Direct RIG-I activation in human NK cells induces TRAIL-dependent cytotoxicity toward autologous melanoma cells

Int J Cancer. 2019 Apr 1;144(7):1645-1656. doi: 10.1002/ijc.31874. Epub 2019 Jan 9.

Abstract

Activation of the innate immune receptor retinoic acid-inducible gene I (RIG-I) by its specific ligand 5'-triphosphate RNA (3pRNA) triggers anti-tumor immunity, which is dependent on natural killer (NK) cell activation and cytokine induction. However, to date, RIG-I expression and the functional consequences of RIG-I activation in NK cells have not been examined. Here, we show for the first time the expression of RIG-I in human NK cells and their activation upon RIG-I ligand (3pRNA) transfection. 3pRNA-activated NK cells killed melanoma cells more efficiently than NK cells activated by type I interferon. Stimulation of RIG-I in NK cells specifically increased the surface expression of membrane-bound TNF-related apoptosis-inducing ligand (TRAIL) on NK cells, while activated NK cell receptors were not affected. RIG-I-induced membrane-bound TRAIL initiated death-receptor-pathway-mediated apoptosis not only in allogeneic but also in autologous human leukocyte antigen (HLA) class I-positive and HLA class I-negative melanoma cells. These results identify the direct activation of RIG-I in NK cells as a novel mechanism for how RIG-I can trigger enhanced NK cell killing of tumor cells, underscoring the potential of RIG-I activation for tumor immunotherapy.

Keywords: RIG-I; TRAIL; innate immunity; melanoma; natural killer (NK) cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis
  • Coculture Techniques
  • Cytotoxicity, Immunologic
  • DEAD Box Protein 58 / metabolism*
  • Humans
  • Killer Cells, Natural / cytology*
  • Killer Cells, Natural / immunology
  • Ligands
  • Lysosomal-Associated Membrane Protein 1 / metabolism
  • Melanoma / immunology*
  • Melanoma / therapy*
  • RNA / genetics
  • RNA / metabolism*
  • Receptors, Immunologic
  • TNF-Related Apoptosis-Inducing Ligand / metabolism*
  • Transfection
  • Transplantation, Autologous
  • Tumor Cells, Cultured

Substances

  • Ligands
  • Lysosomal-Associated Membrane Protein 1
  • Receptors, Immunologic
  • TNF-Related Apoptosis-Inducing Ligand
  • TNFSF10 protein, human
  • RNA
  • RIGI protein, human
  • DEAD Box Protein 58