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Title: High-resolution structure of the Escherichia coli ribosome

Abstract

Protein synthesis by the ribosome is highly dependent on the ionic conditions in the cellular environment, but the roles of ribosome solvation remain poorly understood. Moreover, the function of modifications to ribosomal RNA and ribosomal proteins are unclear. Here we present the structure of the Escherichia coli 70S ribosome to 2.4 Å resolution. The structure reveals details of the ribosomal subunit interface that are conserved in all domains of life, and suggest how solvation contributes to ribosome integrity and function. The structure also suggests how the conformation of ribosomal protein uS12 likely impacts its contribution to messenger RNA decoding. In conclusion, this structure helps to explain the phylogenetic conservation of key elements of the ribosome, including posttranscriptional and posttranslational modifications and should serve as a basis for future antibiotic development.

Authors:
 [1];  [2];  [2];  [2];  [3];  [1]
  1. Univ. of California, Berkeley, CA (United States)
  2. Weill Cornell Medical College, New York, NY (United States)
  3. Weill Cornell Medical College, New York, NY (United States); Rockefeller Univ., New York, NY (United States)
Publication Date:
Research Org.:
Univ. of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1347117
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Structural & Molecular Biology
Additional Journal Information:
Journal Volume: 22; Journal Issue: 4; Journal ID: ISSN 1545-9993
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; drug recovery; evolution; single-molecule biophysics; X-ray crystallography

Citation Formats

Noeske, Jonas, Wasserman, Michael R., Terry, Daniel S., Altman, Roger B., Blanchard, Scott C., and Cate, Jamie H. D. High-resolution structure of the Escherichia coli ribosome. United States: N. p., 2015. Web. doi:10.1038/nsmb.2994.
Noeske, Jonas, Wasserman, Michael R., Terry, Daniel S., Altman, Roger B., Blanchard, Scott C., & Cate, Jamie H. D. High-resolution structure of the Escherichia coli ribosome. United States. doi:10.1038/nsmb.2994.
Noeske, Jonas, Wasserman, Michael R., Terry, Daniel S., Altman, Roger B., Blanchard, Scott C., and Cate, Jamie H. D. Mon . "High-resolution structure of the Escherichia coli ribosome". United States. doi:10.1038/nsmb.2994. https://www.osti.gov/servlets/purl/1347117.
@article{osti_1347117,
title = {High-resolution structure of the Escherichia coli ribosome},
author = {Noeske, Jonas and Wasserman, Michael R. and Terry, Daniel S. and Altman, Roger B. and Blanchard, Scott C. and Cate, Jamie H. D.},
abstractNote = {Protein synthesis by the ribosome is highly dependent on the ionic conditions in the cellular environment, but the roles of ribosome solvation remain poorly understood. Moreover, the function of modifications to ribosomal RNA and ribosomal proteins are unclear. Here we present the structure of the Escherichia coli 70S ribosome to 2.4 Å resolution. The structure reveals details of the ribosomal subunit interface that are conserved in all domains of life, and suggest how solvation contributes to ribosome integrity and function. The structure also suggests how the conformation of ribosomal protein uS12 likely impacts its contribution to messenger RNA decoding. In conclusion, this structure helps to explain the phylogenetic conservation of key elements of the ribosome, including posttranscriptional and posttranslational modifications and should serve as a basis for future antibiotic development.},
doi = {10.1038/nsmb.2994},
journal = {Nature Structural & Molecular Biology},
number = 4,
volume = 22,
place = {United States},
year = {2015},
month = {3}
}

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Works referenced in this record:

Nucleoside triphosphate regeneration decreases the frequency of translation errors.
journal, July 1979

  • Jelenc, P. C.; Kurland, C. G.
  • Proceedings of the National Academy of Sciences, Vol. 76, Issue 7
  • DOI: 10.1073/pnas.76.7.3174

Fluctuations of Transfer RNAs between Classical and Hybrid States
journal, November 2007


Optimization of speed and accuracy of decoding in translation
journal, September 2010

  • Wohlgemuth, Ingo; Pohl, Corinna; Rodnina, Marina V.
  • The EMBO Journal, Vol. 29, Issue 21
  • DOI: 10.1038/emboj.2010.229

