NF-kappaB protects cells from gamma interferon-induced RIP1-dependent necroptosis

Mol Cell Biol. 2011 Jul;31(14):2934-46. doi: 10.1128/MCB.05445-11. Epub 2011 May 16.

Abstract

Interferons (IFNs) are cytokines with well-described immunomodulatory and antiviral properties, but less is known about the mechanisms by which they promote cell survival or cell death. Here, we show that IFN-γ induces RIP1 kinase-dependent necroptosis in mammalian cells deficient in NF-κB signaling. Induction of necroptosis by IFN-γ was found to depend on Jak1 and partially on STAT1. We also demonstrate that IFN-γ activates IκB kinase β (IKKβ)-dependent NF-κB to regulate a transcriptional program that protects cells from necroptosis. IFN-γ induced progressive accumulation of reactive oxygen species (ROS) and eventual loss of mitochondrial membrane potential in cells lacking the NF-κB subunit RelA. Whole-genome microarray analyses identified sod2, encoding the antioxidant enzyme manganese superoxide dismutase (MnSOD), as a RelA target and potential antinecroptotic gene. Overexpression of MnSOD inhibited IFN-γ-mediated ROS accumulation and partially rescued RelA-deficient cells from necroptosis, while RNA interference (RNAi)-mediated silencing of sod2 expression increased susceptibility to IFN-γ-induced cell death. Together, these studies demonstrate that NF-κB protects cells from IFN-γ-mediated necroptosis by transcriptionally activating a survival response that quenches ROS to preserve mitochondrial integrity.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Death / drug effects*
  • Cell Death / physiology
  • Cells, Cultured
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / physiology
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • I-kappa B Kinase / genetics
  • I-kappa B Kinase / metabolism
  • Interferon-gamma / pharmacology*
  • Janus Kinase 1 / metabolism
  • Membrane Potential, Mitochondrial / physiology
  • Mice
  • Mice, Knockout
  • Mitochondria / metabolism
  • Oligonucleotide Array Sequence Analysis
  • RNA Interference
  • Reactive Oxygen Species / metabolism
  • Receptor-Interacting Protein Serine-Threonine Kinases / genetics
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism*
  • STAT1 Transcription Factor / metabolism
  • Signal Transduction / physiology
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / metabolism
  • Transcription Factor RelA / genetics
  • Transcription Factor RelA / metabolism*
  • Transcription, Genetic
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Reactive Oxygen Species
  • STAT1 Transcription Factor
  • Transcription Factor RelA
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • Superoxide Dismutase
  • superoxide dismutase 2
  • Janus Kinase 1
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • I-kappa B Kinase