Department of Biochemistry and Molecular Biophysics, Kansas State University, Manhattan, KS, 66506, USA.
Department of Cell Biology and Biophysics, School of Biological Sciences, University of Missouri-Kansas, Kansas City, MO, 64110, USA.
Cell Death Dis. 2018 Jul 3;9(7):740. doi: 10.1038/s41419-018-0756-x.
In holometabolous insects, developmentally controlled programmed cell death (PCD) is a conserved process that destroys a subset of larval tissues for the eventual creation of new adult structures. This process of histolysis is relatively well studied in salivary gland and midgut tissues, while knowledge concerning larval muscle destruction is limited. Here, we have examined the histolysis of a group of Drosophila larval abdominal muscles called the dorsal external oblique muscles (DEOMs). Previous studies have defined apoptosis as the primary mediator of DEOM breakdown, whose timing is controlled by ecdysone signaling. However, very little is known about other factors that contribute to DEOM destruction. In this paper, we examine the role of thin (tn), which encodes for the Drosophila homolog of mammalian TRIM32, in the regulation of DEOM histolysis. We find that loss of Tn blocks DEOM degradation independent of ecdysone signaling. Instead, tn genetically functions in a pathway with the death-associated inhibitor of apoptosis (DIAP1), Dronc, and death-associated APAF1-related killer (Dark) to regulate apoptosis. Importantly, blocking Tn results in the absence of active Caspase-3 immunostaining, upregulation of DIAP1 protein levels, and inhibition of Dronc activation. DIAP1 and Dronc mRNA levels are not altered in tn mutants, showing that Tn acts post-transcriptionally on DIAP1 to regulate apoptosis. Herein, we also find that the RING domain of Tn is required for DEOM histolysis as loss of this domain results in higher DIAP1 levels. Together, our results suggest that the direct control of DIAP1 levels, likely through the E3 ubiquitin ligase activity of Tn, provides a mechanism to regulate caspase activity and to facilitate muscle cell death.
在完全变态的昆虫中,发育调控的程序性细胞死亡(PCD)是一个保守的过程,它会破坏幼虫组织的一部分,为新的成虫结构的形成创造条件。这个组织溶解的过程在唾液腺和中肠组织中已经得到了相对较好的研究,而关于幼虫肌肉破坏的知识则有限。在这里,我们研究了一组被称为背外侧外肌(DEOMs)的果蝇幼虫腹侧肌肉的组织溶解。先前的研究已经将凋亡定义为 DEOM 分解的主要介导者,其时间由蜕皮激素信号控制。然而,关于有助于 DEOM 破坏的其他因素知之甚少。在本文中,我们研究了果蝇同源物 TRIM32 的瘦素(tn)在 DEOM 组织溶解中的作用。我们发现,tn 的缺失会阻止 DEOM 的降解,而不依赖于蜕皮激素信号。相反,tn 在与凋亡相关的抑制因子(DIAP1)、Dronc 和凋亡相关 APAF1 相关杀手(Dark)的遗传途径中发挥作用,以调节凋亡。重要的是,阻断 tn 会导致活性 Caspase-3 免疫染色缺失、DIAP1 蛋白水平上调以及 Dronc 激活抑制。tn 突变体中 DIAP1 和 Dronc mRNA 水平没有改变,表明 tn 在后转录水平上作用于 DIAP1 以调节凋亡。此外,我们还发现 tn 的 RING 结构域是 DEOM 组织溶解所必需的,因为该结构域的缺失会导致更高的 DIAP1 水平。总之,我们的结果表明,通过 tn 的 E3 泛素连接酶活性直接控制 DIAP1 水平,为调节 Caspase 活性和促进肌肉细胞死亡提供了一种机制。