Programmed cell death during Drosophila embryogenesis (original) (raw)

Developmentally programmed cell death in Drosophila

Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 2013

During the development of metazoans, programmed cell death (PCD) is essential for tissue patterning, removal of unwanted cells and maintaining homeostasis. In the past 20 years Drosophila melanogaster has been one of the systems of choice for studies involving developmental cell death, providing an ideal genetically tractable model of intermediary complexity between Caenorhabditis elegans and mammals. The lessons learned from studies using Drosophila indicate both the conserved nature of the many cell death pathways as well as novel and unexpected mechanisms. In this article we review the understanding of PCD during Drosophila development, highlighting the key mechanisms that are evolutionarily conserved as well as apparently unusual pathways, which indicate divergence, but provide evidence of complexity acquired during organismic evolution. This article is part of a Special Section entitled: Cell Death Pathways.

Death to flies: Drosophila as a model system to study programmed cell death

Journal of Immunological Methods, 2002

Programmed cell death (PCD) is essential for the removal of unwanted cells and is critical for both restricting cell numbers and for tissue patterning during development. Components of the cell death machinery are remarkably conserved through evolution, from worms to mammals. Central to the PCD process is the family of cysteine proteases, known as caspases, which are activated by death-inducing signals. Comparisons between C. elegans and mammalian PCD have shown that there is additional complexity in the regulation of PCD in mammals. The fruitfly, Drosophila melanogaster, is proving an ideal genetically tractable model organism, of intermediary complexity between C. elegans and mammals, in which to study the intricacies of PCD. Here, we review the literature on PCD during Drosophila development, highlighting the methods used in these studies. D 2002 Published by Elsevier Science B.V.

Programmed death during Drosophila embryogenesis

Development

changes responsible for the selective affinity to these dyes. Cell death begins at stage 11 (~7 hours) of embryogenesis and thereafter becomes widespread, affecting many different tissues and regions of the embryo. Although the distribution of dying cells changes drastically over time, the overall pattern of cell death is highly reproducible for any given developmental stage. Detailed analysis of cell death in the central nervous system of stage 16 embryos (13-16 hours) revealed asymmetries in the exact number and position of dying cells on either side of the midline, suggesting that the decision to die may not be strictly predetermined at this stage. This work provides the basis for further molecular genetic studies on the control and execution of programmed cell death in Drosophila.

Programmed Cell Death in Animal Development

Cell, 1997

condense, and the organelles and plasma membrane retain their integrity in a process Kerr and his colleagues and Martin C. Raff Developmental Neurobiology Programme named apoptosis. The dead cells or their fragments are rapidly phagocytosed by neighboring cells or macro-MRC Laboratory for Molecular Cell Biology University College London phages before there is any leakage of the contents of the cells, and thus they do not induce an inflammatory London, WC1E 6BT United Kingdom response. Apoptotic cells in developing tissues are almost always inside other cells (Figures 1A-1C), suggesting that dying cells are usually phagocytosed before they display the morphological changes of apoptosis. Programmed cell death (PCD) occurs during the devel-Because apoptotic cell deaths usually look so similar opment of all animals that have been studied, but only from tissue to tissue and animal to animal (Figures 1Arecently has its molecular basis been discovered. In this 1C), Kerr and his colleagues proposed that these deaths review, we briefly consider some of the main events reflect the operation of an active, intracellular death proin the history of PCD in animal development. We then gram that can be activated or inhibited by a variety of summarize what has been learned about the molecular physiological or pathological environmental stimuli. mechanism of PCD and some of the intracellular pro-It took almost another 20 years, however, before the teins that control it. We next discuss the functions of idea that animal cells have a built-in death, or suicide, PCD in development and how PCD is regulated during program became generally accepted, largely through development by signals from other cells. Finally, we genetic studies in the nematode Caenorhabditis elegans consider what the evolutionary origins of PCD may have that identified genes that seem dedicated to the death been. program and its control (Horvitz et al., 1982; Ellis and Horvitz, 1986), and then through the finding that some Some History of these genes were homologous to mammalian genes Soon after it was recognized in the middle of the last

The head involution defective gene of Drosophila melanogaster functions in programmed cell death

Genes & Development, 1995

Access the most recent version at doi: 1995 9: 1694-1708 Genes Dev. M E Grether, J M Abrams, J Agapite, et al. functions in programmed cell death. The head involution defective gene of Drosophila melanogaster References http://genesdev.cshlp.org/content/9/14/1694#related-urls Article cited in: http://genesdev.cshlp.org/content/9/14/1694.refs.html Deletions of chromosomal region, 75C1,2 block virtually all programmed cell death (PCD) in the Drosophila embryo. We have identified a gene previously in this interval, reaper {rpr), which encodes an important regulator of PCD. Here we report the isolation of a second gene in this region, head involution defective (hid}, which plays a similar role in PCD. hid mutant embryos have decreased levels of cell death and contain extra cells in the head. We have cloned the hid gene and find that its expression is sufficient to induce PCD in cell death defective mutants. The hid gene appears to encode a novel 410-amino-acid protein, and its mRNA is expressed in regions of the embryo where cell death occurs. Ectopic expression of hid in the Drosophila retina results in eye ablation. This phenotype can be suppressed completely by expression of the anti-apoptotic p35 protein from baculovirus, indicating that p35 may act genetically downstream from hid. Cell deaths that occur during the development of essentially all metazoan animals display a characteristic ultrastructural morphology known as apoptosis [Kerr et al. WyUie et al. 1980). Because it is thought that these natural cell deaths result from the execution of an active, gene-directed cell suicide program, the process of apoptosis is also referred to as programmed cell death (PCD). Strong support for this concept has come from genetic studies in the nematode Caenorhabditis elegans, where a large number of mutations affecting specific aspects of PCD have been isolated and ordered into a genetic pathway [for review, see Hengartner and Horvitz 1994a, b). In particular, three genes, ced-3, ced-4, and ced-9, have been shown to control the onset of all somatic PCDs in the nematode. Interestingly, two of these genes, ced-3 and ced-9, have mammalian homologs that are believed to play a similar function during apoptosis. The ced-3 gene is homologous to a family of cysteine proteases that includes interleukin-l[3 converting enzyme, and ced-9 is a member of the bcl-2 family . Moreover, expression of human Bcl-2 can suppress some PCD in C. elegans and can partially Present addresses: ~University

Genetic control of programmed cell death in Drosophila

Science, 1994

Apoptosis is a genetically controlled form of cell death that is an important feature of animal development and homeostasis. The genes involved in the control and execution of apoptosis are conserved throughout evolution. However, the actual molecular mechanisms used by these genes vary from species to species. In this review, we focus on the genetic components of apoptosis in the fruit fly Drosophila melanogaster, and compare their mode of action to the one employed by the homologous genes in mammals. We also cover recent advances that show that apoptotic genes have a requirement in processes other than apoptosis.

A comparison of programmed cell death between species

Genome biology, 2000

Key components of the programmed cell death pathway are conserved between Caenorhabditis elegans, Drosophila melanogaster and humans. The search for additional homologs has been facilitated by the availability of the entire genomic sequence for each of these organisms.