STAT3 promotes CD1d-mediated lipid antigen presentation by regulating a critical gene in glycosphingolipid biosynthesis

Immunology. 2015 Nov;146(3):444-55. doi: 10.1111/imm.12521. Epub 2015 Sep 21.

Abstract

Cytokines that regulate the immune response signal through the Janus kinase / signal transducer and activation of transcription (JAK/STAT) pathway, but whether this pathway can regulate CD1d-mediated lipid antigen presentation to natural killer T (NKT) cells is unknown. Here, we found that STAT3 promotes antigen presentation by CD1d. Antigen-presenting cells (APCs) in which STAT3 expression was inhibited exhibited markedly reduced endogenous lipid antigen presentation to NKT cells without an impact on exogenous lipid antigen presentation by CD1d. Consistent with this observation, in APCs where STAT3 was knocked down, dramatically decreased levels of UDP glucose ceramide glucosyltransferase (UGCG), an enzyme involved in the first step of glycosphingolipid biosynthesis, were observed. Impaired lipid antigen presentation was reversed by ectopic expression of UGCG in STAT3-silenced CD1d(+) APCs. Hence, by controlling a fundamental step in CD1d-mediated lipid antigen presentation, STAT3 signalling promotes innate immune responses driven by CD1d.

Keywords: Janus kinase / signal transducer and activation of transcription; antigen presentation; signal transduction.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antigen Presentation
  • Antigen-Presenting Cells / immunology
  • Antigen-Presenting Cells / metabolism
  • Antigens, CD1d / metabolism*
  • Cell Line
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Gene Expression Regulation
  • Gene Knockdown Techniques
  • Glucosyltransferases / metabolism
  • Glycosphingolipids / biosynthesis*
  • HEK293 Cells
  • Histocompatibility Antigens Class II / metabolism
  • Humans
  • Immunity, Innate
  • Lipids / immunology*
  • Mice
  • Natural Killer T-Cells / immunology
  • Natural Killer T-Cells / metabolism
  • STAT3 Transcription Factor / antagonists & inhibitors
  • STAT3 Transcription Factor / genetics
  • STAT3 Transcription Factor / immunology*
  • Signal Transduction / immunology

Substances

  • Antigens, CD1d
  • CD1D protein, human
  • CD1d antigen, mouse
  • Glycosphingolipids
  • Histocompatibility Antigens Class II
  • Lipids
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Glucosyltransferases
  • ceramide glucosyltransferase