Thompson Michelle L, Chen Pan, Yan Xiaohui, Kim Hanna, Borom Akeem R, Roberts Nathan B, Caldwell Kim A, Caldwell Guy A
Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL 35487, USA.
Dis Model Mech. 2014 Feb;7(2):233-43. doi: 10.1242/dmm.013615. Epub 2013 Dec 5.
Molecular mechanisms underlying neurodegenerative diseases converge at the interface of pathways impacting cellular stress, protein homeostasis and aging. Targeting the intrinsic capacities of neuroprotective proteins to restore neuronal function and/or attenuate degeneration represents a potential means toward therapeutic intervention. The product of the human DYT1 gene, torsinA, is a member of the functionally diverse AAA+ family of proteins and exhibits robust molecular-chaperone-like activity, both in vitro and in vivo. Although mutations in DYT1 are associated with a rare form of heritable generalized dystonia, the native function of torsinA seems to be cytoprotective in maintaining the cellular threshold to endoplasmic reticulum (ER) stress. Here we explore the potential for torsinA to serve as a buffer to attenuate the cellular consequences of misfolded-protein stress as it pertains to the neurodegenerative disease amyotrophic lateral sclerosis (ALS). The selective vulnerability of motor neurons to degeneration in ALS mouse models harboring mutations in superoxide dismutase (SOD1) has been found to correlate with regional-specific ER stress in brains. Using Caenorhabditis elegans as a system to model ER stress, we generated transgenic nematodes overexpressing either wild-type or mutant human SOD1 to evaluate their relative impact on ER stress induction in vivo. These studies revealed a mutant-SOD1-specific increase in ER stress that was further exacerbated by changes in temperature, all of which was robustly attenuated by co-expression of torsinA. Moreover, through complementary behavioral analysis, torsinA was able to restore normal neuronal function in mutant G85R SOD1 animals. Furthermore, torsinA targeted mutant SOD1 for degradation via the proteasome, representing mechanistic insight on the activity that torsinA has on aggregate-prone proteins. These results expand our understanding of proteostatic mechanisms influencing neuronal dysfunction in ALS, while simultaneously highlighting the potential for torsinA as a novel target for therapeutic development.
神经退行性疾病的分子机制汇聚于影响细胞应激、蛋白质稳态和衰老的信号通路的交汇处。靶向神经保护蛋白的内在能力以恢复神经元功能和/或减轻退化是一种潜在的治疗干预手段。人类DYT1基因的产物扭转蛋白A是功能多样的AAA+蛋白家族的成员,在体外和体内均表现出强大的分子伴侣样活性。尽管DYT1基因突变与一种罕见的遗传性全身性肌张力障碍有关,但扭转蛋白A的天然功能似乎在维持细胞对内质网(ER)应激的阈值方面具有细胞保护作用。在这里,我们探讨了扭转蛋白A作为一种缓冲剂来减轻错误折叠蛋白应激对细胞的影响的潜力,因为这种应激与神经退行性疾病肌萎缩侧索硬化症(ALS)有关。在携带超氧化物歧化酶(SOD1)突变的ALS小鼠模型中,运动神经元对退化的选择性易感性已被发现与大脑中区域特异性的ER应激相关。利用秀丽隐杆线虫作为模拟ER应激的系统,我们生成了过表达野生型或突变型人类SOD1的转基因线虫,以评估它们对体内ER应激诱导的相对影响。这些研究揭示了ER应激中突变型SOD1特异性的增加,这种增加在温度变化时会进一步加剧,而所有这些都通过扭转蛋白A的共表达得到了显著缓解。此外,通过互补的行为分析,扭转蛋白A能够恢复突变型G85R SOD1动物的正常神经元功能。此外,扭转蛋白A通过蛋白酶体靶向突变型SOD1进行降解,这代表了对扭转蛋白A对易聚集蛋白的活性的机制性洞察。这些结果扩展了我们对影响ALS中神经元功能障碍的蛋白质稳态机制的理解,同时突出了扭转蛋白A作为治疗开发新靶点的潜力。