Huo Dong, Yang Ruicheng, Fu Jiyang, Chen Jiaqi, Tan Chen, Chen Huanchun, Wang Xiangru
National Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, China.
Key Laboratory of Preventive Veterinary Medicine in Hubei Province, The Cooperative Innovation Center for Sustainable Pig Production, Huazhong Agricultural University, Wuhan, China.
PLoS Pathog. 2025 Sep 10;21(9):e1013464. doi: 10.1371/journal.ppat.1013464. eCollection 2025 Sep.
Neuroinflammation within the central nervous system (CNS) is recognized as a critical pathological process in meningitic Escherichia coli (E. coli) infection, leading to severe neurodegenerative disorders and long-term sequelae. Astrocyte reactivity plays a pivotal role in driving the neuroinflammatory cascade in response to pathological stimuli from peripheral sources or other cellular components of the CNS. The involvement of astrocyte reactivity in the inflammatory process induced by bacterial infection within the CNS warrants further investigation. In this study, we observed an astrocyte reaction likely mediated by brain microvascular endothelial cells (BMEC) during meningitic E. coli infection in both a mouse model and a BMEC-astrocyte coculture system. Through label-free quantitative proteomics analysis of the BMEC secretome, we identified CK2 as a potential trigger for astrocyte reactivity. Inhibition of CK2 attenuated the reaction of hippocampal astrocytes in E. coli meningitis. Furthermore, we demonstrated that CK2 enhances NF-κB activation via its interaction with myosin 9, thereby increasing astrocyte reactivity and the inflammatory response both in vivo and in vitro. By conditionally knocking out CK2β in microvessel, we blocked CK2 secretion, resulting in reduced astrocyte reactivity and neuroinflammation during the early stages of infection. Compared to wild-type mice, CK2βVas-/- mice exhibited a significantly higher survival rate. Collectively, our findings highlight the essential role of endothelial-glial communication mediated by CK2 interaction with myosin 9 in activating the downstream NF-κB pathway, contributing to astrocyte reactivity and neuroinflammation. These results provide novel insights into the treatment of CNS inflammation caused by bacterial blood-borne infections.
中枢神经系统(CNS)内的神经炎症被认为是脑膜炎性大肠杆菌(E. coli)感染中的关键病理过程,会导致严重的神经退行性疾病和长期后遗症。星形胶质细胞反应性在驱动神经炎症级联反应中起关键作用,以应对来自外周源或中枢神经系统其他细胞成分的病理刺激。星形胶质细胞反应性在中枢神经系统细菌感染诱导的炎症过程中的作用值得进一步研究。在本研究中,我们在小鼠模型和脑微血管内皮细胞(BMEC)-星形胶质细胞共培养系统中观察到,在脑膜炎性大肠杆菌感染期间,星形胶质细胞反应可能由脑微血管内皮细胞介导。通过对BMEC分泌组进行无标记定量蛋白质组学分析,我们确定CK2是星形胶质细胞反应性的潜在触发因素。抑制CK2可减轻大肠杆菌脑膜炎中海马星形胶质细胞的反应。此外,我们证明CK2通过与肌球蛋白9相互作用增强NF-κB激活,从而在体内和体外增加星形胶质细胞反应性和炎症反应。通过有条件地敲除微血管中的CK2β,我们阻断了CK2分泌,导致感染早期星形胶质细胞反应性和神经炎症减少。与野生型小鼠相比,CK2βVas-/-小鼠的存活率显著更高。总的来说,我们的研究结果突出了由CK2与肌球蛋白9相互作用介导的内皮-胶质细胞通讯在激活下游NF-κB途径中的重要作用,这有助于星形胶质细胞反应性和神经炎症。这些结果为治疗由细菌血行感染引起的中枢神经系统炎症提供了新的见解。