Specific inhibition of histone deacetylase 8 reduces gene expression and production of proinflammatory cytokines in vitro and in vivo

J Biol Chem. 2015 Jan 23;290(4):2368-78. doi: 10.1074/jbc.M114.618454. Epub 2014 Dec 1.

Abstract

ITF2357 (generic givinostat) is an orally active, hydroxamic-containing histone deacetylase (HDAC) inhibitor with broad anti-inflammatory properties, which has been used to treat children with systemic juvenile idiopathic arthritis. ITF2357 inhibits both Class I and II HDACs and reduces caspase-1 activity in human peripheral blood mononuclear cells and the secretion of IL-1β and other cytokines at 25-100 nm; at concentrations >200 nm, ITF2357 is toxic in vitro. ITF3056, an analog of ITF2357, inhibits only HDAC8 (IC50 of 285 nm). Here we compared the production of IL-1β, IL-1α, TNFα, and IL-6 by ITF2357 with that of ITF3056 in peripheral blood mononuclear cells stimulated with lipopolysaccharide (LPS), heat-killed Candida albicans, or anti-CD3/anti-CD28 antibodies. ITF3056 reduced LPS-induced cytokines from 100 to 1000 nm; at 1000 nm, the secretion of IL-1β was reduced by 76%, secretion of TNFα was reduced by 88%, and secretion of IL-6 was reduced by 61%. The intracellular levels of IL-1α were 30% lower. There was no evidence of cell toxicity at ITF3056 concentrations of 100-1000 nm. Gene expression of TNFα was markedly reduced (80%), whereas IL-6 gene expression was 40% lower. Although anti-CD3/28 and Candida stimulation of IL-1β and TNFα was modestly reduced, IFNγ production was 75% lower. Mechanistically, ITF3056 reduced the secretion of processed IL-1β independent of inhibition of caspase-1 activity; however, synthesis of the IL-1β precursor was reduced by 40% without significant decrease in IL-1β mRNA levels. In mice, ITF3056 reduced LPS-induced serum TNFα by 85% and reduced IL-1β by 88%. These data suggest that specific inhibition of HDAC8 results in reduced inflammation without cell toxicity.

Keywords: Anti-inflammatory; Cell Death; Cytokine; Histone Deacetylase Inhibitor (HDAC Inhibitor) (HDI); Human Peripheral Blood Mononuclear Cells; ITF2357; ITF3056; Inflammation; Lipopolysaccharide (LPS).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Candida / metabolism
  • Caspase 1 / metabolism
  • Caspase 3 / metabolism
  • Caspase 7 / metabolism
  • Cells, Cultured
  • Cytokines / metabolism*
  • Gene Expression Regulation, Enzymologic*
  • Histone Deacetylase Inhibitors / chemistry*
  • Histone Deacetylases / metabolism
  • Humans
  • Inflammation
  • Inhibitory Concentration 50
  • Interleukin-1alpha / metabolism
  • Interleukin-1beta / metabolism
  • Interleukin-6 / metabolism
  • Leukocytes, Mononuclear / cytology
  • Leukocytes, Mononuclear / metabolism
  • Lipopolysaccharides / chemistry
  • Mice
  • Mice, Inbred C57BL
  • Monocytes / cytology
  • RNA, Messenger / metabolism
  • Real-Time Polymerase Chain Reaction
  • Repressor Proteins / antagonists & inhibitors*
  • Repressor Proteins / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Cytokines
  • Histone Deacetylase Inhibitors
  • Interleukin-1alpha
  • Interleukin-1beta
  • Interleukin-6
  • Lipopolysaccharides
  • RNA, Messenger
  • Repressor Proteins
  • Tumor Necrosis Factor-alpha
  • Caspase 3
  • Caspase 7
  • Caspase 1
  • HDAC8 protein, human
  • Histone Deacetylases