Zolboot Norjin, Xiao Yao, Du Jessica X, Ghanem Marwan M, Choi Su Yeun, Junn Miranda J, Zampa Federico, Huang Zeyi, MacRae Ian J, Lippi Giordano
Department of Neuroscience, The Scripps Research Institute, La Jolla, CA 92037, USA.
Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA 92037, USA.
Neuron. 2025 May 21;113(10):1629-1646.e15. doi: 10.1016/j.neuron.2025.03.009. Epub 2025 Apr 2.
MicroRNAs (miRNAs) are critical for brain development; however, if, when, and how miRNAs drive neuronal subtype specification remains poorly understood. To address this, we engineered technologies with vastly improved spatiotemporal resolution that allow the dissection of cell-type-specific miRNA-target networks. Fast and reversible miRNA loss of function showed that miRNAs are necessary for Purkinje cell (PC) differentiation, which previously appeared to be miRNA independent, and identified distinct critical miRNA windows for dendritogenesis and climbing fiber synaptogenesis, structural features defining PC identity. Using new mouse models that enable miRNA-target network mapping in rare cell types, we uncovered PC-specific post-transcriptional programs. Manipulation of these programs revealed that the PC-enriched miR-206 and targets Shank3, Prag1, En2, and Vash1, which are uniquely repressed in PCs, are critical regulators of PC-specific dendritogenesis and synaptogenesis, with miR-206 knockdown and target overexpression partially phenocopying miRNA loss of function. Our results suggest that gene expression regulation by miRNAs, beyond transcription, is critical for neuronal subtype specification.
微小RNA(miRNA)对大脑发育至关重要;然而,miRNA如何驱动神经元亚型特化、何时驱动以及如何驱动,目前仍知之甚少。为了解决这一问题,我们设计了具有极大提高的时空分辨率的技术,能够剖析细胞类型特异性的miRNA-靶标网络。快速且可逆的miRNA功能丧失表明,miRNA对于浦肯野细胞(PC)的分化是必需的,而此前PC的分化似乎与miRNA无关,并且确定了树突形成和攀缘纤维突触形成的不同关键miRNA窗口,这些结构特征定义了PC的特性。利用能够在罕见细胞类型中绘制miRNA-靶标网络的新型小鼠模型,我们发现了PC特异性的转录后程序。对这些程序的操纵表明,PC中富集的miR-206靶向Shank3、Prag1、En2和Vash1,这些基因在PC中被独特地抑制,它们是PC特异性树突形成和突触形成的关键调节因子,miR-206敲低和靶标过表达部分模拟了miRNA功能丧失的表型。我们的结果表明,miRNA对基因表达的调控,除了转录之外,对神经元亚型特化也至关重要。