Skip to main content
SpringerLink
Log in

Apoptosis in Drosophila

  • Chapter
Apoptosis Genes

  • 137 Accesses

Abstract

Holometabolous insects, such as the dipteran Drosophila, exhibit two distinct life forms and undergo a complete metamorphosis. The Drosophila embryo develops over the course of one day and hatches into a motile and feeding first instar larva, which grows and subsequently moults twice (Figure 1). The first and second larval instars each last about a day, while the third instar lasts approximately three days. At the end of the third larval instar, the animal ceases to feed, climbs up a suitable substrate, and initiates pupariation. The pupal stage lasts approximately four days, during which time the larva metamorphoses into the adult fly. The ease of rearing Drosophila, their fecundity, and short life cycle have all contributed to their use as a genetic model system (see Ashburner, 1989). In addition, the Drosophila genome is relatively small (∼1.6 X 108 base pairs per haploid genome), and is organised into only four chromosomes which are all linked by a common chromocentre. The large polytene chromosomes of the larval salivary gland greatly facilitate the cytological mapping of chromosomal rearrangements as well as the localisation of cloned genes via in situ hybridisation. In addition, the use of balancer chromosomes, which repress recombination and provide dominant phenotypic markers, greatly facilitates genetic screens and the stable maintenance of homozygous lethal chromosomes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abbott, M.K. and Lengyel, J.A. (1991) Embryonic head involution and rotation of male terminalia require the Drosophila locus head involution defective. Genetics 129}: 783–7

    PubMed  CAS  Google Scholar 

  • Abrams, J.M., Lux, A., Steller, H. and Krieger, M. (1992) Macrophages in Drosophila embryos and L2 cells exhibit scavenger receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA 89: 10375–10379.

    PubMed  CAS  Google Scholar 

  • Abrams, J.M., White K., Fessler, L. I. and Steller, H. (1993) Programmed cell death during Drosophila embryogenesis. Development 117: 29–43.

    PubMed  CAS  Google Scholar 

  • Alman, B.A., Li, C, Pajerski, M.E., et al. (1997) Increased beta-catenin protein and somatic APC mutations in sporadic fibromatoses. Am. J. Pathol. 151: 329–334.

    PubMed  CAS  Google Scholar 

  • Alnemri, E.S., Livingston, D.J., Nicholson, D.W., et al. (1996) Human ICE/CED-3 protease nomenclature. Cell 87: 171.

    PubMed  CAS  Google Scholar 

  • Ashburner, M. (1989) Drosophila a laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.

    Google Scholar 

  • Bellamy, C.O., Malcolmson, R.D., Harrison, D.J. and Wyllie, A.H. (1995) Cell death in health and disease: the biology and regulation of apoptosis. Semin. Cancer Biol. 6: 3–16.

    CAS  Google Scholar 

  • Bellen, H.J., O‘Kane, C.J., Wilson, C., et al. (1989) P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 3: 1288–1300.

    PubMed  CAS  Google Scholar 

  • Bender, W., Spierer, P. and Hogness, D.S. (1983a) Chromosomal walking and jumping to isolate DNA from the ACE and rosy loci and the Bithorax complex in Drosophila melanogaster. J. Mol. Biol. 168: 17–33.

    PubMed  CAS  Google Scholar 

  • Bender, W., Akam, M.E., Karch, F., et al. (1983b) Molecular genetics of the Bithorax complex in Drosophila melanogaster. Science 221: 23–29.

    PubMed  CAS  Google Scholar 

  • Bergeron L. Perez G.I. MacDonald G. et al. 1998. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev. 12 1304–1314

    Google Scholar 

  • Bernardoni, R., Vivancos, B. and Giangrande, A. (1997) glide/gcm is expressed and required in the scavenger cell lineage. Dev. Biol. 191: 118–130.

    PubMed  CAS  Google Scholar 

  • Bier, E., Vassin, H., Shepherd, S., et al. (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 3: 1273–1287.

    PubMed  CAS  Google Scholar 

  • Birnbaum, M.J., Clem, R.J. and Miller, L.K. (1994) An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a peptide with Cys/His sequence motifs. J. Virol. 68: 2521–3328.

    PubMed  CAS  Google Scholar 

  • Brancolini, C, Benedetti, M. and Schneider, C. (1995) Microfilament reorganization during apoptosis: the role of Gas2, a possible substrate for ICE-like proteases. EMBO J. 14: 5179–5190.

    PubMed  CAS  Google Scholar 

  • Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415.

    PubMed  CAS  Google Scholar 

  • Bump, N.J., Hackett, M., Hugunin, M., et al. (1995) Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269: 1885–1888.

    PubMed  CAS  Google Scholar 

  • Campos-Ortega, J.A. and Hartenstein, V. (1997) in The Embryonic Development of Drosophila melanogaster. Springer-Verlag.

