MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay

EMBO J. 2004 Mar 24;23(6):1313-24. doi: 10.1038/sj.emboj.7600163. Epub 2004 Mar 11.

Abstract

Stress granules (SGs) are dynamic cytoplasmic foci at which stalled translation initiation complexes accumulate in cells subjected to environmental stress. SG-associated proteins such as TIA-1, TIAR and HuR bind to AU-rich element (ARE)-containing mRNAs and control their translation and stability. Here we show that tristetraprolin (TTP), an ARE-binding protein that destabilizes ARE-mRNAs, is recruited to SGs that are assembled in response to FCCP-induced energy deprivation, but not arsenite-induced oxidative stress. Exclusion of TTP from arsenite-induced SGs is a consequence of MAPKAP kinase-2 (MK2)-induced phosphorylation at serines 52 and 178, which promotes the assembly of TTP:14-3-3 complexes. 14-3-3 binding excludes TTP from SGs and inhibits TTP-dependent degradation of ARE-containing transcripts. In activated RAW 264.7 macrophages, endogenous TTP:14-3-3 complexes bind to ARE-RNA. Our data reveal the mechanism by which the p38-MAPK/MK2 kinase cascade inhibits TTP-mediated degradation of ARE-containing transcripts and thereby contributes to lipopolysaccharide-induced TNFalpha expression.

Publication types

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

MeSH terms

  • 14-3-3 Proteins / metabolism*
  • Adenosine / genetics
  • Animals
  • Arsenites / pharmacology
  • Binding Sites
  • Cell Line
  • Chlorocebus aethiops
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Enzyme Activation
  • Humans
  • Immediate-Early Proteins / genetics
  • Immediate-Early Proteins / metabolism*
  • Intracellular Signaling Peptides and Proteins
  • MAP Kinase Signaling System
  • Macrophages / metabolism
  • Mice
  • Mutation / genetics
  • Protein Binding
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • RNA Stability*
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism*
  • Regulatory Sequences, Ribonucleic Acid / genetics*
  • Serine / genetics
  • Serine / metabolism
  • Stress, Physiological
  • Tristetraprolin
  • Uridine / genetics
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • 14-3-3 Proteins
  • Arsenites
  • DNA-Binding Proteins
  • Immediate-Early Proteins
  • Intracellular Signaling Peptides and Proteins
  • RNA, Messenger
  • Regulatory Sequences, Ribonucleic Acid
  • Tristetraprolin
  • ZFP36 protein, human
  • Zfp36 protein, mouse
  • Serine
  • MAP-kinase-activated kinase 2
  • Protein Serine-Threonine Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Adenosine
  • arsenite
  • Uridine