Inducible tumor necrosis factor (TNF) receptor-associated factor-1 expression couples the canonical to the non-canonical NF-κB pathway in TNF stimulation

J Biol Chem. 2013 May 17;288(20):14612-14623. doi: 10.1074/jbc.M113.464081. Epub 2013 Mar 29.

Abstract

The NF-κB transcription factor mediates the inflammatory response through distinct (canonical and non-canonical) signaling pathways. The mechanisms controlling utilization of either of these pathways are largely unknown. Here we observe that TNF stimulation induces delayed NF-κB2/p100 processing and investigate the coupling mechanism. TNF stimulation induces TNF-associated factor-1 (TRAF-1) that directly binds NF-κB-inducing kinase (NIK) and stabilizes it from degradation by disrupting its interaction with TRAF2·cIAP2 ubiquitin ligase complex. We show that TRAF1 depletion prevents TNF-induced NIK stabilization and reduces p52 production. To further examine the interactions of TRAF1 and NIK with NF-κB2/p100 processing, we mathematically modeled TRAF1·NIK as a coupling signaling complex and validated computational inference by siRNA knockdown to show non-canonical pathway activation is dependent not only on TRAF1 induction but also NIK stabilization by forming TRAF1·NIK complex. Thus, these integrated computational-experimental studies of TNF-induced TRAF1 expression identified TRAF1·NIK as a central complex linking canonical and non-canonical pathways by disrupting the TRAF2-cIAP2 ubiquitin ligase complex. This feed-forward kinase pathway is essential for the activation of non-canonical pathway.

Keywords: Inflammation; Mathematical Modeling; NF-κB Transcription Factor; NIK; TRAF; Tumor Necrosis Factor (TNF).

Publication types

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

MeSH terms

  • Cell Line, Tumor
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Lung Neoplasms / metabolism
  • Mass Spectrometry
  • Microscopy, Confocal
  • Models, Theoretical
  • NF-kappa B p52 Subunit / metabolism*
  • NF-kappaB-Inducing Kinase
  • Protein Serine-Threonine Kinases / metabolism*
  • RNA, Small Interfering / metabolism
  • Signal Transduction*
  • Subcellular Fractions / metabolism
  • TNF Receptor-Associated Factor 1 / metabolism*

Substances

  • NF-kappa B p52 Subunit
  • NFKB2 protein, human
  • RNA, Small Interfering
  • TNF Receptor-Associated Factor 1
  • Protein Serine-Threonine Kinases