KIR downregulation by IL-12/15/18 unleashes human NK cells from KIR/HLA-I inhibition and enhances killing of tumor cells

Eur J Immunol. 2018 Feb;48(2):355-365. doi: 10.1002/eji.201747128. Epub 2017 Nov 29.

Abstract

To exploit autologous NK cells for cancer immunotherapy, it is highly relevant to circumvent killer cell immunoglobulin-like receptor (KIR)-mediated self-inhibition of human NK cells by HLA-I-expressing tumor cells. Here, we show that stimulation of NK cells with IL-12/15/18 for two days led to downregulation of surface expression of the inhibitory KIR2DL2/L3, KIR2DL1 and KIR3DL1 receptors on peripheral blood NK cells. Downregulation of KIR expression was attributed to decreased KIR mRNA levels which could be re-induced already 3 days after re-culture in IL-2. Reduced KIR2DL2/L3 expression on IL-12/15/18-activated NK cells resulted in less inhibition upon antibody-mediated KIR engagement and increased CD16-dependent cytotoxicity in redirected lysis assays. Most importantly, downregulated KIR2DL2/L3 expression enabled enhanced cytotoxicity of IL-12/15/18-stimulated NK cells against tumor cells expressing cognate HLA-I molecules. NK cells pre-activated with IL-12/15/18 were previously shown to exert potent anti-tumor activity and memory-like long-lived functionality, mediating remission in a subset of acute myeloid leukemia (AML) patients in a clinical trial. Our study reveals a novel mechanism of IL-12/15/18 in improving the cytotoxicity of NK cells by reducing their sensitivity to inhibition by self-HLA-I due to decreased KIR expression, highlighting the potency of IL-12/15/18-activated NK cells for anti-tumor immunotherapy protocols.

Keywords: Cancer immunotherapy; IL-12/15/18 activation; Killer cell immunoglobulin-like receptors (KIRs); NK cell receptors; NK cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibody-Dependent Cell Cytotoxicity
  • Cancer Vaccines / immunology*
  • Cell Line, Tumor
  • Down-Regulation
  • HLA Antigens / metabolism
  • Humans
  • Immunotherapy, Adoptive / methods*
  • Interleukin-12 / metabolism
  • Interleukin-15 / metabolism
  • Interleukin-18 / metabolism
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / transplantation
  • Leukemia, Myeloid, Acute / immunology
  • Leukemia, Myeloid, Acute / therapy*
  • Lymphocyte Activation
  • Mice
  • Receptors, KIR2DL2 / metabolism*
  • Receptors, KIR2DL3 / metabolism*
  • Receptors, KIR3DL1 / metabolism*

Substances

  • Cancer Vaccines
  • HLA Antigens
  • Interleukin-15
  • Interleukin-18
  • KIR2DL2 protein, human
  • KIR2DL3 protein, human
  • Receptors, KIR2DL2
  • Receptors, KIR2DL3
  • Receptors, KIR3DL1
  • Interleukin-12