Neural Lineages of the<i>Drosophila</i>Brain: A Three-Dimensional Digital Atlas of the Pattern of Lineage Location and Projection at the Late Larval Stage

Pereanu, Wayne; Hartenstein, Volker

doi:10.1523/jneurosci.4708-05.2006

Cited by 127 publications

(234 citation statements)

References 60 publications

(71 reference statements)

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“…By contrast, the secondary neurons produced during the postembryonic neurogenic phase are much more homogeneous (Truman et al, 2004;Pereanu and Hartenstein, 2006;Brown and Truman, 2009;Zhou et al, 2009). As seen in Fig.…”

Section: Effects Of Notch On Neuronal Fates Of the Secondary Neurons mentioning

confidence: 88%

Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster

et al. 2010

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SUMMARYThe secondary neurons generated in the thoracic central nervous system of Drosophila arise from a hemisegmental set of 25 neuronal stem cells, the neuroblasts (NBs). Each NB undergoes repeated asymmetric divisions to produce a series of smaller ganglion mother cells (GMCs), which typically divide once to form two daughter neurons. We find that the two daughters of the GMC consistently have distinct fates. Using both loss-of-function and gain-of-function approaches, we examined the role of Notch signaling in establishing neuronal fates within all of the thoracic secondary lineages. In all cases, the 'A' (Notch ON ) sibling assumes one fate and the 'B' (Notch OFF ) sibling assumes another, and this relationship holds throughout the neurogenic period, resulting in two major neuronal classes: the A and B hemilineages. Apparent monotypic lineages typically result from the death of one sibling throughout the lineage, resulting in a single, surviving hemilineage. Projection neurons are predominantly from the B hemilineages, whereas local interneurons are typically from A hemilineages. Although sibling fate is dependent on Notch signaling, it is not necessarily dependent on numb, a gene classically involved in biasing Notch activation. When Numb was removed at the start of larval neurogenesis, both A and B hemilineages were still generated, but by the start of the third larval instar, the removal of Numb resulted in all neurons assuming the A fate. The need for Numb to direct Notch signaling correlated with a decrease in NB cell cycle time and may be a means for coping with multiple sibling pairs simultaneously undergoing fate decisions.

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Section: Effects Of Notch On Neuronal Fates Of the Secondary Neurons mentioning

confidence: 88%

Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster

et al. 2010

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“…Development 136 (20) of cell bodies, projection of secondary axon tracts, and the innervated set of compartments, we identified these four lineages, according to criteria and terminology established by Pereanu and Hartenstein (Pereanu and Hartenstein, 2006), as DPLam (AC), DALv2 (MC1), DALv3 (MC2) and BAla3 (PC); the AC, MC1 and MC2 lineages are thus protocerebral and the PC lineage is deutocerebral (Kumar et al, 2009). …”

Section: Research Articlementioning

confidence: 99%

“…Following a brief period of quiescence, during postembryonic larval development, neuroblasts re-enter the cell cycle and continue to divide in this asymmetric mode, giving rise to adult-specific neurons, which make up more than 90% of the adult central nervous system (CNS) (Prokop and Technau, 1991;Truman and Bate, 1988). The adult-specific neurons generated during larval life from each neuroblast form a lineage-related cluster of immature neurons, which wait until metamorphosis to differentiate and form functional circuits in the adult (Dumstrei et al, 2003;Pereanu and Hartenstein, 2006;Truman et al, 2004;Zheng et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Lineage-specific cell death in postembryonic brain development ofDrosophila

2009

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The Drosophila central brain is composed of thousands of neurons that derive from approximately 100 neuroblasts per hemisphere. Functional circuits in the brain require precise neuronal wiring and tight control of neuronal numbers. How this accurate control of neuronal numbers is achieved during neural development is largely unclear. Specifically, the role of programmed cell death in control of cell numbers has not been studied in the central brain neuroblast lineages. Here, we focus on four postembryonic neuroblast lineages in the central brain identified on the basis that they express the homeobox gene engrailed (en). For each lineage,we determine the total number of adult-specific neurons generated as well as number and pattern of en-expressing cells. We then demonstrate that programmed cell death has a pronounced effect on the number of cells in the four lineages; approximately half of the immature adult-specific neurons in three of the four lineages are eliminated by cell death during postembryonic development. Moreover, we show that programmed cell death selectively affects en-positive versus en-negative cells in a lineage-specific manner and, thus, controls the relative number of en-expressing neurons in each lineage. Furthermore, we provide evidence that Notch signaling is involved in the regulation of en expression. Based on our findings, we conclude that lineage-specific programmed cell death plays a prominent role in the generation of neuronal number and lineage diversity in the Drosophila brain.

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“…Neurons born in the embryo control larval behavior and may become reorganized during metamorphosis to contribute to the adult neural circuitry (Lee et al, 1999;Marin et al, 2005;Technau and Heisenberg, 1982;Truman et al, 2004). After a period of mitotic quiescence, embryonic brain NBs (now called postembryonic NBs) become reactivated in the larva to add large numbers of adult-specific neural cells (Ito and Hotta, 1992;Pereanu and Hartenstein, 2006). About 100 postembryonic cell lineages (per hemisphere) have been recognized in the larval brain (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…About 100 postembryonic cell lineages (per hemisphere) have been recognized in the larval brain (e.g. Cardona et al, 2010;Kumar et al, 2009;Lai et al, 2008;Larsen et al, 2009;Lichtneckert et al, 2007;Pereanu and Hartenstein, 2006;Yu et al, 2009;Yu et al, 2010), suggesting that almost all embryonic brain NBs become reactivated postembryonically. However, the assignment to individually identified NBs (Urbach and Technau, 2003a) and an analysis of the embryonic components of these brain lineages are still pending.…”

Section: Introductionmentioning

confidence: 99%

Origin ofDrosophilamushroom body neuroblasts and generation of divergent embryonic lineages

et al. 2012

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Key to understanding the mechanisms that underlie the specification of divergent cell types in the brain is knowledge about the neurectodermal origin and lineages of their stem cells. Here, we focus on the origin and embryonic development of the four neuroblasts (NBs) per hemisphere in Drosophila that give rise to the mushroom bodies (MBs), which are central brain structures essential for olfactory learning and memory. We show that these MBNBs originate from a single field of proneural gene expression within a specific mitotic domain of procephalic neuroectoderm, and that Notch signaling is not needed for their formation. Subsequently, each MBNB occupies a distinct position in the developing MB cortex and expresses a specific combination of transcription factors by which they are individually identifiable in the brain NB map. During embryonic development each MBNB generates an individual cell lineage comprising different numbers of neurons, including intrinsic γ-neurons and various types of non-intrinsic neurons that do not contribute to the MB neuropil. This contrasts with the postembryonic phase of MBNB development during which they have been shown to produce identical populations of intrinsic neurons. We show that different neuron types are produced in a lineage-specific temporal order and that neuron numbers are regulated by differential mitotic activity of the MBNBs. Finally, we demonstrate that γ-neuron axonal outgrowth and spatiotemporal innervation of the MB lobes follows a lineage-specific mode. The MBNBs are the first stem cells of the Drosophila CNS for which the origin and complete cell lineages have been determined.

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Neural Lineages of theDrosophilaBrain: A Three-Dimensional Digital Atlas of the Pattern of Lineage Location and Projection at the Late Larval Stage

Cited by 127 publications

References 60 publications

Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster

Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster

Lineage-specific cell death in postembryonic brain development ofDrosophila

Origin ofDrosophilamushroom body neuroblasts and generation of divergent embryonic lineages

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