    Google Scholar 

  • Capobianco, A.J., Zagouras, P., Blaumueller, C.M., et al. (1997) Neoplastic transformation by truncated alleles of human NOTCH/TAN1 and NOTCH2. Mol. Cell Biol. 17: 6265–6273.

    PubMed  CAS  Google Scholar 

  • Cerretti, D.P., Kozlosky, C.J., Mosley, B., et al. (1992) Molecular cloning of the interleukin-1 beta converting enzyme. Science 256: 97–100.

    PubMed  CAS  Google Scholar 

  • Chen, P., Nordstrom, W., Gish, B. and Abrams, J.M. (1996a) grim, a novel cell death gene in Drosophila. Genes Dev. 10: 1773–1782.

    PubMed  CAS  Google Scholar 

  • Chen, P., Lee, P., Otto, L. and Abrams, J. (1996b) Apoptotic activity of REAPER is distinct from signaling by the tumor necrosis factor receptor 1 death domain. J. Biol. Chem. 271: 25735–25737.

    PubMed  CAS  Google Scholar 

  • Cheng, E.H.-Y., Kirsch, D.G., Clem, R.J., et al. (1997) Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278: 1966–1968.

    PubMed  CAS  Google Scholar 

  • Chinnaiyan, A.M. and Dixit, V.M. (1996). The cell-death machine. Curr. Biol. 6: 555–562.

    PubMed  CAS  Google Scholar 

  • Chinnaiyan, A.M., O‘Rourke, K., Lane, B.R. and Dixit, V.M. (1997) Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science 275: 1122–1126.

    PubMed  CAS  Google Scholar 

  • Clem, R.J., Fechheimer, M. and Miller, L.K. (1991) Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254: 1388–1390.

    PubMed  CAS  Google Scholar 

  • Clem, R.J. and Miller, L.K. (1994) Control of programmed cell death by the baculovirus genes p35 and iap. Mol Cell Biol 14: 5212–5222.

    PubMed  CAS  Google Scholar 

  • Cleveland, J.L. and Ihle, J.N. (1995) Contenders in Fas/TNF death signalling. Cell 81: 479–482.

    PubMed  CAS  Google Scholar 

  • Crook, N.E., Clem, R.J. and Miller, L.K. (1993) An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol 67: 2168–2174.

    PubMed  CAS  Google Scholar 

  • Davidson, F.F. and Steller, H. (1998) Blocking apoptosis prevents blindness in Drosophila retinal degeneration mutants. Nature 391: 587–591.

    PubMed  CAS  Google Scholar 

  • Davis, E.J., Foster, T.D. and Thomas, W.E. (1994) Cellular forms and functions of brain microglia. Brain Res. Bull 34: 73–78.

    PubMed  CAS  Google Scholar 

  • Demerec, M. (1950) in Biology of Drosophila. John Wiley & Sons, Inc., New York; Chapman & Hall, Limited, London; (1994) re-issued by Cold Spring Harbor Laboratory Press, Cold Spring Harbor.

    Google Scholar 

  • DeRobertis, E.M. and Sasai, Y. (1996) A common plan for dorsoventral patterning in Bilateria. Nature 380: 37–40.

    CAS  Google Scholar 

  • Devereaux, Q.L., Takahashi, R., Salvesen, G.S. and Reed, J.C. (1997) X-linked lap is a direct inhibitor of cell-death proteases. Nature 388: 300–304.

    CAS  Google Scholar 

  • Dorn, R., Krauss, V., Reuter, G. and Saweber, H. (1993) The enhancer of position-effect variegation of Drosophila E (var)3-93 D codes for a chromatin protein containing a conserved domain common to several transcription factors. Proc. Natl Acad. Sci. USA 90: 11376–11380.

    PubMed  CAS  Google Scholar 

  • Driscoll, M. (1992) Molecular genetics of cell death in the nematode Caenorhabditis elegans. J. Neurobiol 23: 1327–1351.

    PubMed  CAS  Google Scholar 

  • Dryja, T.P., McGee, T.L., Reichal., E., et al (1990) A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature 343: 364–366.

    PubMed  CAS  Google Scholar 

  • Ellis, R., Yuan, J. and Horvitz, H.R. (1991) Mechanisms and functions of cell death. Ann. Rev. Cell Biol. 7: 663–698.

    PubMed  CAS  Google Scholar 

  • Ellis, H.M. and Horvitz, H.R. (1986). Genetic control of programmed cell death in the nematode C. elegans. Cell 44: 817–829

    PubMed  CAS  Google Scholar 

  • Evans, E.K., Kuwana, T., Strum, S.L., et al (1997) Reaper-induced apoptosis in a vertebrate system. EMBO J. 16: 7372–7381.

    PubMed  CAS  Google Scholar 

  • Fan, H., Oro, A.E. Scott, M.P. and Khavari, P.A. (1997) Induction of basal cell carcinoma features in transgenic human skin expressing Sonic Hedgehog. Nature Med. 3: 788–792.

