N 6-methyladenosine RNA modification-mediated cellular metabolism rewiring inhibits viral replication

Science. 2019 Sep 13;365(6458):1171-1176. doi: 10.1126/science.aax4468. Epub 2019 Aug 22.

Abstract

Host cell metabolism can be modulated by viral infection, affecting viral survival or clearance. Yet the cellular metabolism rewiring mediated by the N 6-methyladenosine (m6A) modification in interactions between virus and host remains largely unknown. Here we report that in response to viral infection, host cells impair the enzymatic activity of the RNA m6A demethylase ALKBH5. This behavior increases the m6A methylation on α-ketoglutarate dehydrogenase (OGDH) messenger RNA (mRNA) to reduce its mRNA stability and protein expression. Reduced OGDH decreases the production of the metabolite itaconate that is required for viral replication. With reduced OGDH and itaconate production in vivo, Alkbh5-deficient mice display innate immune response-independent resistance to viral exposure. Our findings reveal that m6A RNA modification-mediated down-regulation of the OGDH-itaconate pathway reprograms cellular metabolism to inhibit viral replication, proposing potential targets for controlling viral infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine / analogs & derivatives*
  • Adenosine / chemistry
  • AlkB Homolog 5, RNA Demethylase / metabolism*
  • Animals
  • Cells, Cultured
  • Cellular Reprogramming
  • Humans
  • Immunity, Innate*
  • Ketoglutarate Dehydrogenase Complex / metabolism*
  • Macrophages, Peritoneal / virology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Protein Processing, Post-Translational
  • RAW 264.7 Cells
  • RNA Interference
  • RNA Stability
  • RNA, Messenger / chemistry
  • Succinates
  • THP-1 Cells
  • Vesiculovirus / pathogenicity*
  • Vesiculovirus / physiology
  • Virus Replication*

Substances

  • RNA, Messenger
  • Succinates
  • N-methyladenosine
  • ALKBH5 protein, mouse
  • AlkB Homolog 5, RNA Demethylase
  • Ketoglutarate Dehydrogenase Complex
  • Adenosine
  • itaconic acid