Impairment of the Ability of HDL From Patients With Metabolic Syndrome but Without Diabetes Mellitus to Activate eNOS: Correction by S1P Enrichment

Arterioscler Thromb Vasc Biol. 2017 May;37(5):804-811. doi: 10.1161/ATVBAHA.117.309287. Epub 2017 Mar 30.

Abstract

Objective: High-density lipoprotein (HDL) from nondiabetic patients with metabolic syndrome (MetS) displays abnormalities in their lipidome, such as triglyceride enrichment and sphingosine-1-phosphate depletion. We hypothesized that these abnormalities could impair the ability of HDL to stimulate endothelial nitric oxide synthase (eNOS).

Approach and results: Compared with HDL from control subjects, HDL from normoglycemic patients with MetS was 39% richer in triglycerides (P<0.01) and 15% poorer in sphingosine-1-phosphate (P<0.05; n=23 in each group). eNOS activity, assessed by the conversion of L-[3H]arginine to L-[3H]citrulline, was 69% lower in human umbilical vein endothelial cells incubated with HDL from MetS patients than in cells incubated with HDL from controls (P<0.0001). In addition, the activating phosphorylation of eNOS at serine (Ser) 1177 and of Akt (protein kinase B) at Ser473 was 37% (P<0.001) and 39% (P<0.05) lower, respectively, with HDL from MetS patients. Sphingosine-1-phosphate enrichment of HDL from MetS patients restored their ability to stimulate eNOS activity (P<0.05), in relation with a significant increase in eNOS phosphorylation at Ser1177 (P<0.05) and in Akt phosphorylation at Ser473 (P=0.05). By contrast, triglyceride enrichment of HDL from control subjects did not modify eNOS activity (P=0.90) and phosphorylation at Ser1177 (P=0.87).

Conclusions: We provide evidence that the activation of eNOS by HDL is decreased in MetS patients before the appearance of diabetes mellitus and that sphingosine-1-phosphate depletion of HDL is the main factor responsible for this defect. This has important consequences on the impairment of HDL functionality and antiatherogenic properties in these patients.

Keywords: HDL; eNOS; metabolic syndrome; sphingosine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Case-Control Studies
  • Cells, Cultured
  • Diabetes Mellitus / blood
  • Diabetes Mellitus / diagnosis
  • Diabetes Mellitus / enzymology*
  • Disease Progression
  • Enzyme Activation
  • Female
  • Human Umbilical Vein Endothelial Cells / enzymology*
  • Humans
  • Lipoproteins, HDL / blood*
  • Lysophospholipids / blood*
  • Male
  • Metabolic Syndrome / blood
  • Metabolic Syndrome / diagnosis
  • Metabolic Syndrome / enzymology*
  • Middle Aged
  • Nitric Oxide Synthase Type III / metabolism*
  • Phosphorylation
  • Proto-Oncogene Proteins c-akt / metabolism
  • Sphingosine / analogs & derivatives*
  • Sphingosine / blood

Substances

  • Lipoproteins, HDL
  • Lysophospholipids
  • sphingosine 1-phosphate
  • NOS3 protein, human
  • Nitric Oxide Synthase Type III
  • Proto-Oncogene Proteins c-akt
  • Sphingosine