5lmp › Citations

Large-Scale Movements of IF3 and tRNA during Bacterial Translation Initiation.

Hussain T, Llácer JL, Wimberly BT, Kieft JS, Ramakrishnan V
Cell 167 133-144.e13 (2016)
Related entries: 5lmn, 5lmo, 5lmq, 5lmr, 5lms, 5lmt, 5lmu, 5lmv

Cited: 79 times
EuropePMC logo PMID: 27662086

Abstract

In bacterial translational initiation, three initiation factors (IFs 1-3) enable the selection of initiator tRNA and the start codon in the P site of the 30S ribosomal subunit. Here, we report 11 single-particle cryo-electron microscopy (cryoEM) reconstructions of the complex of bacterial 30S subunit with initiator tRNA, mRNA, and IFs 1-3, representing different steps along the initiation pathway. IF1 provides key anchoring points for IF2 and IF3, thereby enhancing their activities. IF2 positions a domain in an extended conformation appropriate for capturing the formylmethionyl moiety charged on tRNA. IF3 and tRNA undergo large conformational changes to facilitate the accommodation of the formylmethionyl-tRNA (fMet-tRNA(fMet)) into the P site for start codon recognition.

Articles - 5lmp mentioned but not cited (6)

  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. Large-Scale Movements of IF3 and tRNA during Bacterial Translation Initiation. Hussain T, Llácer JL, Wimberly BT, Kieft JS, Ramakrishnan V. Cell 167 133-144.e13 (2016)
  3. Detecting protein and DNA/RNA structures in cryo-EM maps of intermediate resolution using deep learning. Wang X, Alnabati E, Aderinwale TW, Maddhuri Venkata Subramaniya SR, Terashi G, Kihara D. Nat Commun 12 2302 (2021)
  4. How the initiating ribosome copes with ppGpp to translate mRNAs. Vinogradova DS, Zegarra V, Maksimova E, Nakamoto JA, Kasatsky P, Paleskava A, Konevega AL, Milón P. PLoS Biol. 18 e3000593 (2020)
  5. Interactions of 2'-O-methyl oligoribonucleotides with the RNA models of the 30S subunit A-site. Jasiński M, Kulik M, Wojciechowska M, Stolarski R, Trylska J. PLoS ONE 13 e0191138 (2018)
  6. Using Curriculum Learning in Pattern Recognition of 3-dimensional Cryo-electron Microscopy Density Maps. Deng Y, Mu Y, Sazzed S, Sun J, He J. ACM BCB 2020 112 (2020)


Reviews citing this publication (16)

  1. Structural Insights into the Mechanism of Scanning and Start Codon Recognition in Eukaryotic Translation Initiation. Hinnebusch AG. Trends Biochem. Sci. 42 589-611 (2017)
  2. Ribosome Hibernation. Prossliner T, Skovbo Winther K, Sørensen MA, Gerdes K. Annu Rev Genet 52 321-348 (2018)
  3. Ribosome states signal RNA quality control. D'Orazio KN, Green R. Mol Cell 81 1372-1383 (2021)
  4. Translation initiation in mammalian mitochondria- a prokaryotic perspective. Ayyub SA, Varshney U. RNA Biol 17 165-175 (2020)
  5. The Structural Dynamics of Translation. Korostelev AA. Annu Rev Biochem 91 245-267 (2022)
  6. Translation in Prokaryotes. Rodnina MV. Cold Spring Harb Perspect Biol 10 (2018)
  7. Translation initiation by cap-dependent ribosome recruitment: Recent insights and open questions. Shirokikh NE, Preiss T. Wiley Interdiscip Rev RNA 9 e1473 (2018)
  8. Ribosome Structure, Function, and Early Evolution. Opron K, Burton ZF. Int J Mol Sci 20 (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. Structural Heterogeneities of the Ribosome: New Frontiers and Opportunities for Cryo-EM. Poitevin F, Kushner A, Li X, Dao Duc K. Molecules 25 E4262 (2020)
  11. The diversity of Shine-Dalgarno sequences sheds light on the evolution of translation initiation. Wen JD, Kuo ST, Chou HD. RNA Biol 18 1489-1500 (2021)
  12. Bacterial Ribosome Rescue Systems. Kurita D, Himeno H. Microorganisms 10 372 (2022)
  13. Exploring the Structural Variability of Dynamic Biological Complexes by Single-Particle Cryo-Electron Microscopy. DiIorio MC, Kulczyk AW. Micromachines (Basel) 14 118 (2022)
  14. Mechanisms of ribosome recycling in bacteria and mitochondria: a structural perspective. Seely SM, Gagnon MG. RNA Biol 19 662-677 (2022)
  15. Recent Advances in Archaeal Translation Initiation. Schmitt E, Coureux PD, Kazan R, Bourgeois G, Lazennec-Schurdevin C, Mechulam Y. Front Microbiol 11 584152 (2020)
  16. Single-Molecule Fluorescence Applied to Translation. Prabhakar A, Puglisi EV, Puglisi JD. Cold Spring Harb Perspect Biol 11 (2019)

