Griesi-Oliveira K, Acab A, Gupta A R, Sunaga D Y, Chailangkarn T, Nicol X, Nunez Y, Walker M F, Murdoch J D, Sanders S J, Fernandez T V, Ji W, Lifton R P, Vadasz E, Dietrich A, Pradhan D, Song H, Ming G-L, Gu X, Haddad G, Marchetto M C N, Spitzer N, Passos-Bueno M R, State M W, Muotri A R
Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular and Molecular Medicine, Stem Cell Program, University of California San Diego, School of Medicine, La Jolla, CA, USA.
Departamento de Genética e Biologia Evolutiva, Centro de Estudos do Genoma Humano, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brasil.
Mol Psychiatry. 2015 Nov;20(11):1350-65. doi: 10.1038/mp.2014.141. Epub 2014 Nov 11.
An increasing number of genetic variants have been implicated in autism spectrum disorders (ASDs), and the functional study of such variants will be critical for the elucidation of autism pathophysiology. Here, we report a de novo balanced translocation disruption of TRPC6, a cation channel, in a non-syndromic autistic individual. Using multiple models, such as dental pulp cells, induced pluripotent stem cell (iPSC)-derived neuronal cells and mouse models, we demonstrate that TRPC6 reduction or haploinsufficiency leads to altered neuronal development, morphology and function. The observed neuronal phenotypes could then be rescued by TRPC6 complementation and by treatment with insulin-like growth factor-1 or hyperforin, a TRPC6-specific agonist, suggesting that ASD individuals with alterations in this pathway may benefit from these drugs. We also demonstrate that methyl CpG binding protein-2 (MeCP2) levels affect TRPC6 expression. Mutations in MeCP2 cause Rett syndrome, revealing common pathways among ASDs. Genetic sequencing of TRPC6 in 1041 ASD individuals and 2872 controls revealed significantly more nonsynonymous mutations in the ASD population, and identified loss-of-function mutations with incomplete penetrance in two patients. Taken together, these findings suggest that TRPC6 is a novel predisposing gene for ASD that may act in a multiple-hit model. This is the first study to use iPSC-derived human neurons to model non-syndromic ASD and illustrate the potential of modeling genetically complex sporadic diseases using such cells.
越来越多的基因变异与自闭症谱系障碍(ASD)有关,对这些变异的功能研究对于阐明自闭症的病理生理学至关重要。在此,我们报告了一名非综合征自闭症个体中阳离子通道TRPC6的新生平衡易位破坏。使用多种模型,如牙髓细胞、诱导多能干细胞(iPSC)衍生的神经元细胞和小鼠模型,我们证明TRPC6的减少或单倍剂量不足会导致神经元发育、形态和功能改变。然后,通过TRPC6互补以及用胰岛素样生长因子-1或TRPC6特异性激动剂贯叶连翘提取物进行治疗,可以挽救观察到的神经元表型,这表明该途径发生改变的ASD个体可能会从这些药物中受益。我们还证明甲基CpG结合蛋白2(MeCP2)水平会影响TRPC6的表达。MeCP2突变会导致雷特综合征,揭示了ASD之间的共同途径。对1041名ASD个体和2872名对照进行的TRPC6基因测序显示,ASD人群中的非同义突变明显更多,并在两名患者中鉴定出具有不完全外显率的功能丧失突变。综上所述,这些发现表明TRPC6是ASD的一个新的易感基因,可能在多重打击模型中起作用。这是第一项使用iPSC衍生的人类神经元对非综合征ASD进行建模的研究,并说明了使用此类细胞对遗传复杂的散发性疾病进行建模的潜力。