ADP-stimulated activation of Akt during integrin outside-in signaling promotes platelet spreading by inhibiting glycogen synthase kinase-3β

Arterioscler Thromb Vasc Biol. 2012 Sep;32(9):2232-40. doi: 10.1161/ATVBAHA.112.254680. Epub 2012 Jul 19.

Abstract

Objective: Integrins mediate platelet adhesion and transmit outside-in signals leading to platelet spreading. Phosphoinositide 3-kinases (PI3Ks) play a critical role in outside-in signaling and platelet spreading; however, the mechanisms of PI3K activation and function in outside-in signaling are unclear. We sought to determine the role of the Akt family of serine/threonine kinases and activation mechanisms of the PI3K/Akt pathway in outside-in signaling.

Methods and results: Akt inhibitors and Akt3 knockout inhibited platelet spreading on fibrinogen, indicating that Akt is important in integrin outside-in signaling. Akt inhibitors and Akt3 knockout also diminished integrin-dependent phosphorylation of glycogen synthase kinase-3β. Inhibition of glycogen synthase kinase-3β reversed the inhibitory effects of Akt3 knockout and inhibitors of Akt or PI3K on platelet spreading, indicating that glycogen synthase kinase-3β is a downstream target of Akt in outside-in signaling. Integrin-dependent activation of the PI3K-Akt pathway requires Src family kinase. Akt phosphorylation is also significantly inhibited in ADP receptor P2Y12 knockout platelets and further inhibited in P2Y12 knockout platelets treated with a P2Y1 antagonist. Consistently, P2Y12 knockout and P2Y1 inhibition together reduced platelet spreading.

Conclusions: These results demonstrate that integrin outside-in signaling and platelet spreading requires Src family kinase-dependent and ADP receptor-amplified activation of the PI3K-Akt-GSK-3β pathway.

Publication types

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

MeSH terms

  • Adenosine Diphosphate / metabolism*
  • Animals
  • Blood Platelets / drug effects
  • Blood Platelets / enzymology*
  • Cell Shape* / drug effects
  • Enzyme Activation
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors
  • Glycogen Synthase Kinase 3 / metabolism*
  • Glycogen Synthase Kinase 3 beta
  • Humans
  • Integrins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphorylation
  • Platelet Activation* / drug effects
  • Protein Kinase Inhibitors / pharmacology
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / deficiency
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Purinergic P2Y Receptor Antagonists / pharmacology
  • Receptors, Purinergic P2Y1 / drug effects
  • Receptors, Purinergic P2Y1 / metabolism
  • Receptors, Purinergic P2Y12 / drug effects
  • Receptors, Purinergic P2Y12 / genetics
  • Receptors, Purinergic P2Y12 / metabolism
  • Signal Transduction* / drug effects
  • Time Factors
  • src-Family Kinases / metabolism

Substances

  • Integrins
  • P2RY12 protein, human
  • P2ry12 protein, mouse
  • Protein Kinase Inhibitors
  • Purinergic P2Y Receptor Antagonists
  • Receptors, Purinergic P2Y1
  • Receptors, Purinergic P2Y12
  • Adenosine Diphosphate
  • Phosphatidylinositol 3-Kinases
  • src-Family Kinases
  • Akt1 protein, mouse
  • Akt2 protein, mouse
  • Akt3 protein, mouse
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Gsk3b protein, mouse
  • Proto-Oncogene Proteins c-akt
  • Glycogen Synthase Kinase 3