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Mathematical model of coagulation under flow: understanding the role of cell surfaces for inhibition and a clinical application

Miyazawa, Kenji
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2023
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Abstract
Coagulation is a self-defense mechanism to stop the bleeding at an injury site. The process involves an intricate biochemical reaction network that is balanced by pro-coagulant and anti-coagulant factors. Natural coagulation inhibitors, tissue factor pathway inhibitor (TFPI) and antithrombin (AT) effectively inhibit coagulation and thus have been identified as potential therapeutic targets for bleeding disorders and other clinical applications. However, due to the complexity of the coagulation network, biochemical experiments alone are not sufficient to provide insights into the hidden mechanisms of coagulation inhibitors in a cost-efficient and timely manner. Mathematical models are powerful tool to assess how thrombin, the main enzyme generated in coagulation, is altered under different conditions and can unveil non-intuitive mechanisms underlying the behavior. In this dissertation, we address two questions using mathematical models: 1) how do the TFPI and AT-mediated inhibitory reactions on platelet surfaces affect the coagulation system under flow? And 2) how cell surfaces can be important for the mechanism of actions of a treatment for hemophilia A, a genetic disorder characterized with inability to form a strong clot? Platelet surfaces are essential for the formation of pro-coagulant complexes that regulate the positive feedback of coagulation. However, whether platelet surfaces are also important for inhibition is not fully understood. Therefore, one motivation for this study is to mathematically investigate how platelet surface-mediated inhibitory reactions will impede thrombin production. An experimentally validated mathematical model of coagulation under flow was extended with known and newly found biochemical inhibitory reaction network mediated by TFPI and AT. Simulation results revealed that platelet surfaces play an important role for efficient inhibition by TFPI and AT, and TFPI was identified as potential therapeutic target to recover thrombin generation. This result motivated us to further apply this model in context of hemophilia A blood, and to investigate the mechanisms of action of a specific drug being developed for hemophilia A treatment. The clinical application of this model provided proof of concept of the drug’s mechanisms of actions. Simulation results demonstrated that in addition to the platelet surfaces, endothelial and subendothelial surfaces are also key regulators of coagulation.
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