Nitrergic cardiovascular regulation in the African lungfish, Protopterus aethiopicus

Comp Biochem Physiol A Mol Integr Physiol. 2017 May:207:52-56. doi: 10.1016/j.cbpa.2016.12.030. Epub 2017 Feb 17.

Abstract

As a ubiquitous signaling molecule, nitric oxide (NO) exerts various important effects on the cardiovascular system and is involved in the regulation of vascular tone and myocardial metabolism in vertebrates. Lungfishes are closely related to tetrapods and provide an interesting possibility to understand the transition from water to land. Lungfishes are endowed with both systemic and pulmonary circulations, and their incompletely divided ventricle allows for blood to bypass either circuit. Lungfishes inhabit ephemeral waterbodies that may enforce prolonged aestivation during drought, throughout which nitric oxide synthase (NOS) expression is upregulated. To better understand the physiological relevance of NO on cardiovascular regulation in this transitory group, we measured vascular reactivity to muscarinic agonist acetylcholine, α- and β-adrenergic agonists (phenylephrine and isoproterenol, respectively), or the NO donor, sodium nitroprusside (SNP) on four vessel segments-efferent branchial arteries, gill artery, ductus arteriosus and pulmonary artery-from the African lungfish, Protopterus aethiopicus. In a simultaneous study, we measured oxygen consumption and twitch force in myocardial preparations in the presence and absence of an NOS inhibitor (asymmetric dimethylarginine; ADMA). Only the ductus arteriosus vasodilated in response to SNP. Isoproterenol caused vasodilation, whereas acetylcholine and phenylephrine vasoconstricted all vessel segments. NOS inhibition decreased myocardial force relative to oxygen consumption, indicating a lowered efficiency. We provide novel evidence that NO affects the vasculature of lungfish that may be derived from perivascular nitrergic nerves limited to the ductus arteriosus. Our data also suggests that NO exerts a tonic dampening of myocardial oxygen consumption which may be particularly important during aestivation.

Keywords: Autonomic regulation; Myocardium; Nitric oxide; Oxygenation; Respiratory vessels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / administration & dosage
  • Animals
  • Arginine / administration & dosage
  • Arginine / analogs & derivatives
  • Arteries / drug effects*
  • Arteries / metabolism
  • Arteries / physiology
  • Cardiovascular System / drug effects
  • Cardiovascular System / metabolism*
  • Fishes / metabolism
  • Fishes / physiology*
  • Gills / drug effects*
  • Gills / physiology
  • Isoproterenol / administration & dosage
  • Myocardium / metabolism
  • Myocardium / pathology
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / metabolism
  • Nitroprusside / administration & dosage
  • Oxygen Consumption / drug effects
  • Phenylephrine / administration & dosage
  • Pulmonary Circulation / drug effects

Substances

  • dimethylarginine
  • Nitroprusside
  • Phenylephrine
  • Nitric Oxide
  • Arginine
  • Nitric Oxide Synthase
  • Isoproterenol
  • Acetylcholine