Blockade of PAR-1 Signaling Attenuates Cardiac Hypertrophy and Fibrosis in Renin-Overexpressing Hypertensive Mice

J Am Heart Assoc. 2020 Jun 16;9(12):e015616. doi: 10.1161/JAHA.119.015616. Epub 2020 Jun 4.

Abstract

Background Although PAR-1 (protease-activated receptor-1) exerts important functions in the pathophysiology of the cardiovascular system, the role of PAR-1 signaling in heart failure development remains largely unknown. We tested the hypothesis that PAR-1 signaling inhibition has protective effects on the progression of cardiac remodeling induced by chronic renin-angiotensin system activation using renin-overexpressing hypertensive (Ren-Tg) mice. Methods and Results We treated 12- to 16-week-old male wild-type (WT) mice and Ren-Tg mice with continuous subcutaneous infusion of the PAR-1 antagonist SCH79797 or vehicle for 4 weeks. The thicknesses of interventricular septum and the left ventricular posterior wall were greater in Ren-Tg mice than in WT mice, and SCH79797 treatment significantly decreased these thicknesses in Ren-Tg mice. The cardiac fibrosis area and monocyte/macrophage deposition were greater in Ren-Tg mice than in WT mice, and both conditions were attenuated by SCH79797 treatment. Cardiac mRNA expression levels of PAR-1, TNF-α (tumor necrosis factor-α), TGF-β1 (transforming growth factor-β1), and COL3A1 (collagen type 3 α1 chain) and the ratio of β-myosin heavy chain (β-MHC) to α-MHC were all greater in Ren-Tg mice than in WT mice; SCH79797 treatment attenuated these increases in Ren-Tg mice. Prothrombin fragment 1+2 concentration and factor Xa in plasma were greater in Ren-Tg mice than in WT mice, and both conditions were unaffected by SCH79797 treatment. In isolated cardiac fibroblasts, both thrombin and factor Xa enhanced ERK1/2 (extracellular signal-regulated kinase 1/2) phosphorylation, and SCH79797 pretreatment abolished this enhancement. Furthermore, gene expression of PAR-1, TGF-β1, and COL3A1 were enhanced by factor Xa, and all were inhibited by SCH79797. Conclusions The results indicate that PAR-1 signaling is involved in cardiac remodeling induced by renin-angiotensin system activation, which may provide a novel therapeutic target for heart failure.

Keywords: cardiac fibrosis; cardiac hypertrophy; factor Xa; protease‐activated receptor; renin–angiotensin system.

MeSH terms

  • Animals
  • Collagen Type III / genetics
  • Collagen Type III / metabolism
  • Cytokines / metabolism
  • Disease Models, Animal
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Fibrosis
  • HEK293 Cells
  • Humans
  • Hypertension / drug therapy*
  • Hypertension / genetics
  • Hypertension / metabolism
  • Hypertension / physiopathology
  • Hypertrophy, Left Ventricular / genetics
  • Hypertrophy, Left Ventricular / metabolism
  • Hypertrophy, Left Ventricular / physiopathology
  • Hypertrophy, Left Ventricular / prevention & control*
  • Inflammation Mediators / metabolism
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Myocardium / metabolism*
  • Myocardium / pathology
  • Pyrroles / pharmacology*
  • Quinazolines / pharmacology*
  • Receptor, PAR-1 / antagonists & inhibitors*
  • Receptor, PAR-1 / genetics
  • Receptor, PAR-1 / metabolism
  • Renin / genetics
  • Renin / metabolism*
  • Signal Transduction
  • Transforming Growth Factor beta1 / genetics
  • Transforming Growth Factor beta1 / metabolism
  • Up-Regulation
  • Ventricular Function, Left / drug effects*
  • Ventricular Remodeling / drug effects*

Substances

  • COL3A1 protein, mouse
  • Collagen Type III
  • Cytokines
  • Inflammation Mediators
  • N3-cyclopropyl-7-((4-(1-methylethyl)phenyl)methyl)-7H-pyrrolo(3, 2-f)quinazoline-1,3-diamine
  • Pyrroles
  • Quinazolines
  • Receptor, PAR-1
  • Tgfb1 protein, mouse
  • Transforming Growth Factor beta1
  • Extracellular Signal-Regulated MAP Kinases
  • Renin