Abstract
Despite the importance of precisely regulating stem cell division, the molecular basis for this control is still elusive. Here, we show that surface glia in the developing Drosophila brain play essential roles in regulating the proliferation of neural stem cells, neuroblasts (NBs). We found that two classes of extracellular factors, Dally-like (Dlp), a heparan sulfate proteoglycan, and Glass bottom boat (Gbb), a BMP homologue, are required for proper NB proliferation. Interestingly, Dlp expressed in perineural glia (PG), the most outer layer of the surface glia, is responsible for NB proliferation. Consistent with this finding, functional ablation of PG using a dominant-negative form of dynamin showed that PG has an instructive role in regulating NB proliferation. Gbb acts not only as an autocrine proliferation factor in NBs but also as a paracrine survival signal in the PG. We propose that bidirectional communication between NBs and glia through TGF-β signaling influences mutual development of these two cell types. We also discuss the possibility that PG and NBs communicate via direct membrane contact or transcytotic transport of membrane components. Thus, our study shows that the surface glia acts not only as a simple structural insulator but also a dynamic regulator of brain development.
Highlights
The Drosophila CNS develops from neural stem cells called neuroblasts (NBs)[1,2,3]
This observation suggests that one or more heparan sulfate proteoglycans (HSPGs) molecules are required for normal NB proliferation
No obvious small brain phenotype is caused by mutations in dally, one of two integral-membrane HSPGs of the glypican type (Fig. 1D), or dSyndecan, the only Drosophila Syndecan homologue
Summary
The Drosophila CNS develops from neural stem cells called neuroblasts (NBs)[1,2,3]. The self-renewal and differentiation of NBs are thought to be controlled by both intrinsic programs in the NBs as well as extrinsic cues. The TGF-β pathway is an evolutionarily conserved signal transduction module that mediates diverse biological processes in animals, including stem cell control. Like in mammals, both the BMP and Activin branches are required for Drosophila development and homeostasis[24]. Activin branch ligands play diverse roles in growth and patterning in Drosophila, including control of imaginal cell proliferation[30,31,32], neuroblast proliferation[6], neuron remodeling[33,34], axon guidance[35,36], and sugar homeostasis[37]. The biological role of surface glia in regulating neural development remains to be elucidated
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