Regulation of NF-kappaB by NSD1/FBXL11-dependent reversible lysine methylation of p65

Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):46-51. doi: 10.1073/pnas.0912493107. Epub 2009 Dec 22.

Abstract

NF-kappaB, a central coordinator of immune and inflammatory responses, must be tightly regulated. We describe a NF-kappaB regulatory pathway that is driven by reversible lysine methylation of the p65 subunit, carried out by a lysine methylase, the nuclear receptor-binding SET domain-containing protein 1 (NSD1), and a lysine demethylase, F-box and leucine-rich repeat protein 11 (FBXL11). Overexpression of FBXL11 inhibits NF-kappaB activity, and a high level of NSD1 activates NF-kappaB and reverses the inhibitory effect of FBXL11, whereas reduced expression of NSD1 decreases NF-kappaB activation. The targets are K218 and K221 of p65, which are methylated in cells with activated NF-kappaB. Overexpression of FBXL11 slowed the growth of HT29 cancer cells, whereas shRNA-mediated knockdown had the opposite effect, and these phenotypes were dependent on K218/K221 methylation. In mouse embryo fibroblasts, the activation of most p65-dependent genes relied on K218/K221 methylation. Importantly, expression of the FBXL11 gene is driven by NF-kappaB, revealing a negative regulatory feedback loop. We conclude that reversible lysine methylation of NF-kappaB is an important element in the complex regulation of this key transcription factor.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • Cells, Cultured
  • Cytokines / metabolism
  • Embryo, Mammalian / cytology
  • F-Box Proteins / genetics
  • F-Box Proteins / metabolism*
  • Fibroblasts / cytology
  • Fibroblasts / physiology
  • Gene Expression Regulation
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism
  • Histone Methyltransferases
  • Histone-Lysine N-Methyltransferase
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Jumonji Domain-Containing Histone Demethylases / genetics
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • Lysine / metabolism*
  • Methylation
  • Mice
  • Mice, Knockout
  • Molecular Sequence Data
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Oxidoreductases, N-Demethylating
  • Protein Methyltransferases / genetics
  • Protein Methyltransferases / metabolism
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Transcription Factor RelA / genetics
  • Transcription Factor RelA / metabolism*

Substances

  • Cytokines
  • F-Box Proteins
  • Intracellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • Protein Subunits
  • Transcription Factor RelA
  • FBXL11 protein, mouse
  • Histone Demethylases
  • Jumonji Domain-Containing Histone Demethylases
  • KDM2A protein, human
  • Oxidoreductases, N-Demethylating
  • Histone Methyltransferases
  • Protein Methyltransferases
  • Histone-Lysine N-Methyltransferase
  • NSD1 protein, human
  • Lysine