School of Biosciences and Veterinary Medicine, University of Camerino, Via Gentile III da Varano, 62032, Camerino, MC, Italy.
Department of Pharmaceutical Sciences, Università del Piemonte Orientale, Via Bovio 6, 28100, Novara, Italy.
Mol Neurobiol. 2023 May;60(5):2787-2800. doi: 10.1007/s12035-023-03231-z. Epub 2023 Feb 2.
Alzheimer's disease (AD) is a progressive neurodegeneration with dysfunctions in both the ubiquitin-proteasome system (UPS) and autophagy. Astroglia participation in AD is an attractive topic of research, but molecular patterns are partially defined and available in vitro models have technical limitations. Immortalized astrocytes from the hippocampus of 3xTg-AD and wild-type mice (3Tg-iAstro and WT-iAstro, respectively) have been obtained as an attempt to overcome primary cell line limitations and this study aims at characterizing their proteolytic systems, focusing on UPS and autophagy. Both 26S and 20S proteasomal activities were downregulated in 3Tg-iAstro, in which a shift in catalytic subunits from constitutive 20S proteasome to immunoproteasome occurred, with consequences on immune functions. In fact, immunoproteasome is the specific complex in charge of clearing damaged proteins under inflammatory conditions. Parallelly, augmented expression and activity of the lysosomal cathepsin B, enhanced levels of lysosomal-associated membrane protein 1, beclin1, and LC3-II, together with an increased uptake of monodansylcadaverine in autophagic vacuoles, suggested autophagy activation in 3Tg-iAstro. The two proteolytic pathways were linked by p62 that accumulated in 3Tg-iAstro due to both increased synthesis and decreased degradation in the UPS defective astrocytes. Treatment with 4-phenylbutyric acid, a neuroprotective small chemical chaperone, partially restored proteasome and autophagy-mediated proteolysis in 3Tg-iAstro. Our data shed light on the impaired proteostasis in 3Tg-iAstro with proteasome inhibition and autophagic compensatory activation, providing additional validation of this AD in vitro model, and propose a new mechanism of action of 4-phenylbutyric acid in neurodegenerative disorders.
阿尔茨海默病(AD)是一种进行性神经退行性疾病,其泛素-蛋白酶体系统(UPS)和自噬功能均出现障碍。星形胶质细胞参与 AD 的作用是一个备受关注的研究课题,但分子模式部分定义明确,并且现有的体外模型存在技术限制。从 3xTg-AD 和野生型小鼠的海马中获得永生化星形胶质细胞(分别为 3Tg-iAstro 和 WT-iAstro),试图克服原代细胞系的局限性,本研究旨在对其蛋白水解系统进行特征分析,重点关注 UPS 和自噬。在 3Tg-iAstro 中,26S 和 20S 蛋白酶体活性均下调,其中催化亚基从组成性 20S 蛋白酶体向免疫蛋白酶体转移,从而影响免疫功能。事实上,免疫蛋白酶体是在炎症条件下清除受损蛋白的特异性复合物。平行地,溶酶体组织蛋白酶 B 的表达和活性增强,溶酶体相关膜蛋白 1、beclin1 和 LC3-II 的水平升高,以及单丹磺酰尸胺在自噬小体中的摄取增加,提示 3Tg-iAstro 中自噬的激活。两条蛋白水解途径通过 p62 连接,由于 UPS 缺陷的星形胶质细胞中合成增加和降解减少,p62 在 3Tg-iAstro 中积累。用神经保护的小分子化学伴侣 4-苯丁酸处理,可部分恢复 3Tg-iAstro 中的蛋白酶体和自噬介导的蛋白水解。我们的数据阐明了 3Tg-iAstro 中蛋白酶体抑制和自噬补偿性激活导致的蛋白质稳态受损,为该 AD 体外模型提供了更多的验证,并提出了 4-苯丁酸在神经退行性疾病中的新作用机制。