Erratum: Aminoglycoside activity observed on single pre-translocation ribosome complexes
journal, March 2010

  • Feldman, Michael B.; Terry, Daniel S.; Altman, Roger B.
  • Nature Chemical Biology, Vol. 6, Issue 3
  • DOI: 10.1038/nchembio0310-244c

Correlated conformational events in EF-G and the ribosome regulate translocation
journal, November 2010

  • Munro, James B.; Wasserman, Michael R.; Altman, Roger B.
  • Nature Structural & Molecular Biology, Vol. 17, Issue 12
  • DOI: 10.1038/nsmb.1925

Solvent-accessible surfaces of nucleic acids
journal, August 1979


The RNA Modification Database: 1999 update
journal, January 1999

  • Rozenski, J.; Crain, P. F.; McCloskey, J. A.
  • Nucleic Acids Research, Vol. 27, Issue 1
  • DOI: 10.1093/nar/27.1.196

Expanding the Nucleotide Repertoire of the Ribosome with Post-Transcriptional Modifications
journal, September 2007

  • Chow, Christine S.; Lamichhane, Tek N.; Mahto, Santosh K.
  • ACS Chemical Biology, Vol. 2, Issue 9
  • DOI: 10.1021/cb7001494

Predicting the Minimal Translation Apparatus: Lessons from the Reductive Evolution of Mollicutes
journal, May 2014


Pseudouridylation of helix 69 of 23S rRNA is necessary for an effective translation termination
journal, November 2007

  • Ejby, M.; Sorensen, M. A.; Pedersen, S.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 49
  • DOI: 10.1073/pnas.0706558104

YgdE is the 2′- O- ribose methyltransferase RlmM specific for nucleotide C2498 in bacterial 23S rRNA
journal, June 2009


Sudestada1, a Drosophila ribosomal prolyl-hydroxylase required for mRNA translation, cell homeostasis, and organ growth
journal, February 2014

  • Katz, M. J.; Acevedo, J. M.; Loenarz, C.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 11
  • DOI: 10.1073/pnas.1314485111

Hydroxylation of the eukaryotic ribosomal decoding center affects translational accuracy
journal, February 2014

  • Loenarz, C.; Sekirnik, R.; Thalhammer, A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 11
  • DOI: 10.1073/pnas.1311750111

OGFOD1 catalyzes prolyl hydroxylation of RPS23 and is involved in translation control and stress granule formation
journal, February 2014

  • Singleton, R. S.; Liu-Yi, P.; Formenti, F.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 11
  • DOI: 10.1073/pnas.1314482111

How Should We Think About the Ribosome?
journal, June 2012


A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome
journal, August 2014

  • Polikanov, Yury S.; Steitz, Thomas A.; Innis, C. Axel
  • Nature Structural & Molecular Biology, Vol. 21, Issue 9
  • DOI: 10.1038/nsmb.2871

Amicoumacin A Inhibits Translation by Stabilizing mRNA Interaction with the Ribosome
journal, November 2014


Structures of the Ribosome in Intermediate States of Ratcheting
journal, August 2009

  • Zhang, W.; Dunkle, J. A.; Cate, J. H. D.
  • Science, Vol. 325, Issue 5943, p. 1014-1017
  • DOI: 10.1126/science.1175275

Linking Crystallographic Model and Data Quality
journal, May 2012


MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

  • Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
  • DOI: 10.1107/S0907444909042073

Posttranslational Modifications of Ribosomal Proteins in Escherichia coli
journal, June 2011


Oxygenase-catalyzed ribosome hydroxylation occurs in prokaryotes and humans
journal, October 2012

  • Ge, Wei; Wolf, Alexander; Feng, Tianshu
  • Nature Chemical Biology, Vol. 8, Issue 12
  • DOI: 10.1038/nchembio.1093

A novel partial modification at C2501 in Escherichia coli 23S ribosomal RNA
journal, June 2004


