Serine metabolism antagonizes antiviral innate immunity by preventing ATP6V0d2-mediated YAP lysosomal degradation

Cell Metab. 2021 May 4;33(5):971-987.e6. doi: 10.1016/j.cmet.2021.03.006. Epub 2021 Apr 1.

Abstract

Serine metabolism promotes tumor oncogenesis and regulates immune cell functions, but whether it also contributes to antiviral innate immunity is unknown. Here, we demonstrate that virus-infected macrophages display decreased expression of serine synthesis pathway (SSP) enzymes. Suppressing the SSP key enzyme phosphoglycerate dehydrogenase (PHGDH) by genetic approaches or by treatment with the pharmaceutical inhibitor CBR-5884 and by exogenous serine restriction enhanced IFN-β-mediated antiviral innate immunity in vitro and in vivo. Mechanistic experiments showed that virus infection or serine metabolism deficiency increased the expression of the V-ATPase subunit ATP6V0d2 by inhibiting S-adenosyl methionine-dependent H3K27me3 occupancy at the promoter. ATP6V0d2 promoted YAP lysosomal degradation to relieve YAP-mediated blockade of the TBK1-IRF3 axis and, thus, enhance IFN-β production. These findings implicate critical functions of PHGDH and the key immunometabolite serine in blunting antiviral innate immunity and also suggest manipulation of serine metabolism as a therapeutic strategy against virus infection.

Keywords: ATP6V0d2; H3K27me3; PHGDH; SAM; YAP; antiviral; serine metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Line
  • Histones / metabolism
  • Humans
  • Immunity, Innate*
  • Interferon-beta / genetics
  • Interferon-beta / metabolism
  • Lysosomes / metabolism*
  • Macrophages / cytology
  • Macrophages / metabolism
  • Macrophages / virology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phosphoglycerate Dehydrogenase / antagonists & inhibitors
  • Phosphoglycerate Dehydrogenase / genetics
  • Phosphoglycerate Dehydrogenase / metabolism
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • S-Adenosylmethionine / pharmacology
  • Serine / metabolism*
  • Signal Transduction / drug effects
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Vacuolar Proton-Translocating ATPases / genetics
  • Vacuolar Proton-Translocating ATPases / metabolism*
  • Vesicular stomatitis Indiana virus / physiology

Substances

  • Cell Cycle Proteins
  • Histones
  • RNA, Small Interfering
  • Transcription Factors
  • YY1AP1 protein, human
  • Serine
  • Interferon-beta
  • S-Adenosylmethionine
  • Phosphoglycerate Dehydrogenase
  • Vacuolar Proton-Translocating ATPases