Luo Hong-Bin, Xia Yi-Yuan, Shu Xi-Ji, Liu Zan-Chao, Feng Ye, Liu Xing-Hua, Yu Guang, Yin Gang, Xiong Yan-Si, Zeng Kuan, Jiang Jun, Ye Keqiang, Wang Xiao-Chuan, Wang Jian-Zhi
Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China;
Department of Pathology and Pathophysiology, School of Medicine, Jianghan University, Wuhan 430056, China;
Proc Natl Acad Sci U S A. 2014 Nov 18;111(46):16586-91. doi: 10.1073/pnas.1417548111. Epub 2014 Nov 5.
Intracellular accumulation of the abnormally modified tau is hallmark pathology of Alzheimer's disease (AD), but the mechanism leading to tau aggregation is not fully characterized. Here, we studied the effects of tau SUMOylation on its phosphorylation, ubiquitination, and degradation. We show that tau SUMOylation induces tau hyperphosphorylation at multiple AD-associated sites, whereas site-specific mutagenesis of tau at K340R (the SUMOylation site) or simultaneous inhibition of tau SUMOylation by ginkgolic acid abolishes the effect of small ubiquitin-like modifier protein 1 (SUMO-1). Conversely, tau hyperphosphorylation promotes its SUMOylation; the latter in turn inhibits tau degradation with reduction of solubility and ubiquitination of tau proteins. Furthermore, the enhanced SUMO-immunoreactivity, costained with the hyperphosphorylated tau, is detected in cerebral cortex of the AD brains, and β-amyloid exposure of rat primary hippocampal neurons induces a dose-dependent SUMOylation of the hyperphosphorylated tau. Our findings suggest that tau SUMOylation reciprocally stimulates its phosphorylation and inhibits the ubiquitination-mediated tau degradation, which provides a new insight into the AD-like tau accumulation.
异常修饰的tau蛋白在细胞内的积累是阿尔茨海默病(AD)的标志性病理特征,但导致tau蛋白聚集的机制尚未完全明确。在此,我们研究了tau蛋白的SUMO化对其磷酸化、泛素化和降解的影响。我们发现,tau蛋白的SUMO化会在多个与AD相关的位点诱导tau蛋白过度磷酸化,而在K340R位点(SUMO化位点)对tau蛋白进行位点特异性诱变或用银杏酸同时抑制tau蛋白的SUMO化,会消除小泛素样修饰蛋白1(SUMO-1)的作用。相反,tau蛋白过度磷酸化会促进其SUMO化;后者反过来会抑制tau蛋白的降解,同时降低tau蛋白的溶解度和泛素化水平。此外,在AD患者大脑的大脑皮层中检测到增强的SUMO免疫反应性,且与过度磷酸化的tau蛋白共定位,大鼠原代海马神经元暴露于β-淀粉样蛋白会诱导过度磷酸化的tau蛋白发生剂量依赖性SUMO化。我们的研究结果表明,tau蛋白的SUMO化相互刺激其磷酸化,并抑制泛素化介导的tau蛋白降解,这为类似AD的tau蛋白积累提供了新的见解。