Blockage of citrate export prevents TCA cycle fragmentation via Irg1 inactivation

Cell Rep. 2022 Feb 15;38(7):110391. doi: 10.1016/j.celrep.2022.110391.

Abstract

The metabolism of activated macrophages relies on aerobic glycolysis, while mitochondrial oxidation is disrupted. In lipopolysaccharide-activated macrophages, the citrate carrier (CIC) exports citrate from mitochondria to enhance glycolytic genes through histone acetylation. CIC inhibition or Slc25a1 knockdown reduces the occupancy of H3K9ac to hypoxia-inducible factor-1α (HIF-1α) binding sites in promoters of glycolytic genes to restrain glycolysis. HIF-1α also transcriptionally upregulates immune-responsive gene 1 for itaconate production, which is inhibited by CIC blocking. Isotopic tracing of [U-13C6] glucose shows that CIC blockage prevents citrate accumulation and itaconate production by reducing glycolytic flux and facilitating metabolic flux in the TCA cycle. Isotopic tracing of [U-13C5] glutamine reveals that CIC inhibition reduces succinate accumulation from glutaminolysis and the gamma-aminobutyric acid shunt by enhancing mitochondrial oxidation. By restraining glycolysis, CIC inhibition increases NAD+ content to ensure mitochondrial biogenesis for oxidative phosphorylation. Furthermore, blockage of citrate export reduces cerebral thrombosis by inactivation of peripheral macrophages.

Keywords: HIF-1α; Irg1; citrate carrier; itaconate; succinate.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Animals
  • Biological Transport
  • Carrier Proteins / metabolism
  • Citric Acid / metabolism*
  • Citric Acid Cycle*
  • Histones / metabolism
  • Hydro-Lyases / metabolism*
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Macrophage Activation
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / metabolism
  • NAD / metabolism
  • Organelle Biogenesis
  • Oxidation-Reduction
  • Succinates
  • Succinic Acid / metabolism
  • Thrombosis / pathology
  • Thrombosis / prevention & control
  • Transcription, Genetic
  • Zebrafish

Substances

  • Carrier Proteins
  • Histones
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Succinates
  • citrate-binding transport protein
  • NAD
  • Citric Acid
  • Succinic Acid
  • Hydro-Lyases
  • Irg1 protein, mouse
  • itaconic acid