Inherited human gp91phox deficiency is associated with impaired isoprostane formation and platelet dysfunction

Arterioscler Thromb Vasc Biol. 2011 Feb;31(2):423-34. doi: 10.1161/ATVBAHA.110.217885. Epub 2010 Nov 11.

Abstract

Object: Platelet isoprostane 8-ISO-prostaglandin F2α (8-iso-PGF2α), a proaggregating molecule, is believed to derive from nonenzymatic oxidation of arachidonic acid. We hypothesized that NADPH is implicated in isoprostane formation and platelet activation.

Methods and results: We studied 8-iso-PGF2α in platelets from 8 male patients with hereditary deficiency of gp91(phox), the catalytic subunit of NADPH oxidase, and 8 male controls. On stimulation, platelets from controls produced 8-iso-PGF2α, which was inhibited -8% by aspirin and -58% by a specific inhibitor of gp91(phox). Platelets from patients with gp91(phox) hereditary deficiency had normal thromboxane A(2) formation but marked 8-iso-PGF2α reduction compared with controls. In normal platelets incubated with a gp91(phox) inhibitor or with SQ29548, a thromboxane A(2)/isoprostane receptor inhibitor, platelet recruitment, an in vitro model of thrombus growth, was reduced by 44% and 64%, respectively; a lower effect (-17%) was seen with aspirin. Moreover, thrombus formation under shear stress (blood perfusion at the wall shear rate of 1500 s(-1)) was reduced in samples in which isoprostane formation was inhibited by NADPH oxidase inhibitors. In gp91(phox)-deficient patients, agonist-induced platelet aggregation was within the normal range, whereas platelet recruitment was reduced compared with controls. Incubation of platelets from gp91(phox)-deficient patients with 8-iso-PGF2α dose-dependently (1 to 100 pmol/L) increased platelet recruitment by mobilizing platelet Ca(2+) and activating gpIIb/IIIa; a further increase in platelet recruitment was detected by platelet coincubation with l-NAME, an inhibitor of NO synthase.

Conclusions: This study provides the first evidence that platelet 8-iso-PGF2α maximally derives from gp91(phox) activation and contributes to platelet recruitment via activation of gpIIb/IIIa.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aspirin / pharmacology
  • Blood Platelets / cytology
  • Blood Platelets / drug effects
  • Blood Platelets / metabolism*
  • Calcium / metabolism
  • Case-Control Studies
  • Deficiency Diseases / metabolism*
  • Deficiency Diseases / pathology
  • Dinoprost / analogs & derivatives
  • Dinoprost / pharmacology
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Isoprostanes / metabolism*
  • Male
  • Membrane Glycoproteins / antagonists & inhibitors
  • Membrane Glycoproteins / deficiency*
  • Membrane Glycoproteins / genetics
  • NADP / metabolism
  • NADPH Oxidase 2
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / deficiency*
  • NADPH Oxidases / genetics
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Platelet Aggregation Inhibitors / pharmacology
  • Platelet Glycoprotein GPIIb-IIIa Complex / metabolism

Substances

  • Enzyme Inhibitors
  • Isoprostanes
  • Membrane Glycoproteins
  • Platelet Aggregation Inhibitors
  • Platelet Glycoprotein GPIIb-IIIa Complex
  • 8-epi-prostaglandin F2alpha
  • NADP
  • Dinoprost
  • Nitric Oxide Synthase
  • CYBB protein, human
  • NADPH Oxidase 2
  • NADPH Oxidases
  • Aspirin
  • Calcium
  • NG-Nitroarginine Methyl Ester