GRK2-mediated inhibition of adrenergic and dopaminergic signaling in right ventricular hypertrophy: therapeutic implications in pulmonary hypertension

Circulation. 2012 Dec 11;126(24):2859-69. doi: 10.1161/CIRCULATIONAHA.112.109868. Epub 2012 Nov 2.

Abstract

Background: The cause and consequences of impaired adrenergic signaling in right ventricular failure/hypertrophy (RVH) are poorly understood. We hypothesized that G protein-coupled receptor kinase-2 (GRK2)-mediated uncoupling of β-adrenergic receptor signaling impairs inotropic reserve. The implications of right ventricular (RV) adrenergic remodeling for inotrope selection and the therapeutic benefit of interrupting Gβγ-GRK2 interaction, using gallein, were tested.

Methods and results: Chamber-specificity and cellular localization of adrenergic remodeling were compared in rodent RVH associated with pulmonary arterial hypertension (PAH-RVH; SU5416+chronic-hypoxia or Monocrotaline) versus pulmonary artery banding-induced RVH (PAB-RVH). Results were corroborated in RV arrays from 10 PAH patients versus controls. Inotropic reserve was assessed in RV- and left ventricular-Langendorff models and in vivo. Gallein therapy (1.8 mg/kg/day ×2-weeks) was assessed. Despite similar RVH, cardiac output (58.3±4.9 versus 82.9±4.8 mL/min; P<0.001) and treadmill distance (41.5±11.6 versus 244.1±12.4 m; P<0.001) were lower in PAH-RVH versus PAB-RVH. In PAH-RVH versus PAB-RVH there was greater downregulation of β1-, α1- and dopamine-1 receptors, more left ventricular involvement, and greater impairment of RV contractile reserve. RV GRK2 activity increased in parallel with a reduction in both adrenergic receptor expression and inotrope-stimulated cAMP levels (P<0.01). β1-receptor downregulation also occurred in human PAH-RVH. Dobutamine was superior to dopamine as an RV inotrope, both ex vivo and in vivo.

Conclusions: GRK2-mediated desensitization-downregulation of adrenergic and dopaminergic receptors impairs inotropic reserve in PAH-RVH. Acute inotropic support in RVH is best accomplished by dobutamine, reflecting its better coupling to adenylyl cyclase and the reliance of dopamine on dopamine-1-receptor signaling, which is impaired in RVH. Inhibiting Gβγ-GRK2 interactions has therapeutic benefit in RVH.

Publication types

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

MeSH terms

  • Animals
  • Cardiotonic Agents / pharmacology
  • Cells, Cultured
  • Dobutamine / pharmacology
  • Dopamine / pharmacology
  • Down-Regulation / drug effects
  • Down-Regulation / physiology
  • Female
  • G-Protein-Coupled Receptor Kinase 2 / metabolism*
  • Humans
  • Hypertension, Pulmonary / drug therapy*
  • Hypertension, Pulmonary / metabolism
  • Hypertension, Pulmonary / pathology
  • Hypertrophy, Right Ventricular / drug therapy*
  • Hypertrophy, Right Ventricular / metabolism
  • Hypertrophy, Right Ventricular / pathology
  • Male
  • Myocardial Contraction / drug effects
  • Myocardial Contraction / physiology
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / drug effects
  • Oligonucleotide Array Sequence Analysis
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Adrenergic, beta / genetics
  • Receptors, Adrenergic, beta / metabolism*
  • Receptors, Dopamine D1 / genetics
  • Receptors, Dopamine D1 / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Xanthenes / pharmacology*

Substances

  • Cardiotonic Agents
  • Receptors, Adrenergic, beta
  • Receptors, Dopamine D1
  • Xanthenes
  • Dobutamine
  • gallein
  • Grk2 protein, rat
  • G-Protein-Coupled Receptor Kinase 2
  • Dopamine