Glycolysis-dependent histone deacetylase 4 degradation regulates inflammatory cytokine production

Mol Biol Cell. 2014 Nov 1;25(21):3300-7. doi: 10.1091/mbc.E13-12-0757. Epub 2014 Sep 3.

Abstract

Activation of the inflammatory response is accompanied by a metabolic shift to aerobic glycolysis. Here we identify histone deacetylase 4 (HDAC4) as a new component of the immunometabolic program. We show that HDAC4 is required for efficient inflammatory cytokine production activated by lipopolysaccharide (LPS). Surprisingly, prolonged LPS treatment leads to HDAC4 degradation. LPS-induced HDAC4 degradation requires active glycolysis controlled by GSK3β and inducible nitric oxide synthase (iNOS). Inhibition of GSK3β or iNOS suppresses nitric oxide (NO) production, glycolysis, and HDAC4 degradation. We present evidence that sustained glycolysis induced by LPS treatment activates caspase-3, which cleaves HDAC4 and triggers its degradation. Of importance, a caspase-3-resistant mutant HDAC4 escapes LPS-induced degradation and prolongs inflammatory cytokine production. Our findings identify the GSK3β-iNOS-NO axis as a critical signaling cascade that couples inflammation to metabolic reprogramming and a glycolysis-driven negative feedback mechanism that limits inflammatory response by triggering HDAC4 degradation.

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

  • Animals
  • Caspase 3 / metabolism
  • Cell Line / drug effects
  • Cytokines / metabolism*
  • Glycogen Synthase Kinase 3 / metabolism
  • Glycogen Synthase Kinase 3 beta
  • Glycolysis / drug effects
  • Glycolysis / physiology*
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism*
  • Inflammation / metabolism*
  • Lipopolysaccharides / pharmacology
  • Macrophages / metabolism
  • Mice
  • Microglia / cytology
  • Microglia / metabolism
  • Mutation
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type II / metabolism
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism

Substances

  • Cytokines
  • Lipopolysaccharides
  • Nitric Oxide
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • Glycogen Synthase Kinase 3 beta
  • Gsk3b protein, mouse
  • Ribosomal Protein S6 Kinases, 70-kDa
  • Glycogen Synthase Kinase 3
  • Caspase 3
  • Hdac5 protein, mouse
  • Histone Deacetylases