Parenteau Julie, Tsang Jasmine, Downs Sara R, Zhou Delong, Scott Michelle S, Pleiss Jeffrey A, Abou Elela Sherif
RNA Group, Département de microbiologie et d'infectiologie, Faculté de médecine et des sciences de la santé, Université de Sherbrooke, Sherbrooke, Québec J1E 4K8, Canada.
Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, United States.
Nucleic Acids Res. 2025 Jun 20;53(12). doi: 10.1093/nar/gkaf525.
Introns are common features of eukaryotic genes, typically removed through splicing to produce functional RNAs. In yeast, some introns play roles beyond host gene expression, mediating cellular responses to nutrient depletion. However, the mechanisms underlying these functions remain unclear. Here, we show that intron-dependent resistance to starvation is mediated by changes in spliceosome stoichiometry driven by a differential increase in the abundance of U1 small nuclear ribonucleoprotein (snRNP). Increased levels of U1 snRNP enhance its binding to, and promote splicing of, introns needed for improved tolerance to starvation. Nutrient depletion both increases and decreases the removal of different sets of introns. Remarkably, only introns that are more efficiently spliced out under starvation conditions are essential for resisting starvation. By investigating the mechanism using immunoprecipitation assays of different spliceosomal components, we found that the two sets of introns are differentially bound by U1 snRNP: starvation-induced introns are highly bound by U1, whereas underspliced introns bind less U1 snRNP in nutrient-limited conditions. Consistently, disrupting U1 interactions by mutating the 5' splice site or deleting nonessential U1 components significantly impairs starvation tolerance. These findings reveal a spliceosome-driven mechanism in which selective U1 recruitment to specific introns adapts cells to nutrient stress.
内含子是真核基因的常见特征,通常通过剪接去除以产生功能性RNA。在酵母中,一些内含子的作用超出了宿主基因表达的范畴,介导细胞对营养物质耗尽的反应。然而,这些功能背后的机制仍不清楚。在这里,我们表明,对饥饿的内含子依赖性抗性是由U1小核核糖核蛋白(snRNP)丰度差异增加驱动的剪接体化学计量变化介导的。U1 snRNP水平的增加增强了其与提高饥饿耐受性所需内含子的结合,并促进这些内含子的剪接。营养物质耗尽既增加也减少了不同组内含子的去除。值得注意的是,只有在饥饿条件下更有效地剪接出去的内含子对于抵抗饥饿才是必不可少的。通过使用不同剪接体成分的免疫沉淀试验研究机制,我们发现这两组内含子与U1 snRNP的结合存在差异:饥饿诱导的内含子与U1高度结合,而在营养受限条件下剪接不足的内含子与U1 snRNP的结合较少。一致地,通过突变5'剪接位点或删除非必需的U1成分来破坏U1相互作用会显著损害饥饿耐受性。这些发现揭示了一种剪接体驱动的机制,其中选择性地将U1招募到特定内含子可使细胞适应营养应激。