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Major Scenarios of Genetically Regulated Cell Death during Oogenesis in Drosophilamelanogaster

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Abstract

The process of regulated cell death (RCD), as well as proliferation and differentiation, is an important and integral part of the development of any multicellular organism. There are a number of different mechanisms of RCD that can be activated in response to developmental and environmental signals. In this review, we focus on the new insights into the main cellular events and molecular mechanisms characterizing different cell death pathways during oogenesis in Drosophila melanogaster. During Drosophila oogenesis, at least five different stage-specific RCD scenarios are realized, including (1) caspase-dependent death of the germline cells (GCs) in early oogenesis, which is mediated by autophagy; (2) canonical apoptosis, which removes the excess of somatic polar cells at stages 4–5 of oogenesis; (3) RCD of mid-stage egg chambers, which begins with caspase-dependent death of GCs with the participation of autophagy and finishes with their engulfment by the surrounding follicle cells (FCs); (4) non-apoptotic RCD of late-stage nurse cells, initiated and controlled by the surrounding FCs; (5) caspase-independent death of the FCs that have fulfilled their functions through autophagy at the end of stage 14.

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REFERENCES

  1. Schweichel, J.U. and Merker, H.J., The morphology of various types of cell death in prenatal tissues, Teratology, 1973, vol. 7, no. 3, pp. 253—266. https://doi.org/10.1002/tera.1420070306

    Article  CAS  PubMed  Google Scholar 

  2. Galluzzi, L., Vitale, I., Aaronson, S.A., et al., Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018, Cell Death Differ., 2018, vol. 25, no. 3, pp. 486—541. https://doi.org/10.1038/s41418-017-0012-4

    Article  PubMed  PubMed Central  Google Scholar 

  3. Jenkins, V.K., Timmons, A.K., and McCall, K., Diversity of cell death pathways: insight from the fly ovary, Trends Cell Biol., 2013, vol. 23, no. 11, pp. 567—574. https://doi.org/10.1016/j.tcb.2013.07.005

    Article  CAS  PubMed  Google Scholar 

  4. King, R.C., Ovarian Development in Drosophila melanogaster, New York: Acad. Press, 1970.

    Google Scholar 

  5. King, R.C., Rubinson, A.C., and Smith, R.F., Oogenesis in adult Drosophila melanogaster,Growth, 1956, vol. 20, no. 2, pp. 121—157.

    CAS  PubMed  Google Scholar 

  6. Ables, E.T. and Drummond-Barbosa, D., The steroid hormone ecdysone functions with intrinsic chromatin remodeling factors to control female germline stem cells in Drosophila,Cell Stem Cell, 2010, vol. 7, no. 5, pp. 581—592. https://doi.org/10.1016/j.stem.2010.10.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Belles, X. and Piulachs, M.D., Ecdysone signalling and ovarian development in insects: from stem cells to ovarian follicle formation, Biochim. Biophys. Acta, 2015, vol. 1849, no. 2, pp. 181—186. https://doi.org/10.1016/j.bbagrm.2014.05.025

    Article  CAS  PubMed  Google Scholar 

  8. Badisco, L., van Wielendaele, P., and Vanden Broeck, J., Eat to reproduce: a key role for the insulin signaling pathway in adult insects, Front. Physiol., 2013, vol. 4, article 202. https://doi.org/10.3389/fphys.2013.00202

    Article  PubMed  PubMed Central  Google Scholar 

  9. Buszczak, M. and Cooley, L., Eggs to die for: cell death during Drosophila oogenesis, Cell Death Differ., 2000, vol. 7, no. 11, pp. 1071—1074. https://doi.org/10.1038/sj.cdd.4400755

    Article  CAS  PubMed  Google Scholar 

  10. McCall, K., Eggs over easy: cell death in the Drosophila ovary, Dev. Biol., 2004, vol. 274, no. 1, pp. 3—14. https://doi.org/10.1016/j.ydbio.2004.07.017

