Abstract
BackgroundIn the mammalian brain, neural stem cells divide asymmetrically and often amplify the number of progeny they generate via symmetrically dividing intermediate progenitors. Here we investigate whether specific neural stem cell-like neuroblasts in the brain of Drosophila might also amplify neuronal proliferation by generating symmetrically dividing intermediate progenitors.ResultsCell lineage-tracing and genetic marker analysis show that remarkably large neuroblast lineages exist in the dorsomedial larval brain of Drosophila. These lineages are generated by brain neuroblasts that divide asymmetrically to self renew but, unlike other brain neuroblasts, do not segregate the differentiating cell fate determinant Prospero to their smaller daughter cells. These daughter cells continue to express neuroblast-specific molecular markers and divide repeatedly to produce neural progeny, demonstrating that they are proliferating intermediate progenitors. The proliferative divisions of these intermediate progenitors have novel cellular and molecular features; they are morphologically symmetrical, but molecularly asymmetrical in that key differentiating cell fate determinants are segregated into only one of the two daughter cells.ConclusionOur findings provide cellular and molecular evidence for a new mode of neurogenesis in the larval brain of Drosophila that involves the amplification of neuroblast proliferation through intermediate progenitors. This type of neurogenesis bears remarkable similarities to neurogenesis in the mammalian brain, where neural stem cells as primary progenitors amplify the number of progeny they generate through generation of secondary progenitors. This suggests that key aspects of neural stem cell biology might be conserved in brain development of insects and mammals.
Highlights
In the mammalian brain, neural stem cells divide asymmetrically and often amplify the number of progeny they generate via symmetrically dividing intermediate progenitors
Large neuroblast lineages are located in the dorsomedial brain hemispheres Since most of the secondary, adult-specific neurons of the brain are generated during larval development [38], we used mosaic-based MARCM techniques to label NB lineages in the developing larval nervous system [39]
We identify a novel intermediate neural progenitor generated by asymmetric division of a subset of the Drosophila brain neuroblasts during the postembryonic phase of neurogenesis
Summary
Neural stem cells divide asymmetrically and often amplify the number of progeny they generate via symmetrically dividing intermediate progenitors. We investigate whether specific neural stem cell-like neuroblasts in the brain of Drosophila might amplify neuronal proliferation by generating symmetrically dividing intermediate progenitors. Understanding how neural stem cells maintain their pluripotent state and how their progeny differentiate into distinct neural fates is of central importance for understanding nervous system development (for recent reviews, see [13]). Drosophila neural stem cells, called neuroblasts (NBs), delaminate as single cells from the neuroectoderm and undergo repeated asymmetric cell divisions, each of which self-renew the NB while producing a smaller neural progenitor cell called a ganglion mother cell (GMC). Following a period of quiescence, most NBs resume their asymmetric mode of proliferative divisions during post-embryonic development and generate the lineage-related clusters of secondary adult-specific neurons that make up the bulk of the adult central brain and thoracic ganglia [13,14,15,16]
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