    PubMed  CAS  Google Scholar 

  • Fessler, J.H. and Fessler, L.I. (1989) Drosophila extracellular matrix. Ann. Rev. Cell Biol. 5: 309–339.

    PubMed  CAS  Google Scholar 

  • Fisher, G.H., Rosenberg, F.J., Straus, S.E., et al (1995). Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 16: 935–946.

    Google Scholar 

  • Foley, K. and Cooley, L. (1998) Apoptosis in late stage Drosophila nurse cells does not require genes within the H99 deficiency. Development 125: 1075–1082.

    PubMed  CAS  Google Scholar 

  • Fraser, A.G. and Evan, G.I. (1997) Identification of a Drosophila melanogaster ICE/CED-3-related protease, drICE. EMBO J. 16: 2805–2813.

    PubMed  CAS  Google Scholar 

  • Gavrieli, Y., Sherman, Y. and Ben Sassoon, S. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119: 493–501.

    PubMed  CAS  Google Scholar 

  • Gerasimova, T.I., Gdula, D.A., Gerasimov, D.V., et al (1995) A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position effect variegation. Cell 82: 587–597.

    PubMed  CAS  Google Scholar 

  • Gerhart, J. and Kirschner, M. (1997) in Cells, Embryos, and Evolution. Blackwell Science Inc., Maiden.

    Google Scholar 

  • Golstein, P., Marguet, D. and Depraetere, V. (1995) Homology between Reaper and the cell death domains of Fas and TNFR1. Cell 81: 18–185

    PubMed  CAS  Google Scholar 

  • Golic, K.G. and Lindquist, S. (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59: 499–509.

    PubMed  CAS  Google Scholar 

  • Grether, M.E., Abrams, J.M., Agapite, J., et al. (1995) The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9: 1694–1708.

    PubMed  CAS  Google Scholar 

  • Haimovitz-Friedman, A., Kolesnick, R.N. and Fulks, Z. (1997) Ceramide signalling in apoptosis. Br. Med. Bull. 53: 539–553.

    PubMed  CAS  Google Scholar 

  • Halder, G., Callaerts, P. and Gehring, W. J. (1995) New perspectives on eye evolution. Curr. Opin. Gene. Dev. 5: 602–609

    CAS  Google Scholar 

  • Hannun, Y.A. and Obeid, L.M. (1995) Ceramide: an intracellular signal for apoptosis. Trends Biochem. Sci. 20: 73–77.

    PubMed  CAS  Google Scholar 

  • Harvey, AJ., Bidwai, A.P. and Miller, L.K. (1997) Doom, a product of the Drosophila mod(mgd4) gene, induces apoptosis and binds to baculovirus inhibitor-of-apoptosis. Mol. Cell Biol. 17: 2835–2843.

    PubMed  CAS  Google Scholar 

  • Hay, B.A., Wolff, T. and Rubin, G.M. (1994) Expression of baculovirus P35 prevents cell death in Drosophila. Development 120: 2121–2129.

    PubMed  CAS  Google Scholar 

  • Hay, B.A., Wassarman, D.A. and Rubin, G.M. (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83: 1253–1262.

    PubMed  CAS  Google Scholar 

  • Hengartner, M.O., Ellis, R. and Horvitz, H.R. (1992) Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356: 494–501.

    PubMed  CAS  Google Scholar 

  • Hengartner, M.O. and Horvitz, R.H. (1994) Programmed cell death in Caenorhabditis elegans. Curr. Opin. Gen. Dev. 4: 581–586.

    CAS  Google Scholar 

  • Horvitz, H.R., Ellis, H.M. and Sternberg, P.W. (1982) Programmed cell death in nematode development. Neurosci. Comm. 1: 56–65.

    Google Scholar 

  • Horvitz, H.R., Shaham, S. and Hengartner, M. O. (1994) The genetics of programmed cell death in the nematode Caenorhabditis elegans. Cold Spring Harbor Symp. Quant. Biol. 59: 377–385.

    CAS  Google Scholar 

  • Itoh, N., Yonehara S., Ishii, A., et al. (1991) The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66: 233–243.

    PubMed  CAS  Google Scholar 

  • Jiang, C, Baehrecke, E.H. and Thummel, C. (1997) Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124: 4673–4683.

    PubMed  CAS  Google Scholar 

  • Johnson, R.L., Rothman, A.L., Xie, J., et al. (1996) Human homolog of patched, a candidate gene for basal cell nevus syndrome. Science 272: 1668–1671.

    PubMed  CAS  Google Scholar 

  • Jürgens, G., Wieschaus, E, Nüsslein-Volhard, C. and Kluding, H. (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Roux Arch. Dev. Biol. 193: 283–295.

    Google Scholar 

  • Kerr, J.F.R., Wyllie, A. and Currie, A.R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26: 239–257.

