Department of Chemistry, Case Western Reserve University, Cleveland, OH, 44106, USA; Department of Ophthalmology and Visual Sciences, Case Western Reserve University, USA.
Department of Chemistry, Case Western Reserve University, Cleveland, OH, 44106, USA.
Free Radic Biol Med. 2020 May 20;152:280-294. doi: 10.1016/j.freeradbiomed.2020.03.017. Epub 2020 Mar 25.
Retinal pigment epithelial (RPE) cell dysfunction and death play vital roles in age-related macular degeneration (AMD) pathogenesis. Previously we showed that oxidative cleavage of docosahexenoate (DHA) phospholipids generates an α,β-unsaturated aldehyde, 4-hydroxy-7-oxohept-4-enoic acid (HOHA) lactone, that forms ω-carboxyethylpyrrole (CEP) derivatives through adduction to proteins and ethanolamine phospholipids. CEP derivatives and autoantibodies accumulate in the retinas and blood plasma of individuals with AMD and are a biomarker of AMD. They promote the choroidal neovascularization of "wet AMD". Immunization of mice with CEP-modified mouse serum albumin induces "dry AMD"-like lesions in their retinas as well as interferon-gamma and interleukin-17 production by CEP-specific T cells that promote inflammatory M1 polarization of macrophages. The present study confirms that oxidative stress or inflammatory stimulus produces CEP in both the primary human ARPE-19 cell line and hRPE cells. Exposure of these cells to HOHA lactone fosters production of reactive oxygen species. Thus, HOHA lactone participates in a vicious cycle, promoting intracellular oxidative stress leading to oxidative cleavage of DHA to produce more HOHA lactone. We now show that HOHA lactone is cytotoxic, inducing apoptotic cell death through activation of the intrinsic pathway. This suggests that therapeutic interventions targeting HOHA lactone-induced apoptosis may prevent the loss of RPE cells during the early phase of AMD. We also discovered that ARPE-19 cells are more susceptible than hRPE cells to HOHA lactone cytotoxicity. This is consistent with the view that, compared to normal RPE cells, ARPE-19 cells exhibit a diseased RPE phenotype that also includes elevated expression of the mesenchymal indicator vimentin, elevated integrin a5 promotor strength and deficient secretion of the anti-VEGF molecule pigment-epithelium-derived factor fostering weaker tight junctions.
视网膜色素上皮 (RPE) 细胞功能障碍和死亡在年龄相关性黄斑变性 (AMD) 的发病机制中起着至关重要的作用。我们之前曾表明,二十二碳六烯酸 (DHA) 磷脂的氧化裂解会生成一种α,β-不饱和醛,即 4-羟基-7-氧庚酸 (HOHA) 内酯,它通过与蛋白质和乙醇胺磷脂加成形成ω-羧乙基吡咯 (CEP) 衍生物。CEP 衍生物和自身抗体在 AMD 患者的视网膜和血浆中积累,是 AMD 的生物标志物。它们促进了“湿性 AMD”的脉络膜新生血管形成。用 CEP 修饰的鼠血清白蛋白免疫小鼠会在其视网膜中诱导出“干性 AMD”样病变,以及 CEP 特异性 T 细胞产生的干扰素-γ和白细胞介素-17,促进巨噬细胞的炎症 M1 极化。本研究证实,氧化应激或炎症刺激会在原代人 RPE-19 细胞系和 hRPE 细胞中产生 CEP。这些细胞暴露于 HOHA 内酯会促进活性氧的产生。因此,HOHA 内酯参与了一个恶性循环,促进细胞内氧化应激,导致 DHA 的氧化裂解产生更多的 HOHA 内酯。我们现在表明,HOHA 内酯具有细胞毒性,通过激活内在途径诱导细胞凋亡。这表明,针对 HOHA 内酯诱导的细胞凋亡的治疗干预可能会防止 AMD 早期 RPE 细胞的损失。我们还发现,ARPE-19 细胞比 hRPE 细胞对 HOHA 内酯的细胞毒性更敏感。这与以下观点一致,即与正常 RPE 细胞相比,ARPE-19 细胞表现出患病的 RPE 表型,还包括间充质标志物波形蛋白的表达升高、整合素 a5 启动子强度升高和抗 VEGF 分子色素上皮衍生因子的分泌不足,促进了较弱的紧密连接。