Ng Hang Pong, Zafar Atif, Diamond-Zaluski Rachel, Kim Gun-Dong, Bhat Kartik, Meadows Owen, Pantra Yashwant, Chan E Ricky, Smith Jonathan D, Mahabeleshwar Ganapati H
Department of Pathology, Case Western Reserve University School of Medicine, Cleveland, Ohio.
Institute for Computational Biology, Case Western Reserve University School of Medicine, Cleveland, Ohio.
Am J Pathol. 2025 Sep;195(9):1719-1735. doi: 10.1016/j.ajpath.2025.05.014. Epub 2025 Jun 18.
A hallmark event in the development of atherosclerotic plaque is the accumulation of lipid-laden macrophages in the subendothelial layers of affected blood vessels. Macrophages are key players in all stages of atherogenesis, including plaque initiation, growth, and rupture, as well as healing of ruptured plaques. In this context, macrophages are the principal innate immune cells that modulate atherogenesis by engaging in various processes, such as inflammation, extracellular matrix degradation, phagocytosis, and efferocytosis. In the current study, Kruppel-like transcription factor 6 (KLF6) deficiency attenuated proinflammatory gene expression in macrophages and experimentally induced atherosclerotic plaque development. In vivo studies showed that myeloid-KLF6 deficiency on Apoe-null background significantly curtailed high-fat/high-cholesterol diet-induced atherosclerotic lesion formation and macrophage abundance in atherosclerotic plaques. Integrated transcriptomics and Gene Set Enrichment Analysis showed that KLF6 deficiency significantly curtailed a large number of tumor necrosis factor (TNF)-induced gene targets, TNF-induced interferon-γ response, interferon-α response, and inflammatory response signaling in macrophages. At the molecular level, KLF6 promoted interferon regulatory factor 1 (IRF1) signaling to enhance TNF-induced proinflammatory gene expression in macrophages. Collectively, study results show that KLF6 promoted proinflammatory gene expression in macrophages and enhanced experimentally induced atherosclerotic plaque formation in vivo.
动脉粥样硬化斑块形成过程中的一个标志性事件是在受影响血管的内皮下层积聚富含脂质的巨噬细胞。巨噬细胞在动脉粥样硬化形成的各个阶段都起着关键作用,包括斑块起始、生长和破裂,以及破裂斑块的愈合。在此背景下,巨噬细胞是主要的固有免疫细胞,通过参与炎症、细胞外基质降解、吞噬作用和胞葬作用等各种过程来调节动脉粥样硬化的发生。在本研究中,Kruppel样转录因子6(KLF6)缺乏减弱了巨噬细胞中促炎基因的表达,并实验性地诱导了动脉粥样硬化斑块的形成。体内研究表明,在载脂蛋白E基因敲除背景下的髓系KLF6缺乏显著减少了高脂/高胆固醇饮食诱导的动脉粥样硬化病变形成以及动脉粥样硬化斑块中的巨噬细胞数量。综合转录组学和基因集富集分析表明,KLF6缺乏显著减少了巨噬细胞中大量肿瘤坏死因子(TNF)诱导的基因靶点、TNF诱导的干扰素-γ反应、干扰素-α反应和炎症反应信号。在分子水平上,KLF6促进干扰素调节因子1(IRF1)信号传导,以增强TNF诱导的巨噬细胞促炎基因表达。总体而言,研究结果表明,KLF6促进了巨噬细胞中促炎基因的表达,并增强了体内实验性诱导的动脉粥样硬化斑块形成。