Moujalled Diane, Grubman Alexandra, Acevedo Karla, Yang Shu, Ke Yazi D, Moujalled Donia M, Duncan Clare, Caragounis Aphrodite, Perera Nirma D, Turner Bradley J, Prudencio Mercedes, Petrucelli Leonard, Blair Ian, Ittner Lars M, Crouch Peter J, Liddell Jeffrey R, White Anthony R
Department of Pathology, The University of Melbourne, Victoria 3010, Australia.
The Australian School of Advanced Medicine, Macquarie University, NSW 2109, Australia.
Hum Mol Genet. 2017 May 1;26(9):1732-1746. doi: 10.1093/hmg/ddx093.
TAR DNA binding protein 43 (TDP-43) is a major disease-associated protein involved in the pathogenesis of amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration with ubiquitin-positive inclusions (FTLD-U). Our previous studies found a direct association between TDP-43 and heterogeneous nuclear ribonucleoprotein K (hnRNP K). In this study, utilizing ALS patient fibroblasts harboring a TDP-43M337V mutation and NSC-34 motor neuronal cell line expressing TDP-43Q331K mutation, we show that hnRNP K expression is impaired in urea soluble extracts from mutant TDP-43 cell models. This was confirmed in vivo using TDP-43Q331K and inducible TDP-43A315T murine ALS models. We further investigated the potential pathological effects of mutant TDP-43-mediated changes to hnRNP K metabolism by RNA binding immunoprecipitation analysis. hnRNP K protein was bound to antioxidant NFE2L2 transcripts encoding Nrf2 antioxidant transcription factor, with greater enrichment in TDP-43M337V patient fibroblasts compared to healthy controls. Subsequent gene expression profiling revealed an increase in downstream antioxidant transcript expression of Nrf2 signaling in the spinal cord of TDP-43Q331K mice compared to control counterparts, yet the corresponding protein expression was not up-regulated in transgenic mice. Despite the elevated expression of antioxidant transcripts, we observed impaired levels of glutathione (downstream Nrf2 antioxidant) in TDP-43M337V patient fibroblasts and astrocyte cultures from TDP-43Q331K mice, indicative of elevated oxidative stress and failure of some upregulated antioxidant genes to be translated into protein. Our findings indicate that further exploration of the interplay between hnRNP K (or other hnRNPs) and Nrf2-mediated antioxidant signaling is warranted and may be an important driver for motor neuron degeneration in ALS.
TAR DNA结合蛋白43(TDP-43)是一种与疾病密切相关的蛋白,参与肌萎缩侧索硬化症(ALS)和伴有泛素阳性包涵体的额颞叶痴呆(FTLD-U)的发病机制。我们之前的研究发现TDP-43与不均一核核糖核蛋白K(hnRNP K)之间存在直接关联。在本研究中,利用携带TDP-43M337V突变的ALS患者成纤维细胞以及表达TDP-43Q331K突变的NSC-34运动神经元细胞系,我们发现突变型TDP-43细胞模型的尿素可溶性提取物中hnRNP K的表达受损。使用TDP-43Q331K和诱导型TDP-43A315T小鼠ALS模型在体内证实了这一点。我们通过RNA结合免疫沉淀分析进一步研究了突变型TDP-43介导的hnRNP K代谢变化的潜在病理效应。hnRNP K蛋白与编码Nrf2抗氧化转录因子的抗氧化剂NFE2L2转录本结合,与健康对照相比,在TDP-43M337V患者成纤维细胞中的富集程度更高。随后的基因表达谱分析显示,与对照小鼠相比,TDP-43Q331K小鼠脊髓中Nrf2信号下游抗氧化转录本的表达增加,但转基因小鼠中相应的蛋白表达并未上调。尽管抗氧化转录本表达升高,但我们在TDP-43M337V患者成纤维细胞和TDP-43Q331K小鼠的星形胶质细胞培养物中观察到谷胱甘肽(Nrf2下游抗氧化剂)水平受损,这表明氧化应激升高以及一些上调的抗氧化基因无法翻译成蛋白质。我们的研究结果表明,有必要进一步探索hnRNP K(或其他hnRNPs)与Nrf2介导的抗氧化信号之间的相互作用,这可能是ALS运动神经元变性的重要驱动因素。