    Article  CAS  PubMed  Google Scholar 

  11. Pritchett, T.L., Tanner, E.A., and McCall, K., Cracking open cell death in the Drosophila ovary, Apoptosis, 2009, vol. 14, no. 8, pp. 969—979. https://doi.org/10.1007/s10495-009-0369-z

    Article  PubMed  PubMed Central  Google Scholar 

  12. Drummond-Barbosa, D. and Spradling, A.C., Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis, Dev. Biol., 2001, vol. 231, no. 1, pp. 265—278. https://doi.org/10.1006/dbio.2000.0135

    Article  CAS  PubMed  Google Scholar 

  13. Ogienko, A.A., Fedorova, S.A., and Baricheva, E.M., Basic aspects of ovarian development in Drosophila melanogaster,Russ. J. Genet., 2007, vol. 43, no. 10, pp. 1120—1134. https://doi.org/10.1134/S1022795407100055

    Article  CAS  Google Scholar 

  14. Wu, X., Tanwar, P.S., and Raftery, L.A., Drosophila follicle cells: morphogenesis in an eggshell, Semin. Cell Dev. Biol., 2008, vol. 19, no. 3, pp. 271—282. https://doi.org/10.1016/j.semcdb.2008.01.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kumar, S., Caspase function in programmed cell death, Cell Death Differ., 2007, vol. 14, no. 1, pp. 32—43. https://doi.org/10.1038/sj.cdd.4402060

    Article  CAS  PubMed  Google Scholar 

  16. Kumar, S. and Doumanis, J., The fly caspases, Cell Death Differ., 2000, vol. 7, no. 11, pp. 1039—1044. https://doi.org/10.1038/sj.cdd.4400756

    Article  CAS  PubMed  Google Scholar 

  17. Dorstyn, L., Colussi, P.A., Quinn, L.M., et al., DRONC, an ecdysone-inducible Drosophila caspase, Proc. Natl. Acad. Sci. U.S.A., 1999, vol. 96, no. 8, pp. 4307—4312. https://doi.org/10.1073/pnas.96.8.4307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Fraser, A.G., McCarthy, N.J., and Evan, G.I., drICE is an essential caspase required for apoptotic activity in Drosophila cells, EMBO J., 1997, vol. 16, no. 20, pp. 6192—6199. https://doi.org/10.1093/emboj/16.20.6192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Song, Z., McCall, K., and Steller, H., DCP-1, a Drosophila cell death protease essential for development, Science, 1997, vol. 275, no. 5299, pp. 536—540. https://doi.org/10.1126/science.275.5299.536

    Article  CAS  PubMed  Google Scholar 

  20. Xu, D., Li, Y., Arcaro, M., et al., The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila,Development, 2005, vol. 132, no. 9, pp. 2125—2134. https://doi.org/10.1242/dev.01790

    Article  CAS  PubMed  Google Scholar 

  21. Xu, D., Wang, Y., Willecke, R., et al., The effector caspases drICE and dcp-1 have partially overlapping functions in the apoptotic pathway in Drosophila,Cell Death Differ., 2006, vol. 13, no. 10, pp. 1697—1706. https://doi.org/10.1038/sj.cdd.4401920

    Article  CAS  PubMed  Google Scholar 

  22. Deveraux, Q.L. and Reed, J.C., IAP family proteins-suppressors of apoptosis, Genes Dev., 1999, vol. 13, no. 3, pp. 239—252. https://doi.org/10.1101/gad.13.3.239

    Article  CAS  PubMed  Google Scholar 

  23. Orme, M. and Meier, P., Inhibitor of apoptosis proteins in Drosophila: gatekeepers of death, Apoptosis, 2009, vol. 14, no. 8, pp. 950—960. https://doi.org/10.1007/s10495-009-0358-2

