Transcription of Tnfaip3 is regulated by NF-κB and p38 via C/EBPβ in activated macrophages

PLoS One. 2013 Sep 2;8(9):e73153. doi: 10.1371/journal.pone.0073153. eCollection 2013.

Abstract

Macrophages play a pivotal role in the immune system through recognition and elimination of microbial pathogens. Toll-like receptors (TLRs) on macrophages interact with microbial substances and initiate signal transduction through intracellular adapters. TLR4, which recognizes the lipopolysaccharides (LPS) on Gram-positive and Gram-negative bacteria, triggers downstream signaling mediators and eventually activates IκB kinase (IKK) complex and mitogen-activated protein kinases (MAPKs) such as p38. Previous reports revealed that, in addition to NF-κB, a core transcription factor of the innate immune response, the induction of some LPS-induced genes in macrophages required another transcription factor whose activity depends on p38. However, these additional transcription factors remain to be identified. In order to identify p38-activated transcription factors that cooperate with NF-κB in response to LPS stimulation, microarrays were used to identify genes regulated by both NF-κB and p38 using wild-type, IKK-depleted, and p38 inhibitor-treated mouse bone marrow-derived macrophages (BMDMs). In silico analysis of transcription factor binding sites was used to predict the potential synergistic transcription factors from the co-expressed genes. Among these genes, NF-κB and C/EBPβ, a p38 downstream transcription factor, were predicted to co-regulate genes in LPS-stimulated BMDMs. Based on the subsequent results of a chromatin immunoprecipitation assay and TNFAIP3 expression in C/EBPβ-ablated macrophages, we demonstrated that Tnfaip3 is regulated by both NF-κB and p38-dependent C/EBPβ. These results identify a novel regulatory mechanism in TLR4-mediated innate immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Cells / cytology
  • CCAAT-Enhancer-Binding Protein-beta / metabolism*
  • Cell Line
  • Chromatin Immunoprecipitation
  • Cysteine Endopeptidases / genetics*
  • DNA-Binding Proteins / genetics
  • Gene Expression Regulation / drug effects
  • Intracellular Signaling Peptides and Proteins / genetics*
  • Lipopolysaccharides / pharmacology
  • Macrophage Activation* / drug effects
  • Macrophages / cytology
  • Macrophages / drug effects
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Mice
  • Promoter Regions, Genetic / genetics
  • Signal Transduction / drug effects
  • Toll-Like Receptor 4 / metabolism
  • Transcription Factor RelA / metabolism*
  • Transcription, Genetic* / drug effects
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Ubiquitin-Protein Ligases / genetics
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • CCAAT-Enhancer-Binding Protein-beta
  • DNA-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • Lipopolysaccharides
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Transcription Factor RelA
  • Ubiquitin-Protein Ligases
  • p38 Mitogen-Activated Protein Kinases
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Cysteine Endopeptidases
  • Tnfaip3 protein, mouse

Grants and funding

This research was supported in part by grants from the Department of Health of Taiwan (Grant No. DOH98-TD-G-111-014) and the National Health Research Institutes of Taiwan (Grant No. NHRI-EX102-10257SI). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.