IFN-γ and TNF-α synergistically induce mesenchymal stem cell impairment and tumorigenesis via NFκB signaling

Stem Cells. 2013 Jul;31(7):1383-95. doi: 10.1002/stem.1388.

Abstract

An inflammatory microenvironment may cause organ degenerative diseases and malignant tumors. However, the precise mechanisms of inflammation-induced diseases are not fully understood. Here, we show that the proinflammatory cytokines interferon-γ (IFN-γ) and tumor necrosis factor α (TNF-α) synergistically impair self-renewal and differentiation of mesenchymal stem cells (MSCs) via nuclear factor κB (NFκB)-mediated activation of mothers against decapentaplegic homolog 7 (SMAD7) in ovariectomized (OVX) mice. More interestingly, a long-term elevated levels of IFN-γ and TNF-α result in significantly increased susceptibility to malignant transformation in MSCs through NFκB-mediated upregulation of the oncogenes c-Fos and c-Myc. Depletion of either IFN-γ or TNF-α in OVX mice abolishes MSC impairment and the tendency toward malignant transformation with no NFκB-mediated oncogene activation. Systemic administration of aspirin, which significantly reduces the levels of IFN-γ and TNF-α, results in blockage of MSC deficiency and tumorigenesis by inhibition of NFκB/SMAD7 and NFκB/c-FOS and c-MYC pathways in OVX mice. In summary, this study reveals that inflammation factors, such as IFN-γ and TNF-α, synergistically induce MSC deficiency via NFκB/SMAD7 signaling and tumorigenesis via NFκB-mediated oncogene activation.

Keywords: Cancer; Cytokines; Differentiation; Mesenchymal stem cells; Stem cell-microenvironment interactions.

Publication types

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

MeSH terms

  • Animals
  • Aspirin / pharmacology
  • Carcinogenesis
  • Cell Differentiation / physiology
  • Female
  • Genes, fos
  • Genes, myc
  • Interferon-gamma / deficiency
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism*
  • Mesenchymal Stem Cells / metabolism*
  • Mice
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Nude
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / deficiency
  • NF-kappa B / genetics
  • NF-kappa B / metabolism*
  • Signal Transduction
  • Smad7 Protein / metabolism
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / deficiency
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism*

Substances

  • NF-kappa B
  • Smad7 Protein
  • Smad7 protein, mouse
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • Aspirin