Elongation factor-Tu can repetitively engage aminoacyl-tRNA within the ribosome during the proofreading stage of tRNA selection
Abstract
The substrate for ribosomes actively engaged in protein synthesis is a ternary complex of elongation factor Tu (EF-Tu), aminoacyl-tRNA (aa-tRNA), and GTP. EF-Tu plays a critical role in mRNA decoding by increasing the rate and fidelity of aa-tRNA selection at each mRNA codon. Here, using three-color single-molecule fluorescence resonance energy transfer imaging and molecular dynamics simulations, we examine the timing and role of conformational events that mediate the release of aa-tRNA from EF-Tu and EF-Tu from the ribosome after GTP hydrolysis. Our investigations reveal that conformational changes in EF-Tu coordinate the rate-limiting passage of aa-tRNA through the accommodation corridor en route to the peptidyl transferase center of the large ribosomal subunit. Experiments using distinct inhibitors of the accommodation process further show that aa-tRNA must at least partially transit the accommodation corridor for EF-Tu∙GDP to release. aa-tRNAs failing to undergo peptide bond formation at the end of accommodation corridor passage after EF-Tu release can be reengaged by EF-Tu∙GTP from solution, coupled to GTP hydrolysis. These observations suggest that additional rounds of ternary complex formation can occur on the ribosome during proofreading, particularly when peptide bond formation is slow, which may serve to increase both the rate and fidelity of protein synthesismore »
- Authors:
-
[2];
[5]
- Weill Cornell Medicine, New York, NY (United States). Dept. of Physiology and Biophysics
- Univ. of Lethbridge, AB (Canada)
- St. Jude Children’s Research Hospital, Memphis, TN (United States). Dept. of Structural Biology
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics Group, Theoretical Div.
- Weill Cornell Medicine, New York, NY (United States). Dept. of Physiology and Biophysics; St. Jude Children’s Research Hospital, Memphis, TN (United States). Dept. of Structural Biology
- Publication Date:
- Research Org.:
- Los Alamos National Lab (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA); National Institutes of Health (NIH) National Institute of General Medical Sciences (NIGMS); Natural Sciences and Engineering Research Council; Alberta Innovates Strategic Chairs Program
- OSTI Identifier:
- 1625035
- Grant/Contract Number:
- AC52-06NA25396; R01-GM079238-13; R01-GM098859-07; R01-GM072686; RGPIN-2016-05199; SC60-T2
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 117; Journal Issue: 7; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics
Citation Formats
Morse, Justin C., Girodat, Dylan, Burnett, Benjamin J., Holm, Mikael, Altman, Roger B., Sanbonmatsu, Karissa Y., Wieden, Hans-Joachim, and Blanchard, Scott C. Elongation factor-Tu can repetitively engage aminoacyl-tRNA within the ribosome during the proofreading stage of tRNA selection. United States: N. p., 2020.
Web. doi:10.1073/pnas.1904469117.
Morse, Justin C., Girodat, Dylan, Burnett, Benjamin J., Holm, Mikael, Altman, Roger B., Sanbonmatsu, Karissa Y., Wieden, Hans-Joachim, & Blanchard, Scott C. Elongation factor-Tu can repetitively engage aminoacyl-tRNA within the ribosome during the proofreading stage of tRNA selection. United States. https://doi.org/10.1073/pnas.1904469117
Morse, Justin C., Girodat, Dylan, Burnett, Benjamin J., Holm, Mikael, Altman, Roger B., Sanbonmatsu, Karissa Y., Wieden, Hans-Joachim, and Blanchard, Scott C. Wed .
"Elongation factor-Tu can repetitively engage aminoacyl-tRNA within the ribosome during the proofreading stage of tRNA selection". United States. https://doi.org/10.1073/pnas.1904469117. https://www.osti.gov/servlets/purl/1625035.
@article{osti_1625035,
title = {Elongation factor-Tu can repetitively engage aminoacyl-tRNA within the ribosome during the proofreading stage of tRNA selection},
author = {Morse, Justin C. and Girodat, Dylan and Burnett, Benjamin J. and Holm, Mikael and Altman, Roger B. and Sanbonmatsu, Karissa Y. and Wieden, Hans-Joachim and Blanchard, Scott C.},
abstractNote = {The substrate for ribosomes actively engaged in protein synthesis is a ternary complex of elongation factor Tu (EF-Tu), aminoacyl-tRNA (aa-tRNA), and GTP. EF-Tu plays a critical role in mRNA decoding by increasing the rate and fidelity of aa-tRNA selection at each mRNA codon. Here, using three-color single-molecule fluorescence resonance energy transfer imaging and molecular dynamics simulations, we examine the timing and role of conformational events that mediate the release of aa-tRNA from EF-Tu and EF-Tu from the ribosome after GTP hydrolysis. Our investigations reveal that conformational changes in EF-Tu coordinate the rate-limiting passage of aa-tRNA through the accommodation corridor en route to the peptidyl transferase center of the large ribosomal subunit. Experiments using distinct inhibitors of the accommodation process further show that aa-tRNA must at least partially transit the accommodation corridor for EF-Tu∙GDP to release. aa-tRNAs failing to undergo peptide bond formation at the end of accommodation corridor passage after EF-Tu release can be reengaged by EF-Tu∙GTP from solution, coupled to GTP hydrolysis. These observations suggest that additional rounds of ternary complex formation can occur on the ribosome during proofreading, particularly when peptide bond formation is slow, which may serve to increase both the rate and fidelity of protein synthesis at the expense of GTP hydrolysis.},
doi = {10.1073/pnas.1904469117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 7,
volume = 117,
place = {United States},
year = {Wed Feb 05 00:00:00 EST 2020},
month = {Wed Feb 05 00:00:00 EST 2020}
}
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How EF-Tu can contribute to efficient proofreading of aa-tRNA by the ribosome
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Single-molecule imaging of non-equilibrium molecular ensembles on the millisecond timescale
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Ribosome-targeting antibiotics and mechanisms of bacterial resistance
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tRNA selection and kinetic proofreading in translation
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tRNA dynamics on the ribosome during translation
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