Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK; and.
Department of Biochemistry and Molecular Biology, University of Oklahoma Health Sciences Center, Oklahoma City, OK.
Blood Adv. 2022 Feb 8;6(3):931-945. doi: 10.1182/bloodadvances.2021005836.
Plasmodium falciparum-derived histidine-rich protein II (HRPII) has been shown to inhibit heparin-dependent anticoagulant activity of antithrombin (AT) and induce inflammation in vitro and in vivo. In a recent study, we showed that HRPII interacts with the AT-binding vascular glycosaminoglycans (GAGs) not only to disrupt the barrier-permeability function of endothelial cells but also to inhibit the antiinflammatory signaling function of AT. Here we investigated the mechanisms of the proinflammatory function of HRPII and the protective activity of AT in cellular and animal models. We found that AT competitively inhibits the GAG-dependent HRPII-mediated activation of NF-κB and expression of intercellular cell adhesion molecule 1 (ICAM1) in endothelial cells. Furthermore, AT inhibits HRPII-mediated histone H3 citrullination and neutrophil extracellular trap (NET) formation in HL60 cells and freshly isolated human neutrophils. In vivo, HRPII induced Mac1 expression on blood neutrophils, MPO release in plasma, neutrophil infiltration, and histone H3 citrullination in the lung tissues. HRPII also induced endothelial cell activation as measured by increased ICAM1 expression and elevated vascular permeability in the lungs. AT effectively inhibited HRPII-mediated neutrophil infiltration, NET formation, and endothelial cell activation in vivo. AT also inhibited HRPII-meditated deposition of platelets and fibrin(ogen) in the lungs and circulating level of von Willebrand factor in the plasma. We conclude that AT exerts protective effects against pathogenic effects of P falciparum-derived HRPII in both cellular and animal models.
疟原虫衍生的组氨酸丰富蛋白 II(HRPII)已被证明可抑制抗凝血酶(AT)的肝素依赖性抗凝活性,并在体外和体内诱导炎症。在最近的一项研究中,我们表明 HRPII 不仅与 AT 结合的血管糖胺聚糖(GAG)相互作用以破坏内皮细胞的屏障通透性功能,还抑制 AT 的抗炎信号功能。在这里,我们研究了 HRPII 的促炎功能和 AT 在细胞和动物模型中的保护活性的机制。我们发现 AT 竞争性抑制 GAG 依赖性 HRPII 介导的 NF-κB 激活和内皮细胞中细胞间黏附分子 1(ICAM1)的表达。此外,AT 抑制 HRPII 介导的 HL60 细胞和新鲜分离的人嗜中性粒细胞中的组蛋白 H3 瓜氨酸化和中性粒细胞胞外陷阱(NET)形成。在体内,HRPII 诱导血液中性粒细胞上的 Mac1 表达、血浆中 MPO 的释放、中性粒细胞浸润以及肺组织中的组蛋白 H3 瓜氨酸化。HRPII 还诱导内皮细胞激活,如肺组织中 ICAM1 表达增加和血管通透性升高。AT 在体内有效抑制 HRPII 介导的中性粒细胞浸润、NET 形成和内皮细胞激活。AT 还抑制 HRPII 介导的血小板和纤维蛋白原(原)在肺中的沉积以及血浆中血管性血友病因子的循环水平。我们得出结论,AT 在细胞和动物模型中均对疟原虫衍生的 HRPII 的致病作用发挥保护作用。