Li Ziyi, Martin Negin P, Epstein Jacob, Chen Shih-Heng, Hao Ying, Ramos Daniel M, Andersh Kate M, Jarreau Paige, Weller Cory, Nalls Mike A, Pantazis Caroline B, Ferrucci Luigi, Cookson Mark R, Singleton Andrew B, Qi Yue Andy, Yakel Jerrel L
Center for Alzheimer's and Related Dementias (CARD), National Institute on Aging and National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA.
DataTecnica LLC, Washington, DC 20812, USA.
bioRxiv. 2025 Mar 17:2025.03.17.643709. doi: 10.1101/2025.03.17.643709.
Endemic viral infections with low pathogenicity are often overlooked due to their mild symptoms, yet they can exert long-term effects on cellular function and contribute to disease pathogenesis. While viral infections have been implicated in neurodegenerative disorders, their impact on the neuronal proteome remains poorly understood. Here, we differentiated human induced pluripotent stem cells (KOLF2.1J) into mature neurons to investigate virus-induced proteomic changes following infection with five neurotropic endemic human viruses: Herpes simplex virus 1 (HSV-1), Human coronavirus 229E (HCoV-229E), Epstein-Barr virus (EBV), Varicella-Zoster virus (VZV), and Influenza A virus (H1N1). Given that these viruses can infect adults and have the potential to cross the placental barrier, their molecular impact on neurons may be relevant across the lifespan. Using mass spectrometry-based proteomics with a customized library for simultaneous detection of human and viral proteins, we confirmed successful infections and identified virus-specific proteomic signatures. Notably, virus-induced protein expression changes converged on key neuronal pathways, including those associated with neurodegeneration. Gene co-expression network analysis identified protein modules correlated with viral proteins. Pathway enrichment analysis of these modules revealed associations with the nervous system, including pathways linked to Alzheimer's and Parkinson's disease. Remarkably, several viral-induced proteomic alterations overlapped with changes observed in postmortem Alzheimer's patient brains, suggesting a mechanistic connection between viral exposure and neurodegenerative disease progression. These findings provide molecular insights into how common viral infections perturb neuronal homeostasis and may contribute to neurodegenerative pathology, highlighting the need to consider endemic viruses as potential environmental risk factors in neurological disorders.
致病性低的地方性病毒感染因其症状轻微往往被忽视,然而它们可对细胞功能产生长期影响并促成疾病发病机制。虽然病毒感染与神经退行性疾病有关,但其对神经元蛋白质组的影响仍知之甚少。在此,我们将人诱导多能干细胞(KOLF2.1J)分化为成熟神经元,以研究感染五种嗜神经地方性人类病毒后病毒诱导的蛋白质组变化,这五种病毒分别是:单纯疱疹病毒1型(HSV-1)、人冠状病毒229E(HCoV-229E)、爱泼斯坦-巴尔病毒(EBV)、水痘-带状疱疹病毒(VZV)和甲型流感病毒(H1N1)。鉴于这些病毒可感染成年人并有穿越胎盘屏障的潜力,它们对神经元的分子影响可能在整个生命周期都具有相关性。我们使用基于质谱的蛋白质组学和一个定制文库来同时检测人类和病毒蛋白,证实了成功感染并鉴定出病毒特异性蛋白质组特征。值得注意的是,病毒诱导的蛋白质表达变化集中在关键的神经元通路,包括与神经退行性变相关的通路。基因共表达网络分析确定了与病毒蛋白相关的蛋白质模块。对这些模块的通路富集分析揭示了与神经系统的关联,包括与阿尔茨海默病和帕金森病相关的通路。值得注意的是,一些病毒诱导的蛋白质组改变与在阿尔茨海默病患者尸检大脑中观察到的变化重叠,这表明病毒暴露与神经退行性疾病进展之间存在机制上的联系。这些发现为常见病毒感染如何扰乱神经元稳态并可能促成神经退行性病理提供了分子见解,强调了将地方性病毒视为神经系统疾病潜在环境风险因素的必要性。