Articles citing this publication (57)

  1. Late steps in bacterial translation initiation visualized using time-resolved cryo-EM. Kaledhonkar S, Fu Z, Caban K, Li W, Chen B, Sun M, Gonzalez RL, Frank J. Nature 570 400-404 (2019)
  2. Structural and Functional Insights into Human Re-initiation Complexes. Weisser M, Schäfer T, Leibundgut M, Böhringer D, Aylett CHS, Ban N. Mol. Cell 67 447-456.e7 (2017)
  3. Cryo-EM structure of the spinach chloroplast ribosome reveals the location of plastid-specific ribosomal proteins and extensions. Graf M, Arenz S, Huter P, Dönhöfer A, Novácek J, Wilson DN. Nucleic Acids Res. 45 2887-2896 (2017)
  4. Distinct pre-initiation steps in human mitochondrial translation. Khawaja A, Itoh Y, Remes C, Spåhr H, Yukhnovets O, Höfig H, Amunts A, Rorbach J. Nat Commun 11 2932 (2020)
  5. Structure of a 30S pre-initiation complex stalled by GE81112 reveals structural parallels in bacterial and eukaryotic protein synthesis initiation pathways. López-Alonso JP, Fabbretti A, Kaminishi T, Iturrioz I, Brandi L, Gil-Carton D, Gualerzi CO, Fucini P, Connell SR. Nucleic Acids Res. 45 2179-2187 (2017)
  6. The Universally Conserved ATPase YchF Regulates Translation of Leaderless mRNA in Response to Stress Conditions. Landwehr V, Milanov M, Angebauer L, Hong J, Jüngert G, Hiersemenzel A, Siebler A, Schmit F, Öztürk Y, Dannenmaier S, Drepper F, Warscheid B, Koch HG. Front Mol Biosci 8 643696 (2021)
  7. Contributions of the N- and C-Terminal Domains of Initiation Factor 3 to Its Functions in the Fidelity of Initiation and Antiassociation of the Ribosomal Subunits. Ayyub SA, Dobriyal D, Varshney U. J. Bacteriol. 199 (2017)
  8. Mechanism of mitoribosomal small subunit biogenesis and preinitiation. Itoh Y, Khawaja A, Laptev I, Cipullo M, Atanassov I, Sergiev P, Rorbach J, Amunts A. Nature 606 603-608 (2022)
  9. Selection on start codons in prokaryotes and potential compensatory nucleotide substitutions. Belinky F, Rogozin IB, Koonin EV. Sci Rep 7 12422 (2017)
  10. Structural and molecular basis for Cardiovirus 2A protein as a viral gene expression switch. Hill CH, Pekarek L, Napthine S, Kibe A, Firth AE, Graham SC, Caliskan N, Brierley I. Nat Commun 12 7166 (2021)
  11. Alternative conformations and motions adopted by 30S ribosomal subunits visualized by cryo-electron microscopy. Jahagirdar D, Jha V, Basu K, Gomez-Blanco J, Vargas J, Ortega J. RNA 26 2017-2030 (2020)
  12. Conformational Response of 30S-bound IF3 to A-Site Binders Streptomycin and Kanamycin. Chulluncuy R, Espiche C, Nakamoto JA, Fabbretti A, Milón P. Antibiotics (Basel) 5 (2016)
  13. Evolutionary shift toward protein-based architecture in trypanosomal mitochondrial ribosomes. Ramrath DJF, Niemann M, Leibundgut M, Bieri P, Prange C, Horn EK, Leitner A, Boehringer D, Schneider A, Ban N. Science 362 (2018)
  14. Molecular architecture of 40S translation initiation complexes on the hepatitis C virus IRES. Brown ZP, Abaeva IS, De S, Hellen CUT, Pestova TV, Frank J. EMBO J 41 e110581 (2022)
