The pseudokinase MLKL activates PAD4-dependent NET formation in necroptotic neutrophils

Sci Signal. 2018 Sep 4;11(546):eaao1716. doi: 10.1126/scisignal.aao1716.

Abstract

Neutrophil extracellular trap (NET) formation can generate short-term, functional anucleate cytoplasts and trigger loss of cell viability. We demonstrated that the necroptotic cell death effector mixed lineage kinase domain-like (MLKL) translocated from the cytoplasm to the plasma membrane and stimulated downstream NADPH oxidase-independent ROS production, loss of cytoplasmic granules, breakdown of the nuclear membrane, chromatin decondensation, histone hypercitrullination, and extrusion of bacteriostatic NETs. This process was coordinated by receptor-interacting protein kinase-1 (RIPK1), which activated the caspase-8-dependent apoptotic or RIPK3/MLKL-dependent necroptotic death of mouse and human neutrophils. Genetic deficiency of RIPK3 and MLKL prevented NET formation but did not prevent cell death, which was because of residual caspase-8-dependent activity. Peptidylarginine deiminase 4 (PAD4) was activated downstream of RIPK1/RIPK3/MLKL and was required for maximal histone hypercitrullination and NET extrusion. This work defines a distinct signaling network that activates PAD4-dependent NET release for the control of methicillin-resistant Staphylococcus aureus (MRSA) infection.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis*
  • Caspase 8 / genetics
  • Caspase 8 / metabolism
  • Cells, Cultured
  • Extracellular Traps / genetics
  • Extracellular Traps / metabolism*
  • Histones / metabolism
  • Humans
  • Methicillin-Resistant Staphylococcus aureus / physiology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Electron, Transmission
  • Neutrophils / metabolism*
  • Neutrophils / microbiology
  • Neutrophils / ultrastructure
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Protein-Arginine Deiminase Type 4
  • Protein-Arginine Deiminases / genetics
  • Protein-Arginine Deiminases / metabolism*
  • Receptor-Interacting Protein Serine-Threonine Kinases / genetics
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism

Substances

  • Histones
  • MLKL protein, human
  • Protein Kinases
  • RIPK1 protein, human
  • RIPK3 protein, human
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • Caspase 8
  • PADI4 protein, human
  • Protein-Arginine Deiminase Type 4
  • Protein-Arginine Deiminases
  • peptidylarginine deiminase 4, mouse