Concerted 2-5A-Mediated mRNA Decay and Transcription Reprogram Protein Synthesis in the dsRNA Response

Mol Cell. 2019 Sep 19;75(6):1218-1228.e6. doi: 10.1016/j.molcel.2019.07.027. Epub 2019 Sep 4.

Abstract

Viral and endogenous double-stranded RNA (dsRNA) is a potent trigger for programmed RNA degradation by the 2-5A/RNase L complex in cells of all mammals. This 2-5A-mediated decay (2-5AMD) is a conserved stress response switching global protein synthesis from homeostasis to production of interferons (IFNs). To understand this mechanism, we examined 2-5AMD in human cells and found that it triggers polysome collapse characteristic of inhibited translation initiation. We determined that translation initiation complexes and ribosomes purified from translation-arrested cells remain functional. However, spike-in RNA sequencing (RNA-seq) revealed cell-wide decay of basal mRNAs accompanied by rapid accumulation of mRNAs encoding innate immune proteins. Our data attribute this 2-5AMD evasion to better stability of defense mRNAs and positive feedback in the IFN response amplified by RNase L-resistant molecules. We conclude that 2-5AMD and transcription act in concert to refill mammalian cells with defense mRNAs, thereby "prioritizing" the synthesis of innate immune proteins.

Keywords: RNase L; dsRNA; innate immunity; interferon; mRNA decay; reprogramming; translation.

Publication types

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

MeSH terms

  • A549 Cells
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism*
  • Humans
  • Immunity, Innate
  • Protein Biosynthesis*
  • RNA Stability*
  • RNA, Double-Stranded / genetics
  • RNA, Double-Stranded / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • Transcription, Genetic*

Substances

  • RNA, Double-Stranded
  • RNA, Messenger
  • Endoribonucleases
  • 2-5A-dependent ribonuclease