  15. RsgA couples the maturation state of the 30S ribosomal decoding center to activation of its GTPase pocket. López-Alonso JP, Kaminishi T, Kikuchi T, Hirata Y, Iturrioz I, Dhimole N, Schedlbauer A, Hase Y, Goto S, Kurita D, Muto A, Zhou S, Naoe C, Mills DJ, Gil-Carton D, Takemoto C, Himeno H, Fucini P, Connell SR. Nucleic Acids Res. 45 6945-6959 (2017)
  16. Structure of Human Mitochondrial Translation Initiation Factor 3 Bound to the Small Ribosomal Subunit. Koripella RK, Sharma MR, Haque ME, Risteff P, Spremulli LL, Agrawal RK. iScience 12 76-86 (2019)
  17. eIF2A, an initiator tRNA carrier refractory to eIF2α kinases, functions synergistically with eIF5B. Kim E, Kim JH, Seo K, Hong KY, An SWA, Kwon J, Lee SV, Jang SK. Cell. Mol. Life Sci. 75 4287-4300 (2018)
  18. Staphylococcus aureus 30S Ribosomal Subunit Purification and Its Biochemical and Cryo-EM Analysis. Belinite M, Khusainov I, Marzi S. Bio Protoc 12 e4532 (2022)
  19. A Complementary Mechanism of Bacterial mRNA Translation Inhibition by Tetracyclines. Barrenechea V, Vargas-Reyes M, Quiliano M, Milón P. Front Microbiol 12 682682 (2021)
  20. A conformational switch in initiation factor 2 controls the fidelity of translation initiation in bacteria. Caban K, Pavlov M, Ehrenberg M, Gonzalez RL. Nat Commun 8 1475 (2017)
  21. Cryo-EM study of an archaeal 30S initiation complex gives insights into evolution of translation initiation. Coureux PD, Lazennec-Schurdevin C, Bourcier S, Mechulam Y, Schmitt E. Commun Biol 3 58 (2020)
  22. IF2 and unique features of initiator tRNAfMet help establish the translational reading frame. Roy B, Liu Q, Shoji S, Fredrick K. RNA Biol 15 604-613 (2018)
  23. Large-scale movement of eIF3 domains during translation initiation modulate start codon selection. Llácer JL, Hussain T, Dong J, Villamayor L, Gordiyenko Y, Hinnebusch AG. Nucleic Acids Res 49 11491-11511 (2021)
  24. Multi-scale ensemble properties of the Escherichia coli RNA degradosome. Dendooven T, Paris G, Shkumatov AV, Islam MS, Burt A, Kubańska MA, Yang TY, Hardwick SW, Luisi BF. Mol Microbiol 117 102-120 (2022)
  25. Multiplexed genomic encoding of non-canonical amino acids for labeling large complexes. Desai BJ, Gonzalez RL. Nat Chem Biol 16 1129-1135 (2020)
  26. Role of aIF5B in archaeal translation initiation. Kazan R, Bourgeois G, Lazennec-Schurdevin C, Larquet E, Mechulam Y, Coureux PD, Schmitt E. Nucleic Acids Res 50 6532-6548 (2022)
  27. Selection of start codon during mRNA scanning in eukaryotic translation initiation. Basu I, Gorai B, Chandran T, Maiti PK, Hussain T. Commun Biol 5 587 (2022)
  28. Translation initiation of leaderless and polycistronic transcripts in mammalian mitochondria. Remes C, Khawaja A, Pearce SF, Dinan AM, Gopalakrishna S, Cipullo M, Kyriakidis V, Zhang J, Dopico XC, Yukhnovets O, Atanassov I, Firth AE, Cooperman B, Rorbach J. Nucleic Acids Res 51 891-907 (2023)
