Factor Xa activation of factor V is of paramount importance in initiating the coagulation system: lessons from a tick salivary protein

Circulation. 2013 Jul 16;128(3):254-66. doi: 10.1161/CIRCULATIONAHA.113.003191. Epub 2013 Jul 1.

Abstract

Background: Generation of active procoagulant cofactor factor Va (FVa) and its subsequent association with the enzyme activated factor X (FXa) to form the prothrombinase complex is a pivotal initial event in blood coagulation and has been the subject of investigative effort, speculation, and controversy. The current paradigm assumes that FV activation is initiated by limited proteolysis by traces of (meizo) thrombin.

Methods and results: Recombinant tick salivary protein TIX-5 was produced and anticoagulant properties were studied with the use of plasma, whole blood, and purified systems. Here, we report that TIX-5 specifically inhibits FXa-mediated FV activation involving the B domain of FV and show that FXa activation of FV is pivotal for plasma and blood clotting. Accordingly, tick feeding is impaired on TIX-5 immune rabbits, displaying the in vivo importance of TIX-5.

Conclusions: Our data elucidate a unique molecular mechanism by which ticks inhibit the host's coagulation system. From our data, we propose a revised blood coagulation scheme in which direct FXa-mediated FV activation occurs in the initiation phase during which thrombin-mediated FV activation is restrained by fibrinogen and inhibitors.

Keywords: anticoagulants; blood coagulation; ticks.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anticoagulants / blood
  • Anticoagulants / chemistry
  • Anticoagulants / pharmacology*
  • Arthropod Proteins / chemistry
  • Arthropod Proteins / genetics
  • Arthropod Proteins / pharmacology*
  • Blood Coagulation / drug effects*
  • Blood Coagulation / physiology
  • Blood Coagulation Tests
  • Dose-Response Relationship, Drug
  • Factor V / antagonists & inhibitors
  • Factor V / metabolism*
  • Factor Xa / metabolism*
  • Factor Xa Inhibitors
  • Feeding Behavior
  • Fibrinogen / metabolism
  • Humans
  • Ixodes / chemistry
  • Ixodes / genetics
  • Ixodes / physiology
  • Mutagenesis
  • Protein Structure, Tertiary
  • Rabbits
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / pharmacology
  • Salivary Proteins and Peptides / chemistry
  • Salivary Proteins and Peptides / genetics
  • Salivary Proteins and Peptides / pharmacology*
  • Surface Plasmon Resonance
  • Thrombin / metabolism

Substances

  • Anticoagulants
  • Arthropod Proteins
  • Factor Xa Inhibitors
  • Recombinant Proteins
  • Salivary Proteins and Peptides
  • TIX-5 protein, tick
  • Factor V
  • Fibrinogen
  • Thrombin
  • Factor Xa