Vagus nerve stimulation mitigates intrinsic cardiac neuronal remodeling and cardiac hypertrophy induced by chronic pressure overload in guinea pig

Am J Physiol Heart Circ Physiol. 2016 May 15;310(10):H1349-59. doi: 10.1152/ajpheart.00939.2015. Epub 2016 Mar 18.

Abstract

Our objective was to determine whether chronic vagus nerve stimulation (VNS) mitigates pressure overload (PO)-induced remodeling of the cardioneural interface. Guinea pigs (n = 48) were randomized to right or left cervical vagus (RCV or LCV) implant. After 2 wk, chronic left ventricular PO was induced by partial (15-20%) aortic constriction. Of the 31 animals surviving PO induction, 10 were randomized to RCV VNS, 9 to LCV VNS, and 12 to sham VNS. VNS was delivered at 20 Hz and 1.14 ± 0.03 mA at a 22% duty cycle. VNS commenced 10 days after PO induction and was maintained for 40 days. Time-matched controls (n = 9) were evaluated concurrently. Echocardiograms were obtained before and 50 days after PO. At termination, intracellular current-clamp recordings of intrinsic cardiac (IC) neurons were studied in vitro to determine effects of therapy on soma characteristics. Ventricular cardiomyocyte sizes were assessed with histology along with immunoblot analysis of selected proteins in myocardial tissue extracts. In sham-treated animals, PO increased cardiac output (34%, P < 0.004), as well as systolic (114%, P < 0.04) and diastolic (49%, P < 0.002) left ventricular volumes, a hemodynamic response prevented by VNS. PO-induced enhancements of IC synaptic efficacy and muscarinic sensitivity of IC neurons were mitigated by chronic VNS. Increased myocyte size, which doubled in PO (P < 0.05), was mitigated by RCV. PO hypertrophic myocardium displayed decreased glycogen synthase (GS) protein levels and accumulation of the phosphorylated (inactive) form of GS. These PO-induced changes in GS were moderated by left VNS. Chronic VNS targets IC neurons accompanying PO to obtund associated adverse cardiomyocyte remodeling.

Keywords: autonomic regulation therapy; cardiac hypertrophy; guinea pig; intrinsic cardiac nervous system; pressure overload; vagus nerve stimulation.

MeSH terms

  • Animals
  • Apoptosis
  • Disease Models, Animal
  • Glycogen Synthase / metabolism
  • Guinea Pigs
  • Heart / innervation*
  • Hypertrophy, Left Ventricular / etiology
  • Hypertrophy, Left Ventricular / metabolism
  • Hypertrophy, Left Ventricular / physiopathology
  • Hypertrophy, Left Ventricular / therapy*
  • Male
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology
  • Phosphorylation
  • Synaptic Transmission
  • Time Factors
  • Vagus Nerve / physiopathology*
  • Vagus Nerve Stimulation*
  • Ventricular Function, Left*
  • Ventricular Pressure*
  • Ventricular Remodeling*

Substances

  • Glycogen Synthase