    PubMed  CAS  Google Scholar 

  • Kimura, K.I. and Truman, J.W. (1990) Postmetamorphic cell death in the nervous and muscular systems of Drosophila melanogaster. J. Neurosci. 10: 403–411.

    PubMed  CAS  Google Scholar 

  • Klingensmith, J., Noll, N. and Perrimon, N. (1989) The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death. Dev. Biol. 134: 130–145.

    PubMed  CAS  Google Scholar 

  • Kluck, R.M., Bossy-Wetzel, E., Green, D.R. and Newmeyer, D.D. (1997) The release of cytochrome c from mitochondria: a primary site of Bcl-2 regulation of apoptosis. Science 275: 1132–1136.

    PubMed  CAS  Google Scholar 

  • Knudson, C.M. and Korsmeyer, S.J. (1997) Bcl-2 and Bax function independently to regulate cell death. Nature Genet. 16: 358–363.

    PubMed  CAS  Google Scholar 

  • Knudson, C.M, Tung, K.S., Tourtellotte, W.G., et al. (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270: 96–99.

    PubMed  CAS  Google Scholar 

  • Koelle, M.R., Talbot, W.S., Segraves, W.A., et al. (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67: 59–77.

    PubMed  CAS  Google Scholar 

  • Kohler, R.E. (1994) In: Lords of the Fly. The University of Chicago Press, Chicago.

    Google Scholar 

  • Kondo, T., Yokokura, T. and Nagata, S. (1997) Activation of distinct caspase-like protease by fas and reaper in Drosophila cells. Proc. Natl. Acad.Sci. USA 94: 11951–11956.

    PubMed  CAS  Google Scholar 

  • Kothakota, S., Azuma, T., Reinhard, C, et al. (1997) Caspase-3-Generated Fragment of Gelsolin: Effector of Morphological Change in Apoptosis. Science 278: 294–298.

    PubMed  CAS  Google Scholar 

  • Krieger, M., Abrams, J.M., Lux, A. and Steller, H. (1992) Molecular flypaper, athlerosclerosis, and host defense: structure and function of the macrophage scavenger receptor. Cold Spring Harbor Symp. Quant. Biol. 57: 605–609.

    CAS  Google Scholar 

  • Kuida, K., Lippke, J.A., Ku, G., et al. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1ß converting enzyme. Science 267: 2000–2003.

    PubMed  CAS  Google Scholar 

  • Kuida, K., Zheng, T.S., Na, S., et al. (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 28: 368–372.

    Google Scholar 

  • Lawrence, P.A. (1992) The making of a fly. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • Lazebnik, Y.A., Takahashi, A., Moir, R.D., et al. (1995) Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92: 9042–9046.

    PubMed  CAS  Google Scholar 

  • Lee, F.S., Lane, T.F., Kuo, A., et al. (1995) Insertional mutagenesis identifies a member of the Wnt gene family as a candidate oncogene in the mammary epithelium of int-2/Fgf-3 transgenic mice. Proc. Natl. Acad. Sci. USA 92: 2268–2272.

    PubMed  CAS  Google Scholar 

  • Leonard, D.S., Bowman, V.D., Ready, D.F. and Pak, W.L. (1992) Degeneration of photoreceptors in rhodopsin mutants of Drosophila. J. Neurobiol. 23: 605–626.

    PubMed  CAS  Google Scholar 

  • Lewis, E.B. (1978) A gene complex controlling segmentation in Drosophila. Nature 276: 565–570.

    PubMed  CAS  Google Scholar 

  • Lindsley, D.L. and Zimm, G.G. (1992) In: The genome of Drosophila Melanogaster. Academic Press, San Diego.

    Google Scholar 

  • Liston, P., Roy, N., Tamai, K., et al. (1996) Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature 379: 349–353.

    PubMed  CAS  Google Scholar 

  • Liu, X., Zou, H., Slaughter, C. and Wang, X. (1997) DFF, a heterodimeric protein that functions Downstream of Caspase-3 to trigger DNA Fragmentation during Apoptosis. Cell 89: 175–184.

    PubMed  CAS  Google Scholar 

  • Liu, X., Kim, C.N., Yang, J., et al. (1996). Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147–157.

    PubMed  CAS  Google Scholar 

  • Liu, Z.G., Smith, S., McLaughlin, K.A., et al. (1994) Apoptotic signals delivered through the T cell receptor require the immediate early gene nur77. Nature 367: 281–284.

    PubMed  CAS  Google Scholar 

  • Lockshin, R.A. and Williams, C.M. (1965) Programmed cell death: Cytology of degeneration in the intersegmental muscles of the silkmoth. J. Insect Physiol 11: 123–33.

    PubMed  CAS  Google Scholar 

  • Lockshin, R.A. (1969) Activation of lysis by a mechanism involving the synthesis of protein. J. Insect Physiol. 15: 1505–1516.

