5uyq › Citations

Ensemble cryo-EM elucidates the mechanism of translation fidelity.

<div class='caption-title'>Cryo-EM structures of cognate or near-cognate ternary complex on the 70S ribosome</div>
<div class='caption-title'>Interactions of cognate ternary complex with the 30S subunit</div>
<div class='caption-title'>Decoding-center rearrangements in Structures I to III</div>
Loveland AB, Demo G, Grigorieff N, Korostelev AA
OpenAccess logo Nature 546 113-117 (2017)
Related entries: 5uyk, 5uyl, 5uym, 5uyn, 5uyp

Cited: 88 times
EuropePMC logo PMID: 28538735

Abstract

Gene translation depends on accurate decoding of mRNA, the structural mechanism of which remains poorly understood. Ribosomes decode mRNA codons by selecting cognate aminoacyl-tRNAs delivered by elongation factor Tu (EF-Tu). Here we present high-resolution structural ensembles of ribosomes with cognate or near-cognate aminoacyl-tRNAs delivered by EF-Tu. Both cognate and near-cognate tRNA anticodons explore the aminoacyl-tRNA-binding site (A site) of an open 30S subunit, while inactive EF-Tu is separated from the 50S subunit. A transient conformation of decoding-centre nucleotide G530 stabilizes the cognate codon-anticodon helix, initiating step-wise 'latching' of the decoding centre. The resulting closure of the 30S subunit docks EF-Tu at the sarcin-ricin loop of the 50S subunit, activating EF-Tu for GTP hydrolysis and enabling accommodation of the aminoacyl-tRNA. By contrast, near-cognate complexes fail to induce the G530 latch, thus favouring open 30S pre-accommodation intermediates with inactive EF-Tu. This work reveals long-sought structural differences between the pre-accommodation of cognate and near-cognate tRNAs that elucidate the mechanism of accurate decoding.

Reviews - 5uyq mentioned but not cited (1)

  1. Translation in Prokaryotes. Rodnina MV. Cold Spring Harb Perspect Biol 10 a032664 (2018)

Articles - 5uyq mentioned but not cited (4)

  1. Measurement of atom resolvability in cryo-EM maps with Q-scores. Pintilie G, Zhang K, Su Z, Li S, Schmid MF, Chiu W. Nat Methods 17 328-334 (2020)
  2. Ensemble cryo-EM elucidates the mechanism of translation fidelity. Loveland AB, Demo G, Grigorieff N, Korostelev AA. Nature 546 113-117 (2017)
  3. Structural basis of ABCF-mediated resistance to pleuromutilin, lincosamide, and streptogramin A antibiotics in Gram-positive pathogens. Crowe-McAuliffe C, Murina V, Turnbull KJ, Kasari M, Mohamad M, Polte C, Takada H, Vaitkevicius K, Johansson J, Ignatova Z, Atkinson GC, O'Neill AJ, Hauryliuk V, Wilson DN. Nat Commun 12 3577 (2021)
  4. Geometric alignment of aminoacyl-tRNA relative to catalytic centers of the ribosome underpins accurate mRNA decoding. Girodat D, Wieden HJ, Blanchard SC, Sanbonmatsu KY. Nat Commun 14 5582 (2023)


Reviews citing this publication (22)

