Rapid RNase L-driven arrest of protein synthesis in the dsRNA response without degradation of translation machinery

RNA. 2017 Nov;23(11):1660-1671. doi: 10.1261/rna.062000.117. Epub 2017 Aug 14.

Abstract

Mammalian cells respond to double-stranded RNA (dsRNA) by activating a translation-inhibiting endoribonuclease, RNase L. Consensus in the field indicates that RNase L arrests protein synthesis by degrading ribosomal RNAs (rRNAs) and messenger RNAs (mRNAs). However, here we provide evidence for a different and far more efficient mechanism. By sequencing abundant RNA fragments generated by RNase L in human cells, we identify site-specific cleavage of two groups of noncoding RNAs: Y-RNAs, whose function is poorly understood, and cytosolic tRNAs, which are essential for translation. Quantitative analysis of human RNA cleavage versus nascent protein synthesis in lung carcinoma cells shows that RNase L stops global translation when tRNAs, as well as rRNAs and mRNAs, are still intact. Therefore, RNase L does not have to degrade the translation machinery to stop protein synthesis. Our data point to a rapid mechanism that transforms a subtle RNA cleavage into a cell-wide translation arrest.

Keywords: RNase L; Y-RNA; signaling; tRNA; translation.

Publication types

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

MeSH terms

  • Binding Sites / genetics
  • Cell Line
  • Consensus Sequence
  • Endoribonucleases / metabolism*
  • HeLa Cells
  • Humans
  • Models, Biological
  • Protein Biosynthesis*
  • RNA Cleavage
  • RNA Processing, Post-Transcriptional
  • RNA Stability
  • RNA, Double-Stranded / genetics*
  • RNA, Double-Stranded / metabolism*
  • RNA, Small Untranslated / genetics
  • RNA, Small Untranslated / metabolism
  • RNA, Transfer / genetics
  • RNA, Transfer / metabolism

Substances

  • RNA, Double-Stranded
  • RNA, Small Untranslated
  • RNA, Transfer
  • Endoribonucleases
  • 2-5A-dependent ribonuclease