PD-1 mediates functional exhaustion of activated NK cells in patients with Kaposi sarcoma

Oncotarget. 2016 Nov 8;7(45):72961-72977. doi: 10.18632/oncotarget.12150.

Abstract

Programmed Death-1 (PD-1), an inhibitory receptor expressed by activated lymphocytes, is involved in regulating T- and B-cell responses. PD-1 and its ligands are exploited by a variety of cancers to facilitate tumor escape through PD-1-mediated functional exhaustion of effector T cells. Here, we report that PD-1 is upregulated on Natural Killer (NK) cells from patients with Kaposi sarcoma (KS). PD-1 was expressed in a sub-population of activated, mature CD56dimCD16pos NK cells with otherwise normal expression of NK surface receptors. PD-1pos NK cells from KS patients were hyporesponsive ex vivo following direct triggering of NKp30, NKp46 or CD16 activating receptors, or short stimulation with NK cell targets. PD-1pos NK cells failed to degranulate and release IFNγ, but exogenous IL-2 or IL-15 restored this defect. That PD-1 contributed to NK cell functional impairment and was not simply a marker of dysfunctional NK cells was confirmed in PD-1-transduced NKL cells. In vitro, PD-1 was induced at the surface of healthy control NK cells upon prolonged contact with cells expressing activating ligands, i.e. a condition mimicking persistent stimulation by tumor cells. Thus, PD-1 appears to plays a critical role in mediating NK cell exhaustion. The existence of this negative checkpoint fine-tuning NK activation highlights the possibility that manipulation of the PD-1 pathway may be a strategy for circumventing tumor escape not only from the T cell-, but also the NK-cell mediated immune surveillance.

Keywords: Kaposi sarcoma; NK cells; PD-1; immune checkpoint; tumor escape.

MeSH terms

  • Biomarkers
  • Case-Control Studies
  • Coinfection
  • Cytokines / metabolism
  • Flow Cytometry
  • Gene Expression
  • HIV Infections / complications
  • HIV Infections / virology
  • Hepatitis C / complications
  • Hepatitis C / virology
  • Herpesviridae Infections / complications
  • Herpesviridae Infections / virology
  • Herpesvirus 8, Human
  • Humans
  • Immunohistochemistry
  • Immunomodulation
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism*
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology*
  • Phenotype
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / metabolism*
  • Sarcoma, Kaposi / etiology*
  • Sarcoma, Kaposi / metabolism*
  • Sarcoma, Kaposi / pathology

Substances

  • Biomarkers
  • Cytokines
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor