Activation-induced tumor necrosis factor receptor-associated factor 3 (Traf3) alternative splicing controls the noncanonical nuclear factor κB pathway and chemokine expression in human T cells

J Biol Chem. 2014 May 9;289(19):13651-60. doi: 10.1074/jbc.M113.526269. Epub 2014 Mar 26.

Abstract

The noncanonical nuclear factor κB (ncNFκB) pathway regulates the expression of chemokines required for secondary lymphoid organ formation and thus plays a pivotal role in adaptive immunity. Whereas ncNFκB signaling has been well described in stromal cells and B cells, its role and regulation in T cells remain largely unexplored. ncNFκB activity critically depends on the upstream NFκB-inducing kinase (NIK). NIK expression is negatively regulated by the full-length isoform of TNF receptor-associated factor 3 (Traf3) as formation of a NIK-Traf3-Traf2 complex targets NIK for degradation. Here we show that T cell-specific and activation-dependent alternative splicing generates a Traf3 isoform lacking exon 8 (Traf3DE8) that, in contrast to the full-length protein, activates ncNFκB signaling. Traf3DE8 disrupts the NIK-Traf3-Traf2 complex and allows accumulation of NIK to initiate ncNFκB signaling in activated T cells. ncNFκB activity results in expression of several chemokines, among them B cell chemoattractant (CxCL13), both in a model T cell line and in primary human CD4(+) T cells. Because CxCL13 plays an important role in B cell migration and activation, our data suggest an involvement and provide a mechanistic basis for Traf3 alternative splicing and ncNFκB activation in contributing to T cell-dependent adaptive immunity.

Keywords: Alternative Splicing; Nuclear Factor κB (NFκB); RNA Splicing; T Cell; TRAF.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity / physiology*
  • Alternative Splicing / physiology*
  • Animals
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism*
  • Chemokine CXCL13 / genetics
  • Chemokine CXCL13 / immunology
  • Chemokine CXCL13 / metabolism
  • HeLa Cells
  • Humans
  • NF-kappa B / genetics
  • NF-kappa B / immunology
  • NF-kappa B / metabolism*
  • NF-kappaB-Inducing Kinase
  • Protein Isoforms / biosynthesis
  • Protein Isoforms / genetics
  • Protein Isoforms / immunology
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / immunology
  • Protein Serine-Threonine Kinases / metabolism
  • Signal Transduction / physiology*
  • TNF Receptor-Associated Factor 2 / biosynthesis
  • TNF Receptor-Associated Factor 2 / genetics
  • TNF Receptor-Associated Factor 2 / immunology
  • TNF Receptor-Associated Factor 3 / biosynthesis*
  • TNF Receptor-Associated Factor 3 / genetics
  • TNF Receptor-Associated Factor 3 / immunology

Substances

  • CXCL13 protein, human
  • Chemokine CXCL13
  • NF-kappa B
  • Protein Isoforms
  • TNF Receptor-Associated Factor 2
  • TNF Receptor-Associated Factor 3
  • TRAF3 protein, human
  • Protein Serine-Threonine Kinases