Elongation factor-Tu can repetitively engage aminoacyl-tRNA within the ribosome during the proofreading stage of tRNA selection

Morse, Justin C.; Girodat, Dylan; Burnett, Benjamin J.; Holm, Mikael; Altman, Roger B.; Sanbonmatsu, Karissa Y.; Wieden, Hans-Joachim; Blanchard, Scott C.

doi:10.1073/pnas.1904469117

Elongation factor-Tu can repetitively engage aminoacyl-tRNA within the ribosome during the proofreading stage of tRNA selection

Journal Article · Tue Feb 04 23:00:00 EST 2020 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1904469117· OSTI ID:1625035

Morse, Justin C. ^[1]; Girodat, Dylan ^[2]; Burnett, Benjamin J. ^[3]; Holm, Mikael ^[4]; Altman, Roger B. ^[4]; Sanbonmatsu, Karissa Y. ^[5]; ^[2]; ^[6]

Weill Cornell Medicine, New York, NY (United States). Dept. of Physiology and Biophysics; DOE/OSTI
Univ. of Lethbridge, AB (Canada)
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
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

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.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Lab (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: 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

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1625035

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 7 Vol. 117; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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