Hansen Kasper Daniel, Lareau Liana F, Blanchette Marco, Green Richard E, Meng Qi, Rehwinkel Jan, Gallusser Fabian L, Izaurralde Elisa, Rio Donald C, Dudoit Sandrine, Brenner Steven E
Division of Biostatistics, School of Public Health, University of California Berkeley, Berkeley, CA, USA.
PLoS Genet. 2009 Jun;5(6):e1000525. doi: 10.1371/journal.pgen.1000525. Epub 2009 Jun 19.
Alternative mRNA splicing adds a layer of regulation to the expression of thousands of genes in Drosophila melanogaster. Not all alternative splicing results in functional protein; it can also yield mRNA isoforms with premature stop codons that are degraded by the nonsense-mediated mRNA decay (NMD) pathway. This coupling of alternative splicing and NMD provides a mechanism for gene regulation that is highly conserved in mammals. NMD is also active in Drosophila, but its effect on the repertoire of alternative splice forms has been unknown, as has the mechanism by which it recognizes targets. Here, we have employed a custom splicing-sensitive microarray to globally measure the effect of alternative mRNA processing and NMD on Drosophila gene expression. We have developed a new algorithm to infer the expression change of each mRNA isoform of a gene based on the microarray measurements. This method is of general utility for interpreting splicing-sensitive microarrays and high-throughput sequence data. Using this approach, we have identified a high-confidence set of 45 genes where NMD has a differential effect on distinct alternative isoforms, including numerous RNA-binding and ribosomal proteins. Coupled alternative splicing and NMD decrease expression of these genes, which may in turn have a downstream effect on expression of other genes. The NMD-affected genes are enriched for roles in translation and mitosis, perhaps underlying the previously observed role of NMD factors in cell cycle progression. Our results have general implications for understanding the NMD mechanism in fly. Most notably, we found that the NMD-target mRNAs had significantly longer 3' untranslated regions (UTRs) than the nontarget isoforms of the same genes, supporting a role for 3' UTR length in the recognition of NMD targets in fly.
可变mRNA剪接为黑腹果蝇中数千个基因的表达增添了一层调控。并非所有的可变剪接都会产生功能性蛋白质;它还可能产生带有提前终止密码子的mRNA异构体,这些异构体通过无义介导的mRNA降解(NMD)途径被降解。可变剪接与NMD的这种耦合提供了一种在哺乳动物中高度保守的基因调控机制。NMD在果蝇中也有活性,但其对可变剪接形式库的影响尚不清楚,其识别靶标的机制也不清楚。在这里,我们使用了一种定制的对剪接敏感的微阵列来全面测量可变mRNA加工和NMD对果蝇基因表达的影响。我们开发了一种新算法,根据微阵列测量结果推断基因的每个mRNA异构体的表达变化。这种方法对于解释对剪接敏感的微阵列和高通量序列数据具有普遍实用性。使用这种方法,我们确定了一组高可信度的45个基因,其中NMD对不同的可变异构体有不同的影响,包括许多RNA结合蛋白和核糖体蛋白。可变剪接与NMD的耦合降低了这些基因的表达,这反过来可能对其他基因的表达产生下游影响。受NMD影响的基因在翻译和有丝分裂中发挥的作用富集,这可能是之前观察到的NMD因子在细胞周期进程中的作用的基础。我们的结果对于理解果蝇中的NMD机制具有普遍意义。最值得注意的是,我们发现NMD靶标mRNA的3'非翻译区(UTR)比同一基因的非靶标异构体长得多,这支持了3'UTR长度在果蝇中识别NMD靶标的作用。