Oxylipin metabolism is controlled by mitochondrial β-oxidation during bacterial inflammation

Nat Commun. 2022 Jan 10;13(1):139. doi: 10.1038/s41467-021-27766-8.

Abstract

Oxylipins are potent biological mediators requiring strict control, but how they are removed en masse during infection and inflammation is unknown. Here we show that lipopolysaccharide (LPS) dynamically enhances oxylipin removal via mitochondrial β-oxidation. Specifically, genetic or pharmacological targeting of carnitine palmitoyl transferase 1 (CPT1), a mitochondrial importer of fatty acids, reveal that many oxylipins are removed by this protein during inflammation in vitro and in vivo. Using stable isotope-tracing lipidomics, we find secretion-reuptake recycling for 12-HETE and its intermediate metabolites. Meanwhile, oxylipin β-oxidation is uncoupled from oxidative phosphorylation, thus not contributing to energy generation. Testing for genetic control checkpoints, transcriptional interrogation of human neonatal sepsis finds upregulation of many genes involved in mitochondrial removal of long-chain fatty acyls, such as ACSL1,3,4, ACADVL, CPT1B, CPT2 and HADHB. Also, ACSL1/Acsl1 upregulation is consistently observed following the treatment of human/murine macrophages with LPS and IFN-γ. Last, dampening oxylipin levels by β-oxidation is suggested to impact on their regulation of leukocyte functions. In summary, we propose mitochondrial β-oxidation as a regulatory metabolic checkpoint for oxylipins during inflammation.

Publication types

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

MeSH terms

  • 12-Hydroxy-5,8,10,14-eicosatetraenoic Acid / metabolism*
  • Acyl-CoA Dehydrogenase, Long-Chain / blood
  • Acyl-CoA Dehydrogenase, Long-Chain / genetics
  • Animals
  • Carnitine O-Palmitoyltransferase / blood
  • Carnitine O-Palmitoyltransferase / genetics
  • Coenzyme A Ligases / blood
  • Coenzyme A Ligases / genetics
  • Female
  • Gene Expression Regulation
  • Humans
  • Infant, Newborn
  • Interferon-gamma / pharmacology
  • Lipid Metabolism / genetics*
  • Lipidomics / methods
  • Lipopolysaccharides / pharmacology
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondrial Trifunctional Protein, beta Subunit / blood
  • Mitochondrial Trifunctional Protein, beta Subunit / genetics
  • Oxidation-Reduction
  • Oxylipins / metabolism*
  • Peritonitis / blood
  • Peritonitis / chemically induced
  • Peritonitis / genetics*
  • Peritonitis / pathology
  • RAW 264.7 Cells
  • Sepsis / blood
  • Sepsis / genetics*
  • Sepsis / pathology

Substances

  • Lipopolysaccharides
  • Oxylipins
  • 12-Hydroxy-5,8,10,14-eicosatetraenoic Acid
  • Interferon-gamma
  • Acyl-CoA Dehydrogenase, Long-Chain
  • ACADVL protein, human
  • HADHB protein, human
  • Mitochondrial Trifunctional Protein, beta Subunit
  • CPT1B protein, human
  • Carnitine O-Palmitoyltransferase
  • Coenzyme A Ligases
  • ACSL1 protein, human
  • long-chain-fatty-acid-CoA ligase