Department of Pathophysiology, Beijing Neurosurgical Institute, Beijing Tiantan Hospital, Capital Medical University, Beijing, 100070, China.
Beijing Key Laboratory of Central Nervous System Injury, Beijing, 100070, China.
Acta Pharmacol Sin. 2021 Mar;42(3):382-392. doi: 10.1038/s41401-020-0468-5. Epub 2020 Jul 14.
Brain edema is a common and serious complication of ischemic stroke with limited effective treatment. We previously reported that methylene blue (MB) attenuated ischemic brain edema in rats, but the underlying mechanisms remained unknown. Aquaporin 4 (AQP4) in astrocytes plays a key role in brain edema. We also found that extracellular signal-regulated kinase 1/2 (ERK1/2) activation was involved in the regulation of AQP4 expression in astrocytes. In the present study, we investigated whether AQP4 and ERK1/2 were involved in the protective effect of MB against cerebral edema. Rats were subjected to transient middle cerebral artery occlusion (tMCAO), MB (3 mg/kg, for 30 min) was infused intravenously through the tail vein started immediately after reperfusion and again at 3 h after ischemia (1.5 mg/kg, for 15 min). Brain edema was determined by MRI at 0.5, 2.5, and 48 h after tMCAO. The decreases of apparent diffusion coefficient (ADC) values on diffusion-weighted MRI indicated cytotoxic brain edema, whereas the increase of T2 MRI values reflected vasogenic brain edema. We found that MB infusion significantly ameliorated cytotoxic brain edema at 2.5 and 48 h after tMCAO and decreased vasogenic brain edema at 48 h after tMCAO. In addition, MB infusion blocked the AQP4 increases and ERK1/2 activation in the cerebral cortex in ischemic penumbra at 48 h after tMCAO. In a cell swelling model established in cultured rat astrocyte exposed to glutamate (1 mM), we consistently found that MB (10 μM) attenuated cell swelling, AQP4 increases and ERK1/2 activation. Moreover, the ERK1/2 inhibitor U0126 (10 μM) had the similar effects as MB. These results demonstrate that MB improves brain edema and astrocyte swelling, which may be mediated by the inhibition of AQP4 expression via ERK1/2 pathway, suggesting that MB may be a potential choice for the treatment of brain edema.
脑水肿是缺血性脑卒中的一种常见且严重的并发症,目前治疗方法有限。我们之前的研究表明亚甲蓝(MB)可减轻大鼠缺血性脑水肿,但具体机制尚不清楚。星形胶质细胞中的水通道蛋白 4(AQP4)在脑水肿中起关键作用。我们还发现细胞外信号调节激酶 1/2(ERK1/2)的激活参与了星形胶质细胞中 AQP4 表达的调节。在本研究中,我们研究了 AQP4 和 ERK1/2 是否参与 MB 对脑水肿的保护作用。通过尾静脉输注 MB(3mg/kg,30min),在再灌注后立即开始,并在缺血后 3 小时再次输注(1.5mg/kg,15min),以实现 MB 的重复给药。在 tMCAO 后 0.5、2.5 和 48 小时通过 MRI 测定脑水肿。磁共振扩散加权成像上表观扩散系数(ADC)值的降低表明存在细胞毒性脑水肿,而 T2 磁共振成像值的增加则反映了血管源性脑水肿。我们发现 MB 输注可显著改善 tMCAO 后 2.5 和 48 小时的细胞毒性脑水肿,并降低 tMCAO 后 48 小时的血管源性脑水肿。此外,MB 输注阻断了 tMCAO 后 48 小时缺血半影区皮质中 AQP4 的增加和 ERK1/2 的激活。在谷氨酸(1mM)暴露的培养大鼠星形胶质细胞肿胀模型中,我们一致发现 MB(10μM)可减轻细胞肿胀、AQP4 增加和 ERK1/2 激活。此外,ERK1/2 抑制剂 U0126(10μM)也具有与 MB 类似的作用。这些结果表明,MB 通过抑制 ERK1/2 通路改善脑水肿和星形胶质细胞肿胀,提示 MB 可能是治疗脑水肿的一种潜在选择。