NFAT1 and JunB cooperatively regulate IL-31 gene expression in CD4+ T cells in health and disease

J Immunol. 2015 Feb 15;194(4):1963-74. doi: 10.4049/jimmunol.1401862. Epub 2015 Jan 16.

Abstract

IL-31 is a key mediator of itching in atopic dermatitis (AD) and is preferentially produced by activated CD4(+) T cells and Th2 cells. Although pathophysiological functions of IL-31 have been suggested in diverse immune disorders, the molecular events underlying IL-31 gene regulation are still unclear. In this study we identified the transcription start site and functional promoter involved in IL-31 gene regulation in mouse CD4(+) T cells. TCR stimulation-dependent IL-31 expression was found to be closely linked with in vivo binding of NFAT1 and JunB to the IL-31 promoter. Although NFAT1 alone enhanced IL-31 promoter activity, it was further enhanced in the presence of JunB. Conversely, knockdown of either NFAT1 or JunB resulted in reduced IL-31 expression. NFAT1-deficient CD4(+) T cells showed a significant defect in IL-31 expression compared with wild-type CD4(+) T cells. In agreement with these findings, mice subjected to atopic conditions showed much higher levels of IL-31, which were closely correlated with a significant increase in the number of infiltrated NFAT1(+)CD4(+) T cells into the AD ears. Amelioration of AD progression by cyclosporin A treatment was well correlated with downregulation of IL-31 expressions in CD4(+) T cells and total ear residual cells. In summary, our results suggest a functional cooperation between NFAT1 and JunB in mediating IL-31 gene expression in CD4(+) T cells and indicate that interference with this interaction or their activity has the potential of reducing IL-31-mediated AD symptoms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / immunology*
  • Chromatin Immunoprecipitation
  • Dermatitis, Atopic / genetics
  • Dermatitis, Atopic / immunology*
  • Dermatitis, Atopic / metabolism
  • Disease Models, Animal
  • Female
  • Gene Expression Regulation / immunology*
  • Immunohistochemistry
  • Interleukins / biosynthesis*
  • Interleukins / genetics
  • Interleukins / immunology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mutagenesis, Site-Directed
  • NFATC Transcription Factors / genetics
  • NFATC Transcription Factors / immunology*
  • RNA, Small Interfering
  • Real-Time Polymerase Chain Reaction
  • Transcription Factors / genetics
  • Transcription Factors / immunology*
  • Transcriptome
  • Transfection

Substances

  • Interleukins
  • JunB protein, mouse
  • NFATC Transcription Factors
  • Nfatc2 protein, mouse
  • RNA, Small Interfering
  • Transcription Factors
  • interleukin-31, mouse