The AP-1 Transcription Factor c-Jun Promotes Arthritis by Regulating Cyclooxygenase-2 and Arginase-1 Expression in Macrophages

J Immunol. 2017 May 1;198(9):3605-3614. doi: 10.4049/jimmunol.1601330. Epub 2017 Mar 15.

Abstract

Activation of proinflammatory macrophages is associated with the inflammatory state of rheumatoid arthritis. Their polarization and activation are controlled by transcription factors such as NF-κB and the AP-1 transcription factor member c-Fos. Surprisingly, little is known about the role of the AP-1 transcription factor c-Jun in macrophage activation. In this study, we show that mRNA and protein levels of c-Jun are increased in macrophages following pro- or anti-inflammatory stimulations. Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway enrichment cluster analyses of microarray data using wild-type and c-Jun-deleted macrophages highlight the central function of c-Jun in macrophages, in particular for immune responses, IL production, and hypoxia pathways. Mice deficient for c-Jun in macrophages show an amelioration of inflammation and bone destruction in the serum-induced arthritis model. In vivo and in vitro gene profiling, together with chromatin immunoprecipitation analysis of macrophages, revealed direct activation of the proinflammatory factor cyclooxygenase-2 and indirect inhibition of the anti-inflammatory factor arginase-1 by c-Jun. Thus, c-Jun regulates the activation state of macrophages and promotes arthritis via differentially regulating cyclooxygenase-2 and arginase-1 levels.

MeSH terms

  • Animals
  • Arginase / immunology
  • Arginase / metabolism*
  • Arthritis / immunology*
  • Cells, Cultured
  • Cluster Analysis
  • Cyclooxygenase 2 / immunology
  • Cyclooxygenase 2 / metabolism*
  • Female
  • Inflammation / immunology*
  • Lipopolysaccharides / immunology
  • Macrophages / immunology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NF-kappa B / metabolism
  • Proto-Oncogene Proteins c-jun / genetics
  • Proto-Oncogene Proteins c-jun / metabolism*
  • Transcription Factor AP-1 / immunology
  • Transcription Factor AP-1 / metabolism*
  • Up-Regulation

Substances

  • Lipopolysaccharides
  • NF-kappa B
  • Proto-Oncogene Proteins c-jun
  • Transcription Factor AP-1
  • Cyclooxygenase 2
  • ARG1 protein, human
  • Arginase