Chronic infusion of enalaprilat into hypothalamic paraventricular nucleus attenuates angiotensin II-induced hypertension and cardiac hypertrophy by restoring neurotransmitters and cytokines

Toxicol Appl Pharmacol. 2014 Feb 1;274(3):436-44. doi: 10.1016/j.taap.2013.12.001. Epub 2013 Dec 14.

Abstract

The renin-angiotensin system (RAS) in the brain is involved in the pathogenesis of hypertension. We hypothesized that inhibition of angiotensin-converting enzyme (ACE) in the hypothalamic paraventricular nucleus (PVN) attenuates angiotensin II (ANG II)-induced hypertension via restoring neurotransmitters and cytokines. Rats underwent subcutaneous infusions of ANG II or saline and bilateral PVN infusions of ACE inhibitor enalaprilat (ENL, 2.5μg/h) or vehicle for 4weeks. ANG II infusion resulted in higher mean arterial pressure and cardiac hypertrophy as indicated by increased whole heart weight/body weight ratio, whole heart weight/tibia length ratio, left ventricular weight/tibia length ratio, and mRNA expressions of cardiac atrial natriuretic peptide and beta-myosin heavy chain. These ANG II-infused rats had higher PVN levels of glutamate, norepinephrine, tyrosine hydroxylase, pro-inflammatory cytokines (PICs) and the chemokine monocyte chemoattractant protein-1, and lower PVN levels of gamma-aminobutyric acid, interleukin (IL)-10 and the 67-kDa isoform of glutamate decarboxylase (GAD67), and higher plasma levels of PICs, norepinephrine and aldosterone, and lower plasma IL-10, and higher renal sympathetic nerve activity. However, PVN treatment with ENL attenuated these changes. PVN microinjection of ANG II induced increases in IL-1β and IL-6, and a decrease in IL-10 in the PVN, and pretreatment with angiotensin II type 1 receptor (AT1-R) antagonist losartan attenuated these changes. These findings suggest that ANG II infusion induces an imbalance between excitatory and inhibitory neurotransmitters and an imbalance between pro- and anti-inflammatory cytokines in the PVN, and PVN inhibition of the RAS restores neurotransmitters and cytokines in the PVN, thereby attenuating ANG II-induced hypertension and cardiac hypertrophy.

Keywords: Angiotensin-converting enzyme; Cardiac hypertrophy; Cytokines; Hypertension; Hypothalamic paraventricular nucleus; Neurotransmitters.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / adverse effects
  • Animals
  • Cardiomegaly / chemically induced
  • Cardiomegaly / drug therapy*
  • Chemokine CCL2 / metabolism
  • Enalaprilat / administration & dosage
  • Enalaprilat / therapeutic use*
  • Glutamic Acid / blood
  • Heart / drug effects
  • Hypertension / chemically induced
  • Hypertension / drug therapy*
  • Interleukin-10 / blood
  • Interleukin-1beta / blood
  • Interleukin-6 / blood
  • Kidney / drug effects
  • Kidney / metabolism
  • Losartan / pharmacology
  • Male
  • Neurotransmitter Agents / metabolism
  • Norepinephrine / blood
  • Organ Size / drug effects
  • Paraventricular Hypothalamic Nucleus / drug effects
  • Paraventricular Hypothalamic Nucleus / metabolism
  • Peptidyl-Dipeptidase A / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Angiotensin, Type 1 / metabolism
  • Renin-Angiotensin System / drug effects
  • gamma-Aminobutyric Acid / blood

Substances

  • Chemokine CCL2
  • Interleukin-1beta
  • Interleukin-6
  • Neurotransmitter Agents
  • Receptor, Angiotensin, Type 1
  • Angiotensin II
  • Interleukin-10
  • Glutamic Acid
  • gamma-Aminobutyric Acid
  • Peptidyl-Dipeptidase A
  • Enalaprilat
  • Losartan
  • Norepinephrine