State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, Institutes of Brain Science, Fudan University, Shanghai, China.
Eye Institute and Department of Ophthalmology, Eye & ENT Hospital, NHC Key Laboratory of Myopia, Shanghai Key Laboratory of Visual Impairment and Restoration, Fudan University, Shanghai, China.
Glia. 2024 Nov;72(11):2115-2141. doi: 10.1002/glia.24600. Epub 2024 Jul 23.
Neuroinflammation plays important roles in retinal ganglion cell (RGC) degeneration in glaucoma. MicroRNA-146 (miR-146) has been shown to regulate inflammatory response in neurodegenerative diseases. In this study, whether and how miR-146 could affect RGC injury in chronic ocular hypertension (COH) experimental glaucoma were investigated. We showed that in the members of miR-146 family only miR-146a-5p expression was upregulated in COH retinas. The upregulation of miR-146a-5p was observed in the activated microglia and Müller cells both in primary cultured conditions and in COH retinas, but mainly occurred in microglia. Overexpression of miR-146a-5p in COH retinas reduced the levels pro-inflammatory cytokines and upregulated the levels of anti-inflammatory cytokines, which were further confirmed in the activated primary cultured microglia. Transfection of miR-146a-5p mimic increased the percentage of anti-inflammatory phenotype in the activated BV2 microglia, while transfection of miR-146a-5p inhibitor resulted in the opposite effects. Transfection of miR-146a-5p mimic/agomir inhibited the levels of interleukin-1 receptor associated kinase (IRAK1) and TNF receptor associated factor 6 (TRAF6) and phosphorylated NF-κB subunit p65. Dual luciferase reporter gene assay confirmed that miR-146a-5p could directly target IRAK1 and TRAF6. Moreover, downregulation of IRAK1 and TRAF6 by siRNA techniques or blocking NF-κB by SN50 in cultured microglia reversed the miR-146a-5p inhibitor-induced changes of inflammatory cytokines. In COH retinas, overexpression of miR-146a-5p reduced RGC apoptosis, increased RGC survival, and partially rescued the amplitudes of photopic negative response. Our results demonstrate that overexpression of miR-146a-5p attenuates RGC injury in glaucoma by reducing neuroinflammation through downregulating IRAK1/TRAF6/NF-κB signaling pathway in microglia.
神经炎症在青光眼的视网膜神经节细胞(RGC)变性中起重要作用。microRNA-146(miR-146)已被证明可调节神经退行性疾病中的炎症反应。在这项研究中,研究了 miR-146 是否以及如何影响慢性眼压升高(COH)实验性青光眼的 RGC 损伤。我们表明,在 miR-146 家族成员中,miR-146a-5p 的表达仅在 COH 视网膜中上调。在原代培养条件下和 COH 视网膜中,均观察到 miR-146a-5p 在活化的小胶质细胞和 Müller 细胞中上调,但主要发生在小胶质细胞中。在 COH 视网膜中过表达 miR-146a-5p 降低了促炎细胞因子的水平,并上调了抗炎细胞因子的水平,这在活化的原代培养小胶质细胞中得到了进一步证实。miR-146a-5p 模拟物的转染增加了活化的 BV2 小胶质细胞中抗炎表型的百分比,而 miR-146a-5p 抑制剂的转染则产生相反的效果。miR-146a-5p 模拟物/激动剂的转染抑制了白细胞介素-1 受体相关激酶(IRAK1)和肿瘤坏死因子受体相关因子 6(TRAF6)以及磷酸化 NF-κB 亚单位 p65 的水平。双荧光素酶报告基因测定证实,miR-146a-5p 可直接靶向 IRAK1 和 TRAF6。此外,在培养的小胶质细胞中通过 siRNA 技术下调 IRAK1 和 TRAF6 或通过 SN50 阻断 NF-κB 可逆转 miR-146a-5p 抑制剂诱导的炎症细胞因子变化。在 COH 视网膜中,miR-146a-5p 的过表达通过降低 IRAK1/TRAF6/NF-κB 信号通路减少神经炎症,从而减少 RGC 凋亡,增加 RGC 存活,并部分挽救光幻阴性反应的幅度。我们的结果表明,miR-146a-5p 的过表达通过在小胶质细胞中下调 IRAK1/TRAF6/NF-κB 信号通路减轻神经炎症,从而减轻青光眼的 RGC 损伤。