Cleaved high-molecular-weight kininogen accelerates the onset of endothelial progenitor cell senescence by induction of reactive oxygen species

Arterioscler Thromb Vasc Biol. 2011 Apr;31(4):883-9. doi: 10.1161/ATVBAHA.110.222430. Epub 2011 Jan 20.

Abstract

Objective: Cleaved high-molecular-weight kininogen (HKa), an activation product of the plasma kallikrein-kinin system, inhibits endothelial cell functions. We questioned whether HKa affects the function of endothelial progenitor cells (EPCs) and accelerates their senescence.

Methods and results: Treatment with HKa for 2 weeks markedly inhibited the formation of large colonies and proliferation of EPCs on collagen surfaces, whereas HKa did not affect collagen-mediated EPC adhesion and survival. Concomitantly, treated EPCs displayed flattened and giant cell morphological changes and formation of intracellular vacuoles. As determined by acidic β-galactosidase staining, HKa increased senescent EPCs by 2- and >3-fold after culture for 1 and 2 weeks, respectively. In addition, HKa suppressed the telomerase activity of EPCs. HKa concentration-dependently increased the generation of intracellular reactive oxygen species (ROS) and markedly upregulated p38 kinase phosphorylation and prosenescence molecule p16(INK4a) expression. SB203580, a p38 inhibitor, attenuated the level of HKa-enhanced p16(INK4a) expression. Either quenching of ROS or inhibition of p38 kinase prevented HKa-induced EPC senescence.

Conclusions: HKa accelerates the onset of EPC senescence by activating the ROS-p38 kinase-p16(INK4a) signaling cascade. This novel activity of HKa points out the likelihood of HKa serving as an endogenous inducer of EPC senescence.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Cell Adhesion
  • Cell Proliferation* / drug effects
  • Cell Survival
  • Cells, Cultured
  • Cellular Senescence* / drug effects
  • Collagen / metabolism
  • Cyclin-Dependent Kinase Inhibitor p16 / genetics
  • Cyclin-Dependent Kinase Inhibitor p16 / metabolism
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Free Radical Scavengers / pharmacology
  • Green Fluorescent Proteins / biosynthesis
  • Green Fluorescent Proteins / genetics
  • Humans
  • Kininogen, High-Molecular-Weight / metabolism*
  • Phosphorylation
  • Protein Kinase Inhibitors / pharmacology
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction
  • Stem Cells / drug effects
  • Stem Cells / metabolism*
  • Telomerase / metabolism
  • Time Factors
  • Transfection
  • p38 Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Cyclin-Dependent Kinase Inhibitor p16
  • Free Radical Scavengers
  • Kininogen, High-Molecular-Weight
  • Protein Kinase Inhibitors
  • Reactive Oxygen Species
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Collagen
  • p38 Mitogen-Activated Protein Kinases
  • Telomerase