Abstract
Cell proliferation, specification and terminal differentiation must be precisely coordinated during brain development to ensure the correct production of different neuronal populations. Most Drosophila neuroblasts (NBs) divide asymmetrically to generate a new NB and an intermediate progenitor called ganglion mother cell (GMC) which divides only once to generate two postmitotic cells called ganglion cells (GCs) that subsequently differentiate into neurons. During the asymmetric division of NBs, the homeodomain transcription factor PROSPERO is segregated into the GMC where it plays a key role as cell fate determinant. Previous work on embryonic neurogenesis has shown that PROSPERO is not expressed in postmitotic neuronal progeny. Thus, PROSPERO is thought to function in the GMC by repressing genes required for cell-cycle progression and activating genes involved in terminal differentiation. Here we focus on postembryonic neurogenesis and show that the expression of PROSPERO is transiently upregulated in the newly born neuronal progeny generated by most of the larval NBs of the OL and CB. Moreover, we provide evidence that this expression of PROSPERO in GCs inhibits their cell cycle progression by activating the expression of the cyclin-dependent kinase inhibitor (CKI) DACAPO. These findings imply that PROSPERO, in addition to its known role as cell fate determinant in GMCs, provides a transient signal to ensure a precise timing for cell cycle exit of prospective neurons, and hence may link the mechanisms that regulate neurogenesis and those that control cell cycle progression in postembryonic brain development.
Highlights
In order to give rise to the diversity and specificity of cells types in the brain, cell proliferation, specification and terminal differentiation must be precisely coupled in space and time during development to ensure the correct number of cells in different populations and specify their resulting connectivity
Most of the cells comprising the adult brain are generated from progenitor cells called neuroblasts (NBs) that become quiescent at the end of embryonic development and that re-enter the cell cycle at different times during larval development depending on the region and cell type
Each Type I NB divides asymmetrically several times to generate in each division a new NB and an intermediate ganglion mother cell (GMC) progenitor which divides once to generate two postmitotic daughters called ganglion cells (GCs) that differentiate into neurons [3,6,14] (Fig. 1C)
Summary
In order to give rise to the diversity and specificity of cells types in the brain, cell proliferation, specification and terminal differentiation must be precisely coupled in space and time during development to ensure the correct number of cells in different populations and specify their resulting connectivity. Most of the cells comprising the adult brain are generated from progenitor cells called neuroblasts (NBs) that become quiescent at the end of embryonic development and that re-enter the cell cycle at different times during larval development depending on the region and cell type. Each Type I NB divides asymmetrically several times to generate in each division a new NB and an intermediate GMC progenitor which divides once to generate two postmitotic daughters called ganglion cells (GCs) that differentiate into neurons [3,6,14] (Fig. 1C). We identify the pan-neural bHLH transcription factor DEADPAN (DPN) and the cyclin kinase inhibitor DACAPO (DAP), as candidate downstream effectors of PROS in this function In view of these findings, we discuss the implications of different roles of PROS in embryonic versus post-embryonic neurogenesis of Drosophila
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