Nitric Oxide-Independent Soluble Guanylate Cyclase Activation Improves Vascular Function and Cardiac Remodeling in Sickle Cell Disease

Am J Respir Cell Mol Biol. 2018 May;58(5):636-647. doi: 10.1165/rcmb.2017-0292OC.

Abstract

Sickle cell disease (SCD) is associated with intravascular hemolysis and oxidative inhibition of nitric oxide (NO) signaling. BAY 54-6544 is a small-molecule activator of oxidized soluble guanylate cyclase (sGC), which, unlike endogenous NO and the sGC stimulator, BAY 41-8543, preferentially binds and activates heme-free, NO-insensitive sGC to restore enzymatic cGMP production. We tested orally delivered sGC activator, BAY 54-6544 (17 mg/kg/d), sGC stimulator, BAY 41-8543, sildenafil, and placebo for 4-12 weeks in the Berkeley transgenic mouse model of SCD (BERK-SCD) and their hemizygous (Hemi) littermate controls (BERK-Hemi). Right ventricular (RV) maximum systolic pressure (RVmaxSP) was measured using micro right-heart catheterization. RV hypertrophy (RVH) was determined using Fulton's index and RV corrected weight (ratio of RV to tibia). Pulmonary artery vasoreactivity was tested for endothelium-dependent and -independent vessel relaxation. Right-heart catheterization revealed higher RVmaxSP and RVH in BERK-SCD versus BERK-Hemi, which worsened with age. Treatment with the sGC activator more effectively lowered RVmaxSP and RVH, with 90-day treatment delivering superior results, when compared with other treatments and placebo groups. In myography experiments, acetylcholine-induced (endothelium-dependent) and sodium-nitroprusside-induced (endothelium-independent NO donor) relaxation of the pulmonary artery harvested from placebo-treated BERK-SCD was impaired relative to BERK-Hemi but improved after therapy with sGC activator. By contrast, no significant effect for sGC stimulator or sildenafil was observed in BERK-SCD. These findings suggest that sGC is oxidized in the pulmonary arteries of transgenic SCD mice, leading to blunted responses to NO, and that the sGC activator, BAY 54-6544, may represent a novel therapy for SCD-associated pulmonary arterial hypertension and cardiac remodeling.

Keywords: pulmonary hypertension; sickle cell disease; soluble guanylate cyclase.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anemia, Sickle Cell / complications*
  • Anemia, Sickle Cell / genetics
  • Animals
  • Arterial Pressure / drug effects
  • Disease Models, Animal
  • Enzyme Activation
  • Enzyme Activators / pharmacokinetics
  • Enzyme Activators / pharmacology*
  • Heart Ventricles / drug effects*
  • Heart Ventricles / enzymology
  • Heart Ventricles / physiopathology
  • Hypertension, Pulmonary / drug therapy*
  • Hypertension, Pulmonary / enzymology
  • Hypertension, Pulmonary / genetics
  • Hypertension, Pulmonary / physiopathology
  • Hypertrophy, Left Ventricular / enzymology
  • Hypertrophy, Left Ventricular / genetics
  • Hypertrophy, Left Ventricular / physiopathology
  • Hypertrophy, Left Ventricular / prevention & control*
  • Mice, Transgenic
  • Morpholines / pharmacology
  • Nitric Oxide / metabolism
  • Pulmonary Artery / drug effects*
  • Pulmonary Artery / enzymology
  • Pulmonary Artery / physiopathology
  • Pyrimidines / pharmacology
  • Sildenafil Citrate / pharmacology
  • Soluble Guanylyl Cyclase / metabolism*
  • Vasodilation / drug effects
  • Ventricular Dysfunction, Right / drug therapy*
  • Ventricular Dysfunction, Right / enzymology
  • Ventricular Dysfunction, Right / genetics
  • Ventricular Dysfunction, Right / physiopathology
  • Ventricular Function, Right / drug effects*
  • Ventricular Pressure / drug effects
  • Ventricular Remodeling / drug effects*

Substances

  • BAY 41-8543
  • Enzyme Activators
  • Morpholines
  • Pyrimidines
  • Nitric Oxide
  • Sildenafil Citrate
  • Soluble Guanylyl Cyclase