Ectosomes released by platelets induce differentiation of CD4+T cells into T regulatory cells

Thromb Haemost. 2014 Dec;112(6):1219-29. doi: 10.1160/TH14-03-0281. Epub 2014 Sep 11.

Abstract

Accumulating evidence suggests an immune-modulatory role for platelets (PLT) and PLT-derived microvesicles. In particular, ectosomes, i.e. vesicles budding from PLT surface, have been shown to exert immunosuppressive activities on phagocytes. Here we investigated the effects mediated by PLT-derived ectosomes (PLT-Ecto) on CD4+ T cells. Exposure of activated CD4+ T cells to PLT-Ecto decreased their release of IFNγ, TNFα and IL-6, and increased the production of TGF-β1. Concomitantly, PLT-Ecto-exposed CD4+ T cells displayed increased frequencies of CD25high Foxp3+ cells. These phenomena were dose-dependent and PLT-Ecto specific, since they were not observed in the presence of polymorphonuclear- and erythrocyte-derived ectosomes. Analysis of specific T cell subsets revealed that PLT-Ecto induced differentiation of naïve T cells into Foxp3+ cells, but had no effect on pre-differentiated Foxp3+ regulatory T cells (Tregs). Importantly, PLT-Ecto-induced Foxp3+ cells were as effective as peripheral blood Tregs in suppressing CD8+ T cell proliferation. PLT-Ecto-mediated effects were partly dependent on PLT-derived TGF-β1, as they were to some extent inhibited by PLT-Ecto pretreatment with TGF-β1-neutralising antibodies. Interestingly, ectosome-derived TGF-β1 levels correlated with Foxp3+ T cell frequencies in blood of healthy donors. In conclusion, PLT-Ecto induce differentiation of CD4+ T cells towards functional Tregs. This may represent a mechanism by which PLT-Ecto enhance peripheral tolerance.

Keywords: Microparticles; T cell differentiation; ectosomes; extracellular vesicles; platelet immunology.

MeSH terms

  • Blood Platelets / immunology
  • Blood Platelets / metabolism*
  • CD8-Positive T-Lymphocytes
  • Cell Differentiation*
  • Cell Proliferation
  • Cell-Derived Microparticles / immunology
  • Cell-Derived Microparticles / metabolism*
  • Cells, Cultured
  • Coculture Techniques
  • Forkhead Transcription Factors / metabolism
  • Humans
  • Immune Tolerance
  • Interferon-gamma / metabolism
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Interleukin-6 / metabolism
  • Paracrine Communication*
  • Signal Transduction
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism*
  • Time Factors
  • Transforming Growth Factor beta1 / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • IFNG protein, human
  • IL2RA protein, human
  • IL6 protein, human
  • Interleukin-2 Receptor alpha Subunit
  • Interleukin-6
  • TGFB1 protein, human
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma