Resolution metabolomes activated by hypoxic environment

Sci Adv. 2019 Oct 23;5(10):eaax4895. doi: 10.1126/sciadv.aax4895. eCollection 2019 Oct.

Abstract

Targeting hypoxia-sensitive pathways in immune cells is of interest in treating diseases. Here, we demonstrate that physiologic hypoxia (1% O2), as encountered in bone marrow and spleen, accelerates human M2 macrophage efferocytosis of apoptotic-neutrophils and senescent erythrocytes via lipolysis-dependent biosynthesis of specialized pro-resolving mediators (SPMs), i.e. resolvins, protectins, maresins and lipoxin. SPM-production was enhanced via hypoxia in M2 macrophages interacting with neutrophils and erythrocytes enabling structural elucidation of a novel eicosapentaenoic acid (EPA)-derived resolvin, resolvin E4 (RvE4) that stimulates efferocytosis of senescent erythrocytes and more potently than aspirin in mouse hemorrhagic exudates. In hypoxia, glycolysis inhibition enhanced neutrophil RvE4-SPM biosynthesis. Human macrophage-erythrocyte co-incubations in physiologic hypoxia produced RvE4-SPM from erythrocyte stores of omega-3 fatty acids. These results indicate that hypoxic environments, including bone marrow and spleen as well as sites of inflammation, activate SPM-biosynthetic circuits that in turn stimulate resolution and clearance of senescent erythrocytes and apoptotic neutrophils.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Apoptosis
  • Cell Communication
  • Cell Hypoxia
  • Erythrocyte Membrane / metabolism
  • Erythrocytes / metabolism
  • Glycolysis
  • Hemorrhage / pathology
  • Humans
  • Hypoxia / metabolism*
  • Inflammation Mediators / metabolism
  • Leukocytes / metabolism
  • Macrophages / metabolism
  • Male
  • Metabolome*
  • Neutrophils

Substances

  • Inflammation Mediators