Department of Ophthalmology, Duke University School of Medicine, Durham, NC, USA.
Department of Immunology, Duke University, Durham, NC, USA.
J Exp Med. 2024 Mar 4;221(3). doi: 10.1084/jem.20231011. Epub 2024 Jan 30.
Outer retinal degenerations, including age-related macular degeneration (AMD), are characterized by photoreceptor and retinal pigment epithelium (RPE) atrophy. In these blinding diseases, macrophages accumulate at atrophic sites, but their ontogeny and niche specialization remain poorly understood, especially in humans. We uncovered a unique profile of microglia, marked by galectin-3 upregulation, at atrophic sites in mouse models of retinal degeneration and human AMD. In disease models, conditional deletion of galectin-3 in microglia led to phagocytosis defects and consequent augmented photoreceptor death, RPE damage, and vision loss, indicating protective roles. Mechanistically, Trem2 signaling orchestrated microglial migration to atrophic sites and induced galectin-3 expression. Moreover, pharmacologic Trem2 agonization led to heightened protection but in a galectin-3-dependent manner. In elderly human subjects, we identified this highly conserved microglial population that expressed galectin-3 and Trem2. This population was significantly enriched in the macular RPE-choroid of AMD subjects. Collectively, our findings reveal a neuroprotective population of microglia and a potential therapeutic target for mitigating retinal degeneration.
外视网膜变性,包括年龄相关性黄斑变性(AMD),其特征是光感受器和视网膜色素上皮(RPE)萎缩。在这些致盲性疾病中,巨噬细胞在萎缩部位聚集,但它们的起源和生态位特化仍知之甚少,尤其是在人类中。我们在小鼠视网膜变性和人类 AMD 模型的萎缩部位发现了小胶质细胞的独特特征,其特征是半乳糖凝集素-3 的上调。在疾病模型中,小胶质细胞中半乳糖凝集素-3 的条件性缺失导致吞噬作用缺陷,继而导致光感受器死亡、RPE 损伤和视力丧失,表明具有保护作用。从机制上讲,Trem2 信号协调小胶质细胞向萎缩部位迁移,并诱导半乳糖凝集素-3 的表达。此外,Trem2 的激动剂给药以半乳糖凝集素-3 依赖的方式导致保护作用增强。在老年人类受试者中,我们鉴定出表达半乳糖凝集素-3 和 Trem2 的这种高度保守的小胶质细胞群体。该群体在外周视网膜色素上皮脉络膜中在 AMD 患者中明显富集。总之,我们的研究结果揭示了一种具有神经保护作用的小胶质细胞群,以及一种潜在的治疗靶点,可用于减轻视网膜变性。