Department of Immunobiology, College of Life Science and Technology, Jinan University, Guangzhou, 510632, China.
Department of Nephrology, the First Affiliated Hospital of Jinan University, Guangzhou, 510630, China.
Inflammation. 2024 Feb;47(1):285-306. doi: 10.1007/s10753-023-01909-z. Epub 2023 Sep 27.
Itaconate is an unsaturated dicarboxylic acid that is derived from the decarboxylation of the Krebs cycle intermediate cis-aconitate and has been shown to exhibit anti-inflammatory and anti-bacterial/viral properties. But the mechanisms underlying itaconate's anti-inflammatory activities are not fully understood. Necroptosis, a lytic form of regulated cell death (RCD), is mediated by receptor-interacting protein kinase 1 (RIPK1), RIPK3, and mixed lineage kinase domain-like protein (MLKL) signaling. It has been involved in the pathogenesis of organ injury in many inflammatory diseases. In this study, we aimed to explore whether itaconate and its derivatives can inhibit necroptosis in murine macrophages, a mouse MPC-5 cell line and a human HT-29 cell line in response to different necroptotic activators. Our results showed that itaconate and its derivatives dose-dependently inhibited necroptosis, among which dimethyl itaconate (DMI) was the most effective one. Mechanistically, itaconate and its derivatives inhibited necroptosis by suppressing the RIPK1/RIPK3/MLKL signaling and the oligomerization of MLKL. Furthermore, DMI promoted the nuclear translocation of Nrf2 that is a critical regulator of intracellular redox homeostasis, and reduced the levels of intracellular reactive oxygen species (ROS) and mitochondrial superoxide (mtROS) that were induced by necroptotic activators. Consistently, DMI prevented the loss of mitochondrial membrane potential induced by the necroptotic activators. In addition, DMI mitigated caerulein-induced acute pancreatitis in mice accompanied by reduced activation of the necroptotic signaling in vivo. Collectively, our study demonstrates that itaconate and its derivatives can inhibit necroptosis by suppressing the RIPK1/RIPK3/MLKL signaling, highlighting their potential applications for treating necroptosis-associated diseases.
衣康酸是一种不饱和二羧酸,来源于克雷布斯循环中间产物顺式乌头酸的脱羧,具有抗炎和抗细菌/病毒特性。但是,衣康酸抗炎活性的机制尚未完全阐明。细胞程序性坏死(necroptosis),一种溶酶体依赖性的调控细胞死亡(regulated cell death,RCD)形式,由受体相互作用蛋白激酶 1(receptor-interacting protein kinase 1,RIPK1)、RIPK3 和混合谱系激酶结构域样蛋白(mixed lineage kinase domain-like protein,MLKL)信号通路介导。它参与了许多炎症性疾病中器官损伤的发病机制。在这项研究中,我们旨在探讨衣康酸及其衍生物是否可以抑制不同的细胞程序性坏死激活剂诱导的小鼠巨噬细胞、小鼠 MPC-5 细胞系和人 HT-29 细胞系中的细胞程序性坏死。我们的结果表明,衣康酸及其衍生物呈剂量依赖性抑制细胞程序性坏死,其中二甲基衣康酸(dimethyl itaconate,DMI)最为有效。在机制上,衣康酸及其衍生物通过抑制 RIPK1/RIPK3/MLKL 信号通路和 MLKL 的寡聚化来抑制细胞程序性坏死。此外,DMI 促进了核内易位的核因子红细胞 2 相关因子 2(nuclear factor erythroid 2-related factor 2,Nrf2)的发生,Nrf2 是细胞内氧化还原平衡的关键调节剂,并降低了细胞内活性氧(reactive oxygen species,ROS)和线粒体超氧化物(mitochondrial superoxide,mtROS)的水平,这些水平是由细胞程序性坏死激活剂诱导的。一致地,DMI 防止了细胞程序性坏死激活剂诱导的线粒体膜电位的丧失。此外,DMI 减轻了雨蛙肽诱导的急性胰腺炎,同时体内细胞程序性坏死信号的激活减少。总之,我们的研究表明,衣康酸及其衍生物可以通过抑制 RIPK1/RIPK3/MLKL 信号通路来抑制细胞程序性坏死,这突出了它们在治疗细胞程序性坏死相关疾病方面的潜在应用。