Placental Vascular Defects and Embryonic Lethality Triggered by TFPIα Deficiency in Factor V Leiden Mice

Arterioscler Thromb Vasc Biol. 2025 Jul;45(7):1266-1276. doi: 10.1161/ATVBAHA.125.322650. Epub 2025 May 22.

Abstract

Background: TFPI (tissue factor pathway inhibitor) inhibits the initiation of blood coagulation. TFPIα (TFPI alpha isoform), the only alternatively spliced TFPI isoform in platelets, is abundant in placenta and uniquely inhibits prothrombinase (FXa [activated factor X]-FVa [activated factor V]). This inhibitory activity is reduced when prothrombinase is assembled with FVL (factor V Leiden).

Methods: Effects of TFPIα (TfpiΔα) and platelet (Tfpifl; Pf4-Cre+) specific knockout alleles were characterized in FVL (F5L) mice to examine the physiological effects of the TFPIα-FV interaction.

Results: Genotype frequencies were assessed and revealed that Tfpi+/Δα F5L/L mice survive to adulthood. However, TfpiΔα homozygosity with even a single F5L allele resulted in embryonic lethality during mid-gestation development regardless of maternal FVL status. In contrast, F5L/L Tfpifl/fl Pf4-Cre+ mice were at expected frequencies at weaning, indicating that platelet TFPIα loss alone did not cause mid-gestation lethality in TfpiΔα/Δα F5L mice. Histological analyses showed no fibrin deposition in embryonic or extraembryonic tissues but revealed placental vasculature defects in TfpiΔα/Δα F5L genotypes. Treatment with the direct thrombin inhibitor dabigatran partially rescued the lethality and corrected placental defects, implicating excessive thrombin generation as a factor in TfpiΔα/Δα F5L demise.

Conclusions: These findings suggest that TFPIα and its inhibition of prothrombinase play an important role in placental angiogenesis and embryonic survival.

Keywords: angiogenesis; mice; placenta; pregnancy; thrombin.

MeSH terms

  • Animals
  • Blood Coagulation
  • Blood Platelets / metabolism
  • Disease Models, Animal
  • Factor V* / genetics
  • Factor V* / metabolism
  • Female
  • Fetal Death
  • Homozygote
  • Lipoproteins* / deficiency
  • Lipoproteins* / genetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phenotype
  • Placenta* / blood supply
  • Placenta* / metabolism
  • Pregnancy

Substances

  • Lipoproteins
  • Factor V
  • lipoprotein-associated coagulation inhibitor
  • factor V Leiden