Inflammation Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC 3052, Australia; Department of Medical Biology, University of Melbourne, Parkville, VIC 3010, Australia.
Department of Pharmacology and Therapeutics, University of Melbourne, Parkville, VIC 3010, Australia; Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3010, Australia.
Cell. 2020 Oct 29;183(3):636-649.e18. doi: 10.1016/j.cell.2020.09.020. Epub 2020 Oct 7.
Cytoplasmic accumulation of TDP-43 is a disease hallmark for many cases of amyotrophic lateral sclerosis (ALS), associated with a neuroinflammatory cytokine profile related to upregulation of nuclear factor κB (NF-κB) and type I interferon (IFN) pathways. Here we show that this inflammation is driven by the cytoplasmic DNA sensor cyclic guanosine monophosphate (GMP)-AMP synthase (cGAS) when TDP-43 invades mitochondria and releases DNA via the permeability transition pore. Pharmacologic inhibition or genetic deletion of cGAS and its downstream signaling partner STING prevents upregulation of NF-κB and type I IFN induced by TDP-43 in induced pluripotent stem cell (iPSC)-derived motor neurons and in TDP-43 mutant mice. Finally, we document elevated levels of the specific cGAS signaling metabolite cGAMP in spinal cord samples from patients, which may be a biomarker of mtDNA release and cGAS/STING activation in ALS. Our results identify mtDNA release and cGAS/STING activation as critical determinants of TDP-43-associated pathology and demonstrate the potential for targeting this pathway in ALS.
细胞质中 TDP-43 的积累是许多肌萎缩侧索硬化症 (ALS) 病例的疾病特征,与核因子 κB (NF-κB) 和 I 型干扰素 (IFN) 途径上调相关的神经炎症细胞因子谱有关。在这里,我们表明,当 TDP-43 通过通透性转换孔入侵线粒体并释放 DNA 时,细胞质 DNA 传感器环鸟苷酸单磷酸 (GMP)-AMP 合酶 (cGAS) 驱动这种炎症。cGAS 和其下游信号伙伴 STING 的药理学抑制或基因缺失可防止 TDP-43 在诱导多能干细胞 (iPSC) 衍生的运动神经元和 TDP-43 突变小鼠中诱导的 NF-κB 和 I 型 IFN 的上调。最后,我们记录了来自患者脊髓样本中特定 cGAS 信号代谢物 cGAMP 的水平升高,这可能是 ALS 中线粒体 DNA 释放和 cGAS/STING 激活的生物标志物。我们的研究结果确定了 mtDNA 释放和 cGAS/STING 激活是 TDP-43 相关病理学的关键决定因素,并证明了靶向该途径治疗 ALS 的潜力。