Bajikar Sameer S, Zhou Jian, O'Hara Ryan, Tirumala Harini P, Durham Mark A, Trostle Alexander J, Dias Michelle, Shao Yingyao, Chen Hu, Wang Wei, Yalamanchili Hari Krishna, Wan Ying-Wooi, Banaszynski Laura A, Liu Zhandong, Zoghbi Huda Y
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute at Texas Children's Hospital, Houston, TX 77030, USA.
Cecil H. and Ida Green Center for Reproductive Biology Sciences, Children's Medical Center Research Institute, Department of Obstetrics and Gynecology, UT Southwestern Medical Center, Dallas, TX 75390, USA.
Neuron. 2025 Feb 5;113(3):380-395.e8. doi: 10.1016/j.neuron.2024.11.006. Epub 2024 Dec 16.
Mutations in the X-linked methyl-CpG-binding protein 2 (MECP2) gene cause Rett syndrome, a severe childhood neurological disorder. MeCP2 is a well-established transcriptional repressor, yet upon its loss, hundreds of genes are dysregulated in both directions. To understand what drives such dysregulation, we deleted Mecp2 in adult mice, circumventing developmental contributions and secondary pathogenesis. We performed time series transcriptional, chromatin, and phenotypic analyses of the hippocampus to determine the immediate consequences of MeCP2 loss and the cascade of pathogenesis. We find that loss of MeCP2 causes immediate and bidirectional progressive dysregulation of the transcriptome. To understand what drives gene downregulation, we profiled genome-wide histone modifications and found that a decrease in histone H3 acetylation (ac) at downregulated genes is among the earliest molecular changes occurring well before any measurable deficiencies in electrophysiology and neurological function. These data reveal a molecular cascade that drives disease independent of any developmental contributions or secondary pathogenesis.
X连锁甲基CpG结合蛋白2(MECP2)基因的突变会导致雷特综合征,这是一种严重的儿童神经疾病。MeCP2是一种公认的转录抑制因子,然而在其缺失后,数百个基因在两个方向上都出现了失调。为了了解导致这种失调的原因,我们在成年小鼠中删除了Mecp2,规避了发育贡献和继发性发病机制。我们对海马体进行了时间序列转录、染色质和表型分析,以确定MeCP2缺失的直接后果和发病机制的级联反应。我们发现,MeCP2的缺失会导致转录组立即出现双向渐进性失调。为了了解导致基因下调的原因,我们对全基因组组蛋白修饰进行了分析,发现下调基因处组蛋白H3乙酰化(ac)的减少是最早出现的分子变化之一,远早于电生理和神经功能出现任何可测量的缺陷。这些数据揭示了一种分子级联反应,它驱动疾病的发生,而与任何发育贡献或继发性发病机制无关。