Endothelial deletion of protein tyrosine phosphatase-1B protects against pressure overload-induced heart failure in mice

Cardiovasc Res. 2016 Aug 1;111(3):204-16. doi: 10.1093/cvr/cvw101. Epub 2016 May 20.

Abstract

Aims: Cardiac angiogenesis is an important determinant of heart failure. We examined the hypothesis that protein tyrosine phosphatase (PTP)-1B, a negative regulator of vascular endothelial growth factor (VEGF) receptor-2 activation, is causally involved in the cardiac microvasculature rarefaction during hypertrophy and that deletion of PTP1B in endothelial cells prevents the development of heart failure.

Methods and results: Cardiac hypertrophy was induced by transverse aortic constriction (TAC) in mice with endothelial-specific deletion of PTP1B (End.PTP1B-KO) and controls (End.PTP1B-WT). Survival up to 20 weeks after TAC was significantly improved in mice lacking endothelial PTP1B. Serial echocardiography revealed a better systolic pump function, less pronounced cardiac hypertrophy, and left ventricular dilation compared with End.PTP1B-WT controls. Histologically, banded hearts from End.PTP1B-KO mice exhibited increased numbers of PCNA-positive, proliferating endothelial cells resulting in preserved cardiac capillary density and improved perfusion as well as reduced hypoxia, apoptotic cell death, and fibrosis. Increased relative VEGFR2 and ERK1/2 phosphorylation and greater eNOS expression were present in the hearts of End.PTP1B-KO mice. The absence of PTP1B in endothelial cells also promoted neovascularization following peripheral ischaemia, and bone marrow transplantation excluded a major contribution of Tie2-positive haematopoietic cells to the improved angiogenesis in End.PTP1B-KO mice. Increased expression of caveolin-1 as well as reduced NADPH oxidase-4 expression, ROS generation and TGFβ signalling were observed and may have mediated the cardioprotective effects of endothelial PTP1B deletion.

Conclusions: Endothelial PTP1B deletion improves cardiac VEGF signalling and angiogenesis and protects against chronic afterload-induced heart failure. PTP1B may represent a useful target to preserve cardiac function during hypertrophy.

Keywords: Angiogenesis; Fibrosis; Heart failure; Hypertrophy; PTP1B.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aorta / physiopathology
  • Aorta / surgery
  • Apoptosis
  • Arterial Pressure
  • Caveolin 1 / metabolism
  • Constriction
  • Disease Models, Animal
  • Endothelial Cells / enzymology*
  • Endothelial Cells / pathology
  • Fibrosis
  • Genetic Predisposition to Disease
  • Heart Failure / enzymology
  • Heart Failure / etiology
  • Heart Failure / physiopathology
  • Heart Failure / prevention & control*
  • Hindlimb
  • Hypertrophy, Left Ventricular / enzymology
  • Hypertrophy, Left Ventricular / physiopathology
  • Hypertrophy, Left Ventricular / prevention & control
  • Ischemia / enzymology*
  • Ischemia / genetics
  • Ischemia / physiopathology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Muscle, Skeletal / blood supply*
  • NADPH Oxidase 4
  • NADPH Oxidases / metabolism
  • Neovascularization, Physiologic
  • Nitric Oxide Synthase Type III / metabolism
  • Phenotype
  • Phosphorylation
  • Protein Tyrosine Phosphatase, Non-Receptor Type 1 / deficiency*
  • Protein Tyrosine Phosphatase, Non-Receptor Type 1 / genetics
  • Receptor, TIE-2 / metabolism
  • Signal Transduction
  • Time Factors
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism
  • Ventricular Dysfunction, Left / enzymology
  • Ventricular Dysfunction, Left / physiopathology
  • Ventricular Dysfunction, Left / prevention & control
  • Ventricular Function, Left
  • Ventricular Remodeling

Substances

  • Cav1 protein, mouse
  • Caveolin 1
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • NADPH Oxidase 4
  • NADPH Oxidases
  • Nox4 protein, mouse
  • Kdr protein, mouse
  • Receptor, TIE-2
  • Tek protein, mouse
  • Vascular Endothelial Growth Factor Receptor-2
  • Mapk1 protein, mouse
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Protein Tyrosine Phosphatase, Non-Receptor Type 1
  • Ptpn1 protein, mouse