Department of Pediatrics, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Blood. 2011 Jun 9;117(23):6326-37. doi: 10.1182/blood-2010-08-304915. Epub 2011 Mar 24.
Thrombin is a positive mediator of thrombus formation through the proteolytic activation of protease-activated receptors (PARs), fibrinogen, factor XI (fXI), and other substrates, and a negative regulator through activation of protein C, a natural anticoagulant with anti-inflammatory/cytoprotective properties. Protease-engineering studies have established that 2 active-site substitutions, W215A and E217A (fII(WE)), result in dramatically reduced catalytic efficiency with procoagulant substrates while largely preserving thrombomodulin (TM)-dependent protein C activation. To explore the hypothesis that a prothrombin variant favoring antithrombotic pathways would be compatible with development but limit inflammatory processes in vivo, we generated mice carrying the fII(WE) mutations within the endogenous prothrombin gene. Unlike fII-null embryos, fII(WE/WE) mice uniformly developed to term. Nevertheless, these mice ultimately succumbed to spontaneous bleeding events shortly after birth. Heterozygous fII(WT/WE) mice were viable and fertile despite a shift toward an antithrombotic phenotype exemplified by prolonged tail-bleeding times and times-to-occlusion after FeCl₃ vessel injury. More interestingly, prothrombin(WE) expression significantly ameliorated the development of inflammatory joint disease in mice challenged with collagen-induced arthritis (CIA). The administration of active recombinant thrombin(WE) also suppressed the development of CIA in wild-type mice. These studies provide a proof-of-principle that pro/thrombin variants engineered with altered substrate specificity may offer therapeutic opportunities for limiting inflammatory disease processes.
凝血酶通过蛋白水解激活蛋白酶激活受体 (PARs)、纤维蛋白原、因子 XI (fXI) 和其他底物,是血栓形成的正向调节剂,同时通过激活蛋白 C(具有抗炎/细胞保护特性的天然抗凝剂),又是其负调节剂。蛋白酶工程研究表明,2 个活性位点取代 W215A 和 E217A(fII(WE))导致促凝底物的催化效率显著降低,而血栓调节蛋白(TM)依赖性蛋白 C 激活则基本保留。为了验证这样一个假说,即有利于抗血栓形成途径的凝血酶原变体与发育相容但会限制体内炎症过程,我们在内源性凝血酶原基因中产生了携带 fII(WE)突变的小鼠。与 fII 缺失胚胎不同,fII(WE/WE) 小鼠均匀发育至足月。然而,这些小鼠最终在出生后不久因自发性出血事件而死亡。杂合子 fII(WT/WE) 小鼠具有活力和繁殖力,尽管它们表现出抗血栓形成表型的转变,如尾巴出血时间延长和 FeCl₃血管损伤后的闭塞时间延长。更有趣的是,凝血酶原(WE)表达显著改善了胶原诱导关节炎 (CIA) 小鼠炎症性关节疾病的发展。活性重组凝血酶原(WE)的给药也抑制了野生型小鼠 CIA 的发展。这些研究提供了一个原理性证明,即具有改变的底物特异性的凝血酶原/凝血酶变体可能为限制炎症性疾病过程提供治疗机会。