Hypoxia-induced phenotypic switch of fibroblasts to myofibroblasts through a matrix metalloproteinase 2/tissue inhibitor of metalloproteinase-mediated pathway: implications for venous neointimal hyperplasia in hemodialysis access

J Vasc Interv Radiol. 2010 Jun;21(6):896-902. doi: 10.1016/j.jvir.2010.02.030.

Abstract

Purpose: Hemodialysis grafts fail because of venous neointimal hyperplasia formation caused by adventitial fibroblasts that have become myofibroblasts (ie, alpha-smooth muscle actin [SMA]-positive cells) and migrate to the neointima. There is increased expression of hypoxia-inducible factor (HIF)-1alpha in venous neointimal hyperplasia formation in experimental animal models and clinical samples. It was hypothesized that, under hypoxic stimulus (ie, HIF-1alpha), fibroblasts will convert to myofibroblasts through a matrix metalloproteinase (MMP)-2-mediated pathway.

Materials and methods: Murine AKR-2B fibroblasts were made hypoxic or normoxic for 24, 48, and 72 hours. Protein expression for HIF-1alpha, alpha-SMA, MMP-2, MMP-9, tissue inhibitor of metalloproteinase (TIMP)-1, and TIMP-2 was performed to determine the kinetic changes of these proteins. Immunostaining for alpha-SMA, collagen, and fibronectin was performed.

Results: At all time points, there was significantly increased expression of HIF-1alpha in the hypoxic fibroblasts compared with normoxic fibroblasts (P < .05). There was significantly increased expression of alpha-SMA at all time points, which peaked by 48 hours in hypoxic fibroblasts compared with normoxic fibroblasts (P < .05). There was a significant increase in the expression of active MMP-2 by 48-72 hours and a significant increase in TIMP-1 by 48-72 hours by hypoxic fibroblasts (P < .05). By 72 hours, there was significant increase in TIMP-2 expression (P < .05). Immunohistochemical analysis demonstrated increased expression of alpha-SMA, collagen, and fibronectin as the duration of hypoxia increased.

Conclusions: Under hypoxic conditions, fibroblasts will convert to myofibroblasts through an MMP-2-mediated pathway, which may provide insight into the mechanism of venous neointimal hyperplasia.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation / drug effects
  • Cell Hypoxia / physiology
  • Cell Line
  • Fibroblasts / cytology*
  • Fibroblasts / physiology*
  • Matrix Metalloproteinase 2 / metabolism*
  • Mice
  • Oxygen / metabolism*
  • Renal Dialysis / methods
  • Signal Transduction / physiology*
  • Tissue Inhibitor of Metalloproteinase-1 / metabolism*
  • Tunica Intima / physiopathology

Substances

  • Tissue Inhibitor of Metalloproteinase-1
  • Matrix Metalloproteinase 2
  • Oxygen