Mice Lacking the Inhibitory Collagen Receptor LAIR-1 Exhibit a Mild Thrombocytosis and Hyperactive Platelets

Arterioscler Thromb Vasc Biol. 2017 May;37(5):823-835. doi: 10.1161/ATVBAHA.117.309253. Epub 2017 Mar 23.

Abstract

Objective: Leukocyte-associated immunoglobulin-like receptor-1 (LAIR-1) is a collagen receptor that belongs to the inhibitory immunoreceptor tyrosine-based inhibition motif-containing receptor family. It is an inhibitor of signaling via the immunoreceptor tyrosine-based activation motif-containing collagen receptor complex, glycoprotein VI-FcRγ-chain. It is expressed on hematopoietic cells, including immature megakaryocytes, but is not detectable on platelets. Although the inhibitory function of LAIR-1 has been described in leukocytes, its physiological role in megakaryocytes and in particular in platelet formation has not been explored. In this study, we investigate the role of LAIR-1 in megakaryocyte development and platelet production by generating LAIR-1-deficient mice.

Approach and results: Mice lacking LAIR-1 exhibit a significant increase in platelet counts, a prolonged platelet half-life in vivo, and increased proplatelet formation in vitro. Interestingly, platelets from LAIR-1-deficient mice exhibit an enhanced reactivity to collagen and the glycoprotein VI-specific agonist collagen-related peptide despite not expressing LAIR-1, and mice showed enhanced thrombus formation in the carotid artery after ferric chloride injury. Targeted deletion of LAIR-1 in mice results in an increase in signaling downstream of the glycoprotein VI-FcRγ-chain and integrin αIIbβ3 in megakaryocytes because of enhanced Src family kinase activity.

Conclusions: Findings from this study demonstrate that ablation of LAIR-1 in megakaryocytes leads to increased Src family kinase activity and downstream signaling in response to collagen that is transmitted to platelets, rendering them hyper-reactive specifically to agonists that signal through Syk tyrosine kinases, but not to G-protein-coupled receptors.

Keywords: LAIR-1; immunoreceptor tyrosine-based activation motif; immunoreceptor tyrosine-based inhibition motif; platelet hyperactivity, Src Family Kinase; thrombocytosis.

Publication types

  • Video-Audio Media
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Platelets / drug effects
  • Blood Platelets / metabolism*
  • Carrier Proteins / pharmacology
  • Cells, Cultured
  • Chlorides
  • Disease Models, Animal
  • Enzyme Activation
  • Ferric Compounds
  • Genetic Predisposition to Disease
  • Megakaryocytes / drug effects
  • Megakaryocytes / metabolism*
  • Mice, Knockout
  • Peptides / pharmacology
  • Phenotype
  • Platelet Activation* / drug effects
  • Platelet Glycoprotein GPIIb-IIIa Complex / metabolism
  • Platelet Membrane Glycoproteins / agonists
  • Platelet Membrane Glycoproteins / metabolism
  • Receptors, IgG / blood
  • Receptors, Immunologic / deficiency*
  • Receptors, Immunologic / genetics
  • Signal Transduction / drug effects
  • Thrombocytosis / blood*
  • Thrombocytosis / genetics
  • Thrombosis / blood*
  • Thrombosis / chemically induced
  • Thrombosis / genetics
  • src-Family Kinases / blood

Substances

  • Carrier Proteins
  • Chlorides
  • Ferric Compounds
  • Peptides
  • Platelet Glycoprotein GPIIb-IIIa Complex
  • Platelet Membrane Glycoproteins
  • Receptors, IgG
  • Receptors, Immunologic
  • collagen-related peptide
  • leukocyte-associated immunoglobulin-like receptor 1
  • platelet membrane glycoprotein VI
  • src-Family Kinases
  • ferric chloride