  1. The roles of structural dynamics in the cellular functions of RNAs. Ganser LR, Kelly ML, Herschlag D, Al-Hashimi HM. Nat Rev Mol Cell Biol 20 474-489 (2019)
  2. Aminoacyl-tRNA synthetases. Rubio Gomez MA, Ibba M. RNA 26 910-936 (2020)
  3. Translation Elongation and Recoding in Eukaryotes. Dever TE, Dinman JD, Green R. Cold Spring Harb Perspect Biol 10 a032649 (2018)
  4. Translation Termination and Ribosome Recycling in Eukaryotes. Hellen CUT. Cold Spring Harb Perspect Biol 10 a032656 (2018)
  5. Translational recoding: canonical translation mechanisms reinterpreted. Rodnina MV, Korniy N, Klimova M, Karki P, Peng BZ, Senyushkina T, Belardinelli R, Maracci C, Wohlgemuth I, Samatova E, Peske F. Nucleic Acids Res 48 1056-1067 (2020)
  6. How Messenger RNA and Nascent Chain Sequences Regulate Translation Elongation. Choi J, Grosely R, Prabhakar A, Lapointe CP, Wang J, Puglisi JD. Annu Rev Biochem 87 421-449 (2018)
  7. Transfer RNAs: diversity in form and function. Berg MD, Brandl CJ. RNA Biol 18 316-339 (2021)
  8. Ribosome Structure, Function, and Early Evolution. Opron K, Burton ZF. Int J Mol Sci 20 E40 (2018)
  9. Roles of elusive translational GTPases come to light and inform on the process of ribosome biogenesis in bacteria. Gibbs MR, Fredrick K. Mol Microbiol 107 445-454 (2018)
  10. Evolution of Life on Earth: tRNA, Aminoacyl-tRNA Synthetases and the Genetic Code. Lei L, Burton ZF. Life (Basel) 10 E21 (2020)
  11. New Insights into Ribosome Structure and Function. Jobe A, Liu Z, Gutierrez-Vargas C, Frank J. Cold Spring Harb Perspect Biol 11 a032615 (2019)
  12. Single-Particle Reconstruction of Biological Molecules-Story in a Sample (Nobel Lecture). Frank J. Angew Chem Int Ed Engl 57 10826-10841 (2018)
  13. Substrate-Induced Formation of Ribosomal Decoding Center for Accurate and Rapid Genetic Code Translation. Pavlov MY, Ehrenberg M. Annu Rev Biophys 47 525-548 (2018)
  14. How to benchmark RNA secondary structure prediction accuracy. Mathews DH. Methods 162-163 60-67 (2019)
  15. Lighting the way: Recent insights into the structure and regulation of phototropin blue light receptors. Hart JE, Gardner KH. J Biol Chem 296 100594 (2021)
  16. The problem of genetic code misreading during protein synthesis. Joshi K, Cao L, Farabaugh PJ. Yeast 36 35-42 (2019)
  17. The Structural Dynamics of Translation. Korostelev AA. Annu Rev Biochem 91 245-267 (2022)
  18. Evolution of the genetic code. Lei L, Burton ZF. Transcription 12 28-53 (2021)
  19. "Superwobbling" and tRNA-34 Wobble and tRNA-37 Anticodon Loop Modifications in Evolution and Devolution of the Genetic Code. Lei L, Burton ZF. Life (Basel) 12 252 (2022)
  20. Genome Expansion by tRNA +1 Frameshifting at Quadruplet Codons. Gamper H, Masuda I, Hou YM. J Mol Biol 434 167440 (2022)
  21. Mechanisms of ribosome recycling in bacteria and mitochondria: a structural perspective. Seely SM, Gagnon MG. RNA Biol 19 662-677 (2022)
  22. Diversity and Similarity of Termination and Ribosome Rescue in Bacterial, Mitochondrial, and Cytoplasmic Translation. Korostelev AA. Biochemistry (Mosc) 86 1107-1121 (2021)

Articles citing this publication (61)