    PubMed  CAS  Google Scholar 

  • Magrassi, L. and Lawrence, P.A. (1988) The pattern of cell death in fushi tarazu, a segmentation gene of Drosophila. Development 104: 447–451.

    PubMed  CAS  Google Scholar 

  • Martin, D.P., Schmidt, R.E., DiStefano, P.S., et al. (1988) Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106: 829–844.

    PubMed  CAS  Google Scholar 

  • McCall, K. and Steller, H. (1997) Facing death in the fly: Genetic analysis of apoptosis in Drosophila. Trends Genet. 13: 222–226.

    PubMed  CAS  Google Scholar 

  • McCall, K. and Steller, H. (1998) Requirements for DCP-1 caspase during Drosophila oogenesis. Science 279: 230–234.

    PubMed  CAS  Google Scholar 

  • McNabb, S., Baker, J.D., Agapite, J., et al. (1997) Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 19: 813–823.

    PubMed  CAS  Google Scholar 

  • Mignotte, B. and Vayssiere, J.-L. (1998) Mitochondria and apoptosis. Eur. J. Biochem. 252: 1–15.

    PubMed  CAS  Google Scholar 

  • Min, K.T. and Benzer, S. (1997) Spongecake and Eggroll: Two Hereditary diseases in Drosophila resemble patterns of human brain degeneration. Curr. Biol. 7: 885–888.

    PubMed  CAS  Google Scholar 

  • Miura, M., Zhu, H., Rotello, R., et al. (1993) Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75: 653–660.

    PubMed  CAS  Google Scholar 

  • Muzio, M., Salvesen, G.S. and Dixit, V.M. (1997) FLICE-induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J. Biol. Chem. 272: 2952–2956.

    PubMed  CAS  Google Scholar 

  • Nagata, S. (1997) Apoptosis by death factor. Cell 88: 355–365.

    PubMed  CAS  Google Scholar 

  • Nagata, S. and Golstein, P. (1995) The Fas death factor. Science 267: 1449–1456.

    PubMed  CAS  Google Scholar 

  • Namba, R., Pazdera, T.M., Cerrone, R.L. and Minden, J.S. (1997) Drosophila embryonic pattern repair: how embryos respond to bicoid dosage alteration. Development 124: 1393–1403.

    PubMed  CAS  Google Scholar 

  • Newmeyer, D.D., Farschon, D.M. and Reed, J.C. (1994) Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79: 353–364.

    PubMed  CAS  Google Scholar 

  • Nordstrom, W., Chen, P., Steller, H. and Abrams, J.M. (1996) Activation of the reaper gene during ectopic cell killing in Drosophila. Dev. Biol 180: 213–226.

    PubMed  CAS  Google Scholar 

  • Nusslein-Volhard, C. and Wieschaus, E. (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287: 795–801.

    PubMed  CAS  Google Scholar 

  • Nusslein-Volhard, C., Wieschaus, E. and Kluding, H. (1984) Mutations affecting the pattern of the larval cuticle in Drosophila Melanogaster. I. Zygotic loci on the second chromosome. Wilhelm Roux’s Arch. Dev. Biol. 193: 267–282.

    Google Scholar 

  • Oehm, A., Behrmann, I., Falk, W., et al. (1992) Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/ nerve growth factor superfamily. Sequence identity with the Fas antigen. J. Biol. Chem. 267: 10709–10715.

    PubMed  CAS  Google Scholar 

  • Oppenheim, R.W., Prevette, D., Tytell, M. and Homma, S. (1990) Naturally occurring and induced neuronal death in the chick embryo in vivo requires protein and RNA synthesis: evidence for the role of cell death genes. Dev. Biol. 138: 104–113.

    PubMed  CAS  Google Scholar 

  • Oro, A.E., Higgins, K.M., Hu, Z., et al. (1997) Basal carcinomas in mice overexpressing soinc the hedgehog. Science 276: 817–821.

    PubMed  CAS  Google Scholar 

  • Osborne, B.A. (1996) Cell death in vertebrates: lessons from the worm. Trends Genet. 12: 489–491.

    PubMed  CAS  Google Scholar 

  • Osborne, B.A., Smith, S.W., McLaughlin, K.A., et al. (1996) genes that regulate apoptosis in the mouse thymus. J. Cell Biochem. 60: 18–22.

    PubMed  CAS  Google Scholar 

  • Pearson, A., Lux, A. and Krieger, M. (1995) Expression cloning of dSR-CI, a class C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 92: 4056–4060.

    PubMed  CAS  Google Scholar 

  • Pronk, G.J., Ramer, K., Amiri, P. and Williams, L.T. (1996) Requirement of an ICE-like protease for induction of apoptosis and ceramide generation by REAPER. Science 271: 808–810.

    PubMed  CAS  Google Scholar 

  • Rabizadeh, S., LaCount, D.J., Friesen, P.D. and Bredesen, D.E. (1993) Expression of the baculovirus p35 gene inhibits mammalian neural cell death. J. Nuerochem. 61: 2318–2321.

