Tian Limin, Long Guangyu, Zhu Siqi, Wang Yuelong, Xu Pengcheng, Liu Lifeng, Yao Hong, Fang Shentong, Chen Shuqing, Li Suxin
Department of Pharmaceutics, State Key Laboratory of Natural Medicines, China Pharmaceutical University, Nanjing 210009, China.
Department of Pharmaceutical Engineering, College of Pharmacy, Inner Mongolia Medical University, Hohhot 010110, China.
Proc Natl Acad Sci U S A. 2025 Jun 3;122(22):e2427257122. doi: 10.1073/pnas.2427257122. Epub 2025 May 28.
Imbalanced production and clearance of amyloid-β (Aβ) is a hallmark pathological feature of Alzheimer's disease (AD). While several monoclonal antibodies targeting Aβ have shown reductions in amyloid burden, their impact on cognitive function remains controversial, with the added risk of inflammatory side effects. Dysregulated stimulator of interferon genes (STING) signaling is implicated in neurodegenerative disorders, yet the biological interaction between this pathway and Aβ, as well as their combined influence on AD progression, is poorly understood. Here, we show that while microglia play a protective role in clearing extracellular Aβ, excessive Aβ engulfment triggers the cytosolic leakage of mitochondrial DNA for cGAS-STING cascade. This creates a negative feedback loop that not only exacerbates neuroinflammation but also impairs further Aβ clearance. To address this, we present a nanomedicine approach termed "Aβ-STING Synergistic ImmunoSilencing Therapy (ASSIST)". ASSIST comprises STING inhibitors encapsulated within a blood-brain barrier (BBB)-permeable polymeric micelle that also serves as an Aβ scavenger. Through a multivalent interaction mechanism, ASSIST efficiently destabilizes Aβ plaques and prevents monomer aggregation, subsequently promoting the engulfment of the dissociated Aβ by microglia rather than neurocytes. Furthermore, the STING signaling induced by excessive Aβ uptake is blocked, reducing inflammation and restoring microglial homeostatic functions involved in Aβ clearance. Intravenous administration of ASSIST significantly reduces Aβ burden and improves cognition in AD mice, with minimal cerebral amyloid angiopathy or microhemorrhages. We provide a proof-of-concept nanoengineering strategy to target the maladaptive immune feedback loop arising from conventional immunotherapy for AD treatment.
淀粉样蛋白β(Aβ)生成与清除失衡是阿尔茨海默病(AD)的标志性病理特征。虽然几种靶向Aβ的单克隆抗体已显示出淀粉样蛋白负荷降低,但其对认知功能的影响仍存在争议,且存在炎症副作用的额外风险。干扰素基因刺激物(STING)信号失调与神经退行性疾病有关,但该通路与Aβ之间的生物学相互作用以及它们对AD进展的综合影响尚不清楚。在这里,我们表明,虽然小胶质细胞在清除细胞外Aβ中起保护作用,但过量的Aβ吞噬会触发线粒体DNA的胞质泄漏,从而引发cGAS-STING级联反应。这形成了一个负反馈回路,不仅会加剧神经炎症,还会损害进一步的Aβ清除。为了解决这个问题,我们提出了一种纳米药物方法,称为“Aβ-STING协同免疫沉默疗法(ASSIST)”。ASSIST由封装在血脑屏障(BBB)可渗透的聚合物胶束中的STING抑制剂组成,该胶束还可作为Aβ清除剂。通过多价相互作用机制,ASSIST有效地破坏Aβ斑块的稳定性并防止单体聚集,随后促进小胶质细胞而非神经细胞对解离的Aβ的吞噬。此外,过量摄取Aβ诱导的STING信号被阻断,减少炎症并恢复参与Aβ清除的小胶质细胞稳态功能。静脉注射ASSIST可显著降低AD小鼠的Aβ负荷并改善认知,同时脑淀粉样血管病或微出血最少。我们提供了一种概念验证的纳米工程策略,以针对传统免疫疗法治疗AD时出现的适应性免疫反馈回路失调。