One-Carbon Metabolism Supports S-Adenosylmethionine and Histone Methylation to Drive Inflammatory Macrophages

Mol Cell. 2019 Sep 19;75(6):1147-1160.e5. doi: 10.1016/j.molcel.2019.06.039. Epub 2019 Aug 13.

Abstract

Activated macrophages adapt their metabolic pathways to drive the pro-inflammatory phenotype, but little is known about the biochemical underpinnings of this process. Here, we find that lipopolysaccharide (LPS) activates the pentose phosphate pathway, the serine synthesis pathway, and one-carbon metabolism, the synergism of which drives epigenetic reprogramming for interleukin-1β (IL-1β) expression. Glucose-derived ribose and one-carbon units fed by both glucose and serine metabolism are synergistically integrated into the methionine cycle through de novo ATP synthesis and fuel the generation of S-adenosylmethionine (SAM) during LPS-induced inflammation. Impairment of these metabolic pathways that feed SAM generation lead to anti-inflammatory outcomes, implicating SAM as an essential metabolite for inflammatory macrophages. Mechanistically, SAM generation maintains a relatively high SAM:S-adenosylhomocysteine ratio to support histone H3 lysine 36 trimethylation for IL-1β production. We therefore identify a synergistic effect of glucose and amino acid metabolism on orchestrating SAM availability that is intimately linked to the chromatin state for inflammation.

Keywords: H3K36me3; S-adenosylmethionine; amino-acid metabolism; epigenetic reprogramming; glycolysis offshoots; inflammation; one-carbon metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Adult
  • Animals
  • Female
  • Histones / metabolism*
  • Humans
  • Inflammation / chemically induced
  • Inflammation / metabolism
  • Inflammation / pathology
  • Interleukin-1beta / metabolism
  • Lipopolysaccharides / toxicity
  • Macrophages, Peritoneal / metabolism*
  • Macrophages, Peritoneal / pathology
  • Male
  • Methylation / drug effects
  • Mice
  • S-Adenosylmethionine / metabolism*

Substances

  • Histones
  • IL1B protein, human
  • IL1B protein, mouse
  • Interleukin-1beta
  • Lipopolysaccharides
  • S-Adenosylmethionine
  • Adenosine Triphosphate