Biology systems Dpt, University Alcalá (UAH), Madrid, Spain.
Pharmacology, Pharmacognosy and Botanics Dpt, Complutense University (UCM), Madrid, Spain.
Sci Rep. 2020 Mar 6;10(1):4190. doi: 10.1038/s41598-020-61014-1.
Epidemiological studies link long term exposure to xenoestrogen Bisphenol-A to adverse cardiovascular effects. Our previous results show that BPA induces hypertension by a mechanism involving CamKII activation and increased redox stress caused by eNOS uncoupling. Recently, CamKII sustained activation has been recognized as a central mediator of programmed cell death in cardiovascular diseases, including necroptosis. However, the role of necroptosis in cardiac response to BPA had not yet been explored. Mice exposed to BPA for 16 weeks showed altered heart function, electrical conduction, and increased blood pressure. Besides, a stress test showed ST-segment depression, indicative of cardiac ischemia. The hearts exhibited cardiac hypertrophy and reduced vascularization, interstitial edema, and large hemorrhagic foci accompanied by fibrinogen deposits. BPA initiated a cardiac inflammatory response, up-regulation of M1 macrophage polarization, and increased oxidative stress, coinciding with the increased expression of CamKII and the necroptotic effector RIP3. In addition, cell death was especially evident in coronary endothelial cells within hemorrhagic areas, and Evans blue extravasation indicated a vascular leak in response to Bisphenol-A. Consistent with the in vivo findings, BPA increased the necroptosis/apoptosis ratio, the expression of RIP3, and CamKII activation in endothelial cells. Necrostatin-1, an inhibitor of necroptosis, alleviated BPA induced cardiac dysfunction and prevented the inflammatory and hemorrhagic response in mice. Mechanistically, silencing of RIP3 reversed BPA-induced necroptosis and CamKII activation in endothelial cells, while inhibition of CamKII activation by KN-93 had no effect on RIP3 expression but decreased necroptotic cell death suggesting that BPA induced necroptosis is mediated by a RIP 3/CamKII dependent pathway. Our results reveal a novel pathogenic role of BPA on the coronary circulation. BPA induces endothelial cell necroptosis, promotes the weakening of coronary vascular wall, which caused internal ventricular hemorrhages, delaying the reparative process and ultimately leading to cardiac dysfunction.
流行病学研究将长期暴露于外源性雌激素双酚 A 与不良心血管效应联系起来。我们之前的研究结果表明,BPA 通过激活 CamKII 和引起 eNOS 解耦导致的氧化还原应激增加来诱导高血压。最近,CamKII 的持续激活已被认为是心血管疾病中程序性细胞死亡的中心介质,包括坏死性凋亡。然而,坏死性凋亡在心脏对 BPA 的反应中的作用尚未被探索。暴露于 BPA 16 周的小鼠表现出心脏功能、电传导改变和血压升高。此外,应激试验显示 ST 段压低,提示心肌缺血。心脏表现出心脏肥大和血管生成减少、间质水肿和大的出血灶,伴有纤维蛋白原沉积。BPA 引发心脏炎症反应、M1 巨噬细胞极化上调和氧化应激增加,同时 CamKII 和坏死性凋亡效应蛋白 RIP3 的表达增加。此外,在出血区域的冠状动脉内皮细胞中尤其明显的细胞死亡,伊文思蓝外渗表明对 Bisphenol-A 的血管渗漏。与体内发现一致,BPA 增加了内皮细胞中的坏死性凋亡/细胞凋亡比值、RIP3 的表达和 CamKII 的激活。坏死性凋亡抑制剂 Necrostatin-1 减轻了 BPA 诱导的心脏功能障碍,并防止了小鼠的炎症和出血反应。在机制上,沉默 RIP3 逆转了 BPA 诱导的内皮细胞坏死性凋亡和 CamKII 激活,而 KN-93 抑制 CamKII 激活对 RIP3 表达没有影响,但减少了坏死性细胞死亡,这表明 BPA 诱导的坏死性凋亡是通过 RIP3/CamKII 依赖途径介导的。我们的结果揭示了 BPA 对冠状动脉循环的新的致病作用。BPA 诱导内皮细胞坏死性凋亡,促进冠状动脉血管壁减弱,导致心室内部出血,延迟修复过程,最终导致心脏功能障碍。