CalDAG-GEFI is at the nexus of calcium-dependent platelet activation

Blood. 2009 Sep 17;114(12):2506-14. doi: 10.1182/blood-2009-04-218768. Epub 2009 Jul 23.

Abstract

The importance of the second messengers calcium (Ca(2+)) and diacylglycerol (DAG) in platelet signal transduction was established more than 30 years ago. Whereas protein kinase C (PKC) family members were discovered as the targets of DAG, little is known about the molecular identity of the main Ca(2+) sensor(s). We here identify Ca(2+) and DAG-regulated guanine nucleotide exchange factor I (CalDAG-GEFI) as a critical molecule in Ca(2+)-dependent platelet activation. CalDAG-GEFI, through activation of the small GTPase Rap1, directly triggers integrin activation and extracellular signal-regulated kinase-dependent thromboxane A(2) (TxA(2)) release. CalDAG-GEFI-dependent TxA(2) generation provides crucial feedback for PKC activation and granule release, particularly at threshold agonist concentrations. PKC/P2Y12 signaling in turn mediates a second wave of Rap1 activation, necessary for sustained platelet activation and thrombus stabilization. Our results lead to a revised model for platelet activation that establishes one molecule, CalDAG-GEFI, at the nexus of Ca(2+)-induced integrin activation, TxA(2) generation, and granule release. The preferential activation of CalDAG-GEFI over PKC downstream of phospholipase C activation, and the different kinetics of CalDAG-GEFI- and PKC/P2Y12-mediated Rap1 activation demonstrate an unexpected complexity to the platelet activation process, and they challenge the current model that DAG/PKC-dependent signaling events are crucial for the initiation of platelet adhesion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Diphosphate / metabolism
  • Animals
  • Blood Platelets / metabolism
  • Blotting, Western
  • Calcium / metabolism*
  • Cell Proliferation / drug effects
  • Collagen / metabolism
  • Diglycerides / metabolism*
  • Female
  • Flow Cytometry
  • Guanine Nucleotide Exchange Factors / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitogen-Activated Protein Kinases / metabolism
  • Phosphorylation / drug effects
  • Platelet Activation / physiology*
  • Platelet Membrane Glycoproteins / physiology
  • Serotonin / metabolism
  • Thromboxane A2 / metabolism
  • rap1 GTP-Binding Proteins / metabolism

Substances

  • 1,2-diacylglycerol
  • Diglycerides
  • Guanine Nucleotide Exchange Factors
  • Platelet Membrane Glycoproteins
  • platelet membrane glycoprotein VI
  • Serotonin
  • Thromboxane A2
  • Adenosine Diphosphate
  • Collagen
  • Mitogen-Activated Protein Kinases
  • rap1 GTP-Binding Proteins
  • Calcium