TRANSLATION 2: FIDELITY, CATALYSIS, INITIATION AND TERMINATION
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1 Bio Reg Raul Andino February 28, 2013 TRANSLATION 2: FIDELITY, CATALYSIS, INITIATION AND TERMINATION MAJOR POINTS 1. Discrimination of cognate (C) from non-cognate (NC) trna at the ribosomal A site requires a large contribution from the ribosome to amplify the minimal differences in binding energy. Aminoacyl trnas enter the A site on the 30S ribosome in a ternary complex with EFTu.GTP. The anticodon stem-loop binds to the decoding site in 16S rrna, but the aminoacyl moiety is prevented from entering the peptidyl transferase site in 23S rrna until GTP has been hydrolyzed. 2. Kinetic proofreading, driven by induced fit, is used by the ribosome to discriminate between correct and incorrect aa-trna during both initial selection and proofreading. Kinetic proofreading is made possible by the action of the GTPase elongation factor (EF-Tu in bacteria) that delivers aa-trnas to the ribosome in a ternary complex with GTP, allowing for two sequential opportunities to reject an incorrect aa-trna, pre- and post-hydrolysis. 'Induced fit' describes conformational changes that are thought to be responsible for accelerating GTPase activation and trna accommodation upon recognition of cognate trna species. The ribosome recognizes the geometry of codon-anticodon base pairing at the first two positions but monitors the third, or wobble position, less stringently. 3. Codon recognition by cognate trna results in the hydrolysis of GTP by EF-Tu over 75 Å away. Binding energy of cognate trna is used to induce conformational changes in the ribosome that stabilize a transition state for GTP hydrolysis by EF-Tu and subsequently result in accelerated accommodation of trna into the peptidyl transferase center. In addition, the transition state for GTP hydrolysis is characterized, among other things, by a distorted trna. 4. The catalytic site is formed by the 23S rrna with the nearest amino acid is located 1.8 nm away. The center is a highly structured pocket that precisely orient the growing chain and an aminoacyl trna. A ring nitrogen of adenine acts as a functional group in an acid-base reaction. 5. The initiator codon AUG is also used to specify methionine internally. The initiator methionyl trna is specialized to interact with an Initiation Factor (IF2) instead of EFTu and to bind to the P site instead of the A site. 6. In prokaryotes, the initiator codon is constrained to lie a short distance downstream of a polypurine-rich sequence which base-pairs with the 3' end of 16S rrna (the Shine-Dalgarno (SD) interaction). Internal initiation sites can be used as independent ribosome entry sites (if they are not occluded). 1
2 7. In prokaryotes, mrnas that encode a product whose primary function is to bind RNA are often autogenously regulated. When the primary target is saturated, the protein shuts off translation of its secondary target, its own mrna. 8. Peptide release, the reaction that hydrolyzes a completed protein from the peptidyltrna upon completion of translation, is catalyzed in the active site of the large subunit of the ribosome and requires a class I release factor protein. The ribosome and release factor protein cooperate to accomplish two tasks: recognition of the stop codon and catalysis of peptidyltrna hydrolysis REFERENCES I. Reviews 1. Cochella, L. and R. Green, Fidelity in protein synthesis. Curr Biol, (14): p. R Nakamura, Y., K. Ito, L. A. Isaksson Emerging understanding of translation termination. Cell. 87: Green, R., H. F. Noller Ribosomes and translation. Annu Rev Biochem. 66: Korostelev, A., Ermolenko, D. N. & Noller, H. F. Structural dynamics of the ribosome. Curr Opin Chem Biol 12, (2008). 5. Ogle, J.M. and V. Ramakrishnan, Structural insights into translational fidelity. Annu Rev Biochem, : p Youngman, E. M., McDonald, M. E. & Green, R. Peptide release on the ribosome: mechanism and implications for translational control. Annu Rev Microbiol 62, (2008). 7. Rodnina, M and Wintermeyer, W., Fidelity of aminoacyl-trna selection on the ribosome: Kinetic and Structural Mechanisms. Annu Rev Biochem. 70: (2001) II. Fidelity of Decoding at the Ribosomal A site 7. Uhlenbeck, O. C., J. Baller, P. Doty Complementary oligonucleotide binding to the anticodon loop of fmet-transfer RNA. Nature. 225: Grosjean, H. J., H. S. de, D. M. Crothers On the physical basis for ambiguity in genetic coding interactions. Proc Natl Acad Sci U S A. 75: Hopfield, J. J Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc Natl Acad Sci U S A. 71:
3 10. Rosset, R., L. Gorini A ribosomal ambiguity mutation. J Mol Biol. 39: Ruusala, T., D. Andersson, M. Ehrenberg, C. G. Kurland Hyper-accurate ribosomes inhibit growth. Embo J. 3: Pape T, Wintermeyer W, Rodnina MV (1998) Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-trna to the A site of the e.coli ribosome. Embo J 17: Rodnina MV, Wintermeyer W (1998) Form follows function: structure of an elongation factor G-ribosome complex [comment]. Proc Natl Acad Sci U S A 95: Cochella, L. and R. Green, An active role for trna in decoding beyond codon:anticodon pairing. Science, (5725): p *Zaher, H. S. & Green, R. Quality control by the ribosome following peptide bond formation. Nature 457, (2009). III. The Ribosome 15. Noller, H. F., C. R. Woese Secondary structure of 16S ribosomal RNA. Science. 212: Rheinberger, H. J., H. Sternbach, K. H. Nierhaus Three trna binding sites on Escherichia coli ribosomes. Proc Natl Acad Sci U S A. 78: Moazed, D., H. F. Noller Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature. 327: Moazed, D., H. F. Noller Intermediate states in the movement of transfer RNA in the ribosome. Nature. 342: Noller, H. F., V. Hoffarth, L. Zimniak Unusual resistance of peptidyl transferase to protein extraction procedures. Science. 256: Stark, H., E. V. Orlova, A. J. Rinke, N. Junke, F. Mueller, M. Rodnina, W. Wintermeyer, R. Brimacombe, H. M. van Arrangement of trnas in pre- and posttranslocational ribosomes revealed by electron cryomicroscopy. Cell. 88: Agrawal, R. K., P. Penczek, R. A. Grassucci, Y. Li, A. Leith, K. H. Nierhaus, J. Frank Direct visualization of A-, P-, and E-site transfer RNAs in the Escherichia coli ribosome. Science. 271: Fourmy, D., M. I. Recht, S. C. Blanchard, J. D. Puglisi Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science. 274:
4 23. Borowski, C., M. V. Rodnina, W. Wintermeyer Truncated elongation factor G lacking the G domain promotes translocation of the 3' end but not of the anticodon domain of peptidyl- trna. Proc Natl Acad Sci U S A. 93: Joseph S, Weiser B, Noller HF (1997) Mapping the inside of the ribosome with an RNA helical ruler. Science 278: Clemons, W,., May, J., Winberly, B., McCutcheon, J., Capel, M.S.., and Rmaakrishnan, V. (1999). Structure of a bacterial 30S ribosomal subunit at 5.5 A resolution. Nature 400, Selmer, M., et al., Structure of the 70S ribosome complexed with mrna and trna. Science, (5795): p Cate, J. H., Yusupov, M. M., Yusupova, G. Z., Earnest, T. N., and Noller, H. F. (1999). X-ray crystal structures of 70S ribosome functional complexes. Science 285, Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A., The complete atomic structure of the large ribosomal subunit at 2.4 angstrom resolution, Science, 289, (2000). 29. Nissen, P., Hansen, J., Ban, N., Moore, P. B., and Steitz, T. A., The structural basis of ribosome activity in peptide bond synthesis, Science, 289, (2000). 30. *Agirrezabala, X. et al. Visualization of the hybrid state of trna binding promoted by spontaneous ratcheting of the ribosome. Mol Cell 32, (2008). 31. Muth, G. W., Ortoleva-Donnelly, L., and Strobel, S. A., A single adenosine with a neutral pk(a) in the ribosomal peptidyl transferase center, Science, 289, (2000). Thompson, J. et al. Analysis of mutations at residues A2451 and G2447 of 23S rrna in the peptidyltransferase active site of the 50S ribosomal subunit. PNAS, 98, Ogle, J.M. et al. Selection of trna by the ribosome requires a transition from an open to a closed form. Cell, 111, (2002). 33. ***Weinger, J.S., et al., Substrate-assisted catalysis of peptide bond formation by the ribosome. Nat Struct Mol Biol, (11): p IV Initiation: Ribosome binding site in Prokaryotes 11. Varshney, U., Lee, C.P. & RajBhandary, U.L. From elongator trna to initiator trna. Proc Natl Acad Sci U S A 90, (1993). 12. *Hui, A. & de, B.H. Specialized ribosome system: preferential translation of a single mrna species by a subpopulation of mutated ribosomes in Escherichia coli. Proc Natl Acad Sci U S A 84, (1987). Shine-Dalgarno interaction in vivo. "Dedicated ribosome" 4
5 13. von, H.P., et al. Autoregulation of gene expression. Quantitative evaluation of the expression and function of the bacteriophage T4 gene 32 (single-stranded DNA binding) protein system. J Mol Biol 162, (1982). 14. Graffe, M., et al. The specificity of translational control switched with transfer RNA identity rules. Science 255, (1992). Simple autogenous regulatory loop for trna synthetase 15. Spedding, G. & Draper, D.E. Allosteric mechanism for translational repression in the Escherichia coli alpha operon. Proc Natl Acad Sci U S A 90, (1993). 16. Simonetti, A. et al. Structure of the 30S translation initiation complex. Nature 455, (2008). V. The Termination Factors 33. Ito, K., Uno, M., and Nakamura, Y. (2000). A tripeptide 'anticodon' deciphers stop codons in messenger RNA. Nature 403, Arkov, A. L., Freistroffer, D. V., Ehrenberg, M., and Murgola, E. J. (1998). Mutations in RNAs of both ribosomal subunits cause defects in translation termination. Embo Journal 17, Song, H., Mugnier, P., Das, A., Webb, H., Evans, D., Tuite, M., Hemmings, B., and Barford, D. (2000). The crystal structure of human eukaryotic release factor erf-1- mechanism of stop codon recognition and peptidyl-trna hydrolysis. Cell 100, *Ito, K., K. Ebihara, M. Uno, Y. Nakamura Conserved motifs in prokaryotic and eukaryotic polypeptide release factors: trna-protein mimicry hypothesis. Proc Natl Acad Sci U S A. 93: Petry, et al Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell 123, Weixlbaumer, A. et al. Insights into translational termination from the structure of RF2 bound to the ribosome. Science 322, (2008). Brunelle, J. L., Shaw, J. J., Youngman, E. M. & Green, R. Peptide release on the ribosome depends critically on the 2' OH of the peptidyl-trna substrate. Rna 14, (2008). 5
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