  1. cisTEM, user-friendly software for single-particle image processing. Grant T, Rohou A, Grigorieff N. Elife 7 e35383 (2018)
  2. Dynamic basis for dG•dT misincorporation via tautomerization and ionization. Kimsey IJ, Szymanski ES, Zahurancik WJ, Shakya A, Xue Y, Chu CC, Sathyamoorthy B, Suo Z, Al-Hashimi HM. Nature 554 195-201 (2018)
  3. Single particle cryo-EM reconstruction of 52 kDa streptavidin at 3.2 Angstrom resolution. Fan X, Wang J, Zhang X, Yang Z, Zhang JC, Zhao L, Peng HL, Lei J, Wang HW. Nat Commun 10 2386 (2019)
  4. 2'-O-methylation in mRNA disrupts tRNA decoding during translation elongation. Choi J, Indrisiunaite G, DeMirci H, Ieong KW, Wang J, Petrov A, Prabhakar A, Rechavi G, Dominissini D, He C, Ehrenberg M, Puglisi JD. Nat Struct Mol Biol 25 208-216 (2018)
  5. Cryo-EM of elongating ribosome with EF-Tu•GTP elucidates tRNA proofreading. Loveland AB, Demo G, Korostelev AA. Nature 584 640-645 (2020)
  6. Structural basis of amino acid surveillance by higher-order tRNA-mRNA interactions. Li S, Su Z, Lehmann J, Stamatopoulou V, Giarimoglou N, Henderson FE, Fan L, Pintilie GD, Zhang K, Chen M, Ludtke SJ, Wang YX, Stathopoulos C, Chiu W, Zhang J. Nat Struct Mol Biol 26 1094-1105 (2019)
  7. Increased fidelity of protein synthesis extends lifespan. Martinez-Miguel VE, Lujan C, Espie-Caullet T, Martinez-Martinez D, Moore S, Backes C, Gonzalez S, Galimov ER, Brown AEX, Halic M, Tomita K, Rallis C, von der Haar T, Cabreiro F, Bjedov I. Cell Metab 33 2288-2300.e12 (2021)
  8. Structural dynamics of protein S1 on the 70S ribosome visualized by ensemble cryo-EM. Loveland AB, Korostelev AA. Methods 137 55-66 (2018)
  9. Time-resolved cryo-EM visualizes ribosomal translocation with EF-G and GTP. Carbone CE, Loveland AB, Gamper HB, Hou YM, Demo G, Korostelev AA. Nat Commun 12 7236 (2021)
  10. Visualization of translation termination intermediates trapped by the Apidaecin 137 peptide during RF3-mediated recycling of RF1. Graf M, Huter P, Maracci C, Peterek M, Rodnina MV, Wilson DN. Nat Commun 9 3053 (2018)
  11. Glyoxals as in vivo RNA structural probes of guanine base-pairing. Mitchell D, Ritchey LE, Park H, Babitzke P, Assmann SM, Bevilacqua PC. RNA 24 114-124 (2018)
  12. Ribosome inhibition by C9ORF72-ALS/FTD-associated poly-PR and poly-GR proteins revealed by cryo-EM. Loveland AB, Svidritskiy E, Susorov D, Lee S, Park A, Zvornicanin S, Demo G, Gao FB, Korostelev AA. Nat Commun 13 2776 (2022)
  13. Elongation factor-Tu can repetitively engage aminoacyl-tRNA within the ribosome during the proofreading stage of tRNA selection. Morse JC, Girodat D, Burnett BJ, Holm M, Altman RB, Sanbonmatsu KY, Wieden HJ, Blanchard SC. Proc Natl Acad Sci U S A 117 3610-3620 (2020)
  14. Dynamics of the context-specific translation arrest by chloramphenicol and linezolid. Choi J, Marks J, Zhang J, Chen DH, Wang J, Vázquez-Laslop N, Mankin AS, Puglisi JD. Nat Chem Biol 16 310-317 (2020)
  15. Extensive ribosome and RF2 rearrangements during translation termination. Svidritskiy E, Demo G, Loveland AB, Xu C, Korostelev AA. Elife 8 e46850 (2019)
  16. Methodological improvements for the analysis of domain movements in large biomolecular complexes. Veevers R, Hayward S. Biophys Physicobiol 16 328-336 (2019)
  17. Cryo-EM shows stages of initial codon selection on the ribosome by aa-tRNA in ternary complex with GTP and the GTPase-deficient EF-TuH84A. Fislage M, Zhang J, Brown ZP, Mandava CS, Sanyal S, Ehrenberg M, Frank J. Nucleic Acids Res 46 5861-5874 (2018)
  18. Analysis of discrete local variability and structural covariance in macromolecular assemblies using Cryo-EM and focused classification. Zhang C, Cantara W, Jeon Y, Musier-Forsyth K, Grigorieff N, Lyumkis D. Ultramicroscopy 203 170-180 (2019)
  19. Codon-specific effects of tRNA anticodon loop modifications on translational misreading errors in the yeast Saccharomyces cerevisiae. Joshi K, Bhatt MJ, Farabaugh PJ. Nucleic Acids Res 46 10331-10339 (2018)