Effect of polyamines on translation fidelity in vivo
journal, March 1986


tRNA dynamics on the ribosome during translation
journal, August 2004

  • Blanchard, S. C.; Kim, H. D.; Gonzalez, R. L.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 35, p. 12893-12898
  • DOI: 10.1073/pnas.0403884101

tRNA selection and kinetic proofreading in translation
journal, September 2004

  • Blanchard, Scott C.; Gonzalez, Ruben L.; Kim, Harold D.
  • Nature Structural & Molecular Biology, Vol. 11, Issue 10
  • DOI: 10.1038/nsmb831

A guide to ions and RNA structure
journal, March 2004


Structures of the Bacterial Ribosome at 3.5 Å Resolution
journal, November 2005

  • Schuwirth, Barbara S.; Borovinskaya, Maria A.; Hau, Cathy W.
  • Science, Vol. 310, Issue 5749
  • DOI: 10.1126/science.1117230

Structures of the Bacterial Ribosome in Classical and Hybrid States of tRNA Binding
journal, May 2011


RNA tertiary interactions in the large ribosomal subunit: The A-minor motif
journal, April 2001

  • Nissen, P.; Ippolito, J. A.; Ban, N.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 9
  • DOI: 10.1073/pnas.081082398

The Structure of the Eukaryotic Ribosome at 3.0 A Resolution
journal, November 2011


Selective Protein Synthesis by Ribosomes with a Drug-Obstructed Exit Tunnel
journal, October 2012


Macrolide antibiotics allosterically predispose the ribosome for translation arrest
journal, June 2014

  • Sothiselvam, Shanmugapriya; Liu, Bo; Han, Wei
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
  • DOI: 10.1073/pnas.1403586111

Resistance to Macrolide, Lincosamide, Streptogramin, Ketolide, and Oxazolidinone Antibiotics
journal, January 2004


Revisiting the structures of several antibiotics bound to the bacterial ribosome
journal, September 2010

  • Bulkley, D.; Innis, C. A.; Blaha, G.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 40
  • DOI: 10.1073/pnas.1008685107

Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action
journal, September 2010

  • Dunkle, J. A.; Xiong, L.; Mankin, A. S.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 40
  • DOI: 10.1073/pnas.1007988107

High Resolution Structure of the Large Ribosomal Subunit from a Mesophilic Eubacterium
journal, November 2001


SecM-Stalled Ribosomes Adopt an Altered Geometry at the Peptidyl Transferase Center
journal, January 2011


Mechanisms of SecM-Mediated Stalling in the Ribosome
journal, July 2012

  • Gumbart, James; Schreiner, Eduard; Wilson, Daniel N.
  • Biophysical Journal, Vol. 103, Issue 2
  • DOI: 10.1016/j.bpj.2012.06.005

Molecular Basis for the Ribosome Functioning as an L-Tryptophan Sensor
journal, October 2014


Structural Basis for Translational Stalling by Human Cytomegalovirus and Fungal Arginine Attenuator Peptide
journal, October 2010


Crucial elements that maintain the interactions between the regulatory TnaC peptide and the ribosome exit tunnel responsible for Trp inhibition of ribosome function
journal, November 2011

  • Martínez, Allyson K.; Shirole, Nitin H.; Murakami, Shino
  • Nucleic Acids Research, Vol. 40, Issue 5
  • DOI: 10.1093/nar/gkr1052

Structure of the 70S Ribosome Complexed with mRNA and tRNA
journal, September 2006


Conformational flexibility in RNA: the role of dihydrouridine
journal, March 1996


A Proteomic and Transcriptomic Approach Reveals New Insight into β-methylthiolation of Escherichia coli Ribosomal Protein S12
journal, December 2010

  • Strader, Michael Brad; Costantino, Nina; Elkins, Christopher A.
  • Molecular & Cellular Proteomics, Vol. 10, Issue 3
  • DOI: 10.1074/mcp.M110.005199

RimO, a MiaB-like enzyme, methylthiolates the universally conserved Asp88 residue of ribosomal protein S12 in Escherichia coli
journal, February 2008

  • Anton, B. P.; Saleh, L.; Benner, J. S.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 6
  • DOI: 10.1073/pnas.0708608105

Prevalence of syn nucleobases in the active sites of functional RNAs
journal, August 2011