    Article  PubMed  Google Scholar 

  24. Denton, D., Aung-Htut, M.T., and Kumar, S., Developmentally programmed cell death in Drosophila,Biochim. Biophys. Acta, 2013, vol. 1833, no. 12, pp. 3499—3506. https://doi.org/10.1016/j.bbamcr.2013.06.014

    Article  CAS  PubMed  Google Scholar 

  25. Goyal, L., McCall, K., Agapite, J., et al., Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function, EMBO J., 2000, vol. 19, no. 4, pp. 589—597. https://doi.org/10.1093/emboj/19.4.589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chai, J., Yan, N., Huh, J.R., et al., Molecular mechanism of Reaper-Grim-Hid-mediated suppression of DIAP1-dependent Dronc ubiquitination, Nat. Struct. Biol., 2003, vol. 10, no. 11, pp. 892—898. https://doi.org/10.1038/nsb989

    Article  CAS  PubMed  Google Scholar 

  27. Rodriguez, A., Oliver, H., Zou, H., et al., Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway, Nat. Cell Biol., 1999, vol. 1, no. 5, pp. 272—279. https://doi.org/10.1038/12984

    Article  CAS  PubMed  Google Scholar 

  28. Yu, X., Wang, L., Acehan, D., et al., Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer, J. Mol. Biol., 2006, vol. 355, no. 3, pp. 577—589. https://doi.org/10.1016/j.jmb.2005.10.040

    Article  CAS  PubMed  Google Scholar 

  29. Xu, D., Woodfield, S.E., Lee, T.V., et al., Genetic control of programmed cell death (apoptosis) in Drosophila,Fly, 2009, vol. 3, no. 1, pp. 78—90. https://doi.org/10.4161/fly.3.1.7800

    Article  CAS  PubMed  Google Scholar 

  30. Mukae, N., Yokoyama, H., Yokokura, T., et al., Identification and developmental expression of inhibitor of caspase-activated DNase (ICAD) in Drosophila melanogaster,J. Biol. Chem., 2000, vol. 275, no. 28, pp. 21402—21408. https://doi.org/10.1074/jbc.M909611199

    Article  CAS  PubMed  Google Scholar 

  31. Taylor, R.C., Cullen, S.P., and Martin, S.J., Apoptosis: controlled demolition at the cellular level, Nat. Rev. Mol. Cell Biol., 2008, vol. 9, no. 3, pp. 231—241. https://doi.org/10.1038/nrm2312

    Article  CAS  PubMed  Google Scholar 

  32. Adrain, C., Creagh, E.M., Cullen, S.P., and Martin, S.J., Caspase-dependent inactivation of proteasome function during programmed cell death in Drosophila and man, J. Biol. Chem., 2004, vol. 279, no. 35, pp. 36923—36930. https://doi.org/10.1074/jbc.M402638200

    Article  CAS  PubMed  Google Scholar 

  33. Burlacu, A., Regulation of apoptosis by Bcl-2 family proteins, J. Cell. Mol. Med., 2003, vol. 7, no. 3, pp. 249—257. https://doi.org/10.1111/j.1582-4934.2003.tb00225.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Willis, S., Day, C.L., Hinds, M.G., and Huang, D.C.S., The Bcl-2-regulated apoptotic pathway, J. Cell Sci., 2003, vol. 116, no. 20, pp. 4053—4056. https://doi.org/10.1242/jcs.00754

    Article  CAS  PubMed  Google Scholar 

  35. Pang, Y., Bai, X.C., Yan, C., et al., Structure of the apoptosome: mechanistic insights into activation of an initiator caspase from Drosophila,Genes Dev., 2015, vol. 29, no. 3, pp. 277—287. https://doi.org/10.1101/gad.255877.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Abdelwahid, E., Yokokura, T., Krieser, R.J., et al., Mitochondrial disruption in Drosophila apoptosis, Dev. Cell, 2007, vol. 12, no. 5, pp. 793—806. https://doi.org/10.1016/j.devcel.2007.04.004

