University of Chinese Academy of Sciences, Beijing, China.
Key Laboratory of Insect Developmental and Evolutionary Biology, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences; Shanghai, China.
PLoS Genet. 2021 Nov 1;17(11):e1009861. doi: 10.1371/journal.pgen.1009861. eCollection 2021 Nov.
SF3B1 mutations occur in many cancers, and the highly conserved His662 residue is one of the hotspot mutation sites. To address effects on splicing and development, we constructed strains carrying point mutations at the corresponding residue His698 in Drosophila using the CRISPR-Cas9 technique. Two mutations, H698D and H698R, were selected due to their frequent presence in patients and notable opposite charges. Both the sf3b1-H698D and-H698R mutant flies exhibit developmental defects, including less egg-laying, decreased hatching rates, delayed morphogenesis and shorter lifespans. Interestingly, the H698D mutant has decreased resistance to fungal infection, while the H698R mutant shows impaired climbing ability. Consistent with these phenotypes, further analysis of RNA-seq data finds altered expression of immune response genes and changed alternative splicing of muscle and neural-related genes in the two mutants, respectively. Expression of Mef2-RB, an isoform of Mef2 gene that was downregulated due to splicing changes caused by H698R, partly rescues the climbing defects of the sf3b1-H698R mutant. Lariat sequencing reveals that the two sf3b1-H698 mutations cause aberrant selection of multiple intronic branch sites, with the H698R mutant using far upstream branch sites in the changed alternative splicing events. This study provides in vivo evidence from Drosophila that elucidates how these SF3B1 hotspot mutations alter splicing and their consequences in development and in the immune system.
SF3B1 突变发生在许多癌症中,高度保守的 His662 残基是热点突变位点之一。为了研究其对剪接和发育的影响,我们使用 CRISPR-Cas9 技术在果蝇中构建了相应残基 His698 点突变的菌株。由于其在患者中频繁出现且具有显著相反电荷,选择了两种突变,即 H698D 和 H698R。sf3b1-H698D 和-H698R 突变体果蝇均表现出发育缺陷,包括产卵减少、孵化率降低、形态发生延迟和寿命缩短。有趣的是,H698D 突变体对真菌感染的抵抗力降低,而 H698R 突变体表现出爬行能力受损。与这些表型一致,进一步的 RNA-seq 数据分析发现,两种突变体中免疫反应基因的表达发生改变,肌肉和神经相关基因的可变剪接发生改变。由于 H698R 引起的剪接变化导致 Mef2 基因的一种异构体 Mef2-RB 表达下调,该基因的表达部分挽救了 sf3b1-H698R 突变体的爬行缺陷。套索测序显示,这两种 sf3b1-H698 突变导致多个内含子分支位点的选择异常,H698R 突变体在改变的可变剪接事件中使用远上游分支位点。这项研究从果蝇体内提供了证据,阐明了这些 SF3B1 热点突变如何改变剪接及其在发育和免疫系统中的后果。