Medical Scientist Training Program, University of Cincinnati College of Medicine, Cincinnati, OH, United States of America; Neuroscience Graduate Program, University of Cincinnati College of Medicine, Cincinnati, OH, United States of America; Department of Anesthesia, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United States of America.
Neuroscience Graduate Program, University of Cincinnati College of Medicine, Cincinnati, OH, United States of America; Department of Pharmacology and Systems Physiology, University of Cincinnati School of Medicine, Cincinnati, OH, United States of America.
Neurobiol Dis. 2023 Mar;178:106014. doi: 10.1016/j.nbd.2023.106014. Epub 2023 Jan 23.
Status epilepticus (SE) is a life-threatening medical emergency with significant morbidity and mortality. SE is associated with a robust and sustained increase in serum glucocorticoids, reaching concentrations sufficient to activate the dense population of glucocorticoid receptors (GRs) expressed among hippocampal excitatory neurons. Glucocorticoid exposure can increase hippocampal neuron excitability; however, whether activation of hippocampal GRs during SE exacerbates seizure severity remains unknown. To test this, a viral strategy was used to delete GRs from a subset of hippocampal excitatory neurons in adult male and female mice, producing hippocampal GR knockdown mice. Two weeks after GR knockdown, mice were challenged with the convulsant drug pilocarpine to induce SE. GR knockdown had opposing effects on early vs late seizure behaviors, with sex influencing responses. For both male and female mice, the onset of mild behavioral seizures was accelerated by GR knockdown. In contrast, GR knockdown delayed the onset of more severe convulsive seizures and death in male mice. Concordantly, GR knockdown also blunted the SE-induced rise in serum corticosterone in male mice. GR knockdown did not alter survival times or serum corticosterone in females. To assess whether loss of GR affected susceptibility to SE-induced cell death, within-animal analyses were conducted comparing local GR knockdown rates to local cell loss. GR knockdown did not affect the degree of localized neuronal loss, suggesting cell-intrinsic GR signaling neither protects nor sensitizes neurons to acute SE-induced death. Overall, the findings reveal that hippocampal GRs exert an anti-convulsant role in both males and females in the early stages of SE, followed by a switch to a pro-convulsive role for males only. Findings reveal an unexpected complexity in the interaction between hippocampal GR activation and the progression of SE.
癫痫持续状态(SE)是一种危及生命的医学急症,具有显著的发病率和死亡率。SE 与血清糖皮质激素的强烈和持续增加有关,达到足以激活海马兴奋性神经元中大量表达的糖皮质激素受体(GRs)的浓度。糖皮质激素暴露会增加海马神经元的兴奋性;然而,SE 期间海马 GR 的激活是否会加剧癫痫发作的严重程度尚不清楚。为了验证这一点,使用病毒策略从成年雄性和雌性小鼠的海马兴奋性神经元亚群中删除 GR,产生海马 GR 敲低小鼠。GR 敲低后两周,用致惊厥药物匹罗卡品对小鼠进行挑战以诱导 SE。GR 敲低对早期与晚期癫痫行为有相反的影响,性别影响反应。对于雄性和雌性小鼠,GR 敲低加速了轻度行为性癫痫发作的发作。相比之下,GR 敲低延迟了雄性小鼠更严重的惊厥性癫痫发作和死亡的发作。一致地,GR 敲低还减弱了雄性小鼠 SE 诱导的血清皮质酮升高。GR 敲低对雌性小鼠的存活时间或血清皮质酮没有影响。为了评估 GR 缺失是否影响 SE 诱导的细胞死亡的易感性,进行了体内分析,比较了局部 GR 敲低率与局部细胞丢失率。GR 敲低没有影响局部神经元丢失的程度,表明细胞内 GR 信号既不能保护也不能使神经元对急性 SE 诱导的死亡敏感。总的来说,这些发现表明,海马 GR 在 SE 的早期阶段对雄性和雌性都发挥抗惊厥作用,随后仅对雄性发挥促惊厥作用。研究结果揭示了海马 GR 激活与 SE 进展之间相互作用的意外复杂性。