Post-translational regulation of mitogen-activated protein kinase phosphatase (MKP)-1 and MKP-2 in macrophages following lipopolysaccharide stimulation: the role of the C termini of the phosphatases in determining their stability

J Biol Chem. 2014 Oct 17;289(42):28753-64. doi: 10.1074/jbc.M114.591925. Epub 2014 Sep 9.

Abstract

MAPK phosphatases (MKPs) are critical modulators of the innate immune response, and yet the mechanisms regulating their accumulation remain poorly understood. In the present studies, we investigated the role of post-translational modification in the accumulation of MKP-1 and MKP-2 in macrophages following LPS stimulation. We found that upon LPS stimulation, MKP-1 and MKP-2 accumulated with different kinetics: MKP-1 level peaked at ∼1 h, while MKP-2 levels continued to rise for at least 6 h. Accumulation of both MKP-1 and MKP-2 were attenuated by inhibition of the ERK cascade. Interestingly, p38 inhibition prior to LPS stimulation had little effect on MKP-1 and MKP-2 protein levels, but hindered their detection by an M-18 MKP-1 antibody. Studies of the epitope sequence recognized by the M-18 MKP-1 antibody revealed extensive phosphorylation of two serine residues in the C terminus of both MKP-1 and MKP-2 by the ERK pathway. Remarkably, the stability of both MKP-1 and MKP-2 was markedly decreased in macrophages in the presence of an ERK pathway inhibitor. Mutation of the two C-terminal serine residues in MKP-1 and MKP-2 to alanine decreased their half-lives, while mutating these residues to aspartate dramatically increased their half-lives. Deletion of the C terminus from MKP-1 and MKP-2 also considerably increased their stabilities. Surprisingly, enhanced stabilities of the MKP-1 and MKP-2 mutants were not associated with decreased ubiquitination. Degradation of both MKP-1 and MKP-2 was attenuated by proteasomal inhibitors. Our studies suggest that MKP-1 and MKP-2 stability is regulated by ERK-mediated phosphorylation through a degradation pathway independent of polyubiquitination.

Keywords: Lipopolysaccharide (LPS); MAP Kinase Phosphatase; Macrophage; Phosphorylation; Post-translational Modification (PTM); Protein Stability; Ubiquitylation (Ubiquitination).

Publication types

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

MeSH terms

  • Alanine / chemistry
  • Animals
  • Dual Specificity Phosphatase 1 / metabolism*
  • Dual-Specificity Phosphatases / metabolism*
  • Epitopes / metabolism
  • Gene Expression Regulation, Enzymologic
  • HEK293 Cells
  • Humans
  • Lipopolysaccharides / chemistry
  • Macrophages / enzymology*
  • Mice
  • Mitogen-Activated Protein Kinase Phosphatases / metabolism*
  • Phosphorylation
  • Proteasome Inhibitors / chemistry
  • Protein Conformation
  • Protein Processing, Post-Translational*
  • Protein Structure, Tertiary
  • Protein Tyrosine Phosphatases / metabolism*
  • Ubiquitin / metabolism
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Epitopes
  • Lipopolysaccharides
  • Proteasome Inhibitors
  • Ubiquitin
  • p38 Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinase Phosphatases
  • DUSP1 protein, human
  • DUSP4 protein, human
  • Dual Specificity Phosphatase 1
  • Dual-Specificity Phosphatases
  • Dusp1 protein, mouse
  • Dusp4 protein, mouse
  • Protein Tyrosine Phosphatases
  • Alanine