Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand

J Biol Chem. 2005 Dec 9;280(49):40599-608. doi: 10.1074/jbc.M509560200. Epub 2005 Oct 15.

Abstract

Apo2 ligand/tumor necrosis factor (TNF)-related apoptosis-inducing ligand (Apo2L/TRAIL) mainly activates programmed cell death through caspases. By contrast, TNF primarily induces gene transcription through the inhibitor of kappaB kinase (IKK), c-Jun N-terminal kinase (JNK), and p38 mitogen-activated protein kinase pathways. Apo2L/TRAIL also can stimulate these kinases, albeit less strongly; however, the underlying mechanisms of this stimulation and its relation to apoptosis are not well understood. Here we show that Apo2L/TRAIL activates kinase pathways by promoting the association of a secondary signaling complex, subsequent to assembly of a primary, death-inducing signaling complex (DISC). The secondary complex retained the DISC components FADD and caspase-8, but recruited several factors involved in kinase activation by TNF, namely, RIP1, TRAF2, and NEMO/IKKgamma. Secondary complex formation required Fas-associated death domain (FADD), as well as caspase-8 activity. Apo2L/TRAIL stimulation of JNK and p38 further depended on RIP1 and TRAF2, whereas IKK activation required NEMO. Apo2L/TRAIL induced secretion of interleukin-8 and monocyte chemoattractant protein-1, augmenting macrophage migration. Thus, Apo2L/TRAIL and TNF organize common molecular determinants in distinct signaling complexes to stimulate similar kinase pathways. One function of kinase stimulation by Apo2L/TRAIL may be to promote phagocytic engulfment of apoptotic cells.

MeSH terms

  • Adaptor Proteins, Signal Transducing / physiology
  • Animals
  • Apoptosis Regulatory Proteins / pharmacology*
  • Caspase 8
  • Caspases / physiology
  • Cell Line, Tumor
  • Chemokine CCL2 / metabolism
  • Death Domain Receptor Signaling Adaptor Proteins
  • Enzyme Activation / drug effects
  • Fas-Associated Death Domain Protein
  • Humans
  • I-kappa B Kinase / metabolism
  • Interleukin-8 / metabolism
  • Kinetics
  • MAP Kinase Kinase 4 / metabolism
  • Membrane Glycoproteins / pharmacology*
  • Mice
  • Mice, Knockout
  • NF-kappa B / physiology
  • Phosphorylation
  • Protein Kinases / metabolism*
  • RNA, Small Interfering
  • Signal Transduction / physiology
  • TNF Receptor-Associated Factor 2 / physiology
  • TNF-Related Apoptosis-Inducing Ligand
  • Tumor Necrosis Factor Receptor-Associated Peptides and Proteins / physiology
  • Tumor Necrosis Factor-alpha / pharmacology*
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • Chemokine CCL2
  • Death Domain Receptor Signaling Adaptor Proteins
  • FADD protein, human
  • Fadd protein, mouse
  • Fas-Associated Death Domain Protein
  • Interleukin-8
  • Membrane Glycoproteins
  • NF-kappa B
  • RNA, Small Interfering
  • TNF Receptor-Associated Factor 2
  • TNF-Related Apoptosis-Inducing Ligand
  • TNFSF10 protein, human
  • Tnfsf10 protein, mouse
  • Tumor Necrosis Factor Receptor-Associated Peptides and Proteins
  • Tumor Necrosis Factor-alpha
  • Protein Kinases
  • I-kappa B Kinase
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 4
  • CASP8 protein, human
  • Casp8 protein, mouse
  • Caspase 8
  • Caspases