miR-21 Modulates the Immunoregulatory Function of Bone Marrow Mesenchymal Stem Cells Through the PTEN/Akt/TGF-β1 Pathway

Stem Cells. 2015 Nov;33(11):3281-90. doi: 10.1002/stem.2081. Epub 2015 Jul 1.

Abstract

microRNAs (miRNAs) act as regulatory signals for maintaining stemness, self-renewal, and differentiation of mesenchymal stem cells (MSCs), but whether miRNAs modulate the immunoregulatory function of MSCs remains largely unknown. Here, we show that miR-21 negatively regulates the activity of immunoregulatory cytokine transforming growth factor-β1 (TGF-β1) in MSCs. Consistently, bone marrow MSCs (BMMSCs) from miR-21(-/-) mice show enhanced immunosuppressive function by more TGF-β1 secretion and induce more CD4(+) Foxp3(+) regulatory T cells compared with wild-type BMMSCs in vitro, which anti-TGF-β1 antibody abrogates. Mechanistically, miR-21 inhibits TGF-β1 expression by targeting phosphatase and tensin homolog deleted on chromosome 10 (PTEN) in BMMSCs. Downstream of PTEN, miR-21 promotes activation of Akt, and consequently increases activation of NF-κB pathway. Importantly, adoptive transfer of miR-21(-/-) BMMSCs into mice with experimental colitis more effectively ameliorates colonic inflammation in a TGF-β1-dependent manner. Thus, these findings indicate a previously uncovered mechanism of miR-21 control immunoregulatory function of BMMSCs through TGF-β1 inhibition.

Keywords: Immunoregulation; Mesenchymal stem cells; PTEN; Transforming growth factor-β1; miR-21.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Cells / metabolism
  • Cells, Cultured
  • Humans
  • Mesenchymal Stem Cells / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • MicroRNAs / physiology*
  • PTEN Phosphohydrolase / antagonists & inhibitors
  • PTEN Phosphohydrolase / biosynthesis*
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / biosynthesis*
  • Signal Transduction / physiology*
  • Transforming Growth Factor beta1 / antagonists & inhibitors
  • Transforming Growth Factor beta1 / biosynthesis*

Substances

  • MIRN21 microRNA, mouse
  • MicroRNAs
  • Transforming Growth Factor beta1
  • Proto-Oncogene Proteins c-akt
  • PTEN Phosphohydrolase
  • Pten protein, mouse