Trehalase regulates neuroepithelial stem cell maintenance and differentiation in the Drosophila optic lobe.

Xi Chen,Hongbin Wang,Hong Luo,Yaru Quan,Hongyan Wang

doi:10.1371/journal.pone.0101433

Xi Chen, Hongbin Wang + Show 3 more

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https://doi.org/10.1371/journal.pone.0101433

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Abstract

As one of the major hydrolases in Drosophila, trehalase (Treh) catalyzes the hydrolysis of trehalose into glucose providing energy for flight muscle activity. Treh is highly conserved from bacteria to humans, but little is known about its function during animal development. Here, we analyze the function of Treh in Drosophila optic lobe development. In the optic lobe, neuroepithelial cells (NEs) first divide symmetrically to expand the stem cell pool and then differentiate into neuroblasts, which divide asymmetrically to generate medulla neurons. We find that the knockdown of Treh leads to a loss of the lamina and a smaller medulla. Analyses of Treh RNAi-expressing clones and loss-of-function mutants indicate that the lamina and medulla phenotypes result from neuroepithelial disintegration and premature differentiation into medulla neuroblasts. Although the principal role of Treh is to generate glucose, the Treh loss-of-function phenotype cannot be rescued by exogenous glucose. Thus, our results indicate that in addition to being a hydrolase, Treh plays a role in neuroepithelial stem cell maintenance and differentiation during Drosophila optic lobe development.

Highlights

The optic lobe of the Drosophila brain is the visual processing center, which contains four neuropils: the lamina, medulla, lobula and lobula plate (Figure 1C) [1]
To study the function of Treh, we knocked down Treh activity by RNA interference (RNAi) using either c768Gal4 or c855a-Gal4, two drivers that are active in the optic lobe neuroepithelial cells (NEs) from the first instar stage onward [4,18]
We have shown that trehalase plays an important role in the maintenance of neuroepithelial stem cells in the Drosophila larval optic lobe

Summary

Introduction

The optic lobe of the Drosophila brain is the visual processing center, which contains four neuropils: the lamina, medulla, lobula and lobula plate (Figure 1C) [1]. The NEs on the medial edge of the OPC begin to differentiate into medulla neuroblasts (NBs) These neuroblasts undergo asymmetric division producing a neuroblast daughter and a smaller ganglion mother cell (GMC) that divides once to generate two medulla neurons (Figure 1B) [4,5,6,7]. This proliferation and differentiation pattern closely resembles that of neural progenitor cells in the developing vertebrate brain [8,9,10]. Several signals have been identified that regulate the maintenance and differentiation of neuroepithelial stem cells, including the JAK/STAT, Notch, Fat/Hippo and EGFR pathways [11,12,13,14,15,16,17,18,19]

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