Polyubiquitinated tristetraprolin protects from TNF-induced, caspase-mediated apoptosis

J Biol Chem. 2014 Sep 5;289(36):25088-100. doi: 10.1074/jbc.M114.563312. Epub 2014 Jul 23.

Abstract

Binding of TNF to its receptor (TNFR1) elicits the spatiotemporal assembly of two signaling complexes that coordinate the balance between cell survival and cell death. We have shown previously that, following TNF treatment, the mRNA decay protein tristetraprolin (TTP) is Lys-63-polyubiquitinated by TNF receptor-associated factor 2 (TRAF2), suggesting a regulatory role in TNFR signaling. Here we demonstrate that TTP interacts with TNFR1 in a TRAF2-dependent manner, thereby initiating the MEKK1/MKK4-dependent activation of JNK activities. This regulatory function toward JNK activation but not NF-κB activation depends on lysine 105 of TTP, which we identified as the corresponding TRAF2 ubiquitination site. Disabling TTP polyubiquitination results in enhanced TNF-induced apoptosis in cervical cancer cells. Together, we uncover a novel aspect of TNFR1 signaling where TTP, in alliance with TRAF2, acts as a balancer of JNK-mediated cell survival versus death.

Keywords: Apoptosis; Cell Proliferation; NF-κB; Tristetraprolin; Tumor Necrosis Factor (TNF); c-Jun N-terminal Kinase (JNK).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Blotting, Western
  • Caspases / metabolism*
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cells, Cultured
  • Enzyme Activation / drug effects
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Lysine / metabolism
  • MAP Kinase Kinase 4 / metabolism
  • MAP Kinase Kinase Kinase 1 / metabolism
  • Mice, Knockout
  • Mutation
  • NF-kappa B / metabolism
  • Polyubiquitin / metabolism
  • Receptors, Tumor Necrosis Factor, Type I / genetics
  • Receptors, Tumor Necrosis Factor, Type I / metabolism
  • Signal Transduction / drug effects
  • TNF Receptor-Associated Factor 2 / genetics
  • TNF Receptor-Associated Factor 2 / metabolism
  • Tristetraprolin / genetics
  • Tristetraprolin / metabolism*
  • Tumor Necrosis Factor-alpha / pharmacology*
  • Ubiquitination / drug effects

Substances

  • NF-kappa B
  • Receptors, Tumor Necrosis Factor, Type I
  • TNF Receptor-Associated Factor 2
  • Tristetraprolin
  • Tumor Necrosis Factor-alpha
  • Polyubiquitin
  • JNK Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 1
  • MAP Kinase Kinase 4
  • MAP2K4 protein, human
  • Caspases
  • Lysine