Becker Lindsay A, Huang Brenda, Bieri Gregor, Ma Rosanna, Knowles David A, Jafar-Nejad Paymaan, Messing James, Kim Hong Joo, Soriano Armand, Auburger Georg, Pulst Stefan M, Taylor J Paul, Rigo Frank, Gitler Aaron D
Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA.
Stanford Neurosciences Graduate Program, Stanford University School of Medicine, Stanford, California 94305, USA.
Nature. 2017 Apr 20;544(7650):367-371. doi: 10.1038/nature22038. Epub 2017 Apr 12.
Amyotrophic lateral sclerosis (ALS) is a rapidly progressing neurodegenerative disease that is characterized by motor neuron loss and that leads to paralysis and death 2-5 years after disease onset. Nearly all patients with ALS have aggregates of the RNA-binding protein TDP-43 in their brains and spinal cords, and rare mutations in the gene encoding TDP-43 can cause ALS. There are no effective TDP-43-directed therapies for ALS or related TDP-43 proteinopathies, such as frontotemporal dementia. Antisense oligonucleotides (ASOs) and RNA-interference approaches are emerging as attractive therapeutic strategies in neurological diseases. Indeed, treatment of a rat model of inherited ALS (caused by a mutation in Sod1) with ASOs against Sod1 has been shown to substantially slow disease progression. However, as SOD1 mutations account for only around 2-5% of ALS cases, additional therapeutic strategies are needed. Silencing TDP-43 itself is probably not appropriate, given its critical cellular functions. Here we present a promising alternative therapeutic strategy for ALS that involves targeting ataxin-2. A decrease in ataxin-2 suppresses TDP-43 toxicity in yeast and flies, and intermediate-length polyglutamine expansions in the ataxin-2 gene increase risk of ALS. We used two independent approaches to test whether decreasing ataxin-2 levels could mitigate disease in a mouse model of TDP-43 proteinopathy. First, we crossed ataxin-2 knockout mice with TDP-43 (also known as TARDBP) transgenic mice. The decrease in ataxin-2 reduced aggregation of TDP-43, markedly increased survival and improved motor function. Second, in a more therapeutically applicable approach, we administered ASOs targeting ataxin-2 to the central nervous system of TDP-43 transgenic mice. This single treatment markedly extended survival. Because TDP-43 aggregation is a component of nearly all cases of ALS, targeting ataxin-2 could represent a broadly effective therapeutic strategy.
肌萎缩侧索硬化症(ALS)是一种快速进展的神经退行性疾病,其特征是运动神经元丧失,发病后2至5年可导致瘫痪和死亡。几乎所有ALS患者的大脑和脊髓中都有RNA结合蛋白TDP - 43的聚集物,编码TDP - 43的基因中的罕见突变可导致ALS。目前尚无针对ALS或相关TDP - 43蛋白病(如额颞叶痴呆)的有效靶向TDP - 43的疗法。反义寡核苷酸(ASO)和RNA干扰方法正在成为神经疾病中具有吸引力的治疗策略。事实上,用针对Sod1的ASO治疗遗传性ALS大鼠模型(由Sod1突变引起)已被证明可显著减缓疾病进展。然而,由于SOD1突变仅占ALS病例的约2 - 5%,因此需要其他治疗策略。鉴于TDP - 43的关键细胞功能,沉默TDP - 43本身可能不合适。在此,我们提出了一种有前景的ALS替代治疗策略,即靶向ataxin - 2。ataxin - 2的减少可抑制酵母和果蝇中的TDP - 43毒性,ataxin - 2基因中的中等长度多聚谷氨酰胺扩展会增加患ALS的风险。我们使用两种独立方法来测试降低ataxin - 2水平是否可以减轻TDP - 43蛋白病小鼠模型中的疾病。首先,我们将ataxin - 2基因敲除小鼠与TDP - 43(也称为TARDBP)转基因小鼠杂交。ataxin - 2的减少降低了TDP - 43的聚集,显著提高了存活率并改善了运动功能。其次,在一种更具治疗应用价值的方法中,我们将靶向ataxin - 2的ASO注射到TDP - 43转基因小鼠的中枢神经系统中。这种单一治疗显著延长了生存期。由于TDP - 43聚集是几乎所有ALS病例的一个组成部分,靶向ataxin - 2可能代表一种广泛有效的治疗策略。