A dysregulated acetyl/SUMO switch of FXR promotes hepatic inflammation in obesity

EMBO J. 2015 Jan 13;34(2):184-99. doi: 10.15252/embj.201489527. Epub 2014 Nov 25.

Abstract

Acetylation of transcriptional regulators is normally dynamically regulated by nutrient status but is often persistently elevated in nutrient-excessive obesity conditions. We investigated the functional consequences of such aberrantly elevated acetylation of the nuclear receptor FXR as a model. Proteomic studies identified K217 as the FXR acetylation site in diet-induced obese mice. In vivo studies utilizing acetylation-mimic and acetylation-defective K217 mutants and gene expression profiling revealed that FXR acetylation increased proinflammatory gene expression, macrophage infiltration, and liver cytokine and triglyceride levels, impaired insulin signaling, and increased glucose intolerance. Mechanistically, acetylation of FXR blocked its interaction with the SUMO ligase PIASy and inhibited SUMO2 modification at K277, resulting in activation of inflammatory genes. SUMOylation of agonist-activated FXR increased its interaction with NF-κB but blocked that with RXRα, so that SUMO2-modified FXR was selectively recruited to and trans-repressed inflammatory genes without affecting FXR/RXRα target genes. A dysregulated acetyl/SUMO switch of FXR in obesity may serve as a general mechanism for diminished anti-inflammatory response of other transcriptional regulators and provide potential therapeutic and diagnostic targets for obesity-related metabolic disorders.

Keywords: NF‐κB; PIASy; SUMO2; acetylation; steatosis.

Publication types

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

MeSH terms

  • Acetylation
  • Amino Acid Sequence
  • Animals
  • Blotting, Western
  • Cytokines / genetics
  • Cytokines / metabolism
  • Electrophoretic Mobility Shift Assay
  • Gene Expression Profiling
  • Gene Expression Regulation*
  • Immunoenzyme Techniques
  • Immunoprecipitation
  • Inflammation / etiology
  • Inflammation / metabolism
  • Inflammation / pathology*
  • Liver Diseases / etiology
  • Liver Diseases / metabolism
  • Liver Diseases / pathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Obese
  • Molecular Sequence Data
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Obesity / complications*
  • Obesity / physiopathology
  • Protein Conformation
  • Protein Processing, Post-Translational
  • Proteomics
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptors, Cytoplasmic and Nuclear / chemistry
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Homology, Amino Acid
  • Small Ubiquitin-Related Modifier Proteins / chemistry
  • Small Ubiquitin-Related Modifier Proteins / genetics
  • Small Ubiquitin-Related Modifier Proteins / metabolism*
  • Sumoylation
  • Tandem Mass Spectrometry

Substances

  • Cytokines
  • NF-kappa B
  • RNA, Messenger
  • Receptors, Cytoplasmic and Nuclear
  • SUMO2 protein, mouse
  • Small Ubiquitin-Related Modifier Proteins
  • farnesoid X-activated receptor