  20. Conformational Control of Translation Termination on the 70S Ribosome. Svidritskiy E, Korostelev AA. Structure 26 821-828.e3 (2018)
  21. Accuracy of genetic code translation and its orthogonal corruption by aminoglycosides and Mg2+ ions. Zhang J, Pavlov MY, Ehrenberg M. Nucleic Acids Res 46 1362-1374 (2018)
  22. Insights into the base-pairing preferences of 8-oxoguanosine on the ribosome. Thomas EN, Simms CL, Keedy HE, Zaher HS. Nucleic Acids Res 47 9857-9870 (2019)
  23. Mechanism of premature translation termination on a sense codon. Svidritskiy E, Demo G, Korostelev AA. J Biol Chem 293 12472-12479 (2018)
  24. Supramolecular Double Helices from Small C3-Symmetrical Molecules Aggregated in Water. Lafleur RPM, Herziger S, Schoenmakers SMC, Keizer ADA, Jahzerah J, Thota BNS, Su L, Bomans PHH, Sommerdijk NAJM, Palmans ARA, Haag R, Friedrich H, Böttcher C, Meijer EW. J Am Chem Soc 142 17644-17652 (2020)
  25. Mutations in the anticodon stem of tRNA cause accumulation and Met22-dependent decay of pre-tRNA in yeast. Payea MJ, Hauke AC, De Zoysa T, Phizicky EM. RNA 26 29-43 (2020)
  26. Ribosome engineering reveals the importance of 5S rRNA autonomy for ribosome assembly. Huang S, Aleksashin NA, Loveland AB, Klepacki D, Reier K, Kefi A, Szal T, Remme J, Jaeger L, Vázquez-Laslop N, Korostelev AA, Mankin AS. Nat Commun 11 2900 (2020)
  27. Structural basis for +1 ribosomal frameshifting during EF-G-catalyzed translocation. Demo G, Gamper HB, Loveland AB, Masuda I, Carbone CE, Svidritskiy E, Hou YM, Korostelev AA. Nat Commun 12 4644 (2021)
  28. E. coli elongation factor Tu bound to a GTP analogue displays an open conformation equivalent to the GDP-bound form. Johansen JS, Kavaliauskas D, Pfeil SH, Blaise M, Cooperman BS, Goldman YE, Thirup SS, Knudsen CR. Nucleic Acids Res 46 8641-8650 (2018)
  29. Ribosomal ambiguity (ram) mutations promote the open (off) to closed (on) transition and thereby increase miscoding. Hoffer ED, Maehigashi T, Fredrick K, Dunham CM. Nucleic Acids Res 47 1557-1563 (2019)
  30. tRNA Dissociation from EF-Tu after GTP Hydrolysis: Primary Steps and Antibiotic Inhibition. Warias M, Grubmüller H, Bock LV. Biophys J 118 151-161 (2020)
  31. Decoding on the ribosome depends on the structure of the mRNA phosphodiester backbone. Keedy HE, Thomas EN, Zaher HS. Proc Natl Acad Sci U S A 115 E6731-E6740 (2018)
  32. Protein Methylation and Translation: Role of Lysine Modification on the Function of Yeast Elongation Factor 1A. White JT, Cato T, Deramchi N, Gabunilas J, Roy KR, Wang C, Chanfreau GF, Clarke SG. Biochemistry 58 4997-5010 (2019)
  33. Structural dynamics of translation elongation factor Tu during aa-tRNA delivery to the ribosome. Kavaliauskas D, Chen C, Liu W, Cooperman BS, Goldman YE, Knudsen CR. Nucleic Acids Res 46 8651-8661 (2018)
  34. ArfB can displace mRNA to rescue stalled ribosomes. Carbone CE, Demo G, Madireddy R, Svidritskiy E, Korostelev AA. Nat Commun 11 5552 (2020)
  35. Disorder guides domain rearrangement in elongation factor Tu. Yang H, Perrier J, Whitford PC. Proteins 86 1037-1046 (2018)
  36. Mechanistic insights into translation inhibition by aminoglycoside antibiotic arbekacin. Parajuli NP, Mandava CS, Pavlov MY, Sanyal S. Nucleic Acids Res 49 6880-6892 (2021)
  37. The amino acid substitution affects cellular response to mistranslation. Berg MD, Zhu Y, Ruiz BY, Loll-Krippleber R, Isaacson J, San Luis BJ, Genereaux J, Boone C, Villén J, Brown GW, Brandl CJ. G3 (Bethesda) 11 jkab218 (2021)
  38. Biallelic splicing variants in the nucleolar 60S assembly factor RBM28 cause the ribosomopathy ANE syndrome. Bryant CJ, Lorea CF, de Almeida HL, Weinert L, Vedolin L, Pinto E Vairo F, Baserga SJ. Proc Natl Acad Sci U S A 118 e2017777118 (2021)
  39. Disruption of evolutionarily correlated tRNA elements impairs accurate decoding. Nguyen HA, Sunita S, Dunham CM. Proc Natl Acad Sci U S A 117 16333-16338 (2020)
  40. Elongation Factor Tu Switch I Element is a Gate for Aminoacyl-tRNA Selection. Girodat D, Blanchard SC, Wieden HJ, Sanbonmatsu KY. J Mol Biol 432 3064-3077 (2020)
