Department of Biology, University of Pisa, 56127 Pisa, Italy.
Bascom Palmer Eye Institute, University of Miami Miller School of Medicine, Miami, FL 33136, USA.
Cells. 2023 Apr 27;12(9):1272. doi: 10.3390/cells12091272.
Glaucoma is a chronic optic neuropathy characterized by progressive degeneration of retinal ganglion cells (RGCs). Elevated intraocular pressure (IOP) and the resulting mechanical stress are classically considered the main causes of RGC death. However, RGC degeneration and ensuing vision loss often occur independent of IOP, indicating a multifactorial nature of glaucoma, with the likely contribution of glial and vascular function. The aim of the present study was to provide a comprehensive evaluation of the time course of neuro-glial-vascular changes associated with glaucoma progression. We used DBA/2J mice in the age range of 2-15 months as a spontaneous model of glaucoma with progressive IOP elevation and RGC loss typical of human open-angle glaucoma. We found that the onset of RGC degeneration at 10 months of age coincided with that of IOP elevation and vascular changes such as decreased density, increased lacunarity and decreased tight-junction protein zonula occludens (ZO)-1, while hypoxia-inducible factor (HIF)-1α and vascular endothelial growth factor (VEGF) were already significantly upregulated at 6 months of age together with the onset of Müller cell gliosis. Astrocytes, however, underwent significant gliosis at 10 months. These results indicate that Müller cell activation occurs well before IOP elevation, with probable inflammatory consequences, and represents an early event in the glaucomatous process. Early upregulation of HIF-1α and VEGF is likely to contribute to blood retinal barrier failure, facilitating RGC loss. The different time courses of neuro-glial-vascular changes during glaucoma progression provide further insight into the nature of the disease and suggest potential targets for the development of efficient therapeutic intervention aside from IOP lowering.
青光眼是一种慢性视神经病变,其特征是视网膜神经节细胞(RGCs)进行性退化。眼内压(IOP)升高和由此产生的机械应力被经典地认为是 RGC 死亡的主要原因。然而,RGC 退化和随之而来的视力丧失往往独立于 IOP 发生,这表明青光眼具有多因素的性质,可能与神经胶质和血管功能有关。本研究的目的是全面评估与青光眼进展相关的神经胶质血管变化的时间过程。我们使用 2-15 月龄的 DBA/2J 小鼠作为具有进展性 IOP 升高和典型人类开角型青光眼 RGC 丧失的自发性青光眼模型。我们发现,10 月龄时 RGC 退化的发生与 IOP 升高和血管变化同时发生,如密度降低、腔隙性增加和紧密连接蛋白 zonula occludens (ZO)-1 减少,而缺氧诱导因子 (HIF)-1α 和血管内皮生长因子 (VEGF) 在 6 月龄时就已经显著上调,同时伴有 Müller 细胞胶质增生的发生。然而,星形胶质细胞在 10 月龄时发生了明显的胶质增生。这些结果表明,Müller 细胞的激活发生在 IOP 升高之前,可能具有炎症后果,并且是青光眼过程中的早期事件。HIF-1α 和 VEGF 的早期上调可能导致血视网膜屏障的破坏,促进 RGC 的丧失。青光眼进展过程中神经胶质血管变化的不同时间过程进一步深入了解了疾病的性质,并为除降低 IOP 以外的有效治疗干预的发展提供了潜在的靶点。