Lau Kelvin E How, Nguyen Ngoc T, Kesavan Jaideep C, Langa Elena, Fanning Kevin, Brennan Gary P, Sanz-Rodriguez Amaya, Villegas-Salmerón Javier, Yan Yan, Venø Morten T, Mills James D, Rosenow Felix, Bauer Sebastian, Kjems Jørgen, Henshall David C
Department of Physiology and Medical Physics, Royal College of Surgeons in Ireland University of Medicine and Health Sciences, Dublin D02 YN77, Ireland.
FutureNeuro SFI Research Centre, Royal College of Surgeons in Ireland University of Medicine and Health Sciences, Dublin D02 YN77, Ireland.
Brain Commun. 2024 Jan 3;6(1):fcad355. doi: 10.1093/braincomms/fcad355. eCollection 2024.
MicroRNAs have emerged as important regulators of the gene expression landscape in temporal lobe epilepsy. The mechanisms that control microRNA levels and influence target choice remain, however, poorly understood. RNA editing is a post-transcriptional mechanism mediated by the adenosine acting on RNA (ADAR) family of proteins that introduces base modification that diversifies the gene expression landscape. RNA editing has been studied for the mRNA landscape but the extent to which microRNA editing occurs in human temporal lobe epilepsy is unknown. Here, we used small RNA-sequencing data to characterize the identity and extent of microRNA editing in human temporal lobe epilepsy brain samples. This detected low-to-high editing in over 40 of the identified microRNAs. Among microRNA exhibiting the highest editing was miR-376a-3p, which was edited in the seed region and this was predicted to significantly change the target pool. The edited form was expressed at lower levels in human temporal lobe epilepsy samples. We modelled the shift in editing levels of miR-376a-3p in human-induced pluripotent stem cell-derived neurons. Reducing levels of the edited form of miR-376a-3p using antisense oligonucleotides resulted in extensive gene expression changes, including upregulation of mitochondrial and metabolism-associated pathways. Together, these results show that differential editing of microRNAs may re-direct targeting and result in altered functions relevant to the pathophysiology of temporal lobe epilepsy and perhaps other disorders of neuronal hyperexcitability.
微小RNA已成为颞叶癫痫基因表达格局的重要调节因子。然而,控制微小RNA水平并影响靶标选择的机制仍知之甚少。RNA编辑是一种由作用于RNA的腺苷(ADAR)蛋白家族介导的转录后机制,它会引入碱基修饰,从而使基因表达格局多样化。人们已经对mRNA格局中的RNA编辑进行了研究,但在人类颞叶癫痫中微小RNA编辑发生的程度尚不清楚。在这里,我们使用小RNA测序数据来表征人类颞叶癫痫脑样本中微小RNA编辑的特征和程度。这在超过40种已鉴定的微小RNA中检测到了低到高的编辑。在表现出最高编辑水平的微小RNA中,miR-376a-3p在种子区域发生了编辑,预计这会显著改变靶标库。编辑后的形式在人类颞叶癫痫样本中的表达水平较低。我们对人类诱导多能干细胞衍生神经元中miR-376a-3p的编辑水平变化进行了建模。使用反义寡核苷酸降低miR-376a-3p编辑形式的水平会导致广泛的基因表达变化,包括线粒体和代谢相关途径的上调。总之,这些结果表明,微小RNA的差异编辑可能会重新引导靶标定位,并导致与颞叶癫痫病理生理学以及可能其他神经元过度兴奋疾病相关的功能改变。