Interleukin-1 primes human mesenchymal stem cells towards an anti-inflammatory and pro-trophic phenotype in vitro

Stem Cell Res Ther. 2017 Apr 17;8(1):79. doi: 10.1186/s13287-017-0531-4.

Abstract

Background: Inflammation is a key contributor to central nervous system (CNS) injury such as stroke, and is a major target for therapeutic intervention. Effective treatments for CNS injuries are limited and applicable to only a minority of patients. Stem cell-based therapies are increasingly considered for the treatment of CNS disease, because they can be used as in-situ regulators of inflammation, and improve tissue repair and recovery. One promising option is the use of bone marrow-derived mesenchymal stem cells (MSCs), which can secrete anti-inflammatory and trophic factors, can migrate towards inflamed and injured sites or can be implanted locally. Here we tested the hypothesis that pre-treatment with inflammatory cytokines can prime MSCs towards an anti-inflammatory and pro-trophic phenotype in vitro.

Methods: Human MSCs from three different donors were cultured in vitro and treated with inflammatory mediators as follows: interleukin (IL)-1α, IL-1β, tumour necrosis factor alpha (TNF-α) or interferon-γ. After 24 h of treatment, cell supernatants were analysed by ELISA for expression of granulocyte-colony stimulating factor (G-CSF), IL-10, brain-derived neurotrophic factor (BDNF), nerve growth factor (NGF), IL-1 receptor antagonist (IL-1Ra) and vascular endothelial growth factor (VEGF). To confirm the anti-inflammatory potential of MSCs, immortalised mouse microglial BV2 cells were treated with bacterial lipopolysaccharide (LPS) and exposed to conditioned media (CM) of naïve or IL-1-primed MSCs, and levels of secreted microglial-derived inflammatory mediators including TNF-α, IL-10, G-CSF and IL-6 were measured by ELISA.

Results: Unstimulated MSCs constitutively expressed anti-inflammatory cytokines and trophic factors (IL-10, VEGF, BDNF, G-CSF, NGF and IL-1Ra). MSCs primed with IL-1α or IL-1β showed increased secretion of G-CSF, which was blocked by IL-1Ra. Furthermore, LPS-treated BV2 cells secreted less inflammatory and apoptotic markers, and showed increased secretion of the anti-inflammatory IL-10 in response to treatment with CM of IL-1-primed MSCs compared with CM of unprimed MSCs.

Conclusions: Our results demonstrate that priming MSCs with IL-1 increases expression of trophic factor G-CSF through an IL-1 receptor type 1 (IL-1R1) mechanism, and induces a reduction in the secretion of inflammatory mediators in LPS-activated microglial cells. The results therefore support the potential use of preconditioning treatments of stem cells in future therapies.

Keywords: Bone marrow-derived stromal cells; Cytokines; Human mesenchymal stem cells; Interleukin-1; Priming; Stroke.

MeSH terms

  • Adult
  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Biomarkers / metabolism
  • Culture Media, Conditioned / pharmacology
  • Female
  • Granulocyte Colony-Stimulating Factor / pharmacology
  • Humans
  • Interleukin-1alpha / pharmacology*
  • Interleukin-1beta / pharmacology*
  • Interleukin-6 / metabolism
  • Lipopolysaccharides / pharmacology
  • Male
  • Mesenchymal Stem Cells / cytology*
  • Mesenchymal Stem Cells / drug effects
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Microglia / cytology
  • Microglia / drug effects
  • Nerve Growth Factors / pharmacology
  • Phenotype
  • Tumor Necrosis Factor-alpha / metabolism
  • Young Adult

Substances

  • Anti-Inflammatory Agents
  • Biomarkers
  • Culture Media, Conditioned
  • Interleukin-1alpha
  • Interleukin-1beta
  • Interleukin-6
  • Lipopolysaccharides
  • Nerve Growth Factors
  • Tumor Necrosis Factor-alpha
  • Granulocyte Colony-Stimulating Factor