    Article  CAS  PubMed  Google Scholar 

  37. Goyal, G., Fell, B., Sarin, A., et al., Role of mitochondrial remodeling in programmed cell death in Drosophila melanogaster,Dev. Cell, 2007, vol. 12, no. 5, pp. 807—816. https://doi.org/10.1016/j.devcel.2007.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Martinou, J.C. and Youle, R.J., Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics, Dev. Cell, 2011, vol. 21, no. 1, pp. 92—101. https://doi.org/10.1016/j.devcel.2011.06.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Krieser, R.J. and White, K., Inside an enigma: do mitochondria contribute to cell death in Drosophila?, Apoptosis, 2009, vol. 14, no. 8, pp. 961—968. https://doi.org/10.1007/s10495-009-0362-6

    Article  PubMed  PubMed Central  Google Scholar 

  40. Thomenius, M., Freel, C.D., Horn, S., et al., Mitochondrial fusion is regulated by reaper to modulate Drosophila programmed cell death, Cell Death Differ., 2011, vol. 18, no. 10, pp. 1640—1650. https://doi.org/10.1038/cdd.2011.26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Das, G., Shravage, B.V., and Baehrecke, E.H., Regulation and function of autophagy during cell survival and cell death, Cold Spring Harbor Perspect. Biol., 2012, vol. 4, no. 6. a008813. https://doi.org/10.1101/cshperspect.a008813

    Article  CAS  Google Scholar 

  42. Kovaleva, O.V., Shitova, M.S., and Zborovskaya, I.B., Autophagy: cell death or a way to survive?, Klin. Onkogematol., 2014, vol. 7, no. 2, pp. 103—113.

    Google Scholar 

  43. Yu, L., Chen, Y., and Tooze, S.A., Autophagy pathway: cellular and molecular mechanisms, Autophagy, 2018, vol. 14, no. 2, pp. 207—215. https://doi.org/10.1080/15548627.2017.1378838

    Article  CAS  PubMed  Google Scholar 

  44. Zirin, J. and Perrimon, N., Drosophila as a model system to study autophagy, Semin. Immunopathol., 2010, vol. 32, no. 4, pp. 363—372. https://doi.org/10.1007/s00281-010-0223-y

    Article  PubMed  PubMed Central  Google Scholar 

  45. Ryoo, H.D. and Baehrecke, E.H., Distinct death mechanisms in Drosophila development, Curr. Opin. Cell Biol., 2010, vol. 22, no. 6, pp. 889—895. https://doi.org/10.1016/j.ceb.2010.08.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Barth, J.M., Szabad, J., Hafen, E., and Köhler, K., Autophagy in Drosophila ovaries is induced by starvation and is required for oogenesis, Cell Death Differ., 2011, vol. 18, no. 6, pp. 915—924. https://doi.org/10.1038/cdd.2010.157

    Article  CAS  PubMed  Google Scholar 

  47. Kroemer, G., Galluzzi, L., Vandenabeele, P., et al., Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009, Cell Death Differ., 2009, vol. 16, no. 1, pp. 3—11. https://doi.org/10.1038/cdd.2008.150

    Article  CAS  PubMed  Google Scholar 

  48. Vlachos, M. and Tavernarakis, N., Non-apoptotic cell death in Caenorhabditis elegans,Dev. Dyn., 2010, vol. 239, no. 5, pp. 1337—1351. https://doi.org/10.1002/dvdy.22230

    Article  CAS  PubMed  Google Scholar 

  49. Berghe, T., Linkermann, A., Jouan-Lanhouet, S., et al., Regulated necrosis: the expanding network of non-apoptotic cell death pathways, Nat. Rev. Mol. Cell Biol., 2014, vol. 15, no. 2, pp. 134—146. https://doi.org/10.1038/nrm3737

    Article  CAS  Google Scholar 

  50. Dondelinger, Y., Hulpiau, P., Saeys, Y., et al., An evolutionary perspective on the necroptotic pathway, Trends Cell Biol., 2016, vol. 26, no. 10, pp. 721—732. https://doi.org/10.1016/j.tcb.2016.06.004

