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PMID: 16508014 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, and binding to adenine/uridine-rich element.

Molecular and cellular biology ·Vol. 26 ·No. 6 ·2006-03-00 ·Pages 2399-407

Hitti E, Iakovleva T, Brook M, Deppenmeier S, Gruber AD, Radzioch D, Clark AR, Blackshear PJ, Kotlyarov A, Gaestel M

Abstract

The mitogen-activated protein kinase (MAPK) p38/MAPK-activated protein kinase 2 (MK2) signaling pathway plays an important role in the posttranscriptional regulation of tumor necrosis factor (TNF), which is dependent on the adenine/uridine-rich element (ARE) in the 3' untranslated region of TNF mRNA. After lipopolysaccharide (LPS) stimulation, MK2-deficient macrophages show a 90% reduction in TNF production compared to the wild type. Tristetraprolin (TTP), a protein induced by LPS, binds ARE and destabilizes TNF mRNA. Accordingly, macrophages lacking TTP produce large amounts of TNF. Here, we generated MK2/TTP double knockout mice and show that, after LPS stimulation, bone marrow-derived macrophages produce TNF mRNA and protein levels comparable to those of TTP knockout cells, indicating that in the regulation of TNF biosynthesis TTP is genetically downstream of MK2. In addition, we show that MK2 is essential for the stabilization of TTP mRNA, and phosphorylation by MK2 leads to increased TTP protein stability but reduced ARE affinity. These data suggest that MK2 inhibits the mRNA destabilizing activity of TTP and, in parallel, codegradation of TTP together, with the target mRNA resulting in increased cellular levels of TTP.

MeSH Terms
3' Untranslated Regions Abnormalities, Multiple/genetics,pathology Adenine/metabolism Animals Cells, Cultured Down-Regulation Intracellular Signaling Peptides and Proteins Macrophages/metabolism,pathology Mice Mice, Mutant Strains Phosphorylation Protein Biosynthesis Protein Kinases/genetics,metabolism Protein Serine-Threonine Kinases RNA Processing, Post-Transcriptional RNA Stability RNA, Messenger/genetics,metabolism Tristetraprolin/genetics,metabolism Tumor Necrosis Factor-alpha/genetics,metabolism Uridine/metabolism p38 Mitogen-Activated Protein Kinases/metabolism
Chemicals
3' Untranslated Regions Intracellular Signaling Peptides and Proteins RNA, Messenger Tristetraprolin Tumor Necrosis Factor-alpha Zfp36 protein, mouse Protein Kinases MAP-kinase-activated kinase 2 Protein Serine-Threonine Kinases p38 Mitogen-Activated Protein Kinases Adenine Uridine
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Hitti Edward
Medical School Hannover, Institute of Biochemistry, Carl-Neuberg-Str. 1, D-30625 Hannover, Germany.
Iakovleva Tatiana
Brook Matthew
Deppenmeier Stefanie
Gruber Achim D
Radzioch Danuta
Clark Andrew R
Blackshear Perry J
Kotlyarov Alexey
Gaestel Matthias
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Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2006-03-00
Pages
2399-407
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1430282
Subset
IM
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