Abstract
Dynein is a multi-subunit motor protein that moves toward the minus-end of microtubules, and plays important roles in fly development. We identified Dhc64Cm115, a new mutant allele of the fly Dynein heavy chain 64C (Dhc64C) gene whose heterozygotes survive against lethality induced by overexpression of Sol narae (Sona). Sona is a secreted metalloprotease that positively regulates Wingless (Wg) signaling, and promotes cell survival and proliferation. Knockdown of Dhc64C in fly wings induced extensive cell death accompanied by widespread and disorganized expression of Wg. The disrupted pattern of the Wg protein was due to cell death of the Wg-producing cells at the DV midline and overproliferation of the Wg-producing cells at the hinge in disorganized ways. Coexpression of Dhc64C RNAi and p35 resulted in no cell death and normal pattern of Wg, demonstrating that cell death is responsible for all phenotypes induced by Dhc64C RNAi expression. The effect of Dhc64C on Wg-producing cells was unique among components of Dynein and other microtubule motors. We propose that Dhc64C differentially regulates survival of Wg-producing cells, which is essential for maintaining normal expression pattern of Wg for wing development.
Highlights
Apoptosis is a programmed cell death critical for the development and homeostasis of all organisms, which functions by eliminating unwanted cells generated under both normal and stress conditions [1]
Sol narae (Sona) is important for cell survival and compensatory proliferation by increasing the level of Cyclin D for cell division in order to maintain tissue size and shape [11,12]
We report here that sona and Dynein heavy chain 64C (Dhc64C) show a positive genetic interaction, and the knockdown of Dhc64C induces apoptosis of Wg-producing cells in the DV midline, whereas uncontrolled compensatory proliferation of Wg-producing cells originated from the hinge region, which resulted in abnormally high numbers of Wg-producing cells in entire wing discs
Summary
Apoptosis is a programmed cell death critical for the development and homeostasis of all organisms, which functions by eliminating unwanted cells generated under both normal and stress conditions [1]. Apoptosis often occurs concomitantly with compensatory proliferation to maintain tissue size and shape [2]. Drosophila melanogaster is a great model system for studying apoptosis and compensatory proliferation whose mechanism and components are highly conserved during evolution [3,4,5]. The wing imaginal disc, the primordium of the adult wing, is especially suitable for studying these processes because it shows little apoptosis during normal development but develops to a normal wing even with 40–60% of apoptotic cells via efficient compensatory proliferation [6]. Sona is important for cell survival and compensatory proliferation by increasing the level of Cyclin D for cell division in order to maintain tissue size and shape [11,12]
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