Nascent peptide-induced translation discontinuation in eukaryotes impacts biased amino acid usage in proteomes

Yosuke Ito, Yuhei Chadani (), Tatsuya Niwa, Ayako Yamakawa, Kodai Machida, Hiroaki Imataka and Hideki Taguchi ()
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Yosuke Ito: Tokyo Institute of Technology
Yuhei Chadani: Tokyo Institute of Technology
Tatsuya Niwa: Tokyo Institute of Technology
Ayako Yamakawa: Tokyo Institute of Technology
Kodai Machida: University of Hyogo
Hiroaki Imataka: University of Hyogo
Hideki Taguchi: Tokyo Institute of Technology

Nature Communications, 2022, vol. 13, issue 1, 1-16

Abstract: Abstract Robust translation elongation of any given amino acid sequence is required to shape proteomes. Nevertheless, nascent peptides occasionally destabilize ribosomes, since consecutive negatively charged residues in bacterial nascent chains can stochastically induce discontinuation of translation, in a phenomenon termed intrinsic ribosome destabilization (IRD). Here, using budding yeast and a human factor-based reconstituted translation system, we show that IRD also occurs in eukaryotic translation. Nascent chains enriched in aspartic acid (D) or glutamic acid (E) in their N-terminal regions alter canonical ribosome dynamics, stochastically aborting translation. Although eukaryotic ribosomes are more robust to ensure uninterrupted translation, we find many endogenous D/E-rich peptidyl-tRNAs in the N-terminal regions in cells lacking a peptidyl-tRNA hydrolase, indicating that the translation of the N-terminal D/E-rich sequences poses an inherent risk of failure. Indeed, a bioinformatics analysis reveals that the N-terminal regions of ORFs lack D/E enrichment, implying that the translation defect partly restricts the overall amino acid usage in proteomes.

Date: 2022
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DOI: 10.1038/s41467-022-35156-x

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