Nox4 regulates InsP3 receptor-dependent Ca2+ release into mitochondria to promote cell survival

EMBO J. 2020 Oct 1;39(19):e103530. doi: 10.15252/embj.2019103530. Epub 2020 Aug 10.

Abstract

Cells subjected to environmental stresses undergo regulated cell death (RCD) when homeostatic programs fail to maintain viability. A major mechanism of RCD is the excessive calcium loading of mitochondria and consequent triggering of the mitochondrial permeability transition (mPT), which is especially important in post-mitotic cells such as cardiomyocytes and neurons. Here, we show that stress-induced upregulation of the ROS-generating protein Nox4 at the ER-mitochondria contact sites (MAMs) is a pro-survival mechanism that inhibits calcium transfer through InsP3 receptors (InsP3 R). Nox4 mediates redox signaling at the MAM of stressed cells to augment Akt-dependent phosphorylation of InsP3 R, thereby inhibiting calcium flux and mPT-dependent necrosis. In hearts subjected to ischemia-reperfusion, Nox4 limits infarct size through this mechanism. These results uncover a hitherto unrecognized stress pathway, whereby a ROS-generating protein mediates pro-survival effects through spatially confined signaling at the MAM to regulate ER to mitochondria calcium flux and triggering of the mPT.

Keywords: InsP3 receptor; NADPH oxidase-4; calcium signaling; cell death; mitochondria-associated membrane.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Signaling*
  • Cell Survival
  • Inositol 1,4,5-Trisphosphate Receptors / genetics
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism*
  • Mitochondria, Heart / metabolism*
  • Myocardial Reperfusion Injury / genetics
  • Myocardial Reperfusion Injury / metabolism
  • Myocytes, Cardiac / metabolism*
  • NADPH Oxidase 4 / genetics
  • NADPH Oxidase 4 / metabolism*
  • Oxidative Stress
  • Rats

Substances

  • Inositol 1,4,5-Trisphosphate Receptors
  • NADPH Oxidase 4
  • Nox4 protein, mouse
  • Nox4 protein, rat
  • Calcium