    Article  CAS  PubMed  Google Scholar 

  51. Kanda, H., Igakib, T., Okanoa, H., and Miuradet, M., Conserved metabolic energy production pathways govern Eiger/TNFinduced nonapoptotic cell death, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, no. 47, pp. 18977—18982. https://doi.org/10.1073/pnas.1103242108

    Article  PubMed  PubMed Central  Google Scholar 

  52. Yang, Y., Hou, L., Li, Y., Ni, J., and Liu, L., Neuronal necrosis and spreading death in a Drosophila genetic model, Cell Death Differ., 2013, vol. 4, no. 7. e723. https://doi.org/10.1038/cddis.2013.232

    Article  CAS  Google Scholar 

  53. Myllymaki, H., Valanne, S., and Rämet, M., The Drosophila imd signaling pathway, J. Immunol., 2014, vol. 192, no. 8, pp. 3455—3462. https://doi.org/10.4049/jimmunol.1303309

    Article  CAS  PubMed  Google Scholar 

  54. LaFever, L. and Drummond-Barbosa, D., Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila,Science, 2005, vol. 309, no. 5737, pp. 1071—1073. https://doi.org/10.1126/science.1111410

    Article  CAS  PubMed  Google Scholar 

  55. Peterson, J.S., Timmons, A.K., Mondragon, A.A., and McCall, K., The end of the beginning: cell death in the germline, Curr. Top. Dev. Biol., 2015, vol. 114, pp. 93—119. https://doi.org/10.1016/bs.ctdb.2015.07.025

    Article  CAS  PubMed  Google Scholar 

  56. Carney, G.E. and Bender, M., The Drosophila ecdysone receptor (EcR) gene is required maternally for normal oogenesis, Genetics, 2000, vol. 154, no. 3, pp. 1203—1211.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Hou, Y.C., Chittaranjan, S., Barbosa, S.G., et al., Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis, J. Cell Biol., 2008, vol. 182, no. 6, pp. 1127—1139. https://doi.org/10.1083/jcb.200712091

    Article  PubMed  PubMed Central  Google Scholar 

  58. Nezis, I.P., Lamark, T., and Velentzas, A.D., Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy, Autophagy, 2009, vol. 5, no. 3, pp. 298—302. https://doi.org/10.4161/auto.5.3.7454

    Article  CAS  PubMed  Google Scholar 

  59. Besse, F. and Pret, A.M., Apoptosis-mediated cell death within the ovarian polar cell lineage of Drosophila melanogaster,Development, 2003, vol. 130, no. 5, pp. 1017—1027. https://doi.org/10.1242/dev.00313

    Article  CAS  PubMed  Google Scholar 

  60. Khammari, A., Agnès, F., Gandille, P., and Pret, A.-M., Physiological apoptosis of polar cells during Drosophila oogenesis is mediated by Hid-dependent regulation of Diap1, Cell Death Differ., 2011, vol. 18, no. 5, pp. 793—805. https://doi.org/10.1038/cdd.2010.141

    Article  CAS  PubMed  Google Scholar 

  61. Borensztejn, A., Boissoneau, E., Fernandez, G., et al., JAK/STAT autocontrol of ligand-producing cell number through apoptosis, Development, 2013, vol. 140, no. 1, pp. 195—204. https://doi.org/10.1242/dev.079046

    Article  CAS  PubMed  Google Scholar 

  62. Giorgi, F. and Deri, P., Cell death in ovarian chambers of Drosophila melanogaster,J. Emb. Exp. Morph., 1976, vol. 35, no. 3, pp. 521—533.

