Xu Si, Dai Wentao, Wang Tianfeng, Cao Shugang, Du Jing, Pang Xiaonan, Li Qi, Tian Yanghua
Department of Neurology, The Second Affiliated Hospital of Anhui Medical University, Hefei, China.
Department of Critical Care Medicine, Division of Life Science and Medicine, The First Affiliated Hospital of USTCUniversity of Science and Technology of ChinaAnhui Province, Hefei, 230001, China.
Mol Neurobiol. 2025 Jun 23. doi: 10.1007/s12035-025-05160-5.
Neuromyelitis optica spectrum disorder (NMOSD) is a severe autoimmune demyelinating disease characterized by recurrent neuroinflammation and disability. Microglial activation plays a critical role in NMOSD pathogenesis, yet the mechanisms regulating its temporal dynamics remain poorly understood. The interplay between apolipoprotein E (APOE) and triggering receptor expressed on myeloid cells 2 (TREM2), key regulators of microglial function in neurodegenerative diseases, has not yet been explored in NMOSD. We conducted bulk RNA-seq in NMOSD mouse models and integrated transcriptomic sequencing, bioinformatics, and machine learning (LASSO, SVM-RFE, random forest) to identify microglia-associated hub genes in an NMOSD mouse model. Immune cell infiltration was analyzed via ImmuCC. Candidate genes were validated using Western blotting and immunofluorescence. Temporal microglial activation and APOE/TREM2 expression were assessed at 3, 7, and 10 days postmodeling. Transcriptomic analysis identified 94 microglia-associated differentially expressed genes (MDEGs), with APOE and TREM2 emerging as central hubs through machine learning. ImmuCC revealed significant infiltration of macrophages, likely indicating microglial polarization. APOE and TREM2 expression peaked on day 3 postinduction, which was correlated with maximal microglial activation (IBA1 +), followed by a gradual decrease. Experimental validation confirmed elevated APOE and TREM2 protein levels in NMOSD mice, with immunofluorescence showing colocalization in activated microglia. This study establishes the APOE-TREM2 axis as a critical regulator of microglial activation in NMOSD, exhibiting early proinflammatory and later reparative roles. The biphasic expression pattern aligns with microglial phenotypic switching, suggesting therapeutic potential for stage-specific interventions. Our findings bridge computational predictions with experimental validation, offering novel insights into NMOSD mechanisms and actionable targets for therapy.
视神经脊髓炎谱系障碍(NMOSD)是一种严重的自身免疫性脱髓鞘疾病,其特征为反复发生神经炎症和功能障碍。小胶质细胞激活在NMOSD发病机制中起关键作用,但其调节时间动态的机制仍知之甚少。载脂蛋白E(APOE)与髓系细胞上表达的触发受体2(TREM2)之间的相互作用,作为神经退行性疾病中小胶质细胞功能的关键调节因子,尚未在NMOSD中进行探索。我们在NMOSD小鼠模型中进行了批量RNA测序,并整合了转录组测序、生物信息学和机器学习(LASSO、支持向量机递归特征消除法、随机森林),以在NMOSD小鼠模型中鉴定与小胶质细胞相关的枢纽基因。通过ImmuCC分析免疫细胞浸润情况。使用蛋白质免疫印迹法和免疫荧光法验证候选基因。在建模后3天、7天和10天评估小胶质细胞的时间激活情况以及APOE/TREM2表达。转录组分析确定了94个与小胶质细胞相关的差异表达基因(MDEG),通过机器学习,APOE和TREM2成为核心枢纽。ImmuCC显示巨噬细胞有显著浸润,这可能表明小胶质细胞极化。APOE和TREM2表达在诱导后第3天达到峰值,这与最大程度的小胶质细胞激活(IBA1+)相关,随后逐渐下降。实验验证证实NMOSD小鼠中APOE和TREM2蛋白水平升高,免疫荧光显示在活化的小胶质细胞中共定位。本研究确立了APOE-TREM2轴是NMOSD中小胶质细胞激活的关键调节因子,具有早期促炎和后期修复作用。双相表达模式与小胶质细胞表型转换一致,提示阶段特异性干预的治疗潜力。我们的研究结果将计算预测与实验验证相结合,为NMOSD机制提供了新见解以及可用于治疗的靶点。