Journal of Biological Chemistry
Volume 286, Issue 36, 9 September 2011, Pages 31105-31112
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Protein Synthesis and Degradation
Alternative Fates of Paused Ribosomes during Translation Termination*

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The bacterial tmRNA·SmpB system facilitates recycling of stalled translational complexes in a process termed “ribosome rescue.” During ribosome rescue, the nascent chain is tagged with the tmRNA-encoded ssrA peptide, which targets the tagged polypeptide for degradation. Translational pausing also induces a variety of recoding events such as frameshifts, ribosome hops, and stop codon readthrough. To examine the interplay between recoding and ribosome rescue, we determined the various fates of ribosomes that pause during translation termination. We expressed a model protein containing the C-terminal Asp-Pro nascent peptide motif (which interferes with translation termination) and quantified the protein chains produced by recoding and ssrA-peptide tagging. The nature and extent of translational recoding depended upon the codon for the C-terminal Pro residue, with CCU and CCC promoting efficient +1 frameshifting. In contrast, ssrA-peptide tagging was unaffected by C-terminal Pro coding. Moreover, +1 frameshifting was not suppressed by tmRNA·SmpB activity, suggesting that recoding and ribosome rescue are not competing events. However, cells lacking ribosomal protein L9 (ΔL9) exhibited a significant increase in recoding and a concomitant decrease in ssrA-peptide tagging. Pulse-chase analysis revealed that pre-termination ribosomes turn over more rapidly in ΔL9 cells, suggesting that increased recoding alleviates the translational arrest. Together, these results indicate that tmRNA·SmpB does not suppress transient ribosome pauses, but responds to prolonged translational arrest.

MRNA Decay
Protein Degradation
Protein Synthesis
Ribosomes
tmRNA
Frameshifting
Ribosomal Protein L9
Ribosome Pausing
ssrA Peptide Tagging
Translation Termination

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*

This work was supported, in whole or in part, by the National Institutes of Health through Grant GM078634.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables S1 and S2 and Fig. S1.