Histone deacetylase isoforms regulate innate immune responses by deacetylating mitogen-activated protein kinase phosphatase-1

J Leukoc Biol. 2014 Apr;95(4):651-9. doi: 10.1189/jlb.1013565. Epub 2013 Dec 27.

Abstract

The MAPK pathway mediates TLR signaling during innate immune responses. We discovered previously that MKP-1 is acetylated, enhancing its interaction with its MAPK substrates and deactivating TLR signaling. As HDACs modulate inflammation by deacetylating histone and nonhistone proteins, we hypothesized that HDACs may regulate LPS-induced inflammation by deacetylating MKP-1. We found that mouse macrophages expressed a subset of HDAC isoforms (HDAC1, HDAC2, and HDAC3), which all interacted with MKP-1. Genetic silencing or pharmacologic inhibition of HDAC1, -2, and -3 increased MKP-1 acetylation in cells. Furthermore, knockdown or pharmacologic inhibition of HDAC1, -2, and -3 decreased LPS-induced phosphorylation of the MAPK member p38. Also, pharmacologic inhibition of HDAC did not decrease MAPK signaling in MKP-1 null cells. Finally, inhibition of HDAC1, -2, and -3 decreased LPS-induced expression of TNF-α, IL-1β, iNOS (NOS2), and nitrite synthesis. Taken together, our results show that HDAC1, -2, and -3 deacetylate MKP-1 and that this post-translational modification increases MAPK signaling and innate immune signaling. Thus, HDAC1, -2, and -3 isoforms are potential therapeutic targets in inflammatory diseases.

Keywords: cytokine; inflammation; inhibitors; macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Amino Acid Sequence
  • Animals
  • Cells, Cultured
  • Cytokines / biosynthesis
  • Dual Specificity Phosphatase 1 / metabolism*
  • Histone Deacetylases / physiology*
  • Immunity, Innate*
  • Inflammation / etiology
  • Isoenzymes / physiology
  • Lipopolysaccharides / pharmacology
  • MAP Kinase Signaling System
  • Macrophages / enzymology
  • Mice
  • Mice, Inbred C57BL
  • Molecular Sequence Data
  • Phosphorylation
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Cytokines
  • Isoenzymes
  • Lipopolysaccharides
  • p38 Mitogen-Activated Protein Kinases
  • Dual Specificity Phosphatase 1
  • Dusp1 protein, mouse
  • Histone Deacetylases