Johnson William M, Golczak Marcin, Choe Kyonghwan, Curran Pierce L, Miller Olga Gorelenkova, Yao Chen, Wang Wenzhang, Lin Jiusheng, Milkovic Nicole M, Ray Ajit, Ravindranath Vijayalakshmi, Zhu Xiongwei, Wilson Mark A, Wilson-Delfosse Amy L, Chen Shu G, Mieyal John J
Department of Biochemistry and the Redox Biology Center, University of Nebraska-Lincoln , Lincoln, Nebraska 68588, United States.
Centre for Neuroscience, Indian Institute of Science , C.V. Raman Avenue, Bangalore 560012, India.
Biochemistry. 2016 Aug 16;55(32):4519-32. doi: 10.1021/acs.biochem.5b01132. Epub 2016 Aug 1.
Parkinson's disease (PD) is the second most common neurodegenerative disease worldwide, caused by the degeneration of the dopaminergic neurons in the substantia nigra. Mutations in PARK7 (DJ-1) result in early onset autosomal recessive PD, and oxidative modification of DJ-1 has been reported to regulate the protective activity of DJ-1 in vitro. Glutathionylation is a prevalent redox modification of proteins resulting from the disulfide adduction of the glutathione moiety to a reactive cysteine-SH, and glutathionylation of specific proteins has been implicated in regulation of cell viability. Glutaredoxin 1 (Grx1) is the principal deglutathionylating enzyme within cells, and it has been reported to mediate protection of dopaminergic neurons in Caenorhabditis elegans; however many of the functional downstream targets of Grx1 in vivo remain unknown. Previously, DJ-1 protein content was shown to decrease concomitantly with diminution of Grx1 protein content in cell culture of model neurons (SH-SY5Y and Neuro-2A lines). In the current study we aimed to investigate the regulation of DJ-1 by Grx1 in vivo and characterize its glutathionylation in vitro. Here, with Grx(-/-) mice we provide show that Grx1 regulates protein levels of DJ-1 in vivo. Furthermore, with model neuronal cells (SH-SY5Y) we observed decreased DJ-1 protein content in response to treatment with known glutathionylating agents, and with isolated DJ-1 we identified two distinct sites of glutathionylation. Finally, we found that overexpression of DJ-1 in the dopaminergic neurons partly compensates for the loss of the Grx1 homologue in a C. elegans in vivo model of PD. Therefore, our results reveal a novel redox modification of DJ-1 and suggest a novel regulatory mechanism for DJ-1 content in vivo.
帕金森病(PD)是全球第二常见的神经退行性疾病,由黑质中多巴胺能神经元的退化引起。PARK7(DJ-1)基因的突变会导致早发性常染色体隐性帕金森病,并且据报道DJ-1的氧化修饰在体外可调节其保护活性。谷胱甘肽化是一种普遍的蛋白质氧化还原修饰,它是由谷胱甘肽部分与反应性半胱氨酸-SH发生二硫键加成而产生的,特定蛋白质的谷胱甘肽化与细胞活力的调节有关。谷氧还蛋白1(Grx1)是细胞内主要的去谷胱甘肽化酶,据报道它在秀丽隐杆线虫中介导对多巴胺能神经元的保护作用;然而,Grx1在体内的许多功能性下游靶点仍然未知。此前,在模型神经元(SH-SY5Y和Neuro-2A细胞系)的细胞培养中发现,DJ-1蛋白含量会随着Grx1蛋白含量的减少而相应降低。在本研究中,我们旨在探究Grx1在体内对DJ-1的调节作用,并在体外对其谷胱甘肽化进行表征。在此,我们利用Grx(-/-)小鼠证明了Grx1在体内调节DJ-1的蛋白水平。此外,在模型神经元细胞(SH-SY5Y)中,我们观察到用已知的谷胱甘肽化剂处理后DJ-1蛋白含量降低,并且在分离的DJ-1中我们鉴定出了两个不同的谷胱甘肽化位点。最后,我们发现在帕金森病的秀丽隐杆线虫体内模型中,多巴胺能神经元中DJ-1的过表达部分补偿了Grx1同源物的缺失。因此,我们的研究结果揭示了DJ-1一种新的氧化还原修饰,并提出了一种体内DJ-1含量的新调节机制。