Programmed cell death in the embryonic central nervous system of Drosophila melanogaster

Institute of Genetics, University of Mainz, Saarstrasse 21, D-55122 Mainz, Germany.
Development (Impact Factor: 6.46). 02/2007; 134(1):105-16. DOI: 10.1242/dev.02707
Source: PubMed


Although programmed cell death (PCD) plays a crucial role throughout Drosophila CNS development, its pattern and incidence remain largely uninvestigated. We provide here a detailed analysis of the occurrence of PCD in the embryonic ventral nerve cord (VNC). We traced the spatio-temporal pattern of PCD and compared the appearance of, and total cell numbers in, thoracic and abdominal neuromeres of wild-type and PCD-deficient H99 mutant embryos. Furthermore, we have examined the clonal origin and fate of superfluous cells in H99 mutants by DiI labeling almost all neuroblasts, with special attention to segment-specific differences within the individually identified neuroblast lineages. Our data reveal that although PCD-deficient mutants appear morphologically well-structured, there is significant hyperplasia in the VNC. The majority of neuroblast lineages comprise superfluous cells, and a specific set of these lineages shows segment-specific characteristics. The superfluous cells can be specified as neurons with extended wild-type-like or abnormal axonal projections, but not as glia. The lineage data also provide indications towards the identities of neuroblasts that normally die in the late embryo and of those that become postembryonic and resume proliferation in the larva. Using cell-specific markers we were able to precisely identify some of the progeny cells, including the GW neuron, the U motoneurons and one of the RP motoneurons, all of which undergo segment-specific cell death. The data obtained in this analysis form the basis for further investigations into the mechanisms involved in the regulation of PCD and its role in segmental patterning in the embryonic CNS.

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    • "When this process is absent or dysfunctional, a broad spectrum of developmental abnormalities and diseases can occur (Meier et al. 2000). Given its diverse and complex cell populations, the nervous system is particularly reliant on PCD and, thus, a model system for studying the process (Oppenheim 1991; Yeo and Gautier 2004; Rogulja-Ortmann et al. 2007). Indeed, during vertebrate development , 50% of neurons born must undergo PCD and the corpses must be cleared, a massive and necessary task to maintain CNS homeostasis . "
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    Cold Spring Harbor perspectives in biology 07/2015; 7(10). DOI:10.1101/cshperspect.a020545 · 8.68 Impact Factor
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    • "Embryos were fixed as described (Rogulja-Ortmann et al., 2007). Second and third instar larvae (L2/L3) were opened along the dorsal midline and flattened to a silicon ground using minutien fine pins. "
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    Development 07/2013; 140(17). DOI:10.1242/dev.093245 · 6.46 Impact Factor
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    • "Many cells in the developing ventral nerve cord, for example, are known to die in the late embryo (Truman et al. 1992; Abrams et al. 1993; Rogulja-Ortmann et al. 2007). Preventing this cell death results in abnormal axonal projections and failure of ventral nerve cord condensation (Abrams et al. 1993; Rogulja-Ortmann et al. 2007; Page & Olofsson 2008). In the ventral nerve cord, the so-called " pioneer " neurons undergo segment-specific cell death after guiding the so-called " follower " axons (Miguel- Aliaga & Thor 2004). "
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    ABSTRACT: A large number of cells die via programmed cell death during the normal development of the Drosophila optic lobe. In this study, we report the precise spatial and temporal pattern of cell death in this organ. Cell death in the developing optic lobe occurs in two distinct phases. The first phase extends from the start of metamorphosis to the mid-pupal stage. During this phase, a large number of cells die in the optic lobe as a whole, with a peak of cell death at an early pupal stage in the lamina and medulla cortices and the region of the T2/T3/C neurons, and a smaller number of dead cells observed in the lobula plate cortex. The second phase extends from the mid-pupal stage to eclosion. Throughout this period, a small number of dying cells can be observed, with a small peak at a late pupal stage. Most of the dying cells are neurons. During the first phase, dying cells are distributed in specific patterns in cortices. The lamina cortex contains two distinct clusters of dying cells; the medulla cortex, four clusters; the lobula plate cortex, one cluster; and the region of the T2/T3/C neurons, one cluster. Many of the clusters maintain their distinct positions in the optic lobe but others extend the region they cover during development. The presence of distinct clusters of dying cells at different phases suggests that distinct mechanisms control cell death during different stages of optic lobe development in Drosophila.
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