Preconditioning of murine mesenchymal stem cells synergistically enhanced immunomodulation and osteogenesis

Stem Cell Res Ther. 2017 Dec 6;8(1):277. doi: 10.1186/s13287-017-0730-z.

Abstract

Background: Mesenchymal stem cells (MSCs) are capable of immunomodulation and tissue regeneration, highlighting their potential translational application for treating inflammatory bone disorders. MSC-mediated immunomodulation is regulated by proinflammatory cytokines and pathogen-associated molecular patterns such as lipopolysaccharide (LPS). Previous studies showed that MSCs exposed to interferon gamma (IFN-γ) and the proinflammatory cytokine tumor necrosis factor alpha (TNF-α) synergistically suppressed T-cell activation.

Methods: In the current study, we developed a novel preconditioning strategy for MSCs using LPS plus TNF-α to optimize the immunomodulating ability of MSCs on macrophage polarization.

Results: Preconditioned MSCs enhanced anti-inflammatory M2 macrophage marker expression (Arginase 1 and CD206) and decreased inflammatory M1 macrophage marker (TNF-α/IL-1Ra) expression using an in-vitro coculture model. Immunomodulation of MSCs on macrophages was significantly increased compared to the combination of IFN-γ plus TNF-α or single treatment controls. Increased osteogenic differentiation including alkaline phosphate activity and matrix mineralization was only observed in the LPS plus TNF-α preconditioned MSCs. Mechanistic studies showed that increased prostaglandin E2 (PGE2) production was associated with enhanced Arginase 1 expression. Selective cyclooxygenase-2 inhibition by Celecoxib decreased PGE2 production and Arginase 1 expression in cocultured macrophages.

Conclusions: The novel preconditioned MSCs have increased immunomodulation and bone regeneration potential and could be applied to the treatment of inflammatory bone disorders including periprosthetic osteolysis, fracture healing/nonunions, and osteonecrosis.

Keywords: Immunomodulation; Macrophage polarization; Mesenchymal stem cells; Osteogenesis; Prostaglandin E2.

MeSH terms

  • Alkaline Phosphatase / genetics
  • Alkaline Phosphatase / immunology
  • Animals
  • Arginase / genetics
  • Arginase / immunology
  • Celecoxib / pharmacology
  • Cell Differentiation / drug effects
  • Coculture Techniques
  • Cyclooxygenase 2 / genetics
  • Cyclooxygenase 2 / immunology
  • Dinoprostone / biosynthesis
  • Dinoprostone / immunology
  • Gene Expression
  • Immunomodulation / drug effects*
  • Interferon-gamma / pharmacology
  • Interleukin 1 Receptor Antagonist Protein / genetics
  • Interleukin 1 Receptor Antagonist Protein / immunology
  • Lectins, C-Type / genetics
  • Lectins, C-Type / immunology
  • Lipopolysaccharides / pharmacology*
  • Macrophages / cytology
  • Macrophages / drug effects*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mannose Receptor
  • Mannose-Binding Lectins / genetics
  • Mannose-Binding Lectins / immunology
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / drug effects*
  • Mesenchymal Stem Cells / immunology
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Osteogenesis / drug effects*
  • Osteogenesis / genetics
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / immunology
  • Tumor Necrosis Factor-alpha / pharmacology*

Substances

  • Il1rn protein, mouse
  • Interleukin 1 Receptor Antagonist Protein
  • Lectins, C-Type
  • Lipopolysaccharides
  • Mannose Receptor
  • Mannose-Binding Lectins
  • Receptors, Cell Surface
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • Ptgs2 protein, mouse
  • Cyclooxygenase 2
  • Alkaline Phosphatase
  • Arg1 protein, mouse
  • Arginase
  • Celecoxib
  • Dinoprostone