Department of Neurology, Children's Hospital, Boston, Massachusetts, United States of America.
PLoS One. 2012;7(5):e35885. doi: 10.1371/journal.pone.0035885. Epub 2012 May 2.
Early life seizures can result in chronic epilepsy, cognitive deficits and behavioral changes such as autism, and conversely epilepsy is common in autistic children. We hypothesized that during early brain development, seizures could alter regulators of synaptic development and underlie the interaction between epilepsy and autism. The mammalian Target of Rapamycin (mTOR) modulates protein translation and is dysregulated in Tuberous Sclerosis Complex, a disorder characterized by epilepsy and autism. We used a rodent model of acute hypoxia-induced neonatal seizures that results in long term increases in neuronal excitability, seizure susceptibility, and spontaneous seizures, to determine how seizures alter mTOR Complex 1 (mTORC1) signaling. We hypothesized that seizures occurring at a developmental stage coinciding with a critical period of synaptogenesis will activate mTORC1, contributing to epileptic networks and autistic-like behavior in later life. Here we show that in the rat, baseline mTORC1 activation peaks during the first three postnatal weeks, and induction of seizures at postnatal day 10 results in further transient activation of its downstream targets phospho-4E-BP1 (Thr37/46), phospho-p70S6K (Thr389) and phospho-S6 (Ser235/236), as well as rapid induction of activity-dependent upstream signaling molecules, including BDNF, phospho-Akt (Thr308) and phospho-ERK (Thr202/Tyr204). Furthermore, treatment with the mTORC1 inhibitor rapamycin immediately before and after seizures reversed early increases in glutamatergic neurotransmission and seizure susceptibility and attenuated later life epilepsy and autistic-like behavior. Together, these findings suggest that in the developing brain the mTORC1 signaling pathway is involved in epileptogenesis and altered social behavior, and that it may be a target for development of novel therapies that eliminate the progressive effects of neonatal seizures.
早期癫痫发作可导致慢性癫痫、认知障碍和自闭症等行为改变,相反,癫痫在自闭症儿童中很常见。我们假设在大脑早期发育过程中,癫痫发作可能会改变突触发育的调节剂,并为癫痫和自闭症之间的相互作用提供基础。哺乳动物雷帕霉素靶蛋白(mTOR)调节蛋白质翻译,在结节性硬化症中失调,这是一种以癫痫和自闭症为特征的疾病。我们使用了一种急性缺氧诱导的新生鼠癫痫发作模型,该模型导致神经元兴奋性、癫痫易感性和自发性癫痫长期增加,以确定癫痫发作如何改变 mTOR 复合物 1(mTORC1)信号。我们假设,在与突触发生关键期相吻合的发育阶段发生的癫痫发作将激活 mTORC1,导致生命后期的癫痫网络和自闭症样行为。在这里,我们发现在大鼠中,mTORC1 的基础激活在出生后前 3 周达到峰值,在出生后第 10 天诱导癫痫发作会导致其下游靶标磷酸化 4E-BP1(Thr37/46)、磷酸化 p70S6K(Thr389)和磷酸化 S6(Ser235/236)的进一步短暂激活,以及包括 BDNF、磷酸化 Akt(Thr308)和磷酸化 ERK(Thr202/Tyr204)在内的快速诱导活性依赖性上游信号分子。此外,在癫痫发作前后立即用 mTORC1 抑制剂雷帕霉素治疗可逆转早期谷氨酸能神经传递的增加和癫痫易感性,并减轻生命后期的癫痫和自闭症样行为。这些发现表明,在发育中的大脑中,mTORC1 信号通路参与了癫痫发生和改变的社会行为,并且它可能是开发消除新生期癫痫进展影响的新型治疗方法的靶点。