Inhibition of ferrochelatase impairs vascular eNOS/NO and sGC/cGMP signaling

PLoS One. 2018 Jul 9;13(7):e0200307. doi: 10.1371/journal.pone.0200307. eCollection 2018.

Abstract

Ferrochelatase (FECH) is an enzyme necessary for heme synthesis, which is essential for maintaining normal functions of endothelial nitric oxide synthase (eNOS) and soluble guanylyl cyclase (sGC). We tested the hypothesis that inhibition of vascular FECH to attenuate heme synthesis downregulates eNOS and sGC expression, resulting in impaired NO/cGMP-dependent relaxation. To this end, isolated bovine coronary arteries (BCAs) were in vitro incubated without (as controls) or with N-methyl protoporphyrin (NMPP; 10(-5)-10(-7)M; a selective FECH antagonist) for 24 and 72 hours respectively. Tissue FECH activity, heme, nitrite/NO and superoxide levels were sequentially measured. Protein expression of FECH, eNOS and sGC was detected by western blot analysis. Vascular responses to various vasoactive agents were evaluated via isometric tension studies. Treatment of BCAs with NMPP initiated a time- and dose-dependent attenuation of FECH activity without changes in its protein expression, followed by significant reduction in the heme level. Moreover, ACh-induced relaxation and ACh-stimulated release of NO were significant reduced, associated with suppression of eNOS protein expression in NMPP-treated groups. Decreased relaxation to NO donor spermine-NONOate reached the statistical significance in BCAs incubated with NMPP for 72 hours, concomitantly with downregulation of sGCβ1 expression that was independent of heat shock protein 90 (HSP90), nor did it significantly affect BCA relaxation caused by BAY 58-2667 that activates sGC in the heme-deficiency. Neither vascular responses to non-NO/sGC-mediators nor production of superoxide was affected by NMPP-treatment. In conclusion, deletion of vascular heme production via inhibiting FECH elicits downregulation of eNOS and sGC expression, leading to an impaired NO-mediated relaxation in an oxidative stress-independent manner.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acetylcholine / pharmacology
  • Animals
  • Cattle
  • Coronary Vessels / drug effects*
  • Coronary Vessels / metabolism
  • Cyclic GMP / metabolism*
  • Dose-Response Relationship, Drug
  • Ferrochelatase / antagonists & inhibitors*
  • HSP90 Heat-Shock Proteins / metabolism
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase Type III / metabolism*
  • Protoporphyrins / pharmacology
  • Signal Transduction / drug effects*
  • Soluble Guanylyl Cyclase / metabolism*
  • Vasodilation / drug effects
  • Vasodilator Agents / pharmacology

Substances

  • HSP90 Heat-Shock Proteins
  • Protoporphyrins
  • Vasodilator Agents
  • Nitric Oxide
  • N-methylprotoporphyrin IX
  • Nitric Oxide Synthase Type III
  • Soluble Guanylyl Cyclase
  • Ferrochelatase
  • Cyclic GMP
  • Acetylcholine