  29. Translational initiation factor eIF5 replaces eIF1 on the 40S ribosomal subunit to promote start-codon recognition. Llácer JL, Hussain T, Saini AK, Nanda JS, Kaur S, Gordiyenko Y, Kumar R, Hinnebusch AG, Lorsch JR, Ramakrishnan V. Elife 7 (2018)
  30. 1H, 13C and 15N resonance assignments of translation initiation factor 3 from Pseudomonas aeruginosa. Li L, Palmer SO, Gomez EA, Mendiola F, Wang T, Bullard JM, Zhang Y. Biomol NMR Assign 14 93-97 (2020)
  31. CRISPR-RNAa: targeted activation of translation using dCas13 fusions to translation initiation factors. Otoupal PB, Cress BF, Doudna JA, Schoeniger JS. Nucleic Acids Res 50 8986-8998 (2022)
  32. Coevolution of the translational machinery optimizes initiation with unusual initiator tRNAs and initiation codons in mycoplasmas. Ayyub SA, Dobriyal D, Shah RA, Lahry K, Bhattacharyya M, Bhattacharyya S, Chakrabarti S, Varshney U. RNA Biol 15 70-80 (2018)
  33. Compact IF2 allows initiator tRNA accommodation into the P site and gates the ribosome to elongation. Basu RS, Sherman MB, Gagnon MG. Nat Commun 13 3388 (2022)
  34. Comparative Analysis of Structural and Dynamical Features of Ribosome Upon Association With mRNA Reveals Potential Role of Ribosomal Proteins. Bheemireddy S, Sandhya S, Srinivasan N. Front Mol Biosci 8 654164 (2021)
  35. Comparative Analysis of anti-Shine- Dalgarno Function in Flavobacterium johnsoniae and Escherichia coli. McNutt ZA, Gandhi MD, Shatoff EA, Roy B, Devaraj A, Bundschuh R, Fredrick K. Front Mol Biosci 8 787388 (2021)
  36. Drop-off-reinitiation at the amino termini of nascent peptides and its regulation by IF3, EF-G, and RRF. Katoh T, Suga H. RNA 29 663-674 (2023)
  37. Global analysis of protein synthesis in Flavobacterium johnsoniae reveals the use of Kozak-like sequences in diverse bacteria. Baez WD, Roy B, McNutt ZA, Shatoff EA, Chen S, Bundschuh R, Fredrick K. Nucleic Acids Res. 47 10477-10488 (2019)
  38. Influence of the spacer region between the Shine-Dalgarno box and the start codon for fine-tuning of the translation efficiency in Escherichia coli. Komarova ES, Chervontseva ZS, Osterman IA, Evfratov SA, Rubtsova MP, Zatsepin TS, Semashko TA, Kostryukova ES, Bogdanov AA, Gelfand MS, Dontsova OA, Sergiev PV. Microb Biotechnol 13 1254-1261 (2020)
  39. Multifunctional graphene supports for electron cryomicroscopy. Naydenova K, Peet MJ, Russo CJ. Proc. Natl. Acad. Sci. U.S.A. 116 11718-11724 (2019)
  40. Purification of Hibernating and Active C- Ribosomes from Zinc-Starved Mycobacteria. Li Y, Keshavan P, Corro JH, Koripella RK, Agrawal RK, Ojha AK. Methods Mol Biol 2314 151-166 (2021)
  41. RbfA and IF3 couple ribosome biogenesis and translation initiation to increase stress tolerance. Sharma IM, Woodson SA. Nucleic Acids Res 48 359-372 (2020)
  42. Ribosome assembly defects subvert initiation Factor3 mediated scrutiny of bona fide start signal. Sharma H, Anand B. Nucleic Acids Res. 47 11368-11386 (2019)
