High-Resolution Ribosome Profiling Defines Discrete Ribosome Elongation States and Translational Regulation during Cellular Stress

Mol Cell. 2019 Mar 7;73(5):959-970.e5. doi: 10.1016/j.molcel.2018.12.009. Epub 2019 Jan 24.

Abstract

Ribosomes undergo substantial conformational changes during translation elongation to accommodate incoming aminoacyl-tRNAs and translocate along the mRNA template. We used multiple elongation inhibitors and chemical probing to define ribosome conformational states corresponding to differently sized ribosome-protected mRNA fragments (RPFs) generated by ribosome profiling. We show, using various genetic and environmental perturbations, that short 20-22 or classical 27-29 nucleotide RPFs correspond to ribosomes with open or occupied ribosomal A sites, respectively. These distinct states of translation elongation are readily discerned by ribosome profiling in all eukaryotes we tested, including fungi, worms, and mammals. This high-resolution ribosome profiling approach reveals mechanisms of translation-elongation arrest during distinct stress conditions. Hyperosmotic stress inhibits translocation through Rck2-dependent eEF2 phosphorylation, whereas oxidative stress traps ribosomes in a pre-translocation state, independent of Rck2-driven eEF2 phosphorylation. These results provide insights and approaches for defining the molecular events that impact translation elongation throughout biology.

Keywords: eEF2 phosphorylation; ribosome functional states; ribosome profiling; translation elongation.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Codon
  • Gene Expression Profiling / methods*
  • HeLa Cells
  • Humans
  • Nucleic Acid Conformation
  • Osmotic Pressure
  • Oxidative Stress
  • Peptide Chain Elongation, Translational*
  • Peptide Elongation Factor 2 / genetics
  • Peptide Elongation Factor 2 / metabolism
  • Phosphorylation
  • Protein Conformation
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Transfer / chemistry
  • RNA, Transfer / genetics
  • RNA, Transfer / metabolism
  • Ribosomal Proteins / chemistry
  • Ribosomal Proteins / genetics*
  • Ribosomal Proteins / metabolism
  • Ribosomes / chemistry
  • Ribosomes / genetics*
  • Ribosomes / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Stress, Physiological*
  • Structure-Activity Relationship
  • Transcriptome*
  • Transfer RNA Aminoacylation

Substances

  • Caenorhabditis elegans Proteins
  • Codon
  • Peptide Elongation Factor 2
  • RNA, Messenger
  • Ribosomal Proteins
  • Saccharomyces cerevisiae Proteins
  • RNA, Transfer