Lipopolysaccharide-induced activation of NF-κB non-canonical pathway requires BCL10 serine 138 and NIK phosphorylations

Exp Cell Res. 2010 Nov 15;316(19):3317-27. doi: 10.1016/j.yexcr.2010.05.004. Epub 2010 May 11.

Abstract

Background and aims: B-cell lymphoma/leukemia (BCL)-10 and reactive oxygen species mediate two pathways of NF-κB (RelA) activation by lipopolysaccharide (LPS) in human colonic epithelial cells. The pathway for LPS activation of RelB by the non-canonical pathway (RelB) in non-myeloid cells was not yet reported, but important for understanding the range of potential microbial LPS-induced effects in inflammatory bowel disease.

Methods: Experiments were performed in human colonic epithelial cells and in mouse embryonic fibroblasts deficient in components of the IkappaB kinase (IKK) signalosome, in order to detect mediators of the non-canonical pathway of NF-κB activation, including nuclear RelB and p52 and phospho- and total NF-κB inducing kinase (NIK). BCL10 was silenced by siRNA and effects of mutations of specific phosphorylation sites of BCL10 (Ser138Gly and Ser218Gly) were determined.

Results: By the non-canonical pathway, LPS exposure increased nuclear RelB and p52, and phospho-NIK, with no change in total NIK. Phosphorylation of BCL10 serine 138 was required for NIK phosphorylation, since mutation of this residue eliminated the increases in phospho-NIK and nuclear RelB and p52. Mutations of either serine 138 or serine 218 reduced RelA, p50, and phospho-IκBα of the canonical pathway. Effects of LPS stimulation and BCL10 silencing on NIK phosphorylation were demonstrated in confocal images.

Conclusions: LPS induces activation of both canonical and non-canonical pathways of NF-κB in human colonic epithelial cells, and the non-canonical pathway requires phosphorylations of BCL10 (serine 138) and NIK. These findings demonstrate the important role of BCL10 in mediating LPS-induced inflammation in human colonic epithelial cells and may open new avenues for therapeutic interventions.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Aged
  • Animals
  • B-Cell CLL-Lymphoma 10 Protein
  • Colon / cytology
  • Epithelial Cells / drug effects
  • Epithelial Cells / enzymology
  • Fibroblasts / metabolism
  • Gene Silencing
  • Humans
  • I-kappa B Proteins / deficiency
  • I-kappa B Proteins / metabolism
  • Interleukin-8 / metabolism
  • Lipopolysaccharides / pharmacology*
  • Male
  • Mice
  • Mutation / genetics
  • NF-KappaB Inhibitor alpha
  • NF-kappa B / metabolism*
  • NF-kappaB-Inducing Kinase
  • Phosphorylation / drug effects
  • Phosphoserine / metabolism*
  • Protein Serine-Threonine Kinases / metabolism*
  • Signal Transduction / drug effects*
  • Structure-Activity Relationship

Substances

  • Adaptor Proteins, Signal Transducing
  • B-Cell CLL-Lymphoma 10 Protein
  • BCL10 protein, human
  • Bcl10 protein, mouse
  • I kappa B beta protein
  • I-kappa B Proteins
  • Interleukin-8
  • Lipopolysaccharides
  • NF-kappa B
  • NFKBIA protein, human
  • Nfkbia protein, mouse
  • NF-KappaB Inhibitor alpha
  • Phosphoserine
  • Protein Serine-Threonine Kinases