Lim Nastasia K H, Hung Lin W, Pang Terence Y, Mclean Catriona A, Liddell Jeffrey R, Hilton James B, Li Qiao-Xin, White Anthony R, Hannan Anthony J, Crouch Peter J
Department of Pathology.
Bio21 Institute Florey Institute of Neuroscience and Mental Health.
Hum Mol Genet. 2014 Aug 1;23(15):4051-63. doi: 10.1093/hmg/ddu119. Epub 2014 Mar 14.
All cases of Huntington's disease (HD) are caused by mutant huntingtin protein (mhtt), yet the molecular mechanisms that link mhtt to disease symptoms are not fully elucidated. Given glycogen synthase kinase-3 (GSK3) is implicated in several neurodegenerative diseases as a molecular mediator of neuronal decline and widely touted as a therapeutic target, we investigated GSK3 in cells expressing mhtt, brains of R6/1 HD mice and post-mortem human brain samples. Consistency in data across the two models and the human brain samples indicate decreased GSK3 signalling contributes to neuronal dysfunction in HD. Inhibitory phosphorylation of GSK3 (pGSK3) was elevated in mhtt cells and this appeared related to an overall energy metabolism deficit as the mhtt cells had less ATP and inhibiting ATP production in control cells expressing non-pathogenic htt with paraquat also increased pGSK3. pGSK3 was increased and ATP levels decreased in the frontal cortex and striatum of R6/1 mice and levels of cortical pGSK3 inversely correlated with cognitive function of the mice. Consistent with decreased GSK3 activity in the R6/1 mouse brain, β-catenin levels were increased and phosphorylation of collapsin response mediator protein-2 (CRMP2) decreased in the frontal cortex where inhibitory phosphorylation of GSK3 was the greatest. pGSK3 was predominantly undetectable in HD and healthy control human brain samples, but levels of total GSK3 were decreased in the HD-affected frontal cortex and this correlated with decreased pCRMP2. Thus, disruptions to cortical GSK3 signalling, possibly due to localized energy metabolism deficits, appear to contribute to the cognitive symptoms of HD.
所有亨廷顿病(HD)病例均由突变型亨廷顿蛋白(mhtt)引起,但将mhtt与疾病症状联系起来的分子机制尚未完全阐明。鉴于糖原合酶激酶-3(GSK3)作为神经元衰退的分子介质参与了多种神经退行性疾病,并且被广泛吹捧为治疗靶点,我们在表达mhtt的细胞、R6/1 HD小鼠的大脑以及死后人类大脑样本中对GSK3进行了研究。两个模型和人类大脑样本数据的一致性表明,GSK3信号传导减少导致了HD中的神经元功能障碍。GSK3的抑制性磷酸化(pGSK3)在mhtt细胞中升高,这似乎与整体能量代谢缺陷有关,因为mhtt细胞的ATP较少,用百草枯抑制表达非致病性htt的对照细胞中的ATP生成也会增加pGSK3。R6/1小鼠额叶皮质和纹状体中的pGSK3增加而ATP水平降低,皮质pGSK3水平与小鼠的认知功能呈负相关。与R6/1小鼠大脑中GSK3活性降低一致,在额叶皮质中GSK3抑制性磷酸化最高的部位,β-连环蛋白水平升高而塌陷反应介导蛋白-2(CRMP2)的磷酸化降低。在HD和健康对照者的人类大脑样本中,pGSK3主要检测不到,但在受HD影响的额叶皮质中,总GSK3水平降低,这与pCRMP2降低相关。因此,皮质GSK3信号传导的破坏,可能是由于局部能量代谢缺陷,似乎导致了HD的认知症状。