Macrophages and glia participate in the removal of apoptotic neurons from the <i>Drosophila</i> embryonic nervous system

Sonnenfeld, Margaret; Jacobs, J. Roger

doi:10.1002/cne.903590410

Cited by 103 publications

(90 citation statements)

References 59 publications

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“…79 In the Drosophila embryo there is some evidence of phagocy- tosis by glial cells. 80 However, the most efficient embryonic phagocytes are professional`macrophages', the phagocytic hemocytes or blood cells.…”

Section: Phagocytosis Is a Crucial ®Nal Step In Apoptosismentioning

confidence: 99%

Molecular mechanisms of cell death and phagocytosis in Drosophila

2000

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The genetic tools available in Drosophila have facilitated our understanding of how apoptosis is regulated and executed in the context of the developing organism. All embryonic apoptosis is initiated by the activity of three genes, rpr, grim and hid. Each of these genes is independently regulated, allowing developmental apoptosis to be finely controlled. These initiators in turn activate the core apoptotic machinery, including the caspases. Drosophila counterparts to other conserved components of the apoptotic machinery have been recently identified, and we discuss how these may be integrated into the process of normal developmentally regulated cell death. We also outline the role that phagocytosis plays in the final stages of apoptosis and consider the molecular mechanisms guiding the elimination of apoptotic corpses.

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Section: Phagocytosis Is a Crucial ®Nal Step In Apoptosismentioning

confidence: 99%

Molecular mechanisms of cell death and phagocytosis in Drosophila

2000

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“…Several studies over the last decade have identified different kinds of apoptotic cells in the CNS (White et al, 1994;Sonnenfeld and Jacobs, 1995;Hidalgo et al, 2001;Peterson et al, 2002;Lundell et al, 2003;Miguel-Aliaga and Thor, 2004;Karcavich and Doe, 2005). In most cases, the developmental signals responsible for inducing PCD in these cells are unclear.…”

Section: Introductionmentioning

confidence: 99%

“…Other groups have reported PCD occurring in postmitotic differentiated neural cells. Sonnenfeld and Jacobs (Sonnenfeld and Jacobs, 1995) were the first to report degeneration of differentiated midline glial cells upon completing their function in the morphogenesis of commissural axon tracts in early embryogenesis. Hidalgo and colleagues (Hidalgo et al, 2001) showed that survival of longitudinal glia (LG) depends on the Neuregulin trophic factor homolog Vein.…”

Section: Introductionmentioning

confidence: 99%

Programmed cell death in the embryonic central nervous system ofDrosophila melanogaster

et al. 2007

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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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“…Although the existence of the Drosophila homologue of the gene coding for the macrophage PS receptor has been noted (21), its involvement in phagocytosis in Drosophila is unknown. A large number of cells undergo apoptosis during development of Drosophila and are eliminated through phagocytosis by macrophage-like hemocytes or glia (30,31). In the present study, we examined the mode of phagocytosis of apoptotic cells in Drosophila both in vitro and in vivo, focusing on the involvement of PS on target cells and Croquemort and Draper on phagocytes.…”

mentioning

confidence: 99%

Draper-mediated and Phosphatidylserine-independent Phagocytosis of Apoptotic Cells by Drosophila Hemocytes/Macrophages

Manaka

Kuraishi

Shiratsuchi

et al. 2004

Journal of Biological Chemistry

176

174

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The mechanism of phagocytic elimination of dying cells in Drosophila is poorly understood. This study was undertaken to examine the recognition and engulfment of apoptotic cells by Drosophila hemocytes/macrophages in vitro and in vivo. In the in vitro analysis, l(2)mbn cells (a cell line established from larval hemocytes of a tumorous Drosophila mutant) were used as phagocytes. When l(2)mbn cells were treated with the molting hormone 20-hydroxyecdysone, the cells acquired the ability to phagocytose apoptotic S2 cells, another Drosophila cell line. S2 cells undergoing cycloheximide-induced apoptosis exposed phosphatidylserine on their surface, but their engulfment by l(2)mbn cells did not seem to be mediated by phosphatidylserine. The level of Croquemort, a candidate phagocytosis receptor of Drosophila hemocytes/macrophages, increased in l(2)mbn cells after treatment with 20-hydroxyecdysone, whereas that of Draper, another candidate phagocytosis receptor, remained unchanged. However, apoptotic cell phagocytosis was reduced when the expression of Draper, but not of Croquemort, was inhibited by RNA interference in hormone-treated l(2)mbn cells. We next examined whether Draper is responsible for the phagocytosis of apoptotic cells in vivo using an assay for engulfment based on assessing DNA degradation of apoptotic cells in dICAD mutant embryos (which only occurred after ingestion by the phagocytes). RNA interference-mediated decrease in the level of Draper in embryos of mutant flies was accompanied by a decrease in the number of cells containing fragmented DNA. Furthermore, histochemical analyses of dispersed embryonic cells revealed that the level of phagocytosis of apoptotic cells by hemocytes/macrophages was reduced when Draper expression was inhibited. These results indicate that Drosophila hemocytes/macrophages execute Draper-mediated phagocytosis to eliminate apoptotic cells.

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Macrophages and glia participate in the removal of apoptotic neurons from the Drosophila embryonic nervous system

Cited by 103 publications

References 59 publications

Molecular mechanisms of cell death and phagocytosis in Drosophila

Molecular mechanisms of cell death and phagocytosis in Drosophila

Programmed cell death in the embryonic central nervous system ofDrosophila melanogaster

Draper-mediated and Phosphatidylserine-independent Phagocytosis of Apoptotic Cells by Drosophila Hemocytes/Macrophages

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