Sequential activation of necroptosis and apoptosis cooperates to mediate vascular and neural pathology in stroke

Proc Natl Acad Sci U S A. 2020 Mar 3;117(9):4959-4970. doi: 10.1073/pnas.1916427117. Epub 2020 Feb 18.

Abstract

Apoptosis and necroptosis are two regulated cell death mechanisms; however, the interaction between these cell death pathways in vivo is unclear. Here we used cerebral ischemia/reperfusion as a model to investigate the interaction between apoptosis and necroptosis. We show that the activation of RIPK1 sequentially promotes necroptosis followed by apoptosis in a temporally specific manner. Cerebral ischemia/reperfusion insult rapidly activates necroptosis to promote cerebral hemorrhage and neuroinflammation. Ripk3 deficiency reduces cerebral hemorrhage and delays the onset of neural damage mediated by inflammation. Reduced cerebral perfusion resulting from arterial occlusion promotes the degradation of TAK1, a suppressor of RIPK1, and the transition from necroptosis to apoptosis. Conditional knockout of TAK1 in microglial/infiltrated macrophages and neuronal lineages sensitizes to ischemic infarction by promoting apoptosis. Taken together, our results demonstrate the critical role of necroptosis in mediating neurovascular damage and hypoperfusion-induced TAK1 loss, which subsequently promotes apoptosis and cerebral pathology in stroke and neurodegeneration.

Keywords: RIPK1; RIPK3; apoptosis; necroptosis; stroke.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / physiology*
  • Brain Injuries / metabolism
  • Cell Death
  • Inflammation / pathology
  • MAP Kinase Kinase Kinases / metabolism
  • Male
  • Mice
  • Mice, Knockout
  • Necroptosis / physiology*
  • Receptor-Interacting Protein Serine-Threonine Kinases / genetics
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism*
  • Stroke / metabolism*
  • Stroke / pathology

Substances

  • Receptor-Interacting Protein Serine-Threonine Kinases
  • Ripk1 protein, mouse
  • Ripk3 protein, mouse
  • MAP Kinase Kinase Kinases
  • MAP kinase kinase kinase 7