    CAS  Google Scholar 

  • Reed, J.C. (1997) Double identity for proteins of the BCL-2 family. Nature 387: 773–776.

    PubMed  CAS  Google Scholar 

  • Robinow, S., Talbot, W.S., Hogness, D.S. and Truman, J.W. (1993) Programmed cell death in the Drosophila CNS is ecdysone-regulated and coupled with a specific ecdysone receptor isoform. Development 119: 1251–1259.

    PubMed  CAS  Google Scholar 

  • Robinow, S., Draizen, T.A. and Truman, J.W. (1997) Genes that induce apoptosis: Transcriptional regulation in identified, doomed neurons of the Drosophila CNS. Dev. Biol. 190: 206–213.

    PubMed  CAS  Google Scholar 

  • Roessler, E., Belloni, E., Gaudenz, K., et al. (1996) Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nature Genet. 14: 357–360.

    PubMed  CAS  Google Scholar 

  • Rothe, M. Pan, M-G., Henzel, W.J., et al. (1995) The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83: 1243–1252.

    PubMed  CAS  Google Scholar 

  • Roy, N., Mahadevan, M.S., McLean, M., et al. (1995) The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80: 167–178.

    PubMed  CAS  Google Scholar 

  • Roy, N, Devereaux, Q.L., Takahashi, R., et al. (1997) The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J. 16: 6914–6925.

    PubMed  CAS  Google Scholar 

  • Rudin, C.M. and Thompson, C.B. (1997) Apoptosis and disease: regulation and clinical relevence of programmed cell death. Ann. Rev. Med. 48: 267–281.

    PubMed  CAS  Google Scholar 

  • Salvesen, G.S. and Dixit, V.M. (1997) Caspases: intracellular signaling by proteolysis. Cell 14: 443–446.

    Google Scholar 

  • Sawamoto, K., Taguchi, A., Hirota, Y., et al. (1998) Argos induces programmed cell death in the developing Drosophila eye by inhibition of the Ras pathway. Cell Death Diff. 5: 262–270.

    CAS  Google Scholar 

  • Schwartz, L.M., Kosz, L. and Kay, B.K. (1990) Gene activation is required for developmentally programmed cell death. Proc. Natl. Acad. Sci. USA 87: 6594–6598.

    PubMed  CAS  Google Scholar 

  • Schwartz, L.M., Smith, S.W., Jones, M.E. and Osborne, B.A. (1993) Do all programmed cell deaths occur via apoptosis? Proc. Natl. Acad. Sci. USA 90: 980–984.

    PubMed  CAS  Google Scholar 

  • Schwartz, L.M., Milligan, C.E., Bielke, W. and Robinson, S.J. (1994) Cloning cell death genes. J. Neruobiol. 25: 1005–1016.

    Google Scholar 

  • Schwartz, L.M. and Milligan, C.M. (1996) Cold thoughts of death: The role of ICE proteases in neuronal apoptosis. Trends Neurosci. 19: 555–562.

    PubMed  CAS  Google Scholar 

  • Seshagiri, S. and Miller, L.K. (1997) Caenorhabitis elegans CED-4 stimulates CED-3 processing and CED-3 induced apoptosis. Curr Biol 7: 455–460.

    PubMed  CAS  Google Scholar 

  • Shigenaga, A., Funahashi, Y., Kimura, K., et al. (1997) Targeted expression of ced-3 and Ice induces programmed cell death in Drosophila. Cell Death Diff. 4: 371–1377.

    CAS  Google Scholar 

  • Song, Z., McCall, K. and Steller, H. (1997) DCP-1, a Drosophila cell death protease essential for development. Science 275: 536–540.

    PubMed  CAS  Google Scholar 

  • Sonnenfeld, M.J. and JacobsJ, R. (1995a) Macrophages and glia participate in the removal of apoptotic neurons from the Drosophila embryonic nervous system. J. Comp. Neurol. 359: 644–652.

    PubMed  CAS  Google Scholar 

  • Sonnenfeld, M.J. and Jacobs, J.R. (1995b) Apoptosis of midline glia during Drosophila embryogenesis: a correlation with axon contact. Development 121: 569–578.

    PubMed  CAS  Google Scholar 

  • Spector, M.S., Desnoyers, S., Heoppner, D.J. and Hengartner, M.O. (1997) Interaction between the C. elegans cell-death regulators CED-9 and CED-4. Nature 275: 1122–1226.

    Google Scholar 

  • Spradling, A.C. and Rubin, G.M. (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218: 341–347.

    PubMed  CAS  Google Scholar 

  • Spradling, A.C. (1993) Developmental Genetics of Oogenesis. In: The Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 1–70.

    Google Scholar 

  • Stemerdink, C. and Jacobs, J.R. (1997) Argos and Spitz group genes function to regulate midline glial cell number in Drosophila embryos. Development 124: 3787–3796

    PubMed  CAS  Google Scholar 

  • Steller, H. (1995) Mechanisms and genes of cellular suicide. Science 267: 1445–1449.

