Rapamycin has suppressive and stimulatory effects on human plasmacytoid dendritic cell functions

Clin Exp Immunol. 2013 Dec;174(3):389-401. doi: 10.1111/cei.12191.

Abstract

Plasmacytoid dendritic cells (PDC) are involved in innate immunity by interferon (IFN)-α production, and in adaptive immunity by stimulating T cells and inducing generation of regulatory T cells (Treg ). In this study we studied the effects of mammalian target of rapamycin (mTOR) inhibition by rapamycin, a commonly used immunosuppressive and anti-cancer drug, on innate and adaptive immune functions of human PDC. A clinically relevant concentration of rapamycin inhibited Toll-like receptor (TLR)-7-induced IFN-α secretion potently (-64%) but TLR-9-induced IFN-α secretion only slightly (-20%), while the same concentration suppressed proinflammatory cytokine production by TLR-7-activated and TLR-9-activated PDC with similar efficacy. Rapamycin inhibited the ability of both TLR-7-activated and TLR-9-activated PDC to stimulate production of IFN-γ and interleukin (IL)-10 by allogeneic T cells. Surprisingly, mTOR-inhibition enhanced the capacity of TLR-7-activated PDC to stimulate naive and memory T helper cell proliferation, which was caused by rapamycin-induced up-regulation of CD80 expression on PDC. Finally, rapamycin treatment of TLR-7-activated PDC enhanced their capacity to induce CD4(+) forkhead box protein 3 (FoxP3)(+) regulatory T cells, but did not affect the generation of suppressive CD8(+) CD38(+) lymphocyte activation gene (LAG)-3(+) Treg . In general, rapamycin inhibits innate and adaptive immune functions of TLR-stimulated human PDC, but enhances the ability of TLR-7-stimulated PDC to stimulate CD4(+) T cell proliferation and induce CD4(+) FoxP3(+) regulatory T cell generation.

Keywords: IFN-α; Toll-like receptor; mTOR.

MeSH terms

  • Adaptive Immunity / drug effects
  • Antigens, CD / biosynthesis
  • B7-1 Antigen / biosynthesis
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Cytokines / biosynthesis
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Humans
  • Immunity, Innate / drug effects
  • Immunologic Memory / drug effects
  • Immunosuppressive Agents / pharmacology*
  • Interferon-alpha / metabolism
  • Interferon-gamma / metabolism
  • Interleukin-10 / biosynthesis
  • Interleukin-10 / metabolism
  • Lymphocyte Activation / immunology
  • Lymphocyte Activation Gene 3 Protein
  • Sirolimus / pharmacology*
  • T-Lymphocytes, Helper-Inducer / immunology*
  • T-Lymphocytes, Regulatory / immunology*
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • Toll-Like Receptor 7 / antagonists & inhibitors
  • Toll-Like Receptor 7 / metabolism
  • Toll-Like Receptor 9 / antagonists & inhibitors
  • Toll-Like Receptor 9 / metabolism

Substances

  • Antigens, CD
  • B7-1 Antigen
  • Cytokines
  • Immunosuppressive Agents
  • Interferon-alpha
  • TLR7 protein, human
  • TLR9 protein, human
  • Toll-Like Receptor 7
  • Toll-Like Receptor 9
  • Interleukin-10
  • Interferon-gamma
  • MTOR protein, human
  • TOR Serine-Threonine Kinases
  • Sirolimus
  • Lymphocyte Activation Gene 3 Protein
  • Lag3 protein, human