LAV-BPIFB4 isoform modulates eNOS signalling through Ca2+/PKC-alpha-dependent mechanism

Cardiovasc Res. 2017 Jun 1;113(7):795-804. doi: 10.1093/cvr/cvx072.

Abstract

Aims: Ageing is associated with impairment of endothelial nitric oxide synthase (eNOS) and progressive reduction in endothelial function. A genetic study on long-living individuals-who are characterized by delays in ageing and in the onset of cardiovascular disease-previously revealed I229V (rs2070325) in bactericidal/permeability-increasing fold-containing-family-B-member-4 (BPIFB4) as a longevity-associated variant (LAV); the LAV protein enhanced endothelial NO production and vasorelaxation through a protein kinase R-like endoplasmic reticulum kinase/14-3-3/heat shock protein 90 signal. Here, we further characterize the molecular mechanisms underlying LAV-BPIFB4-dependent enhancement of vascular function.

Methods and results: LAV-BPIFB4 upregulated eNOS function via mobilization of Ca2+ and activation of protein kinase C alpha (PKCα). Indeed, the overexpression of LAV-BPIFB4 in human endothelial cells enhanced ATP-induced Ca2+ mobilization and the translocation of PKCα to the plasma membrane. Coherently, pharmacological inhibition of PKCα blunted the positive effect of LAV-BPIFB4 on eNOS and endothelial function. In addition, although LAV-BPIFB4 lost the ability to activate PKCα and eNOS in ex vivo vessels studied in an external Ca2+-free medium and in vessels from eNOS-/- mice, it still potentiated endothelial activity, recruiting an alternative mechanism dependent upon endothelium-derived hyperpolarizing factor (EDHF).

Conclusions: We have identified novel molecular determinants of the beneficial effects of LAV-BPIFB4 on endothelial function, showing the roles of Ca2+ mobilization and PKCα in eNOS activation and of EDHF when eNOS is inhibited. These results highlight the role LAV-BPIFB4 can have in restoring signals that are lost during ageing.

Keywords: BPIFB4; Endothelium; Nitric oxide; PKCα; Vascular function.

MeSH terms

  • Animals
  • Calcium Signaling* / drug effects
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Endothelial Cells / drug effects
  • Endothelial Cells / enzymology*
  • Enzyme Activation
  • Humans
  • Intercellular Signaling Peptides and Proteins
  • Membrane Potentials
  • Mesenteric Arteries / drug effects
  • Mesenteric Arteries / enzymology*
  • Mice, Knockout
  • Nitric Oxide Synthase Type III / deficiency
  • Nitric Oxide Synthase Type III / genetics
  • Nitric Oxide Synthase Type III / metabolism*
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Phosphorylation
  • Protein Isoforms
  • Protein Kinase C-alpha / antagonists & inhibitors
  • Protein Kinase C-alpha / genetics
  • Protein Kinase C-alpha / metabolism*
  • Protein Kinase Inhibitors / pharmacology
  • Protein Transport
  • Transfection
  • Up-Regulation
  • Vasodilation* / drug effects
  • Vasodilator Agents / pharmacology

Substances

  • BPIFB4 protein, human
  • Intercellular Signaling Peptides and Proteins
  • Phosphoproteins
  • Protein Isoforms
  • Protein Kinase Inhibitors
  • Vasodilator Agents
  • NOS3 protein, human
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • PRKCA protein, human
  • Prkca protein, mouse
  • Protein Kinase C-alpha