RIPK3/MLKL-Mediated Neuronal Necroptosis Modulates the M1/M2 Polarization of Microglia/Macrophages in the Ischemic Cortex

Cereb Cortex. 2018 Jul 1;28(7):2622-2635. doi: 10.1093/cercor/bhy089.

Abstract

Cell death and subsequent inflammation are 2 key pathological changes occurring in cerebral ischemia. Active microglia/macrophages play a double-edged role depending on the balance of their M1/M2 phenotypes. Necrosis is the predominant type of cell death following ischemia. However, how necrotic cells modulate the M1/M2 polarization of microglia/macrophages remains poorly investigated. Here, we reported that ischemia induces a rapid RIPK3/MLKL-mediated neuron-dominated necroptosis, a type of programmed necrosis. Ablating RIPK3 or MLKL could switch the activation of microglia/macrophages from M1 to the M2 type in the ischemic cortex. Conditioned medium of oxygen-glucose deprivation (OGD)-treated wild-type (WT) neurons induced M1 polarization, while that of RIPK3-/- neurons favored M2 polarization. OGD treatment induces proinflammatory IL-18 and TNFα in WT but not in RIPK3-/- neurons, which in turn upregulate anti-inflammatory IL-4 and IL-10. Furthermore, the expression of Myd88-a common downstream adaptor of toll-like receptors-is significantly upregulated in the microglia/macrophages of ischemic WT but not of RIPK3-/- or MLKL-/- cortices. Antagonizing the function of Myd88 could phenocopy the effects of RIPK3/MLKL-knockout on the polarization of microglia/macrophages and was neuroprotective. Our data revealed a novel role of necroptotic neurons in modulating the M1/M2 balance of microglia/macrophages in the ischemic cortex, possibly through Myd88 signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Apoptosis / physiology*
  • Brain Ischemia / physiopathology*
  • Cell Hypoxia
  • Cell Polarity / physiology*
  • Cells, Cultured
  • Cerebral Cortex / physiopathology
  • Cytokines / metabolism
  • Disease Models, Animal
  • Embryo, Mammalian
  • Flow Cytometry
  • Glial Fibrillary Acidic Protein / metabolism
  • Glucose / deficiency
  • Macrophages / metabolism
  • Macrophages / physiology*
  • Macrophages / ultrastructure
  • Mice
  • Mice, Transgenic
  • Microglia / metabolism
  • Microglia / physiology*
  • Microglia / ultrastructure
  • Myeloid Differentiation Factor 88 / metabolism
  • Neurons
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • RNA, Messenger / metabolism
  • Receptor-Interacting Protein Serine-Threonine Kinases / genetics
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism*

Substances

  • Cytokines
  • Glial Fibrillary Acidic Protein
  • Myeloid Differentiation Factor 88
  • RNA, Messenger
  • MLKL protein, mouse
  • Protein Kinases
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • Ripk3 protein, mouse
  • Glucose