    PubMed  CAS  Google Scholar 

  • Sugimoto, A., Friesen, P.D. and Rothman, J. (1994) Baculovirus p35 prevents developmentally programmed cell death and rescues a ced-9 mutant in the nematode Caenorhabditis elegans. EMBO J. 13: 2023–2038.

    PubMed  CAS  Google Scholar 

  • Sulston, J.E. and Horvitz, H.R. (1977) Post-embryonic cell lineages of the nematode Caenorhabditis elegans. Dev. Biol. 82: 110–156.0

    Google Scholar 

  • Sulston, J.E., Schierenberg, E., White, J.G. and Thomsom, N., (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100: 64–119.

    PubMed  CAS  Google Scholar 

  • Talbot, W.S., Swyryd, E.A. and Hogness, D.S. (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73: 1323–1337.

    PubMed  CAS  Google Scholar 

  • Tepass, U., Fessler, L.I., Aziz, A. and Hartenstein, V. (1994) Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120: 1829–1837.

    PubMed  CAS  Google Scholar 

  • Thompson, C.B. (1995) Apoptosis in the pathogensis and treatment of disease. Science 267: 1456–1462.

    PubMed  CAS  Google Scholar 

  • Thornberry, N.A., Bull, H.G., Calaycay, J.R., et al. (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356: 768–774.

    PubMed  CAS  Google Scholar 

  • Thornberry, N.A. (1997) The caspase family of cysteine proteases. Br. Med. Bull. 53: 478–490.

    PubMed  CAS  Google Scholar 

  • Thornberry, N.A., Rano, T.A., Peterson, E.P., et al. (1997) A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J. Biol. Chem. 272: 17907–17911

    PubMed  CAS  Google Scholar 

  • Truman, J., Thorn, R. and Robinow, S. (1992) Programmed neuronal death in insect development. J. Neurobiol. 23: 1295–1311.

    PubMed  CAS  Google Scholar 

  • Truman, J.W., Taylor, B.J. and Awad, T.A. (1993) Formation of the adult nervous system. In: The Development of Drosophila melanogaster. pp. 1245–1275. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.

    Google Scholar 

  • Uren, A.G., Pakusch, M., Hawkins, C.J., et al. (1996) Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proc. Natl. Acad. Sci. USA 93: 4974–4978.

    PubMed  CAS  Google Scholar 

  • van Leeuwen, F. and Nusse, R. (1995) Oncogene activation and oncogene cooperation in MMTV-induced mouse mammary cancer. Semin. Cancer Biol. 6: 127–133.

    PubMed  Google Scholar 

  • Vaux, D.L. and Strasser, A. (1996) The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA 93: 2239–2244.

    PubMed  CAS  Google Scholar 

  • Vaux, D.L., Weissman, J.L. and Kim, S.K. (1992) Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 258: 1955–1957.

    PubMed  CAS  Google Scholar 

  • Veis, D.J., Sorenson, C.M., Shutter, J.R. and Korsmeyer, S.J. (1993) Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75: 229–240.

    PubMed  CAS  Google Scholar 

  • Villa, P., Kaufmann, S.H. and Earnshaw, W.C. (1997) Caspases and caspase inhibitors. Trends Biochem. Sci. 22: 388–393.

    PubMed  CAS  Google Scholar 

  • Vucic, D., Kaiser, W.J., Harvey, A.J. and Miller, L.K. (1997a) Inhibition of Reaper-induced apoptosis by interaction with inhibitor of apoptosis proteins (IAPs). Proc. Natl. Acad. Sci. USA 94: 10183–10188.

    PubMed  CAS  Google Scholar 

  • Vucic, D., Seshagiri, S. and Miller, L.K. (1997b) Characterization of Reaper-and FADD-induced apoptosis in a lepitopteran cell line. Mol. Cell Biol. 17: 667–676.

    PubMed  CAS  Google Scholar 

  • Vucic, D., Kaiser, W.J. and Miller, L.K. (1998) Inhibitor of apoptosis proteins physically interact with and block apoptosis induced by Drosophila proteins HID and GRIM. Mol. Cell Biol. In Press.

    Google Scholar 

  • Wang, L., Miura, M., Bergeron, L., et al. (1994) Ich-l, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78: 739–750.

    PubMed  CAS  Google Scholar 

  • Warrick, J.M., Paulson, H.L., Gray-Board, G.L., et al. (1998) Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell 93: 939–949.

    PubMed  CAS  Google Scholar 

  • White, E. (1996) Life, death, and the pursuit of apoptosis. Gen. Dev. 10: 1–15.

    CAS  Google Scholar 

  • White, K., Grether, M.E., Abrams, J.M., et al. (1994) Genetic control of programmed cell death in Drosophila. Science 264: 677–683.

