A mouse model of the protease-activated receptor 4 Pro310Leu variant has reduced platelet reactivity

J Thromb Haemost. 2024 Jun;22(6):1715-1726. doi: 10.1016/j.jtha.2024.03.004. Epub 2024 Mar 19.

Abstract

Background: Protease-activated receptor 4 (PAR4) mediates thrombin signaling on platelets and other cells. Our recent structural studies demonstrated that a single nucleotide polymorphism in extracellular loop 3 and PAR4-P310L (rs2227376) leads to a hyporeactive receptor.

Objectives: The goal of this study was to determine how the hyporeactive PAR4 variant in extracellular loop 3 impacts platelet function in vivo using a novel knock-in mouse model (PAR4-322L).

Methods: A point mutation was introduced into the PAR4 gene F2rl3 via CRISPR/Cas9 to create PAR4-P322L, the mouse homolog to human PAR4-P310L. Platelet response to PAR4 activation peptide (AYPGKF), thrombin, ADP, and convulxin was monitored by αIIbβ3 integrin activation and P-selectin translocation using flow cytometry or platelet aggregation. In vivo responses were determined by the tail bleeding assay and the ferric chloride-induced carotid artery injury model.

Results: PAR4-P/L and PAR4-L/L platelets had a reduced response to AYPGKF and thrombin measured by P-selectin translocation or αIIbβ3 activation. The response to ADP and convulxin was unchanged among genotypes. In addition, both PAR4-P/L and PAR4-L/L platelets showed a reduced response to thrombin in aggregation studies. There was an increase in the tail bleeding time for PAR4-L/L mice. The PAR4-P/L and PAR4-L/L mice both showed an extended time to arterial thrombosis.

Conclusion: PAR4-322L significantly reduced platelet responsiveness to AYPGKF and thrombin, which is in agreement with our previous structural and cell signaling studies. In addition, PAR4-322L had prolonged arterial thrombosis time. Our mouse model provides a foundation to further evaluate the role of PAR4 in other pathophysiological contexts.

Keywords: animal model; blood platelets; protease-activated receptor 4; single nucleotide polymorphisms; thrombin receptor.

MeSH terms

  • Adenosine Diphosphate / metabolism
  • Adenosine Diphosphate / pharmacology
  • Animals
  • Blood Platelets* / metabolism
  • CRISPR-Cas Systems
  • Chlorides
  • Crotalid Venoms / pharmacology
  • Crotalid Venoms / toxicity
  • Disease Models, Animal
  • Ferric Compounds
  • Gene Knock-In Techniques
  • Humans
  • Lectins, C-Type
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Oligopeptides
  • P-Selectin / genetics
  • P-Selectin / metabolism
  • Phenotype
  • Platelet Activation
  • Platelet Aggregation*
  • Platelet Glycoprotein GPIIb-IIIa Complex* / genetics
  • Platelet Glycoprotein GPIIb-IIIa Complex* / metabolism
  • Point Mutation
  • Receptors, Proteinase-Activated
  • Receptors, Thrombin* / genetics
  • Receptors, Thrombin* / metabolism
  • Signal Transduction
  • Thrombin* / metabolism
  • Thrombosis / blood
  • Thrombosis / genetics

Substances

  • Receptors, Thrombin
  • Thrombin
  • Platelet Glycoprotein GPIIb-IIIa Complex
  • alanyl-tyrosyl-prolyl-glycyl-lysyl-phenylalanine
  • protease-activated receptor 4, mouse
  • convulxin
  • protease-activated receptor 4
  • Crotalid Venoms
  • Adenosine Diphosphate
  • P-Selectin
  • ferric chloride
  • Chlorides
  • Ferric Compounds
  • Oligopeptides
  • Lectins, C-Type
  • Receptors, Proteinase-Activated