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Structural mechanism of GTPase-powered ribosome-tRNA movement.

<div class='caption-title'>Snapshots of translocation upon GTP hydrolysis and Pi release by EF-G.</div>
<div class='caption-title'>Timing of complex preparation and high-resolution features.</div>
<div class='caption-title'>Structure of EF-G–GDP–Pi in H1 state.</div>
Petrychenko V, Peng BZ, de A P Schwarzer AC, Peske F, Rodnina MV, Fischer N
OpenAccess logo Nat Commun 12 5933 (2021)
Related entries: 7pjt, 7pju, 7pjw, 7pjx, 7pjy, 7pjz

Cited: 32 times
EuropePMC logo PMID: 34635670

Abstract

GTPases are regulators of cell signaling acting as molecular switches. The translational GTPase EF-G stands out, as it uses GTP hydrolysis to generate force and promote the movement of the ribosome along the mRNA. The key unresolved question is how GTP hydrolysis drives molecular movement. Here, we visualize the GTPase-powered step of ongoing translocation by time-resolved cryo-EM. EF-G in the active GDP-Pi form stabilizes the rotated conformation of ribosomal subunits and induces twisting of the sarcin-ricin loop of the 23 S rRNA. Refolding of the GTPase switch regions upon Pi release initiates a large-scale rigid-body rotation of EF-G pivoting around the sarcin-ricin loop that facilitates back rotation of the ribosomal subunits and forward swiveling of the head domain of the small subunit, ultimately driving tRNA forward movement. The findings demonstrate how a GTPase orchestrates spontaneous thermal fluctuations of a large RNA-protein complex into force-generating molecular movement.

Articles - 7pjv mentioned but not cited (7)

  1. Visualizing translation dynamics at atomic detail inside a bacterial cell. Xue L, Lenz S, Zimmermann-Kogadeeva M, Tegunov D, Cramer P, Bork P, Rappsilber J, Mahamid J. Nature 610 205-211 (2022)
  2. Ratchet, swivel, tilt and roll: a complete description of subunit rotation in the ribosome. Hassan A, Byju S, Freitas FC, Roc C, Pender N, Nguyen K, Kimbrough EM, Mattingly JM, Gonzalez RL, de Oliveira RJ, Dunham CM, Whitford PC. Nucleic Acids Res 51 919-934 (2023)
  3. Structural conservation of antibiotic interaction with ribosomes. Paternoga H, Crowe-McAuliffe C, Bock LV, Koller TO, Morici M, Beckert B, Myasnikov AG, Grubmüller H, Nováček J, Wilson DN. Nat Struct Mol Biol 30 1380-1392 (2023)
  4. Insights into translocation mechanism and ribosome evolution from cryo-EM structures of translocation intermediates of Giardia intestinalis. Majumdar S, Emmerich A, Krakovka S, Mandava CS, Svärd SG, Sanyal S. Nucleic Acids Res 51 3436-3451 (2023)
  5. research-article AP profiling resolves co-translational folding pathway and chaperone interactions in vivo. Chen X, Kaiser CM. bioRxiv 2023.09.01.555749 (2023)
  6. Developing Multichannel smFRET Approach to Dissecting Ribosomal Mechanisms. Lin R, Wang Y. Chem Biomed Imaging 2 501-509 (2024)
  7. Paenilamicins from the honey bee pathogen <i>Paenibacillus larvae</i> are context-specific translocation inhibitors of protein synthesis. Koller TO, Berger MJ, Morici M, Paternoga H, Bulatov T, Di Stasi A, Dang T, Mainz A, Raulf K, Crowe-McAuliffe C, Scocchi M, Mardirossian M, Beckert B, Vázquez-Laslop N, Mankin A, Süssmuth RD, Wilson DN. bioRxiv 2024.05.21.595107 (2024)


Reviews citing this publication (3)

  1. The Structural Dynamics of Translation. Korostelev AA. Annu Rev Biochem 91 245-267 (2022)
  2. Frozen in time: analyzing molecular dynamics with time-resolved cryo-EM. Amann SJ, Keihsler D, Bodrug T, Brown NG, Haselbach D. Structure 31 4-19 (2023)
  3. Mechanisms of ribosome recycling in bacteria and mitochondria: a structural perspective. Seely SM, Gagnon MG. RNA Biol 19 662-677 (2022)

Articles citing this publication (22)

