Silva-Santos Sara, van Woerden Geeske M, Bruinsma Caroline F, Mientjes Edwin, Jolfaei Mehrnoush Aghadavoud, Distel Ben, Kushner Steven A, Elgersma Ype
J Clin Invest. 2015 May;125(5):2069-76. doi: 10.1172/JCI80554. Epub 2015 Apr 13.
Angelman syndrome (AS) is a severe neurodevelopmental disorder that results from loss of function of the maternal ubiquitin protein ligase E3A (UBE3A) allele. Due to neuron-specific imprinting, the paternal UBE3A copy is silenced. Previous studies in murine models have demonstrated that strategies to activate the paternal Ube3a allele are feasible; however, a recent study showed that pharmacological Ube3a gene reactivation in adulthood failed to rescue the majority of neurocognitive phenotypes in a murine AS model. Here, we performed a systematic study to investigate the possibility that neurocognitive rescue can be achieved by reinstating Ube3a during earlier neurodevelopmental windows. We developed an AS model that allows for temporally controlled Cre-dependent induction of the maternal Ube3a allele and determined that there are distinct neurodevelopmental windows during which Ube3a restoration can rescue AS-relevant phenotypes. Motor deficits were rescued by Ube3a reinstatement in adolescent mice, whereas anxiety, repetitive behavior, and epilepsy were only rescued when Ube3a was reinstated during early development. In contrast, hippocampal synaptic plasticity could be restored at any age. Together, these findings suggest that Ube3a reinstatement early in development may be necessary to prevent or rescue most AS-associated phenotypes and should be considered in future clinical trial design.
安吉尔曼综合征(AS)是一种严重的神经发育障碍,由母体泛素蛋白连接酶E3A(UBE3A)等位基因功能丧失引起。由于神经元特异性印记,父本UBE3A拷贝被沉默。先前在小鼠模型中的研究表明,激活父本Ube3a等位基因的策略是可行的;然而,最近一项研究表明,成年期药物性Ube3a基因重新激活未能挽救小鼠AS模型中的大多数神经认知表型。在此,我们进行了一项系统性研究,以探讨在早期神经发育阶段恢复Ube3a是否能够实现神经认知挽救的可能性。我们构建了一个AS模型,该模型允许对母体Ube3a等位基因进行时间可控的Cre依赖性诱导,并确定存在不同的神经发育阶段,在此期间恢复Ube3a可以挽救与AS相关的表型。在青春期小鼠中,通过恢复Ube3a可挽救运动缺陷,而只有在早期发育阶段恢复Ube3a时,焦虑、重复行为和癫痫才能得到挽救。相比之下,海马体突触可塑性在任何年龄都可以恢复。总之,这些发现表明,在发育早期恢复Ube3a可能是预防或挽救大多数AS相关表型的必要条件,应在未来的临床试验设计中予以考虑。