Meningeal lymphatics-microglia axis regulates synaptic physiology

IF 42.5 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Cell Pub Date : 2025-03-21 DOI:10.1016/j.cell.2025.02.022
Kyungdeok Kim, Daviti Abramishvili, Siling Du, Zachary Papadopoulos, Jay Cao, Jasmin Herz, Igor Smirnov, Jean-Leon Thomas, Marco Colonna, Jonathan Kipnis
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Abstract

Meningeal lymphatics serve as an outlet for cerebrospinal fluid, and their dysfunction is associated with various neurodegenerative conditions. Previous studies have demonstrated that dysfunctional meningeal lymphatics evoke behavioral changes, but the neural mechanisms underlying these changes have remained elusive. Here, we show that prolonged impairment of meningeal lymphatics alters the balance of cortical excitatory and inhibitory synaptic inputs, accompanied by deficits in memory tasks. These synaptic and behavioral alterations induced by lymphatic dysfunction are mediated by microglia, leading to increased expression of the interleukin 6 gene (Il6). IL-6 drives inhibitory synapse phenotypes via a combination of trans- and classical IL-6 signaling. Restoring meningeal lymphatic function in aged mice reverses age-associated synaptic and behavioral alterations. Our findings suggest that dysfunctional meningeal lymphatics adversely impact cortical circuitry through an IL-6-dependent mechanism and identify a potential target for treating aging-associated cognitive decline.

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脑膜淋巴-小胶质细胞轴调节突触生理
脑膜淋巴管是脑脊液的出口,其功能障碍与各种神经退行性疾病有关。以往的研究表明,脑膜淋巴管功能障碍会诱发行为变化,但这些变化背后的神经机制仍然难以捉摸。在这里,我们发现脑膜淋巴管长期受损会改变大脑皮层兴奋性和抑制性突触输入的平衡,并伴随记忆任务的缺陷。淋巴功能障碍诱发的这些突触和行为改变是由小胶质细胞介导的,导致白细胞介素6基因(Il6)表达增加。IL-6通过反式和经典IL-6信号传导相结合的方式驱动抑制性突触表型。恢复老龄小鼠的脑膜淋巴功能可逆转与年龄相关的突触和行为改变。我们的研究结果表明,功能失调的脑膜淋巴管通过IL-6依赖性机制对大脑皮层回路产生不利影响,并确定了治疗衰老相关的认知功能衰退的潜在靶点。
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来源期刊
Cell
Cell 生物-生化与分子生物学
CiteScore
110.00
自引率
0.80%
发文量
396
审稿时长
2 months
期刊介绍: Cells is an international, peer-reviewed, open access journal that focuses on cell biology, molecular biology, and biophysics. It is affiliated with several societies, including the Spanish Society for Biochemistry and Molecular Biology (SEBBM), Nordic Autophagy Society (NAS), Spanish Society of Hematology and Hemotherapy (SEHH), and Society for Regenerative Medicine (Russian Federation) (RPO). The journal publishes research findings of significant importance in various areas of experimental biology, such as cell biology, molecular biology, neuroscience, immunology, virology, microbiology, cancer, human genetics, systems biology, signaling, and disease mechanisms and therapeutics. The primary criterion for considering papers is whether the results contribute to significant conceptual advances or raise thought-provoking questions and hypotheses related to interesting and important biological inquiries. In addition to primary research articles presented in four formats, Cells also features review and opinion articles in its "leading edge" section, discussing recent research advancements and topics of interest to its wide readership.
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