Kawakita Fumihiro, Nakano Fumi, Kanamaru Hideki, Asada Reona, Suzuki Hidenori
Department of Neurosurgery, Mie University Graduate School of Medicine, 2-174 Edobashi, Mie , 514-8507, Tsu, Japan.
Transl Stroke Res. 2024 Apr;15(2):462-475. doi: 10.1007/s12975-023-01138-4. Epub 2023 Feb 9.
This study was aimed to investigate if acute neuronal apoptosis is induced by activation of AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole propionate) receptors (AMPARs) and inhibited by a clinically available selective AMPAR antagonist and antiepileptic drug perampanel (PER) in subarachnoid hemorrhage (SAH), and if the mechanisms include upregulation of an inflammation-related matricellular protein periostin. Sham-operated and endovascular perforation SAH mice randomly received an administration of 3 mg/kg PER or the vehicle intraperitoneally. Post-SAH neurological impairments and increased caspase-dependent neuronal apoptosis were associated with activation of AMPAR subunits GluA1 and GluA2, and upregulation of periostin and proinflammatory cytokines interleukins-1β and -6, all of which were suppressed by PER. PER also inhibited post-SAH convulsion-unrelated increases in the total spectral power on video electroencephalogram (EEG) monitoring. Intracerebroventricularly injected recombinant periostin blocked PER's anti-apoptotic effects on neurons. An intracerebroventricular injection of a selective agonist for GluA1 and GluA2 aggravated neurological impairment, neuronal apoptosis as well as periostin upregulation, but did not increase the EEG total spectral power after SAH. A higher dosage (10 mg/kg) of PER had even more anti-apoptotic effects compared with 3 mg/kg PER. Thus, this study first showed that AMPAR activation causes post-SAH neuronal apoptosis at least partly via periostin upregulation. A clinically available AMPAR antagonist PER appears to be neuroprotective against post-SAH early brain injury through the anti-inflammatory and anti-apoptotic effects, independent of the antiepileptic action, and deserves further study.
本研究旨在探讨蛛网膜下腔出血(SAH)时,α-氨基-3-羟基-5-甲基-4-异恶唑丙酸(AMPA)受体(AMPARs)激活是否会诱导急性神经元凋亡,以及临床上可用的选择性AMPAR拮抗剂和抗癫痫药物吡仑帕奈(PER)是否能抑制这种凋亡,其机制是否包括上调炎症相关的基质细胞蛋白骨膜蛋白。假手术组和血管内穿刺SAH小鼠随机腹腔注射3mg/kg PER或溶剂。SAH后神经功能障碍和半胱天冬酶依赖性神经元凋亡增加与AMPAR亚基GluA1和GluA2的激活、骨膜蛋白及促炎细胞因子白细胞介素-1β和-6的上调有关,而这些均被PER抑制。PER还抑制了SAH后视频脑电图(EEG)监测中与惊厥无关的总频谱功率增加。脑室内注射重组骨膜蛋白可阻断PER对神经元的抗凋亡作用。脑室内注射GluA1和GluA2的选择性激动剂会加重神经功能障碍、神经元凋亡以及骨膜蛋白上调,但不会增加SAH后的EEG总频谱功率。与3mg/kg PER相比,更高剂量(10mg/kg)的PER具有更强的抗凋亡作用。因此,本研究首次表明,AMPAR激活至少部分通过上调骨膜蛋白导致SAH后神经元凋亡。临床上可用的AMPAR拮抗剂PER似乎通过抗炎和抗凋亡作用对SAH后脑早期损伤具有神经保护作用,与抗癫痫作用无关,值得进一步研究。