β3 Adrenergic Stimulation Restores Nitric Oxide/Redox Balance and Enhances Endothelial Function in Hyperglycemia

J Am Heart Assoc. 2016 Feb 19;5(2):e002824. doi: 10.1161/JAHA.115.002824.

Abstract

Background: Perturbed balance between NO and O2 (•-). (ie, NO/redox imbalance) is central in the pathobiology of diabetes-induced vascular dysfunction. We examined whether stimulation of β3 adrenergic receptors (β3 ARs), coupled to endothelial nitric oxide synthase (eNOS) activation, would re-establish NO/redox balance, relieve oxidative inhibition of the membrane proteins eNOS and Na(+)-K(+) (NK) pump, and improve vascular function in a new animal model of hyperglycemia.

Methods and results: We established hyperglycemia in male White New Zealand rabbits by infusion of S961, a competitive high-affinity peptide inhibitor of the insulin receptor. Hyperglycemia impaired endothelium-dependent vasorelaxation by "uncoupling" of eNOS via glutathionylation (eNOS-GSS) that was dependent on NADPH oxidase activity. Accordingly, NO levels were lower while O2 (•-) levels were higher in hyperglycemic rabbits. Infusion of the β3 AR agonist CL316243 (CL) decreased eNOS-GSS, reduced O2 (•-), restored NO levels, and improved endothelium-dependent relaxation. CL decreased hyperglycemia-induced NADPH oxidase activation as suggested by co-immunoprecipitation experiments, and it increased eNOS co-immunoprecipitation with glutaredoxin-1, which may reflect promotion of eNOS de-glutathionylation by CL. Moreover, CL reversed hyperglycemia-induced glutathionylation of the β1 NK pump subunit that causes NK pump inhibition, and improved K(+)-induced vasorelaxation that reflects enhancement in NK pump activity. Lastly, eNOS-GSS was higher in vessels of diabetic patients and was reduced by CL, suggesting potential significance of the experimental findings in human diabetes.

Conclusions: β3 AR activation restored NO/redox balance and improved endothelial function in hyperglycemia. β3 AR agonists may confer protection against diabetes-induced vascular dysfunction.

Keywords: endothelial dysfunction; endothelial nitric oxide synthase; hyperglycemia; oxidative stress; β3 adrenergic receptors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic beta-3 Receptor Agonists / pharmacology*
  • Animals
  • Blood Glucose / drug effects
  • Blood Glucose / metabolism
  • Diabetes Mellitus, Experimental / chemically induced
  • Diabetes Mellitus, Experimental / drug therapy*
  • Diabetes Mellitus, Experimental / enzymology
  • Diabetes Mellitus, Experimental / physiopathology
  • Diabetic Angiopathies / chemically induced
  • Diabetic Angiopathies / enzymology
  • Diabetic Angiopathies / physiopathology
  • Diabetic Angiopathies / prevention & control*
  • Dioxoles / pharmacology*
  • Dose-Response Relationship, Drug
  • Endothelium, Vascular / drug effects*
  • Endothelium, Vascular / enzymology
  • Endothelium, Vascular / physiopathology
  • Enzyme Activation
  • Glutathione / metabolism
  • Hyperglycemia / chemically induced
  • Hyperglycemia / drug therapy*
  • Hyperglycemia / enzymology
  • Hyperglycemia / physiopathology
  • Hypoglycemic Agents / pharmacology*
  • Male
  • NADPH Oxidases / metabolism
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase Type III / metabolism
  • Oxidation-Reduction
  • Oxidative Stress / drug effects
  • Peptides
  • Rabbits
  • Receptors, Adrenergic, beta-3 / drug effects*
  • Receptors, Adrenergic, beta-3 / metabolism
  • Signal Transduction / drug effects
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Superoxides / metabolism
  • Time Factors

Substances

  • Adrenergic beta-3 Receptor Agonists
  • Blood Glucose
  • Dioxoles
  • Hypoglycemic Agents
  • Peptides
  • Receptors, Adrenergic, beta-3
  • S961 peptide
  • Superoxides
  • disodium (R,R)-5-(2-((2-(3-chlorophenyl)-2-hydroxyethyl)-amino)propyl)-1,3-benzodioxole-2,3-dicarboxylate
  • Nitric Oxide
  • Nitric Oxide Synthase Type III
  • NADPH Oxidases
  • Sodium-Potassium-Exchanging ATPase
  • Glutathione