MOE Laboratory of Biosystems Homeostasis & Protection and Innovation Center for Cell Signaling Network, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China.
Cancer Center and State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China.
PLoS Biol. 2023 Jul 6;21(7):e3002197. doi: 10.1371/journal.pbio.3002197. eCollection 2023 Jul.
Drosophila melanogaster Down syndrome cell adhesion molecule 1 (Dscam1) encodes 19,008 diverse ectodomain isoforms via the alternative splicing of exon 4, 6, and 9 clusters. However, whether individual isoforms or exon clusters have specific significance is unclear. Here, using phenotype-diversity correlation analysis, we reveal the redundant and specific roles of Dscam1 diversity in neuronal wiring. A series of deletion mutations were performed from the endogenous locus harboring exon 4, 6, or 9 clusters, reducing to 396 to 18,612 potential ectodomain isoforms. Of the 3 types of neurons assessed, dendrite self/non-self discrimination required a minimum number of isoforms (approximately 2,000), independent of exon clusters or isoforms. In contrast, normal axon patterning in the mushroom body and mechanosensory neurons requires many more isoforms that tend to associate with specific exon clusters or isoforms. We conclude that the role of the Dscam1 diversity in dendrite self/non-self discrimination is nonspecifically mediated by its isoform diversity. In contrast, a separate role requires variable domain- or isoform-related functions and is essential for other neurodevelopmental contexts, such as axonal growth and branching. Our findings shed new light on a general principle for the role of Dscam1 diversity in neuronal wiring.
果蝇黑腹果蝇唐氏综合征细胞黏附分子 1(Dscam1)通过外显子 4、6 和 9 簇的选择性剪接,编码 19008 种不同的细胞外结构域同工型。然而,目前尚不清楚是否是特定的同工型或外显子簇具有特定的意义。在这里,我们通过表型多样性相关性分析,揭示了 Dscam1 多样性在神经元连接中的冗余和特异性作用。从包含外显子 4、6 或 9 簇的内源性基因座进行了一系列缺失突变,减少到 396 到 18612 个潜在的细胞外结构域同工型。在所评估的 3 种神经元中,树突自/非自我识别需要最小数量的同工型(约 2000 个),与外显子簇或同工型无关。相比之下,蘑菇体和机械感觉神经元中的正常轴突模式形成需要更多的同工型,这些同工型往往与特定的外显子簇或同工型相关联。我们得出结论,Dscam1 多样性在树突自/非自我识别中的作用是非特异性地由其同工型多样性介导的。相比之下,一个单独的作用需要可变结构域或同工型相关功能,对于其他神经发育背景(如轴突生长和分支)是必不可少的。我们的研究结果为 Dscam1 多样性在神经元连接中的作用提供了一个新的认识。