  43. SHAPE Probing Reveals Human rRNAs Are Largely Unfolded in Solution. Giannetti CA, Busan S, Weidmann CA, Weeks KM. Biochemistry 58 3377-3385 (2019)
  44. Salt-Specific Suppression of the Cold Denaturation of Thermophilic Multidomain Initiation Factor 2. Džupponová V, Tomášková N, Antošová A, Sedlák E, Žoldák G. Int J Mol Sci 24 6787 (2023)
  45. Signal Recognition Particle Suppressor Screening Reveals the Regulation of Membrane Protein Targeting by the Translation Rate. Zhao L, Cui Y, Fu G, Xu Z, Liao X, Zhang D. mBio 12 (2021)
  46. Stabilization of Ribosomal RNA of the Small Subunit by Spermidine in Staphylococcus aureus. Belinite M, Khusainov I, Soufari H, Marzi S, Romby P, Yusupov M, Hashem Y. Front Mol Biosci 8 738752 (2021)
  47. Structural and Functional Elucidation of IF-3 Protein of Chloroflexus aurantiacus Involved in Protein Biosynthesis: An In Silico Approach. Saikat ASM, Uddin ME, Ahmad T, Mahmud S, Imran MAS, Ahmed S, Alyami SA, Moni MA. Biomed Res Int 2021 9050026 (2021)
  48. Structural basis of sequestration of the anti-Shine-Dalgarno sequence in the Bacteroidetes ribosome. Jha V, Roy B, Jahagirdar D, McNutt ZA, Shatoff EA, Boleratz BL, Watkins DE, Bundschuh R, Basu K, Ortega J, Fredrick K. Nucleic Acids Res 49 547-567 (2021)
  49. Structure of a human 48S translational initiation complex. Brito Querido J, Sokabe M, Kraatz S, Gordiyenko Y, Skehel JM, Fraser CS, Ramakrishnan V. Science 369 1220-1227 (2020)
  50. The context of the ribosome binding site in mRNAs defines specificity of action of kasugamycin, an inhibitor of translation initiation. Zhang Y, Aleksashin NA, Klepacki D, Anderson C, Vázquez-Laslop N, Gross CA, Mankin AS. Proc Natl Acad Sci U S A 119 e2118553119 (2022)
  51. The dynamic cycle of bacterial translation initiation factor IF3. Nakamoto JA, Evangelista W, Vinogradova DS, Konevega AL, Spurio R, Fabbretti A, Milón P. Nucleic Acids Res 49 6958-6970 (2021)
  52. The endonuclease Cue2 cleaves mRNAs at stalled ribosomes during No Go Decay. D'Orazio KN, Wu CC, Sinha N, Loll-Krippleber R, Brown GW, Green R. Elife 8 (2019)
  53. The initiation factor 3 (IF3) residues interacting with initiator tRNA elbow modulate the fidelity of translation initiation and growth fitness in Escherichia coli. Singh J, Mishra RK, Ayyub SA, Hussain T, Varshney U. Nucleic Acids Res 50 11712-11726 (2022)
  54. The universally conserved nucleotides of the small subunit ribosomal RNAs. Noller HF, Donohue JP, Gutell RR. RNA 28 623-644 (2022)
  55. Translation initiation site of mRNA is selected through dynamic interaction with the ribosome. Chen YL, Wen JD. Proc Natl Acad Sci U S A 119 e2118099119 (2022)
  56. Translation initiation with exotic amino acids using EF-P-responsive artificial initiator tRNA. Katoh T, Suga H. Nucleic Acids Res 51 8169-8180 (2023)
  57. Weakening the IF2-fMet-tRNA Interaction Suppresses the Lethal Phenotype Caused by GTPase Inactivation. Tomsic J, Caserta E, Pon CL, Gualerzi CO. Int J Mol Sci 22 13238 (2021)


Quick links