Necroptosis Execution Is Mediated by Plasma Membrane Nanopores Independent of Calcium

Cell Rep. 2017 Apr 4;19(1):175-187. doi: 10.1016/j.celrep.2017.03.024.

Abstract

Necroptosis is a form of regulated necrosis that results in cell death and content release after plasma membrane permeabilization. However, little is known about the molecular events responsible for the disruption of the plasma membrane. Here, we find that early increase in cytosolic calcium in TNF-induced necroptosis is mediated by treatment with a Smac mimetic via the TNF/RIP1/TAK1 survival pathway. This does not require the activation of the necrosome and is dispensable for necroptosis. Necroptosis induced by the activation of TLR3/4 pathways does not trigger early calcium flux. We also demonstrate that necroptotic plasma membrane rupture is mediated by osmotic forces and membrane pores around 4 nm in diameter. This late permeabilization step represents a hallmark in necroptosis execution that is cell and treatment independent and requires the RIP1/RIP3/MLKL core. In support of this, treatment with osmoprotectants reduces cell damage in an in vivo necroptosis model of ischemia-reperfusion injury.

Keywords: Smac mimetics; TNF; calcium signaling; membrane pores; necroptosis.

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins
  • Apoptosis*
  • Biomimetics
  • Calcium / metabolism*
  • Cell Membrane / metabolism*
  • HEK293 Cells
  • HT29 Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins / metabolism
  • MAP Kinase Kinase Kinases / metabolism
  • Mice
  • Mitochondrial Proteins / metabolism
  • NIH 3T3 Cells
  • Nanopores
  • Necrosis / metabolism*
  • Osmosis
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism
  • Reperfusion Injury / metabolism
  • Reperfusion Injury / pathology
  • Toll-Like Receptor 3 / metabolism
  • Toll-Like Receptor 4 / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • DIABLO protein, human
  • Intracellular Signaling Peptides and Proteins
  • Mitochondrial Proteins
  • TLR3 protein, human
  • TLR4 protein, human
  • Toll-Like Receptor 3
  • Toll-Like Receptor 4
  • Tumor Necrosis Factor-alpha
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • MAP Kinase Kinase Kinases
  • MAP kinase kinase kinase 7
  • Calcium