Platelet-Derived Ectosomes Reduce NK Cell Function

J Immunol. 2016 Sep 1;197(5):1663-71. doi: 10.4049/jimmunol.1502658. Epub 2016 Jul 22.

Abstract

Platelet (PLT) transfusions are potentially life saving for individuals with low PLT numbers; however, previous work revealed that PLT transfusions are associated with increased infection risk. During storage, PLT intended for transfusion continuously shed ectosomes (Ecto) from their surface, which express immunomodulatory molecules like phosphatidylserine or TGF-β1. Recently, PLT-Ecto were shown to reduce proinflammatory cytokine release by macrophages and to favor the differentiation of naive T cells toward regulatory T cells. Whether PLT-Ecto modify NK cells remains unclear. We exposed purified NK cells and full PBMCs from healthy donors to PLT-Ecto. We found a reduced expression of several activating surface receptors (NKG2D, NKp30, and DNAM-1) and decreased NK cell function, as measured by CD107a expression and IFN-γ production. Pretreatment of PLT-Ecto with anti-TGF-β1 neutralizing Ab restored surface receptor expression and NK cell function. We further observed a TGF-β1-mediated upregulation of miR-183, which, in turn, reduced DAP12, an important protein for stabilization and downstream signaling of several activating NK cell receptors. Again, these effects could antagonized, in part, when PLT-Ecto were preincubated with anti-TGF-β1 Ab. Erythrocyte Ecto did not affect NK cells. Polymorphonuclear cell Ecto expressed MHC class I and inhibited NK cell function. In addition, they induced the secretion of TGF-β1 by NK cells, which participated in an auto/paracrine manner in the suppressive activity of polymorphonuclear cell-derived Ecto. In sum, our study showed that PLT-Ecto could inhibit NK cell effector function in a TGF-β1-dependent manner, suggesting that recipients of PLT transfusions may experience reduced NK cell function.

MeSH terms

  • Adaptor Proteins, Signal Transducing / drug effects
  • Adaptor Proteins, Signal Transducing / genetics
  • Antigens, Differentiation, T-Lymphocyte / genetics
  • Blood Platelets / chemistry*
  • Blood Platelets / physiology
  • Cell-Derived Microparticles / immunology*
  • Cell-Derived Microparticles / metabolism*
  • GPI-Linked Proteins / genetics
  • Genes, MHC Class I
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics
  • Interferon-gamma / biosynthesis
  • Interferon-gamma / metabolism
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism*
  • Lysosomal-Associated Membrane Protein 1 / genetics
  • Membrane Proteins / drug effects
  • Membrane Proteins / genetics
  • MicroRNAs / drug effects
  • MicroRNAs / genetics
  • Monocytes / drug effects
  • Natural Cytotoxicity Triggering Receptor 3 / genetics
  • Neutrophils / chemistry
  • Phosphatidylserines / genetics
  • Receptors, Natural Killer Cell / genetics
  • Receptors, Natural Killer Cell / metabolism
  • Transforming Growth Factor beta / immunology*
  • Transforming Growth Factor beta / metabolism
  • Transforming Growth Factor beta / pharmacology

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, Differentiation, T-Lymphocyte
  • CD226 antigen
  • GPI-Linked Proteins
  • Intercellular Signaling Peptides and Proteins
  • Lysosomal-Associated Membrane Protein 1
  • MIRN183 microRNA, human
  • Membrane Proteins
  • MicroRNAs
  • NCR3 protein, human
  • Natural Cytotoxicity Triggering Receptor 3
  • Phosphatidylserines
  • Receptors, Natural Killer Cell
  • TYROBP protein, human
  • Transforming Growth Factor beta
  • ULBP2 protein, human
  • Interferon-gamma