Sphingosine 1-Phosphate Produced by Sphingosine Kinase 2 Intrinsically Controls Platelet Aggregation In Vitro and In Vivo

Circ Res. 2015 Jul 31;117(4):376-87. doi: 10.1161/CIRCRESAHA.115.306901. Epub 2015 Jun 30.

Abstract

Rationale: Platelets are known to play a crucial role in hemostasis. Sphingosine kinases (Sphk) 1 and 2 catalyze the conversion of sphingosine to the bioactive metabolite sphingosine 1-phosphate (S1P). Although platelets are able to secrete S1P on activation, little is known about a potential intrinsic effect of S1P on platelet function.

Objective: To investigate the role of Sphk1- and Sphk2-derived S1P in the regulation of platelet function.

Methods and results: We found a 100-fold reduction in intracellular S1P levels in platelets derived from Sphk2(-/-) mutants compared with Sphk1(-/-) or wild-type mice, as analyzed by mass spectrometry. Sphk2(-/-) platelets also failed to secrete S1P on stimulation. Blood from Sphk2-deficient mice showed decreased aggregation after protease-activated receptor 4-peptide and adenosine diphosphate stimulation in vitro, as assessed by whole blood impedance aggregometry. We revealed that S1P controls platelet aggregation via the sphingosine 1-phosphate receptor 1 through modulation of protease-activated receptor 4-peptide and adenosine diphosphate-induced platelet activation. Finally, we show by intravital microscopy that defective platelet aggregation in Sphk2-deficient mice translates into reduced arterial thrombus stability in vivo.

Conclusions: We demonstrate that Sphk2 is the major Sphk isoform responsible for the generation of S1P in platelets and plays a pivotal intrinsic role in the control of platelet activation. Correspondingly, Sphk2-deficient mice are protected from arterial thrombosis after vascular injury, but have normal bleeding times. Targeting this pathway could therefore present a new therapeutic strategy to prevent thrombosis.

Keywords: blood platelets; platelet aggregation; sphingosine 1-phosphate; sphingosine kinase; thrombosis.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arachidonic Acid / blood
  • Blood Coagulation
  • Blood Coagulation Tests
  • Blood Platelets / enzymology*
  • Carotid Artery Injuries / blood
  • Carotid Artery Injuries / enzymology
  • Disease Models, Animal
  • Erythrocytes / enzymology
  • Lysophospholipids / blood*
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phosphotransferases (Alcohol Group Acceptor) / blood*
  • Phosphotransferases (Alcohol Group Acceptor) / deficiency
  • Phosphotransferases (Alcohol Group Acceptor) / genetics
  • Platelet Adhesiveness
  • Platelet Aggregation*
  • Platelet Function Tests
  • Receptors, Lysosphingolipid / blood
  • Signal Transduction
  • Sphingosine / analogs & derivatives*
  • Sphingosine / blood
  • Sphingosine-1-Phosphate Receptors
  • Thrombosis / blood
  • Thrombosis / enzymology
  • Thrombosis / prevention & control
  • Thromboxane A2 / blood
  • Vascular System Injuries / blood
  • Vascular System Injuries / enzymology

Substances

  • Lysophospholipids
  • Receptors, Lysosphingolipid
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • sphingosine 1-phosphate
  • Arachidonic Acid
  • Thromboxane A2
  • Phosphotransferases (Alcohol Group Acceptor)
  • sphingosine kinase
  • Sphingosine