Program for RNA Biology, Sanford-Burnham Medical Research Institute, La Jolla, CA 92037.
Proc Natl Acad Sci U S A. 2013 Oct 8;110(41):16520-5. doi: 10.1073/pnas.1315803110. Epub 2013 Sep 25.
RNAi is an evolutionarily conserved gene regulatory process that operates in a wide variety of organisms. During RNAi, long double-stranded RNA precursors are processed by Dicer proteins into ∼21-nt siRNAs. Subsequently, siRNAs are incorporated into the RNA-induced silencing complexes (RISCs) that contain Argonaute-family proteins and guide RISC to target RNAs via complementary base pairing, leading to posttranscriptional gene silencing. Select pre-mRNA splicing factors have been implicated in RNAi in fission yeast, worms, and flies, but the underlying molecular mechanisms are not well understood. Here, we show that SmD1, a core component of the Drosophila small nuclear ribonucleoprotein particle implicated in splicing, is required for RNAi and antiviral immunity in cultured cells and in vivo. SmD1 interacts with both Dicer-2 and dsRNA precursors and is indispensable for optimal siRNA biogenesis. Depletion of SmD1 impairs the assembly and function of the small interfering RISC without significantly affecting the expression of major canonical siRNA pathway components. Moreover, SmD1 physically and functionally associates with components of the small interfering RISC, including Argonaute 2, both in flies and in humans. Notably, RNAi defects resulting from SmD1 silencing can be uncoupled from defects in pre-mRNA splicing, and the RNAi and splicing machineries are physically and functionally distinct entities. Our results suggest that Drosophila SmD1 plays a direct role in RNAi-mediated gene silencing independently of its pre-mRNA splicing activity and indicate that the dual roles of splicing factors in posttranscriptional gene regulation may be evolutionarily widespread.
RNAi 是一种进化上保守的基因调控过程,存在于多种生物体中。在 RNAi 过程中,长双链 RNA 前体被 Dicer 蛋白加工成约 21 个核苷酸的 siRNA。随后,siRNA 被整合到 RNA 诱导的沉默复合物(RISC)中,该复合物包含 Argonaute 家族蛋白,并通过互补碱基配对引导 RISC 靶向 RNA,导致转录后基因沉默。已有研究表明,裂殖酵母、线虫和果蝇中的一些前体 mRNA 剪接因子参与了 RNAi,但其中的分子机制尚不清楚。本文中,我们发现果蝇小核核糖核蛋白颗粒的核心成分 SmD1 参与剪接,它在培养细胞和体内均需要 RNAi 和抗病毒免疫。SmD1 与 Dicer-2 和双链 RNA 前体相互作用,是 siRNA 生物发生的必要条件。SmD1 的缺失会损害小干扰 RISC 的组装和功能,而不会显著影响主要的经典 siRNA 通路成分的表达。此外,SmD1 与小干扰 RISC 的成分,包括 Argonaute 2,在果蝇和人类中都存在物理和功能上的关联。值得注意的是,SmD1 沉默导致的 RNAi 缺陷可以与前体 mRNA 剪接缺陷解耦,并且 RNAi 和剪接机制是物理上和功能上不同的实体。我们的结果表明,果蝇 SmD1 在 RNAi 介导的基因沉默中发挥直接作用,独立于其前体 mRNA 剪接活性,并且表明剪接因子在后转录基因调控中的双重作用可能在进化上广泛存在。