European Institute of Oncology (IEO) IRCCS, Milan, Italy.
Human Technopole, Milan, Italy.
J Clin Invest. 2024 Jul 15;134(14):e168982. doi: 10.1172/JCI168982.
Copy number variation (CNV) at 7q11.23 causes Williams-Beuren syndrome (WBS) and 7q microduplication syndrome (7Dup), neurodevelopmental disorders (NDDs) featuring intellectual disability accompanied by symmetrically opposite neurocognitive features. Although significant progress has been made in understanding the molecular mechanisms underlying 7q11.23-related pathophysiology, the propagation of CNV dosage across gene expression layers and their interplay remains elusive. Here we uncovered 7q11.23 dosage-dependent symmetrically opposite dynamics in neuronal differentiation and intrinsic excitability. By integrating transcriptomics, translatomics, and proteomics of patient-derived and isogenic induced neurons, we found that genes related to neuronal transmission follow 7q11.23 dosage and are transcriptionally controlled, while translational factors and ribosomal genes are posttranscriptionally buffered. Consistently, we found phosphorylated RPS6 (p-RPS6) downregulated in WBS and upregulated in 7Dup. Surprisingly, p-4EBP was changed in the opposite direction, reflecting dosage-specific changes in total 4EBP levels. This highlights different dosage-sensitive dyregulations of the mTOR pathway as well as distinct roles of p-RPS6 and p-4EBP during neurogenesis. Our work demonstrates the importance of multiscale disease modeling across molecular and functional layers, uncovers the pathophysiological relevance of ribosomal biogenesis in a paradigmatic pair of NDDs, and uncouples the roles of p-RPS6 and p-4EBP as mechanistically actionable relays in NDDs.
拷贝数变异(CNV)在 7q11.23 导致威廉姆斯-比伦综合征(WBS)和 7q 微重复综合征(7Dup),这些都是伴有智力障碍和对称性相反神经认知特征的神经发育障碍(NDD)。尽管在理解 7q11.23 相关病理生理学的分子机制方面已经取得了重大进展,但 CNV 剂量在基因表达层之间的传播及其相互作用仍然难以捉摸。在这里,我们揭示了神经元分化和内在兴奋性的 7q11.23 剂量依赖性对称相反动力学。通过整合患者来源的和同源诱导神经元的转录组学、转位组学和蛋白质组学,我们发现与神经元传递相关的基因遵循 7q11.23 剂量并受转录控制,而翻译因子和核糖体基因则受转录后缓冲。一致地,我们发现 WBS 中 p-RPS6(磷酸化 RPS6)下调,而 7Dup 中上调。令人惊讶的是,p-4EBP 的变化方向相反,反映了总 4EBP 水平的剂量特异性变化。这突出了 mTOR 通路的不同剂量敏感的调节以及 p-RPS6 和 p-4EBP 在神经发生过程中的不同作用。我们的工作证明了跨分子和功能层进行多尺度疾病建模的重要性,揭示了核糖体生物发生在一对典型的 NDD 中的病理生理学相关性,并分离了 p-RPS6 和 p-4EBP 作为 NDD 中机械可操作的中继的作用。