  1. 3DFlex: determining structure and motion of flexible proteins from cryo-EM. Punjani A, Fleet DJ. Nat Methods 20 860-870 (2023)
  2. 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)
  3. Structures of the eukaryotic ribosome and its translational states in situ. Hoffmann PC, Kreysing JP, Khusainov I, Tuijtel MW, Welsch S, Beck M. Nat Commun 13 7435 (2022)
  4. Effects of cryo-EM cooling on structural ensembles. Bock LV, Grubmüller H. Nat Commun 13 1709 (2022)
  5. High-resolution structures of a thermophilic eukaryotic 80S ribosome reveal atomistic details of translocation. Kišonaitė M, Wild K, Lapouge K, Ruppert T, Sinning I. Nat Commun 13 476 (2022)
  6. The translating bacterial ribosome at 1.55 Å resolution generated by cryo-EM imaging services. Fromm SA, O'Connor KM, Purdy M, Bhatt PR, Loughran G, Atkins JF, Jomaa A, Mattei S. Nat Commun 14 1095 (2023)
  7. mRNA reading frame maintenance during eukaryotic ribosome translocation. Milicevic N, Jenner L, Myasnikov A, Yusupov M, Yusupova G. Nature 625 393-400 (2024)
  8. The role of GTP hydrolysis by EF-G in ribosomal translocation. Rexroad G, Donohue JP, Lancaster L, Noller HF. Proc Natl Acad Sci U S A 119 e2212502119 (2022)
  9. Gut colonization by Bacteroides requires translation by an EF-G paralog lacking GTPase activity. Han W, Peng BZ, Wang C, Townsend GE, Barry NA, Peske F, Goodman AL, Liu J, Rodnina MV, Groisman EA. EMBO J 42 e112372 (2023)
  10. 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)
  11. The universally conserved nucleotides of the small subunit ribosomal RNAs. Noller HF, Donohue JP, Gutell RR. RNA 28 623-644 (2022)
  12. Hyper-swivel head domain motions are required for complete mRNA-tRNA translocation and ribosome resetting. Nishima W, Girodat D, Holm M, Rundlet EJ, Alejo JL, Fischer K, Blanchard SC, Sanbonmatsu KY. Nucleic Acids Res 50 8302-8320 (2022)
  13. The cyclic octapeptide antibiotic argyrin B inhibits translation by trapping EF-G on the ribosome during translocation. Wieland M, Holm M, Rundlet EJ, Morici M, Koller TO, Maviza TP, Pogorevc D, Osterman IA, Müller R, Blanchard SC, Wilson DN. Proc Natl Acad Sci U S A 119 e2114214119 (2022)
  14. Altered tRNA dynamics during translocation on slippery mRNA as determinant of spontaneous ribosome frameshifting. Poulis P, Patel A, Rodnina MV, Adio S. Nat Commun 13 4231 (2022)
  15. Cryo-electron microscopy structure and translocation mechanism of the crenarchaeal ribosome. Wang YH, Dai H, Zhang L, Wu Y, Wang J, Wang C, Xu CH, Hou H, Yang B, Zhu Y, Zhang X, Zhou J. Nucleic Acids Res 51 8909-8924 (2023)
  16. Mechanistic insights into the alternative ribosome recycling by HflXr. Seely SM, Basu RS, Gagnon MG. Nucleic Acids Res 52 4053-4066 (2024)
  17. Molecular basis of the pleiotropic effects by the antibiotic amikacin on the ribosome. Seely SM, Parajuli NP, De Tarafder A, Ge X, Sanyal S, Gagnon MG. Nat Commun 14 4666 (2023)
  18. Allosteric Effects of EF-G Domain I Mutations Inducing Ribosome Frameshifting Revealed by Multiplexed Force Spectroscopy. Chen Y, Gavriliuc M, Zeng Y, Xu S, Wang Y. Chembiochem 25 e202400130 (2024)
  19. GTP before ATP: The energy currency at the origin of genes. Mrnjavac N, Martin WF. Biochim Biophys Acta Bioenerg 1866 149514 (2024)
  20. Paenilamicins are context-specific translocation inhibitors of protein synthesis. Koller TO, Berger MJ, Morici M, Paternoga H, Bulatov T, Di Stasi A, Dang T, Mainz A, Raulf K, Crowe-McAuliffe C, Scocchi M, Mardirossian M, Beckert B, Vázquez-Laslop N, Mankin AS, Süssmuth RD, Wilson DN. Nat Chem Biol (2024)
  21. Structures of the Staphylococcus aureus ribosome inhibited by fusidic acid and fusidic acid cyclopentane. González-López A, Larsson DSD, Koripella RK, Cain BN, Chavez MG, Hergenrother PJ, Sanyal S, Selmer M. Sci Rep 14 14253 (2024)
  22. The ribosome termination complex remodels release factor RF3 and ejects GDP. Li L, Rybak MY, Lin J, Gagnon MG. Nat Struct Mol Biol (2024)


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