11120 11125
8. K. Fredrick, and H.F. Noller Accurate translocation of mRNA by the ribosome requires a peptidyl group or its analog on the tRNA moving into the 30S P site Mol. Cell 9 2002 1125 1131
9. K. Fredrick, and H.F. Noller Catalysis of ribosomal translocation by sparsomycin Science 300 2003 1159 1162
10. N. Gao, A.V. Zavialov, W. Li, J. Sengupta, M. Valle, R.P. Gursky, M. Ehrenberg, and J. Frank Mechanism for disassembly of the posttermination complex inferred from cryo-EM studies Mol. Cell 18 2005 663 674
11. R.A. Grajevskaja, Y.V. Ivanov, and E.M. Saminsky 70-S ribosomes of Escherichia coli have an additional site for deacylated tRNA binding Eur. J. Biochem. 128 1982 47 52
12. A. Hirashima, and A. Kaji Factor-dependent release of ribosomes from messenger RNA J. Mol. Biol. 65 1972 43 58
13. W. Huggins, and P. Wollenzien A 16S rRNA-tRNA product containing a nucleotide phototrimer and specific for tRNA in the P/E hybrid state in the Escherichia coli ribosome Nucleic Acids Res. 32 2004 6548 6556
14. O. Jerinic, and S. Joseph Conformational changes in the ribosome induced by translational miscoding agents J. Mol. Biol. 304 2000 707 713
15. A. Kaji, M.C. Kiel, G. Hirokawa, A.R. Muto, Y. Inokuchi, and H. Kaji The fourth step of protein synthesis: disassembly of the posttermination complex is catalyzed by elongation factor G and ribosome recycling factor, a near-perfect mimic of tRNA Cold Spring Harb. Symp. Quant. Biol. 66 2001 515 529
16. R. Karimi, M.Y. Pavlov, R.H. Buckingham, and M. Ehrenberg Novel roles for classical factors at the interface between translation termination and initiation Mol. Cell 3 1999 601 609
17. D.F. Kim, and R. Green Base-pairing between 23S rRNA and tRNA in the ribosomal A site Mol. Cell 4 1999 859 864
18. S.V. Kirillov, E.M. Makarov, and P. Semenkov Yu Quantitative study of interaction of deacylated tRNA with Escherichia coli ribosomes. Role of 50 S subunits in formation of the E site FEBS Lett. 157 1983 91 94
19. L. Lancaster, M.C. Kiel, A. Kaji, and H.F. Noller Orientation of ribosome recycling factor in the ribosome from directed hydroxyl radical probing Cell 111 2002 129 140
20. Phe in the exit site of Escherichia coli ribosomes J. Mol. Biol. 203 1988 699 705
21. R. Lill, J.M. Robertson, and W. Wintermeyer Binding of the 3′ terminus of tRNA to 23S rRNA in the ribosomal exit site actively promotes translocation EMBO J. 8 1989 3933 3938
22. V. Márquez, D.N. Wilson, and K.H. Nierhaus Functions and interplay of the tRNA-binding sites of the ribosome Biochem. Soc. Trans. 30 2002 133 140
23. D. Moazed, and H.F. Noller Intermediate states in the movement of transfer RNA in the ribosome Nature 342 1989 142 148
24. P. Nissen, J. Hansen, N. Ban, P.B. Moore, and T.A. Steitz The structural basis of ribosome activity in peptide bond synthesis Science 289 2000 920 930
25. O.W. Odom, W.D. Picking, and B. Hardesty Movement of tRNA but not the nascent peptide during peptide bond formation on ribosomes Biochemistry 29 1990 10734 10744
26. K. Ogawa, and A. Kaji Requirement for ribosome releasing factor for the release of ribosomes at the termination codon J. Biochem. (Tokyo) 58 1975 411 419
27. T. Pape, W. Wintermeyer, and M.V. Rodnina Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome EMBO J. 17 1998 7490 7497
28. T. Pape, W. Wintermeyer, and M. Rodnina Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome EMBO J. 18 1999 3800 3807
29. F. Peske, M. Rodnina, and W. Wintermeyer Sequence of steps in ribosome recycling as defined by kinetic analysis Mol. Cell 18 2005 403 412
30. H.J. Rheinberger, H. Sternbach, and K.H. Nierhaus Three tRNA binding sites on Escherichia coli ribosomes Proc. Natl. Acad. Sci. USA 78 1981 5310 5314
31. J.M. Robertson, and W. Wintermeyer Mechanism of ribosomal translocation: tRNA binds transiently to an exit site before leaving the ribosome during translocation J. Mol. Biol. 196 1987 525 540
32. R.R. Samaha, R. Green, and H.F. Noller A base pair between tRNA and 23S rRNA in the peptidyl transferase centre of the ribosome Nature 377 1995 309 314
33. A. Sarabhai, and S. Brenner A mutant which reinitiates the polypeptide chain after chain termination J. Mol. Biol. 27 1967 145 162
34. T.M. Schmeing, P.B. Moore, and T.A. Steitz Structures of deacylated tRNA mimics bound to the E site of the large ribosomal subunit RNA 9 2003 1345 1352
35. Y.P. Semenkov, M.V. Rodnina, and W. Wintermeyer The "allosteric three-site model" of elongation cannot be confirmed in a well-defined ribosome system from Escherichia coli Proc. Natl. Acad. Sci. USA 93 1996 12183 12188
36. Y.P. Semenkov, M.V. Rodnina, and W. Wintermeyer Energetic contribution of tRNA hybrid state formation to translocation catalysis on the ribosome Nat. Struct. Biol. 7 2000 1027 1031
37. C.M.T. Spahn, and K.H. Nierhaus Models of the elongation cycle: an evaluation Biol. Chem. 379 1998 753 772
38. M. Sprinzl, C. Horn, M. Brown, A. Ioudovitch, and S. Steinberg Compilation of tRNA sequences and sequences of tRNA genes Nucleic Acids Res. 26 1998 148 153
39. M. Valle, A. Zavialov, J. Sengupta, U. Rawat, M. Ehrenberg, and J. Frank Locking and unlocking of ribosomal motions Cell 114 2003 123 134
40. E.M. Youngman, J.L. Brunelle, A.B. Kochaniak, and R. Green The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release Cell 117 2004 589 599
41. M. Yusupov, G. Yusupova, A. Baucom, K. Lieberman, T.N. Earnest, J.H. Cate, and H.F. Noller Crystal structure of the ribosome at 5.5 Å resolution Science 292 2001 883 896
42. A.V. Zavialov, and M. Ehrenberg Peptidyl-tRNA regulates the GTPase activity of translation factors Cell 114 2003 113 122
43. A.V. Zavialov, V.V. Hauryliuk, and M. Ehrenberg Splitting of the posttermination ribosome into subunits by the concerted action of RRF and EF-G Mol. Cell 18 2005 675 686