  41. The mechanism of error induction by the antibiotic viomycin provides insight into the fidelity mechanism of translation. Holm M, Mandava CS, Ehrenberg M, Sanyal S. Elife 8 e46124 (2019)
  42. Modulation of translational decoding by m6A modification of mRNA. Jain S, Koziej L, Poulis P, Kaczmarczyk I, Gaik M, Rawski M, Ranjan N, Glatt S, Rodnina MV. Nat Commun 14 4784 (2023)
  43. Noncanonical amino acid mutagenesis in response to recoding signal-enhanced quadruplet codons. Chen Y, He X, Ma B, Liu K, Gao T, Niu W, Guo J. Nucleic Acids Res 50 e94 (2022)
  44. Structure of the 30S ribosomal decoding complex at ambient temperature. Dao EH, Poitevin F, Sierra RG, Gati C, Rao Y, Ciftci HI, Akşit F, McGurk A, Obrinski T, Mgbam P, Hayes B, De Lichtenberg C, Pardo-Avila F, Corsepius N, Zhang L, Seaberg MH, Hunter MS, Liang M, Koglin JE, Wakatsuki S, Demirci H. RNA 24 1667-1676 (2018)
  45. mRNA decoding in human is kinetically and structurally distinct from bacteria. Holm M, Natchiar SK, Rundlet EJ, Myasnikov AG, Watson ZL, Altman RB, Wang HY, Taunton J, Blanchard SC. Nature 617 200-207 (2023)
  46. Kinetic Analysis Suggests Evolution of Ribosome Specificity in Modern Elongation Factor-Tus from "Generalist" Ancestors. De Tarafder A, Parajuli NP, Majumdar S, Kaçar B, Sanyal S. Mol Biol Evol 38 3436-3444 (2021)
  47. Quality control of protein synthesis in the early elongation stage. Nagao A, Nakanishi Y, Yamaguchi Y, Mishina Y, Karoji M, Toya T, Fujita T, Iwasaki S, Miyauchi K, Sakaguchi Y, Suzuki T. Nat Commun 14 2704 (2023)
  48. Miniature RNAs are embedded in an exceptionally protein-rich mitoribosome via an elaborate assembly pathway. Valach M, Benz C, Aguilar LC, Gahura O, Faktorová D, Zíková A, Oeffinger M, Burger G, Gray MW, Lukeš J. Nucleic Acids Res 51 6443-6460 (2023)
  49. Network theory of the bacterial ribosome. Calvet LE, Matviienko S, Ducluzaux P. PLoS One 15 e0239700 (2020)
  50. Profile of Joachim Frank, Richard Henderson, and Jacques Dubochet, 2017 Nobel Laureates in Chemistry. Nogales E. Proc Natl Acad Sci U S A 115 441-444 (2018)
  51. Stringent Nucleotide Recognition by the Ribosome at the Middle Codon Position. Liu W, Shin D, Ng M, Sanbonmatsu KY, Tor Y, Cooperman BS. Molecules 22 E1427 (2017)
  52. Druggable differences: Targeting mechanistic differences between trans-translation and translation for selective antibiotic action. Srinivas P, Keiler KC, Dunham CM. Bioessays 44 e2200046 (2022)
  53. Multiscale Modeling of Wobble to Watson-Crick-Like Guanine-Uracil Tautomerization Pathways in RNA. Chandorkar S, Raghunathan S, Jaganade T, Priyakumar UD. Int J Mol Sci 22 5411 (2021)
  54. Variable Region Sequences Influence 16S rRNA Performance. Bose N, Moore SD. Microbiol Spectr 11 e0125223 (2023)
  55. A role for circular code properties in translation. Giannerini S, Gonzalez DL, Goracci G, Danielli A. Sci Rep 11 9218 (2021)
  56. Anticodon sequence determines the impact of mistranslating tRNAAla variants. Cozma E, Rao M, Dusick M, Genereaux J, Rodriguez-Mias RA, Villén J, Brandl CJ, Berg MD. RNA Biol 20 791-804 (2023)
  57. Biophysical characterization and ligand-binding properties of the elongation factor Tu from Mycobacterium tuberculosis. Yang J, Hong J, Luo L, Liu K, Meng C, Ji ZL, Lin D. Acta Biochim Biophys Sin (Shanghai) 51 139-149 (2019)
  58. Constraints on error rate revealed by computational study of G•U tautomerization in translation. Kazantsev A, Ignatova Z. Nucleic Acids Res 49 11823-11833 (2021)
  59. Genetic code degeneracy is established by the decoding center of the ribosome. Ye S, Lehmann J. Nucleic Acids Res 50 4113-4126 (2022)
  60. Overview of the Biomolecular Association and Dynamics session at the 20th IUPAB congress, 45th Brazilian congress of SBBF, and the 50th annual meeting of SBBq. Whitford PC. Biophys Rev 13 863-865 (2021)
  61. Structural basis for reduced ribosomal A-site fidelity in response to P-site codon-anticodon mismatches. Nguyen HA, Hoffer ED, Fagan CE, Maehigashi T, Dunham CM. J Biol Chem 299 104608 (2023)


Quick links