Beachum Allison N, Salazar Gabriela, Nachbar Amelia, Krause Kevin, Klose Hannah, Meyer Kate, Maserejian Ariana, Ross Grace, Boyd Hannah, Weigel Thaddeus, Ambaye Lydia, Miller Hayes, Grote Hannah, Coutinho-Budd Jaeda
Department of Neuroscience, University of Virginia, Charlottesville, Virginia, USA.
Department of Biology, University of Vermont, Burlington, Vermont, USA.
Glia. 2025 Aug 6. doi: 10.1002/glia.70072.
Glial cells are essential for nervous system development, homeostasis, and disease response, engaging in close interactions with neurons and other glial cells to carry out their functions. A large focus of glial studies has been on investigating how these cells work with neurons to execute their supportive roles, yet glial-glial interactions are even less well understood. Our previous work established that the loss of the secreted neurotrophin, Spätzle 3 (Spz3), from Drosophila cortex glia (CG) results in the morphological degradation of CG during mid to late larval development, where they lose their intricate interactions with neurons and other glial subtypes. Building on this work, we found that the loss of CG-neuron interactions triggers aberrant infiltration and functional compensation from all neighboring glial cell types-astrocytes, ensheathing glia (EG), and subperineurial glia (SPG)-and that both the CG disruption and surrounding aberrant glial extensions are inhibited by blocking CNS growth. These aberrant glial processes are able to compensate for at least one major CG function, the clearance of apoptotic neuronal corpses via Draper-mediated engulfment. Remarkably, even as astrocytes, EG, and SPG divert their cellular resources to extend into new territories and take on new functions, they continue to maintain their normal homeostatic roles such as synaptic remodeling (astrocytes), post-injury clearance of neurite debris (ensheathing glia), and regulation of the blood-brain barrier (SPG). These findings reveal that multiple glial subtypes can dynamically respond to nearby glial dysfunction to preserve CNS homeostasis, highlighting the resilience and adaptability of glia across subtypes.
神经胶质细胞对于神经系统的发育、稳态维持及疾病反应至关重要,它们与神经元及其他神经胶质细胞密切相互作用以执行其功能。神经胶质细胞研究的一个主要焦点一直是探究这些细胞如何与神经元协作以发挥其支持作用,然而神经胶质细胞之间的相互作用却更不为人所了解。我们之前的研究确定,果蝇皮质神经胶质细胞(CG)分泌的神经营养因子Spätzle 3(Spz3)缺失会导致CG在幼虫发育中后期出现形态退化,在此期间它们失去了与神经元及其他神经胶质细胞亚型的复杂相互作用。基于这项工作,我们发现CG与神经元相互作用的丧失会引发所有相邻神经胶质细胞类型——星形胶质细胞、包被神经胶质细胞(EG)和神经周膜下神经胶质细胞(SPG)——的异常浸润和功能补偿,并且阻断中枢神经系统生长可抑制CG的破坏及周围异常的神经胶质细胞延伸。这些异常的神经胶质细胞过程能够补偿至少一项主要的CG功能,即通过Draper介导的吞噬作用清除凋亡的神经元尸体。值得注意的是,即使星形胶质细胞、EG和SPG将其细胞资源转移以延伸到新区域并承担新功能,它们仍继续维持其正常的稳态作用,如突触重塑(星形胶质细胞)、损伤后神经突碎片的清除(包被神经胶质细胞)以及血脑屏障的调节(SPG)。这些发现揭示了多种神经胶质细胞亚型能够动态响应附近的神经胶质细胞功能障碍以维持中枢神经系统的稳态,突出了不同亚型神经胶质细胞的弹性和适应性。