Faculty of Medicine, Biomedical Neuroscience Institute, University of Chile, Santiago, Chile.
Center for Geroscience, Brain Health and Metabolism, Santiago, Chile.
Acta Neuropathol. 2020 Nov;140(5):737-764. doi: 10.1007/s00401-020-02183-1. Epub 2020 Jul 8.
Impaired neuronal proteostasis is a salient feature of many neurodegenerative diseases, highlighting alterations in the function of the endoplasmic reticulum (ER). We previously reported that targeting the transcription factor XBP1, a key mediator of the ER stress response, delays disease progression and reduces protein aggregation in various models of neurodegeneration. To identify disease modifier genes that may explain the neuroprotective effects of XBP1 deficiency, we performed gene expression profiling of brain cortex and striatum of these animals and uncovered insulin-like growth factor 2 (Igf2) as the major upregulated gene. Here, we studied the impact of IGF2 signaling on protein aggregation in models of Huntington's disease (HD) as proof of concept. Cell culture studies revealed that IGF2 treatment decreases the load of intracellular aggregates of mutant huntingtin and a polyglutamine peptide. These results were validated using induced pluripotent stem cells (iPSC)-derived medium spiny neurons from HD patients and spinocerebellar ataxia cases. The reduction in the levels of mutant huntingtin was associated with a decrease in the half-life of the intracellular protein. The decrease in the levels of abnormal protein aggregation triggered by IGF2 was independent of the activity of autophagy and the proteasome pathways, the two main routes for mutant huntingtin clearance. Conversely, IGF2 signaling enhanced the secretion of soluble mutant huntingtin species through exosomes and microvesicles involving changes in actin dynamics. Administration of IGF2 into the brain of HD mice using gene therapy led to a significant decrease in the levels of mutant huntingtin in three different animal models. Moreover, analysis of human postmortem brain tissue and blood samples from HD patients showed a reduction in IGF2 level. This study identifies IGF2 as a relevant factor deregulated in HD, operating as a disease modifier that buffers the accumulation of abnormal protein species.
神经元蛋白质稳态受损是许多神经退行性疾病的一个显著特征,突出了内质网 (ER) 功能的改变。我们之前报道过,靶向转录因子 XBP1(内质网应激反应的关键介质)可以延迟疾病进展并减少各种神经退行性模型中的蛋白质聚集。为了确定可能解释 XBP1 缺乏的神经保护作用的疾病修饰基因,我们对这些动物的大脑皮层和纹状体进行了基因表达谱分析,发现胰岛素样生长因子 2 (Igf2) 是主要上调的基因。在这里,我们研究了 IGF2 信号对亨廷顿病 (HD) 模型中蛋白质聚集的影响,作为概念验证。细胞培养研究表明,IGF2 处理可减少突变型 huntingtin 和多聚谷氨酰胺肽的细胞内聚集体负荷。这些结果使用来自 HD 患者和脊髓小脑共济失调病例的诱导多能干细胞 (iPSC) 衍生的中脑多巴胺能神经元得到了验证。突变型 huntingtin 的水平降低与细胞内蛋白质半衰期的降低有关。IGF2 触发的异常蛋白质聚集水平的降低与自噬和蛋白酶体途径(突变型 huntingtin 清除的两个主要途径)的活性无关。相反,IGF2 信号通过涉及肌动蛋白动力学变化的外泌体和微泡增强了可溶性突变型 huntingtin 物质的分泌。使用基因治疗将 IGF2 递送到 HD 小鼠的大脑中,导致三种不同动物模型中突变型 huntingtin 的水平显著降低。此外,对 HD 患者的人脑组织和血液样本的分析显示 IGF2 水平降低。这项研究确定 IGF2 是 HD 中失调的相关因素,作为一种疾病修饰因子,缓冲异常蛋白质物质的积累。