Endothelial arginine resynthesis contributes to the maintenance of vasomotor function in male diabetic mice

PLoS One. 2014 Jul 17;9(7):e102264. doi: 10.1371/journal.pone.0102264. eCollection 2014.

Abstract

Aim: Argininosuccinate synthetase (ASS) is essential for recycling L-citrulline, the by-product of NO synthase (NOS), to the NOS substrate L-arginine. Here, we assessed whether disturbed arginine resynthesis modulates endothelium-dependent vasodilatation in normal and diabetic male mice.

Methods and results: Endothelium-selective Ass-deficient mice (Assfl/fl/Tie2Cretg/- = Ass-KOTie2) were generated by crossing Assfl/fl mice ( = control) with Tie2Cre mice. Gene ablation in endothelial cells was confirmed by immunohistochemistry. Blood pressure (MAP) was recorded in 34-week-old male mice. Vasomotor responses were studied in isolated saphenous arteries of 12- and 34-week-old Ass-KOTie2 and control animals. At the age of 10 weeks, diabetes was induced in control and Ass-KOTie2 mice by streptozotocin injections. Vasomotor responses of diabetic animals were studied 10 weeks later. MAP was similar in control and Ass-KOTie2 mice. Depletion of circulating L-arginine by arginase 1 infusion or inhibition of NOS activity with L-NAME resulted in an increased MAP (10 and 30 mmHg, respectively) in control and Ass-KOTie2 mice. Optimal arterial diameter, contractile responses to phenylephrine, and relaxing responses to acetylcholine and sodium nitroprusside were similar in healthy control and Ass-KOTie2 mice. However, in diabetic Ass-KOTie2 mice, relaxation responses to acetylcholine and endothelium-derived NO (EDNO) were significantly reduced when compared to diabetic control mice.

Conclusions: Absence of endothelial citrulline recycling to arginine did not affect blood pressure and systemic arterial vasomotor responses in healthy mice. EDNO-mediated vasodilatation was significantly more impaired in diabetic Ass-KOTie2 than in control mice demonstrating that endothelial arginine recycling becomes a limiting endothelial function in diabetes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology
  • Animals
  • Arginase / metabolism
  • Arginine / biosynthesis*
  • Arginine / blood
  • Argininosuccinate Synthase / genetics*
  • Blood Pressure / genetics
  • Blood Pressure / physiology*
  • Citrulline / blood
  • Citrulline / metabolism
  • Diabetes Mellitus, Experimental / genetics
  • Diabetes Mellitus, Experimental / metabolism*
  • Endothelial Cells / cytology
  • Endothelial Cells / enzymology
  • Endothelium / cytology
  • Endothelium / enzymology
  • Endothelium / metabolism
  • Female
  • Heart Rate / genetics
  • Heart Rate / physiology*
  • Male
  • Mice
  • Mice, Knockout
  • Muscle, Smooth, Vascular / physiology
  • NG-Nitroarginine Methyl Ester
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / metabolism
  • Nitroprusside / pharmacology
  • Phenylephrine / pharmacology
  • Vasoconstrictor Agents / pharmacology
  • Vasodilation / genetics
  • Vasodilation / physiology
  • Vasodilator Agents / pharmacology
  • Vasomotor System / metabolism

Substances

  • Vasoconstrictor Agents
  • Vasodilator Agents
  • Nitroprusside
  • Phenylephrine
  • Citrulline
  • Arginine
  • Nitric Oxide Synthase
  • Arg1 protein, mouse
  • Arginase
  • Argininosuccinate Synthase
  • Acetylcholine
  • NG-Nitroarginine Methyl Ester

Grants and funding

Grant Netherlands Heart Foundation NHF (Nederlands hartstichting; project 2008B107). The website is: https://www.hartstichting.nl/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.