NF-κB inducing kinase, NIK mediates cigarette smoke/TNFα-induced histone acetylation and inflammation through differential activation of IKKs

PLoS One. 2011;6(8):e23488. doi: 10.1371/journal.pone.0023488. Epub 2011 Aug 24.

Abstract

Background: Nuclear factor (NF)-κB inducing kinase (NIK) is a central player in the non-canonical NF κB pathway, which phosphorylates IκB kinase α (IKKα) resulting in enhancement of target gene expression. We have recently shown that IKKα responds to a variety of stimuli including oxidants and cigarette smoke (CS) regulating the histone modification in addition to its role in NF-κB activation. However, the primary signaling mechanism linking CS-mediated oxidative stress and TNFα with histone acetylation and pro-inflammatory gene transcription is not well understood. We hypothesized that CS and TNFα increase NIK levels causing phosphorylation of IKKα, which leads to histone acetylation.

Methodology: To test this hypothesis, we investigated whether NIK mediates effects of CS and TNFα on histone acetylation in human lung epithelial cells in vitro and in lungs of mouse exposed to CS in vivo. CS increased the phosphorylation levels of IKKα/NIK in lung epithelial cells and mouse lungs. NIK is accumulated in the nuclear compartment, and is recruited to the promoters of pro-inflammatory genes, to induce posttranslational acetylation of histones in response to CS and TNFα. Cells in which NIK is knocked down using siRNA showed partial attenuation of CSE- and TNFα-induced acetylation of histone H3 on pro-inflammatory gene promoters. Additional study to determine the role of IKKβ/NF-κB pathway in CS-induced histone acetylation suggests that the canonical pathway does not play a role in histone acetylation particularly in response to CS in mouse lungs.

Conclusions: Overall, our findings provide a novel role for NIK in CS- and TNFα-induced histone acetylation, especially on histone H3K9.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acetylation / drug effects
  • Animals
  • Cell Line
  • Cell Nucleus / drug effects
  • Cell Nucleus / enzymology
  • Enzyme Activation / drug effects
  • Epithelial Cells / drug effects
  • Epithelial Cells / enzymology
  • Epithelial Cells / pathology
  • Gene Knockdown Techniques
  • Histones / metabolism*
  • Humans
  • I-kappa B Kinase / metabolism*
  • Inflammation / complications
  • Inflammation / enzymology
  • Inflammation / genetics
  • Inflammation / pathology*
  • Lung / drug effects
  • Lung / enzymology
  • Lung / pathology
  • Mice
  • Models, Biological
  • NF-kappaB-Inducing Kinase
  • Phosphorylation / drug effects
  • Promoter Regions, Genetic / genetics
  • Protein Binding / drug effects
  • Protein Serine-Threonine Kinases / metabolism*
  • Pulmonary Disease, Chronic Obstructive / complications
  • Pulmonary Disease, Chronic Obstructive / enzymology
  • Pulmonary Disease, Chronic Obstructive / pathology
  • Signal Transduction / drug effects
  • Smoking / adverse effects*
  • Tumor Necrosis Factor-alpha / pharmacology*

Substances

  • Histones
  • Tumor Necrosis Factor-alpha
  • Protein Serine-Threonine Kinases
  • I-kappa B Kinase