Department of Human Genetics, Emory University School of Medicine, Atlanta, Georgia, United States of America.
Division of Neuropharmacology and Neurologic Diseases, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia, United States of America.
PLoS One. 2019 Mar 21;14(3):e0214156. doi: 10.1371/journal.pone.0214156. eCollection 2019.
Huntington's disease (HD) is a devastating monogenic, dominant, hereditary, neurodegenerative disease. HD is caused by the expansion of CAG repeats in exon 1 of the huntingtin (HTT) gene, IT15, resulting in an expanded polyglutamine (polyQ) residue in the N-terminus of the HTT protein. HD is characterized by the accumulation of mutant HTT (mHTT) in neural and somatic cells. Progressive brain atrophy occurs initially in the striatum and extends to different brain regions with progressive decline in cognitive, behavioral and motor functions. Astrocytes are the most abundant cell type in the brain and play an essential role in neural development and maintaining homeostasis in the central nervous system (CNS). There is increasing evidence supporting the involvement of astrocytes in the development of neurodegenerative diseases such as Parkinson's disease (PD), Huntington's disease (HD), Alzheimer's disease (AD), and amyotrophic lateral sclerosis (ALS). We have generated neural progenitor cells (NPCs) from induced pluripotent stem cells (iPSCs) of transgenic HD monkeys as a model for studying HD pathogenesis. We have reported that NPCs can be differentiated in vitro into mature neural cells, such as neurons and glial cells, and are an excellent tool to study the pathogenesis of HD. To better understand the role of astrocytes in HD pathogenesis and discover new therapies to treat HD, we have developed an astrocyte differentiation protocol and evaluated the efficacy of RNAi to ameliorate HD phenotypes in astrocytes. The resultant astrocytes expressed canonical astrocyte-specific markers examined by immunostaining and real-time PCR. Flow cytometry (FACS) analysis showed that the majority of the differentiated NPCs (95.7%) were positive for an astrocyte specific marker, glial fibrillary acidic protein (GFAP). Functionalities of astrocytes were evaluated by glutamate uptake assay and electrophysiology. Expression of mHTT in differentiated astrocytes induced cytosolic mHTT aggregates and nuclear inclusions, suppressed the expression of SOD2 and PGC1, reduced ability to uptake glutamate, decreased 4-aminopyridine (4-AP) response, and shifted I/V plot measured by electrophysiology, which are consistent with previous reports on HD astrocytes and patient brain samples. However, expression of small-hairpin RNA against HTT (shHD) ameliorated and reversed aforementioned HD phenotypes in astrocytes. This represents a demonstration of a novel non-human primate (NHP) astrocyte model for studying HD pathogenesis and a platform for discovering novel HD treatments.
亨廷顿病 (HD) 是一种破坏性的单基因、显性、遗传性、神经退行性疾病。HD 是由亨廷顿 (HTT) 基因外显子 1 中的 CAG 重复扩展引起的,导致 HTT 蛋白的 N 端扩展多聚谷氨酰胺 (polyQ) 残基。HD 的特征是神经和体细胞中突变 HTT (mHTT) 的积累。进行性脑萎缩最初发生在纹状体,并扩展到不同的脑区,导致认知、行为和运动功能逐渐下降。星形胶质细胞是大脑中最丰富的细胞类型,在神经发育和维持中枢神经系统 (CNS) 内稳态方面发挥着重要作用。越来越多的证据支持星形胶质细胞参与帕金森病 (PD)、亨廷顿病 (HD)、阿尔茨海默病 (AD) 和肌萎缩侧索硬化症 (ALS) 等神经退行性疾病的发展。我们已经从转基因 HD 猴的诱导多能干细胞 (iPSC) 中生成神经祖细胞 (NPC),作为研究 HD 发病机制的模型。我们已经报道 NPC 可以在体外分化为成熟的神经细胞,如神经元和神经胶质细胞,是研究 HD 发病机制的极好工具。为了更好地了解星形胶质细胞在 HD 发病机制中的作用并发现治疗 HD 的新疗法,我们开发了一种星形胶质细胞分化方案,并评估了 RNAi 改善星形胶质细胞中 HD 表型的效果。通过免疫染色和实时 PCR 检查,表达的星形胶质细胞表达了典型的星形胶质细胞特异性标记物。流式细胞术 (FACS) 分析表明,分化的 NPC 中绝大多数 (95.7%) 对星形胶质细胞特异性标记物胶质纤维酸性蛋白 (GFAP) 呈阳性。通过谷氨酸摄取测定和电生理学评估星形胶质细胞的功能。分化星形胶质细胞中 mHTT 的表达诱导细胞质 mHTT 聚集物和核内含物,抑制 SOD2 和 PGC1 的表达,降低谷氨酸摄取能力,降低 4-氨基吡啶 (4-AP) 反应,并通过电生理学测量改变 I/V 图,与之前关于 HD 星形胶质细胞和患者脑样本的报告一致。然而,针对 HTT 的短发夹 RNA (shHD) 的表达改善和逆转了星形胶质细胞中上述 HD 表型。这代表了一种新型非人类灵长类动物 (NHP) 星形胶质细胞模型,用于研究 HD 发病机制和发现新型 HD 治疗方法。