Reactive oxygen species induce MMP12-dependent degradation of collagen 5 and fibronectin to promote the motility of human umbilical cord-derived mesenchymal stem cells

Br J Pharmacol. 2014 Jul;171(13):3283-97. doi: 10.1111/bph.12681.

Abstract

Background and purpose: Reactive oxygen species (ROS) are potent regulators of stem cell behaviour; however, their physiological significance as regards MMP-mediated regulation of the motility of human umbilical cord blood-derived mesenchymal stem cells (UCB-MSCs) has not been characterized. In the present study, we investigated the role of hydrogen peroxide (H2O2 ) and associated signalling pathways in promoting UCB-MSCs motility.

Experimental approach: The regulatory effects of H2O2 on the activation of PKC, MAPKs, NF-κB and β-catenin were determined. The expressions of MMP and extracellular matrix proteins were examined. Pharmacological inhibitors and gene-specific siRNA were used to identify the signalling pathways of H2O2 that affect UCB-MSCs motility. An experimental skin wound-healing model was used to confirm the functional role of UCB-MSCs treated with H2O2 in ICR mice.

Key results: H2O2 increased the motility of UCB-MSCs by activating PKCα via a calcium influx mechanism. H2O2 activated ERK and p38 MAPK, which are responsible for the distinct activation of transcription factors NF-κB and β-catenin. UCB-MSCs expressed eight MMP genes, but only MMP12 expression was uniquely regulated by NF-κB and β-catenin activation. H2O2 increased the MMP12-dependent degradation of collagen 5 (COL-5) and fibronectin (FN) associated with UCB-MSCs motility. Finally, topical transplantation of UCB-MSCs treated with H2O2 enhanced skin wound healing in mice.

Conclusions and implications: H2O2 stimulated UCB-MSCs motility by increasing MMP12-dependent degradation of COL-5 and FN through the activation of NF-κB and glycogen synthase kinase-3β/β-catenin, which is critical for providing a suitable microenvironment for MSCs transplantation and re-epithelialization of skin wounds in mice.

Keywords: MMP; extracellular matrix proteins; hydrogen peroxide; motility; skin wound healing; umbilical cord blood-derived mesenchymal stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Movement / physiology
  • Collagen Type V / metabolism
  • Disease Models, Animal
  • Female
  • Fibronectins / metabolism
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Matrix Metalloproteinase 12 / metabolism*
  • Mesenchymal Stem Cell Transplantation / methods*
  • Mesenchymal Stem Cells / cytology
  • Mice
  • Mice, Inbred ICR
  • NF-kappa B / metabolism
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction / physiology
  • Skin / pathology
  • Umbilical Cord
  • Wound Healing / physiology*
  • Wounds and Injuries / pathology
  • beta Catenin / metabolism

Substances

  • Collagen Type V
  • Fibronectins
  • NF-kappa B
  • Reactive Oxygen Species
  • beta Catenin
  • Hydrogen Peroxide
  • Matrix Metalloproteinase 12