Yang Kun, Torres-Ramirez Gustavo, Dobbs Nicole, Han Jie, Asahina Makoto, Fujinawa Reiko, Song Kun, Liu Yun, Lin Weichun, Oviedo Angelica, Chen Chuo, Zhu Lei, Mueller William F, Lee Kevin, Suzuki Tadashi, Yan Nan
Department of Immunology, University of Texas Southwestern Medical Center, Dallas, TX, USA.
Takeda-CiRA Joint Program (T-CiRA) , Kanagawa, Japan.
J Exp Med. 2025 Oct 6;222(10). doi: 10.1084/jem.20242296. Epub 2025 Jul 11.
The STING pathway is increasingly recognized as a key regulator of neuroinflammation in neurodegenerative disease, but its role in noninflammatory conditions remains unclear. We generated a postnatal inducible whole-body Ngly1 knockout mouse (iNgly1-/-) to model NGLY1 deficiency, an early-onset neurodegenerative disorder. iNgly1-/- mice exhibit progressive motor deficits, Purkinje cell loss, and shortened lifespan without evidence of gliosis or immune activation. Cell type-specific deletion of Ngly1 in Purkinje cells or microglia failed to induce disease, suggesting multiple cell-intrinsic and cell-extrinsic signals are required. Genetic ablation of Sting1 in iNgly1-/- mice rescues Purkinje cell loss, improves motor function, and extends lifespan. Single-nucleus RNA sequencing reveals proteostasis disruption in Purkinje cells, altered cerebellar granule cell subpopulations, and STING-dependent suppression of cholesterol biosynthesis in glia. Pharmacological inhibition of STING with an orally bioactive antagonist, VS-X4, significantly mitigates neuropathology and motor disease. These findings identify STING as a key mediator of neuropathology in NGLY1 deficiency and implicate a role of STING in noninflammatory neurological disease.
STING通路越来越被认为是神经退行性疾病中神经炎症的关键调节因子,但其在非炎症性疾病中的作用仍不清楚。我们构建了一种出生后可诱导的全身Ngly1基因敲除小鼠(iNgly1-/-),以模拟NGLY1缺乏症,这是一种早发性神经退行性疾病。iNgly1-/-小鼠表现出进行性运动缺陷、浦肯野细胞丢失和寿命缩短,且无胶质细胞增生或免疫激活的迹象。在浦肯野细胞或小胶质细胞中特异性敲除Ngly1未能诱发疾病,这表明需要多种细胞内在和外在信号。在iNgly1-/-小鼠中对Sting1进行基因敲除可挽救浦肯野细胞丢失,改善运动功能并延长寿命。单核RNA测序揭示了浦肯野细胞中的蛋白质稳态破坏、小脑颗粒细胞亚群改变以及胶质细胞中STING依赖性胆固醇生物合成抑制。用口服生物活性拮抗剂VS-X4对STING进行药理学抑制可显著减轻神经病理学和运动疾病。这些发现确定STING是NGLY1缺乏症中神经病理学的关键介质,并暗示STING在非炎症性神经疾病中的作用。