Signal transducer and activator of transcription-1 is critical for apoptosis in macrophages subjected to endoplasmic reticulum stress in vitro and in advanced atherosclerotic lesions in vivo

Circulation. 2008 Feb 19;117(7):940-51. doi: 10.1161/CIRCULATIONAHA.107.711275. Epub 2008 Jan 28.

Abstract

Background: Macrophage apoptosis is a critical process in the formation of necrotic cores in vulnerable atherosclerotic plaques. In vitro and in vivo data suggest that macrophage apoptosis in advanced atheromata may be triggered by a combination of endoplasmic reticulum stress and engagement of the type A scavenger receptor, which together induce death through a rise in cytosolic calcium and activation of toll-like receptor-4.

Methods and results: Using both primary peritoneal macrophages and studies in advanced atheromata in vivo, we introduce signal transducer and activator of transcription-1 (STAT1) as a critical and necessary component of endoplasmic reticulum stress/type A scavenger receptor-induced macrophage apoptosis. We show that STAT1 is serine phosphorylated in macrophages subjected to type A scavenger receptor ligands and endoplasmic reticulum stress in a manner requiring cytosolic calcium, calcium/calmodulin-dependent protein kinase II, and toll-like receptor-4. Remarkably, apoptosis was inhibited by approximately 80% to 90% (P<0.05) by STAT1 deficiency or calcium/calmodulin-dependent protein kinase II inhibition. In vivo, nuclear Ser-P-STAT1 was found in macrophage-rich regions of advanced murine and human atheromata. Most important, macrophage apoptosis was decreased by 61% (P=0.034) and plaque necrosis by 34% (P=0.02) in the plaques of fat-fed low density lipoprotein receptor null Ldlr-/- mice transplanted with Stat1-/- bone marrow.

Conclusions: STAT1 is critical for endoplasmic reticulum stress/type A scavenger receptor-induced apoptosis in primary tissue macrophages and in macrophage apoptosis in advanced atheromata. These findings suggest a potentially important role for STAT1-mediated macrophage apoptosis in atherosclerotic plaque progression.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / physiology*
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology*
  • Bone Marrow Transplantation
  • Calcium Signaling
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / physiology
  • Endoplasmic Reticulum / physiology*
  • Female
  • Humans
  • In Situ Nick-End Labeling
  • Macrophages, Peritoneal / metabolism
  • Macrophages, Peritoneal / pathology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phosphorylation
  • Phosphoserine / metabolism
  • Protein Processing, Post-Translational
  • Radiation Chimera
  • Receptors, LDL / deficiency
  • Receptors, LDL / genetics
  • STAT1 Transcription Factor / analysis
  • STAT1 Transcription Factor / deficiency
  • STAT1 Transcription Factor / genetics
  • STAT1 Transcription Factor / physiology*
  • Scavenger Receptors, Class A / drug effects
  • Scavenger Receptors, Class A / physiology
  • Toll-Like Receptor 4 / physiology

Substances

  • Receptors, LDL
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Scavenger Receptors, Class A
  • Stat1 protein, mouse
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Phosphoserine
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2