Department of Medical Biotechnology and Translational Medicine (BIOMETRA), University of Milan, Milan, Italy.
Institute of Neuroscience, IN-CNR, Milan, Italy.
JCI Insight. 2021 Feb 8;6(3):133654. doi: 10.1172/jci.insight.133654.
Impairment of the GABAergic system has been reported in epilepsy, autism, attention deficit hyperactivity disorder, and schizophrenia. We recently demonstrated that ataxia telangiectasia mutated (ATM) directly shapes the development of the GABAergic system. Here, we show for the first time to our knowledge how the abnormal expression of ATM affects the pathological condition of autism. We exploited 2 different animal models of autism, the methyl CpG binding protein 2-null (Mecp2y/-) mouse model of Rett syndrome and mice prenatally exposed to valproic acid, and found increased ATM levels. Accordingly, treatment with the specific ATM kinase inhibitor KU55933 (KU) normalized molecular, functional, and behavioral defects in these mouse models, such as (a) delayed GABAergic development, (b) hippocampal hyperexcitability, (c) low cognitive performances, and (d) social impairments. Mechanistically, we demonstrate that KU administration to WT hippocampal neurons leads to (a) higher early growth response 4 activity on Kcc2b promoter, (b) increased expression of Mecp2, and (c) potentiated GABA transmission. These results provide evidence and molecular substrates for the pharmacological development of ATM inhibition in autism spectrum disorders.
GABA 能神经系统的损伤与癫痫、自闭症、注意缺陷多动障碍和精神分裂症有关。我们最近的研究表明,共济失调毛细血管扩张突变(ATM)蛋白可直接影响 GABA 能神经系统的发育。在此,我们首次展示 ATM 异常表达如何影响自闭症的病理状况。我们利用两种自闭症动物模型,雷特综合征的甲基化 CpG 结合蛋白 2 敲除(Mecp2y/-)鼠模型和孕鼠暴露于丙戊酸的鼠模型,发现 ATM 水平升高。相应地,特异性 ATM 激酶抑制剂 KU55933(KU)处理可使这些鼠模型的分子、功能和行为缺陷正常化,如(a)GABA 能发育延迟,(b)海马过度兴奋,(c)认知功能降低,以及(d)社交障碍。从机制上讲,我们证明 KU 处理 WT 海马神经元可导致(a)Kcc2b 启动子上早期生长反应 4 活性增加,(b)Mecp2 表达增加,以及(c)GABA 传递增强。这些结果为在自闭症谱系障碍中抑制 ATM 的药物开发提供了证据和分子基础。