Inhibition of matrix metalloproteinase-2 improves endothelial function and prevents hypertension in insulin-resistant rats

Br J Pharmacol. 2012 Feb;165(3):705-15. doi: 10.1111/j.1476-5381.2011.01583.x.

Abstract

Background and purpose: Insulin resistance is often found to be associated with high blood pressure. We propose that in insulin-resistant hypertension, endothelial dysfunction is the consequence of increased activity of vascular MMP-2. As MMP-2 proteolytically cleaves a number of extracellular matrix proteins, we hypothesized that MMP-2 impairs endothelial function by proteolytic degradation of endothelial NOS (eNOS) or its cofactor, heat shock protein 90 (HSP90).

Experimental approach: We tested our hypothesis in bovine coronary artery endothelial cells and fructose-fed hypertensive rats (FHR), a model of acquired systolic hypertension and insulin resistance.

Key results: Treatment of FHRs with the MMP inhibitor doxycycline, preserved endothelial function as well as prevented the development of hypertension, suggesting that MMPs impair endothelial function. Furthermore, incubating endothelial cells in vitro with a recombinant MMP-2 decreased NO production in a dose-dependent manner. Using substrate cleavage assays and immunofluorescence microscopy studies, we found that MMP-2 not only cleaves and degrades HSP90, an eNOS cofactor but also co-localizes with both eNOS and HSP90 in endothelial cells, suggesting that MMPs functionally interact with the eNOS system. Treatment of FHRs with doxycycline attenuated the decrease in eNOS and HSP90 expression but did not improve insulin sensitivity.

Conclusions and implications: Our data suggest that increased activity of MMP-2 in FHRs impairs endothelial function and promotes hypertension. Inhibition of MMP-2 could be a potential therapeutic strategy for the management of hypertension.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aorta, Thoracic / cytology
  • Cattle
  • Cells, Cultured
  • Doxycycline / pharmacology*
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / physiology
  • Fructose
  • HSP90 Heat-Shock Proteins / metabolism
  • Hypertension / chemically induced
  • Hypertension / metabolism
  • Hypertension / physiopathology
  • Hypertension / prevention & control*
  • Insulin Resistance / physiology
  • Male
  • Matrix Metalloproteinase 2 / physiology
  • Matrix Metalloproteinase Inhibitors*
  • Mesenteric Arteries / drug effects*
  • Mesenteric Arteries / physiology
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type III / metabolism
  • Rats
  • Rats, Wistar

Substances

  • HSP90 Heat-Shock Proteins
  • Matrix Metalloproteinase Inhibitors
  • Fructose
  • Nitric Oxide
  • Nitric Oxide Synthase Type III
  • Matrix Metalloproteinase 2
  • Mmp2 protein, rat
  • Doxycycline