    PubMed  CAS  Google Scholar 

  • White, K., Tahaoglu, E. and Steller, H. (1996) Cell killing by the Drosophila gene reaper. Science 271: 805–807.

    PubMed  CAS  Google Scholar 

  • Wieschaus, E., Nusslein-Volhard, C. and Kluding, H. (1984) Mutations affecting the pattern of the larval cuticle in Drosophila Melanogaster. III. Zygotic loci on the X-chromosome and fourth chromosome. Wilhelm Roux’s Arch. Dev. Biol. 193: 296–307.

    Google Scholar 

  • Wilson, C, Pearson, R.K., Bellen, H.J., et al (1989) P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Gen. Dev. 3: 1301–1313.

    CAS  Google Scholar 

  • Wing, J.P., Zhou, L., Schwartz, L.M. and Nambu, J.R. (1998) Distinct cell killing properties of the Drosophila reaper, head involution defective, and grim genes. Cell Death and Diff. In Press.

    Google Scholar 

  • Woronicz, J.D., Calnan, B., Ngo, V. and Winoto, A. (1994) Requirement for the orphan steroid receptor Nur77 in apoptosis of T-cell hybridomas. Nature 367: 277–281.

    PubMed  CAS  Google Scholar 

  • Wu, D., Wallen, H.D., Inohara, N. and Nunez, G. (1997) Interaction and regulation of the Caenorhabitis elegans death protease CED-3 by CED-4 and CED-9. J. Biol Chem. 272: 21449–21454.

    PubMed  CAS  Google Scholar 

  • Wyllie, A.H., Kerr, J.F.R. and Currie, A.R. (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol. 68: 251–306.

    PubMed  CAS  Google Scholar 

  • Wyllie, A.H., Morris, R.G., Smith, A.L. and Dunlop, D. (1984) Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142: 67–77.

    PubMed  CAS  Google Scholar 

  • Xie, J. Johnson, R.L., Zhang X., Bare, J.W., et al. (1997) Mutations of the PATCHED gene in several types of sporadic extracutaneous tumors. Cancer Res. 57: 2369–2372.

    PubMed  CAS  Google Scholar 

  • Xu, T. and Rubin, G.M. (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223–1237.

    PubMed  CAS  Google Scholar 

  • Xue, D. and Horvitz, H.R. (1995) Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377: 248–251.

    PubMed  CAS  Google Scholar 

  • Xue, D. and Horvitz, H.R. (1997) Caenorhabditis elegans CED-9 protein is a bifunctional cell death inhibitor. Nature 390: 305–308.

    PubMed  CAS  Google Scholar 

  • Yang, X., Chang, H.Y. and Baltimore, D. (1998) Autoproteolytic activation of pro-caspases by oligomerization. Molec. Cell. 1: 319–325.

    PubMed  CAS  Google Scholar 

  • Yao, T.P., Segraves, W.A., Oro, A.E., et al. (1992) Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71: 63–72.

    PubMed  CAS  Google Scholar 

  • Yuan, J. and Horvitz, H.R. (1990) The Caenorhabditis elegans genes ced-3 and ced-4 act cell-autonomously to cause programmed cell death. Dev. Biol. 138: 33–41.

    PubMed  CAS  Google Scholar 

  • Yuan, J., Shaham, S., Ledoux, S., et al. (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75: 641–652.

    PubMed  CAS  Google Scholar 

  • Yuan, J. (1997) Transducing signals of life and death. Curr. Opin. Cell Biol. 9: 247–251.

    PubMed  CAS  Google Scholar 

  • Zhou, L., Hashimi, H., Schwartz, L.M. and Nambu, J.R. (1995) Programmed Cell Death in the Drosophila Central Nervous System Midline. Curr. Biol. 5: 784–790.

    PubMed  CAS  Google Scholar 

  • Zhou, L., Schnitzler, A, Agapite, J., et al. (1997) Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midline cells. Proc. Natl. Acad. Sci. USA 94: 5131–5136.

    PubMed  CAS  Google Scholar 

  • Zou, H., Henzel, W.J., Liu, X., et al. (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405–413.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biology Department and Molecular and Cell Biology Program, University of Massachusetts at Amherst, Amherst, MA, 01003, USA

    John P. Wing & John R. Nambu

Authors
  1. John P. Wing
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John R. Nambu
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Epithelial Biology Laboratory, CRC Section of Cell and Tumour Biology, Patterson Institute for Cancer Research, Manchester, M20 4BX, UK

    James W. Wilson , Catherine Booth  & Christopher S. Potten ,  & 

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media New York

About this chapter

Cite this chapter

Wing, J.P., Nambu, J.R. (1998). Apoptosis in Drosophila . In: Wilson, J.W., Booth, C., Potten, C.S. (eds) Apoptosis Genes. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5287-1_8

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-5287-1_8

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-7412-1

  • Online ISBN: 978-1-4615-5287-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation