Skip to main content
SpringerLink
Log in

Mechanisms of programmed cell death during oogenesis in Drosophila virilis

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

We describe the features of programmed cell death occurring in the egg chambers of Drosophila virilis during mid-oogenesis and late oogenesis. During mid-oogenesis, the spontaneously degenerating egg chambers exhibit typical characteristics of apoptotic cell death. As revealed by propidium iodide, rhodamine-conjugated phalloidin staining, and the TUNEL assay, respectively, the nurse cells contain condensed chromatin, altered actin cytoskeleton, and fragmented DNA. In vitro caspase activity assays and immunostaining procedures demonstrate that the atretic egg chambers possess high levels of caspase activity. Features of autophagic cell death are also observed during D. virilis mid-oogenesis, as shown by monodansylcadaverine staining, together with an ultrastructural examination by transmission electron microscopy. During the late stages of oogenesis in D. virilis, once again, the two mechanisms, viz., nurse cell cluster apoptosis and autophagy, operate together, manifesting features of cell death similar to those detailed above. Moreover, an altered form of cytochrome c seems to be released from the mitochondria in the nurse cells proximal to the oocyte. We propose that apoptosis and autophagy function synergistically during oogenesis in D. virilis in order to achieve a more efficient elimination of the degenerated nurse cells and abnormal egg chambers.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Arama E, Bader M, Srivastava M, Bergmann A, Steller H (2006) The two Drosophila cytochrome c proteins can function in both respiration and caspase activation. EMBO J 25:232–243

    Article  PubMed  CAS  Google Scholar 

  • Baker NE, Yu SY (2001) The EGF receptor defines domains of cell cycle progression and survival to regulate cell number in the developing Drosophila eye. Cell 104:699–708

    Article  PubMed  CAS  Google Scholar 

  • Baum JS, St George JP, McCall K (2005) Programmed cell death in the germline. Semin Cell Dev Biol 16:245–259

    Article  PubMed  CAS  Google Scholar 

  • Berg CA (2005) The Drosophila shell game: patterning and morphological change. Trends Genet 21:346–355

    Article  PubMed  CAS  Google Scholar 

  • Biederbick A, Kern HF, Elsasser HP (1995) Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 66:3–14

    PubMed  CAS  Google Scholar 

  • Bursch W (2001) The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ 8:569–581

    Article  PubMed  CAS  Google Scholar 

  • Bursch W (2004) Multiple cell death programs: Charon’s lifts to Hades. FEMS Yeast Res 5:101–110

    Article  PubMed  CAS  Google Scholar 

  • Buszczak M, Freeman MR, Carlson JR, Bender M, Cooley L, Segraves WA (1999) Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development 126:4581–4589

    PubMed  CAS  Google Scholar 

  • Cavaliere V, Taddei C, Gargiulo G (1998) Apoptosis of nurse cells at the late stages of oogenesis of Drosophila melanogaster. Dev Genes Evol 208:106–112

    Article  PubMed  CAS  Google Scholar 

  • Chao S, Nagoshi RN (1999) Induction of apoptosis in the germline and follicle layer of Drosophila egg chambers. Mech Dev 88:159–172

    Article  PubMed  CAS  Google Scholar 

  • Chwieralski CE, Welte T, Buhling F (2006) Cathepsin-regulated apoptosis. Apoptosis 2:143–149

    Article  Google Scholar 

  • Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berlin) 181:195–213

    CAS  Google Scholar 

  • Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116:205–219

    Article  PubMed  CAS  Google Scholar 

  • De Lorenzo C, Strand D, Mechler BM (1999) Requirement of Drosophila I(2)gl function for survival of the germline cells and organization of the follicle cells in a columnar epithelium during oogenesis. Int J Dev Biol 43:207–217

    PubMed  Google Scholar 

  • Drummond-Barbosa D, Spradling AC (2001) Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev Biol 231:265–278

    Article  PubMed  CAS  Google Scholar 

  • Foley K, 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 

  • Giorgi F, Deri P (1976) Cell death in ovarian chambers of Drosophila melanogaster. J Embryol Exp Morphol 35:521–533

    PubMed  CAS  Google Scholar 

  • Gozuacik D, Kimchi A (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23:2891–2906

    Article  PubMed  CAS  Google Scholar 

  • Juhasz G, Sass M (2005) Hid can induce, but is not required for autophagy in polyploid larval Drosophila tissues. Eur J Cell Biol 84:491–502

    Article  PubMed  CAS  Google Scholar 

  • Kelekar A (2005) Autophagy. Ann NY Acad Sci 1066:259–271

    Article  PubMed  CAS  Google Scholar 

  • King RC (1970) Origin and development of the egg chamber within the adult ovarioles. In: King RC (ed) Ovarian development in Drosophila melanogaster. Academic Press, New York London, pp 38–54

    Google Scholar 

  • Kornbluth S, White K (2005) Apoptosis in Drosophila: neither fish nor fowl (nor man, nor worm). J Cell Sci 118:1779–1787

    Article  PubMed  CAS  Google Scholar 

  • Krieser RJ, White K (2002) Engulfment mechanism of apoptotic cells. Curr Opin Cell Biol 14:734–738

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Doumanis J (2000) The fly caspases. Cell Death Differ 11:1039–1044

    Article  Google Scholar 

  • Laundrie B, Peterson JS, Baum JS, Chang JC, Fileppo D, Thompson SR, McCall K (2003) Germline cell death is inhibited by P-element insertions disrupting the dcp-1/pita nested gene pair in Drosophila. Genetics 165:1881–1888

    PubMed  CAS  Google Scholar 

  • Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy and more. Int J Biochem Cell Biol 36:2405–2419

    Article  PubMed  CAS  Google Scholar 

  • Mahajan-Miklos S, Cooley L (1994) Intercellular cytoplasm transport during Drosophila oogenesis. Dev Biol 165:336–351

    Article  PubMed  CAS  Google Scholar 

  • Margaritis LH (1985) Structure and physiology of the eggshell. In: Gilbert LI, Kerkut GA (eds) Comprehensive insect biochemistry, physiology and pharmacology, vol 1. Pergammon, Oxford New York, pp 151–230

    Google Scholar 

  • Margaritis LH (1986) The eggshell of Drosophila melanogaster. New staging characteristics and fine structural analysis of choriogenesis. Can J Zool 64:2152–2175

    Google Scholar 

  • Martin DN, Baehrecke EH (2004) Caspases function in autophagic programmed cell death in Drosophila. Development 131:275–284

    Article  CAS  Google Scholar 

  • Mazzalupo S, Cooley L (2006) Illuminating the role of caspases during Drosophila oogenesis. Cell Death Differ, DOI 10.1038/sj.cdd.4401892

  • McCall K (2004) Eggs over easy: cell death in the Drosophila ovary. Dev Biol 274:3–14

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mueller CM, Jemmerson R (1996) Maturation of the antibody response to the major epitope on the self antigen mouse cytochrome c. Restricted V gene usage, selected mutations and increased affinity. J Immunol 157:5329–5338

    PubMed  CAS  Google Scholar 

  • Muller F, Adori C, Sass M (2004) Autophagic and apoptotic features during programmed cell death in the fat body of the tobacco hornworm (Manduca sexta). Eur J Cell Biol 83:67–78

    Article  PubMed  CAS  Google Scholar 

  • Nezis IP, Stravopodis DJ, Papassideri I, Robert-Nicoud M, Margaritis LH (2000) Stage-specific apoptotic patterns during Drosophila oogenesis. Eur J Cell Biol 79:610–620

    Article  PubMed  CAS  Google Scholar 

  • Nezis IP, Stravopodis DJ, Papassideri I, Margaritis LH (2001) Actin cytoskeleton reorganization of the apoptotic nurse cells during the late developmental stages of oogenesis in Dacus oleae. Cell Motil Cytoskeleton 48:224–233

    Article  PubMed  CAS  Google Scholar 

  • Nezis IP, Stravopodis DJ, Papassideri I, Robert-Nicoud M, Margaritis LH (2002) The dynamics of apoptosis in the ovarian follicle cells during the late stages of Drosophila oogenesis. Cell Tissue Res 307:401–409

    Article  PubMed  Google Scholar 

  • Nezis IP, Modes V, Mpakou V, Stravopodis DJ, Papassideri IS, Mammali I, Margaritis LH (2003) Modes of programmed cell death during Ceratitis capitata oogenesis. Tissue Cell 35:113–119

    Article  PubMed  CAS  Google Scholar 

  • Nezis IP, Stravopodis DJ, Papassideri IS, Stergiopoulos C, Margaritis LH (2005) Morphological irregularities and features of resistance to apoptosis in the dcp-1/pita double mutated egg chambers during Drosophila oogenesis. Cell Motil Cytoskeleton 60:14–23

    Article  PubMed  Google Scholar 

  • Nezis IP, Stravopodis DJ, Margaritis LH, Papassideri IS (2006a) Follicular atresia during Dacus oleae oogenesis. J Insect Physiol 52:282–290

    Article  CAS  Google Scholar 

  • Nezis IP, Stravopodis DJ, Margaritis LH, Papassideri IS (2006b) Programmed cell death of follicular epithelium during the late developmental stages of oogenesis in the fruit flies Bactrocera oleae and Ceratitis capitata (Diptera, Tephritidae) is mediated by autophagy. Dev Growth Differ 48:189–198

    Article  Google Scholar 

  • Nezis IP, Stravopodis DJ, Margaritis LH, Papassideri IS (2006c) Chromatin condensation of ovarian nurse and follicle cells is regulated independently from DNA fragmentation during Drosophila late oogenesis. Differentiation 74:293–304

    Google Scholar 

  • Peterson JS, Barkett M, McCall K (2003) Stage-specific regulation of caspase activity in Drosophila oogenesis. Dev Biol 260:113–123

    Article  PubMed  CAS  Google Scholar 

  • Richardson H, Kumar S (2002) Death to flies: Drosophila as a model system to study programmed cell death. J Immunol Methods 265:21–38

    Article  PubMed  CAS  Google Scholar 

  • Soller M, Bownes M, Kubli E (1999) Control of oocyte maturation in sexually mature Drosophila females. Dev Biol 208:337–351

    Article  PubMed  CAS  Google Scholar 

  • Srinivasan A, Roth KA, Sayers RO, Shindler KS, Wong AM, Fritz LC, Tomaselli KJ (1998) In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ 5:1004–1016

    Article  PubMed  CAS  Google Scholar 

  • Terashima J, Bownes M (2005) A microarray analysis of genes involved in relating egg production to nutritional intake in Drosophila melanogaster. Cell Death Differ 12:429–440

    Article  PubMed  CAS  Google Scholar 

  • Trougakos IP, Margaritis LH (2002) Novel morphological and physiological aspects of insect eggs. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, pp 3–36

    Google Scholar 

  • Uchida K, Ohmori D, Ueno T, Nishizuka M, Eshita Y, Fukunaga A, Kominami E (2001) Preoviposition activation of cathepsin-like proteinases in degenerating ovarian follicles of the mosquito Culex pipiens pallens. Dev Biol 237:68–78

    Article  PubMed  CAS  Google Scholar 

  • Uchida K, Nishizuka M, Ohmori D, Ueno T, Eshita Y, Fukunaga A (2004) Follicular epithelial cell apoptosis of atretic follicles within developing ovaries of the mosquito Culex pipiens pallens. J Insect Physiol 50:903–912

    Article  PubMed  CAS  Google Scholar 

  • Varkey J, Chen P, Jemmerson R, Abrams JM (1999) Altered cytochrome c display precedes apoptotic cell death in Drosophila. J Cell Biol 144:701–710

    Article  PubMed  CAS  Google Scholar 

  • Velentzas AD, Nezis IP, Stravopodis DJ, Papassideri IS, Margaritis LH (2006) Stage-specific regulation of programmed cell death during oogenesis in the medfly Ceratitis capitata. Int J Dev Biol (in press)

  • Waldhuber M, Emoto K, Petritsch C (2005) The Drosophila caspase DRONC is required for metamorphosis and cell death in response to irradiation and developmental signals. Mech Dev 122:914–927

    Article  PubMed  CAS  Google Scholar 

  • Witkus ER, Altman LG, Taparowsky JA (1980) An investigation of the presence of smooth endoplasmic reticulum and GERL during vitellogenesis in the ovary of Drosophila melanogaster. Exp Cell Biol 48:373–383

    PubMed  CAS  Google Scholar 

  • Yu SY, Yoo SJ, Yang L, Zapata C, Srinivasan A, Hay BA, Baker NE (2002) A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129:3269–3278

    CAS  Google Scholar 

  • Yu X, Wang L, Acehan D, Wang X, Akey CW (2006) Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J Mol Biol 355:577–589

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Professors R. Jemmerson, C. Petritsch, and K. Homma for kindly supplying us with antibodies and to Professor H.M. Moutsopoulos (Department of Pathophysiology, Medical School, University of Athens, Athens, Greece), for kindly providing confocal laser scanning microscope facilities.

Author information

Authors and Affiliations

  1. Faculty of Biology, Department of Cell Biology and Biophysics, University of Athens, Panepistimiopolis 15784, Athens, Greece

    Athanassios D. Velentzas, Ioannis P. Nezis, Dimitrios J. Stravopodis, Issidora S. Papassideri & Lukas H. Margaritis

Authors
  1. Athanassios D. Velentzas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ioannis P. Nezis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dimitrios J. Stravopodis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Issidora S. Papassideri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lukas H. Margaritis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Issidora S. Papassideri.

Additional information

The present study was co-financed within Op. Education by the European Social Fund and by National Resources via a grant (HRAKLEITOS 70/3/7164) to Professor L.H. Margaritis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Velentzas, A.D., Nezis, I.P., Stravopodis, D.J. et al. Mechanisms of programmed cell death during oogenesis in Drosophila virilis . Cell Tissue Res 327, 399–414 (2007). https://doi.org/10.1007/s00441-006-0298-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-006-0298-x

Keywords

Search

Navigation