A novel urokinase receptor-targeted inhibitor for plasmin and matrix metalloproteinases suppresses vein graft disease

Cardiovasc Res. 2010 Nov 1;88(2):367-75. doi: 10.1093/cvr/cvq203. Epub 2010 Jun 17.

Abstract

Aims: Matrix metalloproteinases (MMP) and plasminogen activator (PA)/plasmin-mediated proteolysis, especially at the cell surface, play important roles in matrix degeneration and smooth muscle cell migration, which largely contributes to vein graft failure. In this study, a novel hybrid protein was designed to inhibit both protease systems simultaneously. MMP and plasmin activity were inhibited at the cell surface by this hybrid protein, consisting of the receptor-binding amino-terminal fragment (ATF) of urokinase-type PA, linked to both the tissue inhibitor of metalloproteinases (TIMP-1) and bovine pancreas trypsin inhibitor (BPTI), a potent protease inhibitor. The effect of overexpression of this protein on vein graft disease was studied.

Methods and results: A non-viral expression vector encoding the hybrid protein TIMP-1.ATF.BPTI was constructed and validated. Next, cultured segments of human veins were transfected with this vector. Expressing TIMP-1.ATF.BPTI in vein segments resulted in a mean 36 ± 14% reduction in neointima formation after 4 weeks. In vivo inhibition of vein graft disease by TIMP-1.ATF.BPTI is demonstrated in venous interpositions placed into carotid arteries of hypercholesterolaemic APOE*3Leiden mice. After 4 weeks, vein graft thickening was significantly inhibited in mice treated with the domains TIMP-1, ATF, or BPTI (36-49% reduction). In the TIMP-1.ATF.BPTI-treated mice, vein graft thickening was reduced by 67±4%, which was also significantly stronger when compared with the individual components.

Conclusion: These data provide evidence that cell surface-bound inhibition of the PA and MMP system by the hybrid protein TIMP-1.ATF.BPTI, overexpressed in distant tissues after electroporation-mediated non-viral gene transfer, is a powerful approach to prevent vein graft disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apolipoprotein E3 / genetics
  • Aprotinin / biosynthesis
  • Aprotinin / genetics
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Carotid Arteries / surgery
  • Cattle
  • Cell Line
  • Cell Proliferation*
  • Disease Models, Animal
  • Electroporation
  • Fibrinolysin / antagonists & inhibitors
  • Fibrinolysin / metabolism*
  • Genetic Therapy* / methods
  • Graft Occlusion, Vascular / genetics
  • Graft Occlusion, Vascular / metabolism
  • Graft Occlusion, Vascular / pathology
  • Graft Occlusion, Vascular / prevention & control*
  • Humans
  • Hypercholesterolemia / genetics
  • Hypercholesterolemia / metabolism
  • Hypercholesterolemia / pathology
  • Hyperplasia
  • Male
  • Matrix Metalloproteinase Inhibitors
  • Matrix Metalloproteinases / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Receptors, Urokinase Plasminogen Activator / metabolism*
  • Recombinant Fusion Proteins / biosynthesis
  • Saphenous Vein / metabolism*
  • Saphenous Vein / pathology
  • Saphenous Vein / surgery
  • Time Factors
  • Tissue Culture Techniques
  • Tissue Inhibitor of Metalloproteinase-1 / biosynthesis
  • Tissue Inhibitor of Metalloproteinase-1 / genetics
  • Transfection
  • Urokinase-Type Plasminogen Activator / biosynthesis
  • Urokinase-Type Plasminogen Activator / genetics
  • Venae Cavae / metabolism*
  • Venae Cavae / pathology
  • Venae Cavae / transplantation

Substances

  • Apolipoprotein E3
  • Matrix Metalloproteinase Inhibitors
  • Receptors, Urokinase Plasminogen Activator
  • Recombinant Fusion Proteins
  • Tissue Inhibitor of Metalloproteinase-1
  • Aprotinin
  • Fibrinolysin
  • Urokinase-Type Plasminogen Activator
  • Matrix Metalloproteinases