Molecular and Cellular Biology Graduate Program, School of Neuroscience, Virginia Tech, Blacksburg, VA, USA.
Fralin Biomedical Research Institute, Glial Biology in Health, Disease and Cancer, Virginia Tech, Roanoke, VA, USA.
Physiol Rep. 2020 Oct;8(19):e14567. doi: 10.14814/phy2.14567.
Epileptic seizures are among the most common presenting symptom in patients with glioma. The etiology of glioma-related seizures is complex and not completely understood. Studies using adult glioma patient tissue and adult glioma mouse models, show that neurons adjacent to the tumor mass, peritumoral neurons, are hyperexcitable and contribute to seizures. Although it is established that there are phenotypic and genotypic distinctions in gliomas from adult and pediatric patients, it is unknown whether these established differences in pediatric glioma biology and the microenvironment in which these glioma cells harbor, the developing brain, differentially impacts surrounding neurons. In the present study, we examine the effect of patient-derived pediatric glioma cells on the function of peritumoral neurons using two pediatric glioma models. Pediatric glioma cells were intracranially injected into the cerebrum of postnatal days 2 and 3 (p2/3) mouse pups for 7 days. Electrophysiological recordings showed that cortical layer 2/3 peritumoral neurons exhibited significant differences in their intrinsic properties compared to those of sham control neurons. Peritumoral neurons fired significantly more action potentials in response to smaller current injection and exhibited a depolarization block in response to higher current injection. The threshold for eliciting an action potential and pharmacologically induced epileptiform activity was lower in peritumoral neurons compared to sham. Our findings suggest that pediatric glioma cells increase excitability in the developing peritumoral neurons by exhibiting early onset of depolarization block, which was not previously observed in adult glioma peritumoral neurons.
癫痫发作是脑胶质瘤患者最常见的首发症状之一。脑胶质瘤相关性癫痫的病因复杂,尚未完全阐明。使用成人脑胶质瘤患者组织和成人脑胶质瘤小鼠模型的研究表明,肿瘤块附近的神经元(瘤周神经元)过度兴奋,导致癫痫发作。虽然已经确定成人和儿童脑胶质瘤在表型和基因型上存在差异,但尚不清楚这些已确立的儿童脑胶质瘤生物学差异以及这些胶质瘤细胞所在的微环境(发育中的大脑)是否会对周围神经元产生不同的影响。在本研究中,我们使用两种儿童脑胶质瘤模型研究了患者来源的儿童脑胶质瘤细胞对瘤周神经元功能的影响。将儿童脑胶质瘤细胞颅内注射到出生后第 2 天和第 3 天(p2/3)的幼鼠大脑中,持续 7 天。电生理记录显示,皮层第 2/3 层瘤周神经元的内在特性与假手术对照神经元相比存在显著差异。与假手术对照神经元相比,瘤周神经元在较小的电流刺激下会产生更多的动作电位,并在较高的电流刺激下表现出去极化阻断。诱发动作电位的阈值和药物诱导的癫痫样活动在瘤周神经元中比在假手术对照神经元中更低。我们的研究结果表明,儿童脑胶质瘤细胞通过表现出早期去极化阻断,增加了发育中的瘤周神经元的兴奋性,而这种现象在成人脑胶质瘤瘤周神经元中尚未观察到。