Miyara Santiago J, Shinozaki Koichiro, Hayashida Kei, Shoaib Muhammad, Choudhary Rishabh C, Zafeiropoulos Stefanos, Guevara Sara, Kim Junhwan, Molmenti Ernesto P, Volpe Bruce T, Becker Lance B
Elmezzi Graduate School of Molecular Medicine, Manhasset, NY 11030, USA.
Feinstein Institutes for Medical Research, Manhasset, NY 11030, USA.
Biomedicines. 2024 Aug 1;12(8):1705. doi: 10.3390/biomedicines12081705.
The close interaction between neurons and astrocytes has been extensively studied. However, the specific behavior of these cells after ischemia-reperfusion injury and hypothermia remains poorly characterized. A growing body of evidence suggests that mitochondria function and putative transference between neurons and astrocytes may play a fundamental role in adaptive and homeostatic responses after systemic insults such as cardiac arrest, which highlights the importance of a better understanding of how neurons and astrocytes behave individually in these settings. Brain injury is one of the most important challenges in post-cardiac arrest syndrome, and therapeutic hypothermia remains the single, gold standard treatment for neuroprotection after cardiac arrest. In our study, we modeled ischemia-reperfusion injury by using in vitro enhanced oxygen-glucose deprivation and reperfusion (eOGD-R) and subsequent hypothermia (HPT) (31.5 °C) to cell lines of neurons (HT-22) and astrocytes (C8-D1A) with/without hypothermia. Using cell lysis (LDH; lactate dehydrogenase) as a measure of membrane integrity and cell viability, we found that neurons were more susceptible to eOGD-R when compared with astrocytes. However, they benefited significantly from HPT, while the HPT effect after eOGD-R on astrocytes was negligible. Similarly, eOGD-R caused a more significant reduction in adenosine triphosphate (ATP) in neurons than astrocytes, and the ATP-enhancing effects from HPT were more prominent in neurons than astrocytes. In both neurons and astrocytes, measurement of reactive oxygen species (ROS) revealed higher ROS output following eOGD-R, with a non-significant trend of differential reduction observed in neurons. HPT after eOGD-R effectively downregulated ROS in both cells; however, the effect was significantly more effective in neurons. Lipid peroxidation was higher after eOGD-R in neurons, while in astrocytes, the increase was not statistically significant. Interestingly, HPT had similar effects on the reduction in lipoperoxidation after eOGD-R with both types of cells. While glutathione (GSH) levels were downregulated after eOGD-R in both cells, HPT enhanced GSH in astrocytes, but worsened GSH in neurons. In conclusion, neuron and astrocyte cultures respond differently to eOGD-R and eOGD-R + HTP treatments. Neurons showed higher sensitivity to ischemia-reperfusion insults than astrocytes; however, they benefited more from HPT therapy. These data suggest that given the differential effects from HPT in neurons and astrocytes, future therapeutic developments could potentially enhance HPT outcomes by means of neuronal and astrocytic targeted therapies.
神经元与星形胶质细胞之间的密切相互作用已得到广泛研究。然而,这些细胞在缺血再灌注损伤和低温后的具体行为仍未得到充分表征。越来越多的证据表明,线粒体功能以及神经元与星形胶质细胞之间可能的转移在诸如心脏骤停等全身性损伤后的适应性和稳态反应中可能发挥重要作用,这凸显了更好地了解神经元和星形胶质细胞在这些情况下各自行为的重要性。脑损伤是心脏骤停后综合征最重要的挑战之一,治疗性低温仍然是心脏骤停后神经保护的唯一金标准治疗方法。在我们的研究中,我们通过对神经元(HT - 22)和星形胶质细胞(C8 - D1A)细胞系进行体外增强氧 - 葡萄糖剥夺和再灌注(eOGD - R)以及随后的低温(HPT)(31.5°C)来模拟缺血再灌注损伤,细胞系分为有/无低温处理组。使用细胞裂解(LDH;乳酸脱氢酶)作为膜完整性和细胞活力的指标,我们发现与星形胶质细胞相比,神经元对eOGD - R更敏感。然而,它们从HPT中显著受益,而eOGD - R后HPT对星形胶质细胞的影响可忽略不计。同样,eOGD - R导致神经元中的三磷酸腺苷(ATP)比星形胶质细胞有更显著的降低,并且HPT对ATP的增强作用在神经元中比在星形胶质细胞中更突出。在神经元和星形胶质细胞中,活性氧(ROS)的测量显示eOGD - R后ROS产量更高,在神经元中观察到差异降低的趋势不显著。eOGD - R后的HPT有效下调了两种细胞中的ROS;然而,该作用在神经元中显著更有效。eOGD - R后神经元中的脂质过氧化更高,而在星形胶质细胞中,增加没有统计学意义。有趣的是,HPT对eOGD - R后两种细胞类型脂质过氧化的降低有类似作用。虽然两种细胞在eOGD - R后谷胱甘肽(GSH)水平均下调,但HPT增强了星形胶质细胞中的GSH,但使神经元中的GSH恶化。总之,神经元和星形胶质细胞培养物对eOGD - R和eOGD - R + HTP处理的反应不同。神经元对缺血再灌注损伤的敏感性高于星形胶质细胞;然而,它们从HPT治疗中受益更多。这些数据表明,鉴于HPT对神经元和星形胶质细胞的不同影响,未来的治疗发展可能通过神经元和星形胶质细胞靶向治疗来潜在地提高HPT的效果。