  • Sokoloski, J. E.; Godfrey, S. A.; Dombrowski, S. E.
  • RNA, Vol. 17, Issue 10
  • DOI: 10.1261/rna.2759911

How the ribosome hands the A-site tRNA to the P site during EF-G-catalyzed translocation
journal, September 2014


Structural Insights into the Roles of Water and the 2′ Hydroxyl of the P Site tRNA in the Peptidyl Transferase Reaction
journal, November 2005


Revisiting the Haloarcula marismortui 50S ribosomal subunit model
journal, May 2013

  • Gabdulkhakov, Azat; Nikonov, Stanislav; Garber, Maria
  • Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 6
  • DOI: 10.1107/S0907444913004745

Ordered water in macromolecular structure
journal, October 1994


Structural aspects of messenger RNA reading frame maintenance by the ribosome
journal, April 2010

  • Jenner, Lasse B.; Demeshkina, Natalia; Yusupova, Gulnara
  • Nature Structural & Molecular Biology, Vol. 17, Issue 5
  • DOI: 10.1038/nsmb.1790

Allosteric control of the ribosome by small-molecule antibiotics
journal, August 2012

  • Wang, Leyi; Pulk, Arto; Wasserman, Michael R.
  • Nature Structural & Molecular Biology, Vol. 19, Issue 9
  • DOI: 10.1038/nsmb.2360

Identification of Two Distinct Hybrid State Intermediates on the Ribosome
journal, February 2007


An Oxygen Scavenging System for Improvement of Dye Stability in Single-Molecule Fluorescence Experiments
journal, March 2008

  • Aitken, Colin Echeverría; Marshall, R. Andrew; Puglisi, Joseph D.
  • Biophysical Journal, Vol. 94, Issue 5
  • DOI: 10.1529/biophysj.107.117689

Mitigating Unwanted Photophysical Processes for Improved Single-Molecule Fluorescence Imaging
journal, March 2009


XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

Coot model-building tools for molecular graphics
journal, November 2004

  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

Overview of the CCP 4 suite and current developments
journal, March 2011

  • Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
  • DOI: 10.1107/S0907444910045749

Least-squares phase refinement. II. High-resolution phasing of a small protein
journal, March 1974


The use of Sayre's equation with solvent flattening and histogram matching for phase extension and refinement of protein structures
journal, May 1990

  • Zhang, K. Y. J.; Main, P.
  • Acta Crystallographica Section A Foundations of Crystallography, Vol. 46, Issue 5
  • DOI: 10.1107/S0108767389012158

A Detailed View of a Ribosomal Active Site
journal, May 1999


Energetically significant networks of coupled interactions within an unfolded protein
journal, August 2014

  • Cho, J. -H.; Meng, W.; Sato, S.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 33
  • DOI: 10.1073/pnas.1402054111

Structural basis for the interaction of protein S1 with the Escherichia coli ribosome
journal, December 2014

  • Byrgazov, Konstantin; Grishkovskaya, Irina; Arenz, Stefan
  • Nucleic Acids Research, Vol. 43, Issue 1
  • DOI: 10.1093/nar/gku1314

A Compact Viral Processing Proteinase/Ubiquitin Hydrolase from the OTU Family
journal, August 2013


Extreme Temperature Tolerance of a Hyperthermophilic Protein Coupled to Residual Structure in the Unfolded State
journal, June 2008

  • Wallgren, Marcus; Ådén, Jörgen; Pylypenko, Olena
  • Journal of Molecular Biology, Vol. 379, Issue 4
  • DOI: 10.1016/j.jmb.2008.04.007

Structural and Functional Analysis of the E. coli NusB-S10 Transcription Antitermination Complex
journal, December 2008


FEM: feature-enhanced map
journal, February 2015

  • Afonine, Pavel V.; Moriarty, Nigel W.; Mustyakimov, Marat
  • Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 3
  • DOI: 10.1107/S1399004714028132

Synergy of Streptogramin Antibiotics Occurs Independently of Their Effects on Translation
journal, June 2014

  • Noeske, Jonas; Huang, Jian; Olivier, Nelson B.
  • Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 9
  • DOI: 10.1128/AAC.03389-14

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