Adelman Jacob W, Sukowaty Andrew T, Partridge Kaitlyn J, Gawrys Jessica E, Terhune Scott S, Ebert Allison D
Department of Cell Biology, Neurobiology, and Anatomy, Medical College of Wisconsin, Milwaukee, WI, USA.
Department of Microbiology and Immunology, Medical College of Wisconsin, Milwaukee, WI, USA.
bioRxiv. 2024 Aug 19:2024.08.16.608340. doi: 10.1101/2024.08.16.608340.
Human cytomegalovirus (HCMV) is a prolific human herpesvirus that infects most individuals by adulthood. While typically asymptomatic in adults, congenital infection can induce serious neurological symptoms including hearing loss, visual deficits, cognitive impairment, and microcephaly in 10-15% of cases. HCMV has been shown to infect most neural cells with our group recently demonstrating this capacity in stem cell-derived forebrain neurons. Infection of neurons induces deleterious effects on calcium dynamics and electrophysiological function paired with gross restructuring of neuronal morphology. Here, we utilize an iPSC-derived model of the human forebrain to demonstrate how HCMV infection induces syncytia, drives neurite retraction, and remodels microtubule networks to promote viral production and release. We establish that HCMV downregulates microtubule associated proteins at 14 days postinfection while simultaneously sparing other cytoskeletal elements, and this includes HCMV-driven alterations to microtubule stability. Further, we pharmacologically modulate microtubule dynamics using paclitaxel (stabilize) and colchicine (destabilize) to examine the effects on neurite structure, syncytial morphology, assembly compartment formation, and viral release. With paclitaxel, we found improvement of neurite outgrowth with a corresponding disruption to HCMV-induced syncytia formation and Golgi network disruptions but with limited impact on viral titers. Together, these data suggest that HCMV infection-induced disruption of microtubules in human cortical neurons can be partially mitigated with microtubule stabilization, suggesting a potential avenue for future neuroprotective therapeutic exploration.
人巨细胞病毒(HCMV)是一种多产的人类疱疹病毒,大多数人在成年期就会感染该病毒。虽然在成年人中通常无症状,但先天性感染可诱发严重的神经症状,包括听力丧失、视力缺陷、认知障碍,在10%至15%的病例中还会出现小头畸形。我们团队最近发现,HCMV能够感染大多数神经细胞,在干细胞衍生的前脑神经元中也证实了这一能力。神经元感染会对钙动力学和电生理功能产生有害影响,并伴有神经元形态的总体重塑。在此,我们利用人前脑的诱导多能干细胞(iPSC)衍生模型,来证明HCMV感染如何诱导多核细胞形成、驱动神经突回缩以及重塑微管网络,以促进病毒的产生和释放。我们确定,HCMV在感染后14天会下调微管相关蛋白,同时使其他细胞骨架成分不受影响,这包括HCMV对微管稳定性的改变。此外,我们使用紫杉醇(稳定微管)和秋水仙碱(破坏微管)对微管动力学进行药理学调节,以研究其对神经突结构、多核细胞形态、组装区室形成和病毒释放的影响。使用紫杉醇时,我们发现神经突生长得到改善,同时HCMV诱导的多核细胞形成和高尔基体网络破坏也相应受到干扰,但对病毒滴度的影响有限。这些数据共同表明,HCMV感染诱导的人类皮质神经元微管破坏可通过微管稳定得到部分缓解,这为未来神经保护治疗探索提供了一条潜在途径。