Smargon Aaron A, Pant Deepak, Gomberg Trent A, Fagre Christian, Glynne Sofia, Nguyen Johnathan, Naritomi Jack T, Gilbert Wendy V, Yeo Gene W
Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA, USA.
Sanford Stem Cell Institute Innovation Center and Sanford Consortium for Regenerative Medicine, La Jolla, CA, USA.
Nat Chem Biol. 2025 Sep 18. doi: 10.1038/s41589-025-02026-8.
Endogenous uridine-rich small nuclear RNAs (U snRNAs) form RNA-protein complexes to process eukaryotic pre-mRNA into mRNA. Previous studies have demonstrated programmable U snRNA guide-targeted exon inclusion and exclusion. Here we investigated whether snRNAs can also enhance RNA base editing over state-of-the-art RNA-targeting technologies in human cells. Compared with adenosine deaminase acting on RNA (ADAR)-recruiting circular RNAs, we find that guided A>I snRNAs consistently increase adenosine-to-inosine editing for higher exon count genes, perturb substantially fewer off-target genes and localize more persistently to the nucleus where ADAR is expressed. A>I snRNAs also more efficiently edit long noncoding RNAs and pre-mRNA 3' splice sites to promote splicing changes. Lastly, snRNA-H/ACA box snoRNA fusions (U>Ψ snRNAs) increase targeted RNA pseudouridylation without DKC1 overexpression, facilitating improved CFTR rescue from nonsense-mediated mRNA decay in a cystic fibrosis human bronchial epithelial cell model. Our results advance the endogenous protein-mediated RNA base editing toolbox and RNA-targeting technologies to treat genetic diseases.
内源性富含尿苷的小核RNA(U snRNAs)形成RNA-蛋白质复合物,将真核生物前体mRNA加工成mRNA。先前的研究已经证明了可编程的U snRNA引导靶向外显子包含和排除。在这里,我们研究了在人类细胞中,与最先进的RNA靶向技术相比,snRNAs是否也能增强RNA碱基编辑。与招募腺苷脱氨酶作用于RNA(ADAR)的环状RNA相比,我们发现引导性A>I snRNAs持续增加高外显子计数基因的腺苷到肌苷编辑,干扰的脱靶基因显著减少,并且更持久地定位于表达ADAR的细胞核。A>I snRNAs还更有效地编辑长链非编码RNA和前体mRNA 3'剪接位点以促进剪接变化。最后,snRNA-H/ACA盒小核仁RNA融合体(U>Ψ snRNAs)在不进行DKC1过表达的情况下增加靶向RNA假尿苷化,在囊性纤维化人支气管上皮细胞模型中促进从无义介导的mRNA衰变中更好地挽救囊性纤维化跨膜传导调节因子(CFTR)。我们的结果推进了内源性蛋白质介导的RNA碱基编辑工具箱和RNA靶向技术用于治疗遗传疾病。