Doggett Karen, Morgan Kimberly J, Olthof Anouk M, Mieruszynski Stephen, Williams Benjamin B, Garnham Alexandra L, Milevskiy Michael J G, Whitehead Lachlan, Coates Janine, Buchert Michael, O'Donoghue Robert J J, Hall Thomas E, Putoczki Tracy L, Ernst Matthias, Sutherland Kate D, Kanadia Rahul N, Heath Joan K
Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, 3052, Australia.
Department of Medical Biology, University of Melbourne, Parkville, VIC, 3052, Australia.
EMBO Rep. 2025 Jul 7. doi: 10.1038/s44319-025-00511-8.
Minor splicing is an under-appreciated splicing system required for the correct expression of ~700 genes in the human genome. This small subset of genes (0.35%) harbours introns containing non-canonical splicing sequences that are recognised uniquely by the minor spliceosome and cannot be processed by the major spliceosome. Using in vivo zebrafish and mouse cancer models, we show that heterozygous expression of Rnpc3, encoding a unique protein component of the minor spliceosome, restricts the growth and survival of liver, lung and gastric tumours without impacting healthy cells. RNPC3 knockdown in human lung cancer-derived A549 cells also impairs cell proliferation and RNA-seq analysis reveals a robust and selective disruption to minor intron splicing and transcription-wide effects on gene expression. We further demonstrate that these perturbations are accompanied by DNA replication stress, DNA damage, accumulation of TP53 protein and activation of a Tp53-dependent transcriptional program that induces cell cycle arrest and apoptosis. Together our data reveal a vulnerability of cancer cells to minor splicing inhibition that restricts tumour growth.
小剪接是一种未得到充分重视的剪接系统,对于人类基因组中约700个基因的正确表达至关重要。这一小部分基因(0.35%)含有内含子,这些内含子包含非经典剪接序列,只能被小剪接体特异性识别,而不能被主要剪接体处理。利用体内斑马鱼和小鼠癌症模型,我们发现编码小剪接体独特蛋白质成分的Rnpc3的杂合表达会限制肝、肺和胃肿瘤的生长和存活,而不会影响健康细胞。在人肺癌来源的A549细胞中敲低RNPC3也会损害细胞增殖,RNA测序分析显示小内含子剪接受强烈且选择性的破坏,并对全转录组基因表达产生影响。我们进一步证明,这些扰动伴随着DNA复制应激、DNA损伤、TP53蛋白积累以及Tp53依赖性转录程序的激活,从而诱导细胞周期停滞和凋亡。我们的数据共同揭示了癌细胞对小剪接抑制的脆弱性,这种抑制会限制肿瘤生长。