Dhawka Luvna, Evangelista Baggio A, Arooji Omeed K, Iannone Marie A, Pellegrino Kyle, Traub Rebecca, Li Xiaoyan, Bedlack Richard, Meeker Rick B, Cohen Todd J, Stanley Natalie
Department of Computer Science and Computational Medicine Program, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
Curriculum in Bioinformatics and Computational Biology, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
bioRxiv. 2025 Aug 27:2025.08.26.672381. doi: 10.1101/2025.08.26.672381.
Amyotrophic lateral sclerosis (ALS) progression rates vary dramatically between patients, yet the basis of this heterogeneity remains elusive, with no prognostic biomarkers existing to guide clinical decisions or stratify patients for therapeutic trials. Here, we identify a network of coordinated immune cell types, which exhibit differential disruption across progression groups. Using mass cytometry (CyTOF) to profile 2.2 million immune cells from 35 ALS patients stratified by progression rate and 9 healthy controls, we find that the extent of immune dysfunction cannot be reflected by examining differences in individual cell type frequencies. In contrast, analyses of correlation patterns between cell types revealed distinct immune organization patterns, where coordination complexity varied with disease progression. Across all progression groups, we observed striking immune reorganization in natural killer (NK) cells and a major shift from B cell/basophil coordination hubs in healthy controls to neutrophil/T cell-dominated patterns in ALS. Having established coordinated immune patterns, we developed machine learning models to further improve our ability to stratify between disease and non-disease cohorts, achieving superior performance compared to models using cell frequencies alone. Central and effector memory (CM/EM) CD4+ T cell interactions emerged as top discriminative features for disease status, while plasmacytoid dendritic cell (pDC) relationships, especially their ratio with regulatory T cells (T-regs), distinguished progression rates, supporting T-reg-based therapeutic approaches. These findings reframe ALS as a disease of immune coordination breakdown, pointing towards cell-type specific therapeutics and biomarkers that may extend beyond ALS to other neurodegenerative diseases characterized by immune dysfunction.
肌萎缩侧索硬化症(ALS)患者的病情进展速度差异很大,然而这种异质性的基础仍然难以捉摸,目前尚无预后生物标志物可用于指导临床决策或对患者进行分层以开展治疗试验。在此,我们识别出一个由相互协调的免疫细胞类型组成的网络,该网络在不同进展组中表现出不同程度的破坏。我们使用质谱流式细胞术(CyTOF)对35例根据病情进展速度分层的ALS患者和9名健康对照者的220万个免疫细胞进行分析,发现通过检查单个细胞类型频率的差异无法反映免疫功能障碍的程度。相反,对细胞类型之间相关性模式的分析揭示了不同的免疫组织模式,其中协调复杂性随疾病进展而变化。在所有进展组中,我们观察到自然杀伤(NK)细胞出现了显著的免疫重组,并且从健康对照者中以B细胞/嗜碱性粒细胞为协调中心的模式,主要转变为ALS中以中性粒细胞/T细胞为主导的模式。在建立了协调的免疫模式后,我们开发了机器学习模型,以进一步提高我们区分疾病和非疾病队列的能力,与仅使用细胞频率的模型相比,取得了更优的性能。中枢和效应记忆(CM/EM)CD4 + T细胞相互作用成为区分疾病状态的首要判别特征,而浆细胞样树突状细胞(pDC)的关系,尤其是它们与调节性T细胞(T-regs)的比例,则区分了疾病进展速度,支持基于T-reg的治疗方法。这些发现将ALS重新定义为一种免疫协调破坏的疾病,指向可能不仅适用于ALS,还适用于其他以免疫功能障碍为特征的神经退行性疾病的细胞类型特异性治疗方法和生物标志物。