Cytokine-Induced Memory-Like Differentiation Enhances Unlicensed Natural Killer Cell Antileukemia and FcγRIIIa-Triggered Responses

Biol Blood Marrow Transplant. 2017 Mar;23(3):398-404. doi: 10.1016/j.bbmt.2016.11.018. Epub 2016 Nov 25.

Abstract

Cytokine-induced memory-like natural killer (NK) cells differentiate after short-term preactivation with IL-12, IL-15, and IL-18 and display enhanced effector function in response to cytokines or tumor targets for weeks after the initial preactivation. Conventional NK cell function depends on a licensing signal, classically delivered by an inhibitory receptor engaging its cognate MHC class I ligand. How licensing status integrates with cytokine-induced memory-like NK cell responses is unknown. We investigated this interaction using killer cell immunoglobulin-like receptor- and HLA-genotyped primary human NK cells. Memory-like differentiation resulted in enhanced IFN-γ production triggered by leukemia targets or FcγRIIIa ligation within licensed NK cells, which exhibited the highest functionality of the NK cell subsets interrogated. IFN-γ production by unlicensed memory-like NK cells was also enhanced to a level comparable with that of licensed control NK cells. Mechanistically, differences in responses to FcγRIIIa-based triggering were not explained by alterations in key signaling intermediates, indicating that the underlying biology of memory-like NK cells is distinct from that of adaptive NK cells in human cytomegalovirus-positive individuals. Additionally, memory-like NK cells responded robustly to cytokine receptor restimulation with no impact of licensing status. These results demonstrate that both licensed and unlicensed memory-like NK cell populations have enhanced functionality, which may be translated to improve leukemia immunotherapy.

Keywords: Adoptive immunotherapy; Cytokines; NK cell; NK cell education; NK cell memory.

MeSH terms

  • Cell Differentiation / drug effects
  • Cytokines / pharmacology*
  • HLA Antigens
  • Humans
  • Immunologic Memory / drug effects*
  • Immunotherapy, Adoptive
  • Interferon-gamma / biosynthesis
  • Killer Cells, Natural / immunology*
  • Leukemia / therapy
  • Lymphocyte Activation
  • Receptors, IgG / immunology*
  • Receptors, KIR / immunology*

Substances

  • Cytokines
  • FCGR3A protein, human
  • HLA Antigens
  • Receptors, IgG
  • Receptors, KIR
  • Interferon-gamma