STAT6/Arg1 promotes microglia/macrophage efferocytosis and inflammation resolution in stroke mice

JCI Insight. 2019 Oct 17;4(20):e131355. doi: 10.1172/jci.insight.131355.

Abstract

Efferocytosis, or phagocytic clearance of dead/dying cells by brain-resident microglia and/or infiltrating macrophages, is instrumental for inflammation resolution and restoration of brain homeostasis after stroke. Here, we identify the signal transducer and activator of transcription 6/arginase1 (STAT6/Arg1) signaling axis as a potentially novel mechanism that orchestrates microglia/macrophage responses in the ischemic brain. Activation of STAT6 was observed in microglia/macrophages in the ischemic territory in a mouse model of stroke and in stroke patients. STAT6 deficiency resulted in reduced clearance of dead/dying neurons, increased inflammatory gene signature in microglia/macrophages, and enlarged infarct volume early after experimental stroke. All of these pathological changes culminated in an increased brain tissue loss and exacerbated long-term functional deficits. Combined in vivo analyses using BM chimeras and in vitro experiments using microglia/macrophage-neuron cocultures confirmed that STAT6 activation in both microglia and macrophages was essential for neuroprotection. Adoptive transfer of WT macrophages into STAT6-KO mice reduced accumulation of dead neurons in the ischemic territory and ameliorated brain infarction. Furthermore, decreased expression of Arg1 in STAT6-/- microglia/macrophages was responsible for impairments in efferocytosis and loss of antiinflammatory modality. Our study suggests that efferocytosis via STAT6/Arg1 modulates microglia/macrophage phenotype, accelerates inflammation resolution, and improves stroke outcomes.

Keywords: Inflammation; Neuroscience; Stroke.

Publication types

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

MeSH terms

  • Aged, 80 and over
  • Animals
  • Arginase / metabolism*
  • Brain / pathology
  • Brain Infarction / immunology*
  • Brain Infarction / pathology
  • Cells, Cultured
  • Disease Models, Animal
  • Female
  • Humans
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Male
  • Mice
  • Microglia / immunology*
  • Microglia / metabolism
  • Neurons
  • Phagocytosis
  • Primary Cell Culture
  • STAT6 Transcription Factor / genetics
  • STAT6 Transcription Factor / metabolism*
  • Signal Transduction / immunology

Substances

  • STAT6 Transcription Factor
  • STAT6 protein, human
  • Stat6 protein, mouse
  • ARG1 protein, human
  • Arg1 protein, mouse
  • Arginase