ITAM receptor-mediated generation of reactive oxygen species in human platelets occurs via Syk-dependent and Syk-independent pathways

J Thromb Haemost. 2012 Jun;10(6):1133-41. doi: 10.1111/j.1538-7836.2012.04734.x.

Abstract

Background: Ligation of the platelet-specific collagen receptor, GPVI/FcRγ, causes rapid, transient disulfide-dependent homodimerization, and the production of intracellular reactive oxygen species (ROS) generated by the NADPH oxidase, linked to GPVI via TRAF4.

Objectives: The aim of this study was to evaluate the role of early signaling events in ROS generation following engagement of either GPVI/FcRγ or a second immunoreceptor tyrosine-based activation motif (ITAM)-containing receptor on platelets, FcγRIIa.

Methods and results: Using an H(2) DCF-DA-based flow cytometric assay to measure intracellular ROS, we show that treatment of platelets with either the GPVI agonists, collagen-related peptide (CRP) or convulxin (Cvx), or the FcγRIIa agonist 14A2, increased intraplatelet ROS; other platelet agonists such as ADP and TRAP did not. Basal ROS in platelet-rich plasma from 14 healthy donors displayed little inter-individual variability. CRP, Cvx or 14A2 induced an initial burst of ROS within 2 min followed by additional ROS reaching a plateau after 15-20 min. The Syk inhibitor BAY61-3606, which blocks ITAM-dependent signaling, had no effect on the initial ROS burst, but completely inhibited the second phase.

Conclusions: Together, these results show for the first time that ROS generation downstream of GPVI or FcγRIIa consists of two distinct phases: an initial Syk-independent burst followed by additional Syk-dependent generation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Blood Platelets / drug effects
  • Blood Platelets / enzymology*
  • Carrier Proteins / pharmacology
  • Crotalid Venoms / pharmacology
  • Enzyme Activation
  • Female
  • Flow Cytometry
  • Humans
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Lectins, C-Type
  • Male
  • Niacinamide / analogs & derivatives
  • Niacinamide / pharmacology
  • Peptides / pharmacology
  • Platelet Membrane Glycoproteins / agonists
  • Platelet Membrane Glycoproteins / metabolism*
  • Protein Kinase Inhibitors / pharmacology
  • Protein Structure, Tertiary
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Protein-Tyrosine Kinases / metabolism*
  • Pyrimidines / pharmacology
  • Reactive Oxygen Species / metabolism*
  • Receptors, IgG / agonists
  • Receptors, IgG / metabolism*
  • Signal Transduction* / drug effects
  • Syk Kinase
  • Time Factors

Substances

  • 2-(7-(3,4-dimethoxyphenyl)imidazo(1,2-c)pyrimidin-5-ylamino)nicotinamide
  • Carrier Proteins
  • Crotalid Venoms
  • Fc gamma receptor IIA
  • Intracellular Signaling Peptides and Proteins
  • Lectins, C-Type
  • Peptides
  • Platelet Membrane Glycoproteins
  • Protein Kinase Inhibitors
  • Pyrimidines
  • Reactive Oxygen Species
  • Receptors, IgG
  • collagen-related peptide
  • platelet membrane glycoprotein VI
  • Niacinamide
  • convulxin
  • Protein-Tyrosine Kinases
  • SYK protein, human
  • Syk Kinase