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

PLoS One. 2014 Jul 8;9(7):e101433. doi: 10.1371/journal.pone.0101433. eCollection 2014.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Cell Differentiation* / genetics
  • Drosophila / embryology
  • Drosophila / physiology*
  • Female
  • Gene Expression Regulation, Developmental
  • Gene Expression Regulation, Enzymologic
  • Male
  • Mutation
  • Neuroepithelial Cells / cytology*
  • Neuroepithelial Cells / metabolism
  • Optic Lobe, Nonmammalian / cytology
  • Optic Lobe, Nonmammalian / embryology
  • Optic Lobe, Nonmammalian / metabolism*
  • Stem Cells / cytology*
  • Trehalase / genetics
  • Trehalase / metabolism*

Substances

  • Trehalase

Grants and funding

This work was supported by grants from National Science Foundation of China (grant number: 30671035, http://www.nsfc.gov.cn/), National Basic Sciences Research Program of Ministry of Science and Technology of China (grant number: 2007CB947203, http://www.most.gov.cn) to H. Luo, and National Basic Research Program of Ministry of Science and Technology of China (grant number: 2013CB835100, http://www.most.gov.cn), the Tsinghua University Initiative Scientific Research Program (grant number: 20111080956, http://www.moe.gov.cn) to Y. Zhong. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.