Laboratory of Molecular Neuroscience, Medical Research Institute (MRI), Tokyo Medical and Dental University (TMDU), Tokyo, 113-8510, Japan.
Division of Animal Genetics, Laboratory Animal Research Center, The Institute of Medical Science, The University of Tokyo, Tokyo, 108-8639, Japan.
Hum Mol Genet. 2022 May 4;31(9):1519-1530. doi: 10.1093/hmg/ddab337.
The most frequent genetic cause of focal epilepsies is variations in the GAP activity toward RAGs 1 complex genes DEP domain containing 5 (DEPDC5), nitrogen permease regulator 2-like protein (NPRL2) and nitrogen permease regulator 3-like protein (NPRL3). Because these variations are frequent and associated with a broad spectrum of focal epilepsies, a unique pathology categorized as GATORopathy can be conceptualized. Animal models recapitulating the clinical features of patients are essential to decipher GATORopathy. Although several genetically modified animal models recapitulate DEPDC5-related epilepsy, no models have been reported for NPRL2- or NPRL3-related epilepsies. Here, we conditionally deleted Nprl2 and Nprl3 from the dorsal telencephalon in mice [Emx1cre/+; Nprl2f/f (Nprl2-cKO) and Emx1cre/+; Nprl3f/f (Nprl3-cKO)] and compared their phenotypes with Nprl2+/-, Nprl3+/- and Emx1cre/+; Depdc5f/f (Depdc5-cKO) mice. Nprl2-cKO and Nprl3-cKO mice recapitulated the major abnormal features of patients-spontaneous seizures, and dysmorphic enlarged neuronal cells with increased mechanistic target of rapamycin complex 1 signaling-similar to Depdc5-cKO mice. Chronic postnatal rapamycin administration dramatically prolonged the survival period and inhibited seizure occurrence but not enlarged neuronal cells in Nprl2-cKO and Nprl3-cKO mice. However, the benefit of rapamycin after withdrawal was less durable in Nprl2- and Nprl3-cKO mice compared with Depdc5-cKO mice. Further studies using these conditional knockout mice will be useful for understanding GATORopathy and for the identification of novel therapeutic targets.
局灶性癫痫最常见的遗传原因是 RAGs 1 复合物基因 DEP 结构域包含 5(DEPDC5)、氮渗透调节因子 2 样蛋白(NPRL2)和氮渗透调节因子 3 样蛋白(NPRL3)的 GAP 活性变异。由于这些变异很常见,并且与广泛的局灶性癫痫有关,因此可以将其归类为独特的 GATORopathy 病理学。能够重现患者临床特征的动物模型对于破译 GATORopathy 至关重要。虽然有几种基因修饰的动物模型重现了与 DEPDC5 相关的癫痫,但尚未报道与 NPRL2 或 NPRL3 相关的癫痫的动物模型。在这里,我们在小鼠的背侧端脑中条件性删除了 Nprl2 和 Nprl3 [Emx1cre/+; Nprl2f/f (Nprl2-cKO) 和 Emx1cre/+; Nprl3f/f (Nprl3-cKO)],并将其表型与 Nprl2+/-, Nprl3+/- 和 Emx1cre/+; Depdc5f/f (Depdc5-cKO) 小鼠进行了比较。Nprl2-cKO 和 Nprl3-cKO 小鼠重现了患者的主要异常特征 - 自发性癫痫发作,以及形态异常的扩大神经元细胞,其机械性靶标雷帕霉素复合物 1 信号增加 - 类似于 Depdc5-cKO 小鼠。慢性产后雷帕霉素给药可显著延长 Nprl2-cKO 和 Nprl3-cKO 小鼠的存活期并抑制癫痫发作,但不能抑制神经元细胞的增大。然而,与 Depdc5-cKO 小鼠相比,Nprl2- 和 Nprl3-cKO 小鼠在停药后的雷帕霉素获益持续时间更短。使用这些条件性敲除小鼠的进一步研究将有助于理解 GATORopathy 和鉴定新的治疗靶点。