TGF-β-inducible microRNA-183 silences tumor-associated natural killer cells

Proc Natl Acad Sci U S A. 2014 Mar 18;111(11):4203-8. doi: 10.1073/pnas.1319269111. Epub 2014 Feb 28.

Abstract

Transforming growth factor β1 (TGF-β), enriched in the tumor microenvironment and broadly immunosuppressive, inhibits natural killer (NK) cell function by yet-unknown mechanisms. Here we show that TGF-β-treated human NK cells exhibit reduced tumor cytolysis and abrogated perforin polarization to the immune synapse. This result was accompanied by loss of surface expression of activating killer Ig-like receptor 2DS4 and NKp44, despite intact cytoplasmic stores of these receptors. Instead, TGF-β depleted DNAX activating protein 12 kDa (DAP12), which is critical for surface NK receptor stabilization and downstream signal transduction. Mechanistic analysis revealed that TGF-β induced microRNA (miR)-183 to repress DAP12 transcription/translation. This pathway was confirmed with luciferase reporter constructs bearing the DAP12 3' untranslated region as well as in human NK cells by use of sense and antisense miR-183. Moreover, we documented reduced DAP12 expression in tumor-associated NK cells in lung cancer patients, illustrating this pathway to be consistently perturbed in the human tumor microenvironment.

Keywords: immune suppression; non-small cell lung cancer; posttranscriptional silencing.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / antagonists & inhibitors*
  • Adaptor Proteins, Signal Transducing / metabolism
  • Flow Cytometry
  • Humans
  • Immunoblotting
  • Immunohistochemistry
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Luciferases
  • Membrane Proteins / antagonists & inhibitors*
  • Membrane Proteins / metabolism
  • MicroRNAs / metabolism*
  • Microscopy, Fluorescence
  • Neoplasms / immunology*
  • Receptors, Natural Killer Cell / antagonists & inhibitors*
  • Receptors, Natural Killer Cell / metabolism
  • Signal Transduction / immunology
  • Transforming Growth Factor beta / immunology*
  • Transforming Growth Factor beta / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • MIRN183 microRNA, human
  • Membrane Proteins
  • MicroRNAs
  • Receptors, Natural Killer Cell
  • TYROBP protein, human
  • Transforming Growth Factor beta
  • Luciferases