    CAS  Google Scholar 

  63. Nezis, I.P., Stravopodis, D.J., Papassideri, I., et al., Stage-specific apoptotic patterns during Drosophila oogenesis, Eur. J. Cell Biol., 2000, vol. 79, no. 9, pp. 610—620. https://doi.org/10.1078/0171-9335-00088

    Article  CAS  PubMed  Google Scholar 

  64. Etchegaray, J.I., Timmons, A.K., Klein, A.P., et al., Draper acts through the JNK pathway to control synchronous engulfment of dying germline cells by follicular epithelial cells, Development, 2012, vol. 139, no. 21, pp. 4029—4039. https://doi.org/10.1242/dev.082776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Templeman, N.M. and Murphy, C.T., Regulation of reproduction and longevity by nutrient-sensing pathways, J. Cell Biol., 2018, vol. 217, no. 1, pp. 93—106. https://doi.org/10.1083/jcb.201707168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Terashima, J., Takaki, K., Sakurai, S., and Bownes, M., Nutritional status affects 20-hydroxyecdysone concentration and progression of oogenesis in Drosophila melanogaster,J. Endocrinol., 2005, vol. 187, no. 1, pp. 69—79. https://doi.org/10.1677/joe.1.06220

    Article  CAS  PubMed  Google Scholar 

  67. Terashima, J. and Bownes, M., E75A and E75B have opposite effects on the apoptosis/development choice of the Drosophila egg chamber, Cell Death Differ., 2006, vol. 13, no. 3, pp. 454—464. https://doi.org/10.1038/sj.cdd.4401745

    Article  CAS  PubMed  Google Scholar 

  68. Pritchett, T.L. and McCall, K., Role of the insulin/Tor signaling network in starvation-induced programmed cell death in Drosophila oogenesis, Cell Death Differ., 2012, vol. 19, no. 6, pp. 1069—1079. https://doi.org/10.1038/cdd.2011.200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. McCall, K. and Steller, H., Requirement for DCP-1 caspase during Drosophila oogenesis, Science, 1998, vol. 279, no. 5348, pp. 230—234. https://doi.org/10.1126/science.279.5348.230

    Article  CAS  PubMed  Google Scholar 

  70. Laundrie, B., Peterson, J.S., Baum, J.S., et al., Germline cell death is inhibited by P-element insertions disrupting the dcp-1/pita nested gene pair in Drosophila,Genetics, 2003, vol. 165, no. 4, pp. 1881—1888.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Peterson, J.S., Bass, B.P., Jue, D., et al., Noncanonical cell death pathways act during Drosophila oogenesis, Genesis, 2007, vol. 45, no. 6, pp. 396—404. https://doi.org/10.1002/dvg.20306

    Article  CAS  PubMed  Google Scholar 

  72. Baum, J.S., Arama, E., Steller, H., and McCall, K., The Drosophila caspases Strica and Dronc function redundantly in programmed cell death during oogenesis, Cell Death Differ., 2007, vol. 14, no. 8, pp. 1508—1517. https://doi.org/10.1038/sj.cdd.4402155

    Article  CAS  PubMed  Google Scholar 

  73. DeVorkin, L., Go, N.E., Hou, Y.C., et al., The Drosophila effector caspase Dcp-1 regulates mitochondrial dynamics and autophagic flux via SesB, J. Cell Biol., 2014, vol. 205, no. 4, pp. 477—492. https://doi.org/10.1083/jcb.201303144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Tanner, E.A., Blute, T.A., Brachmann, C.B., and McCall, K., Bcl-2 proteins and autophagy regulate mitochondrial dynamics during programmed cell death in the Drosophila ovary, Development, 2011, vol. 138, no. 2, pp. 327—338. https://doi.org/10.1242/dev.057943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lauber, K., Blumenthal, S.G., Waibel, M., and Wesselborg, S., Clearance of apoptotic cells: getting rid of the corpses, Mol. Cell., 2004, vol. 14, no. 3, pp. 277—287. https://doi.org/10.1016/S1097-2765(04)00237-0

    Article  CAS  PubMed  Google Scholar 

  76. Serizier, S.B. and McCall, K., Scrambled eggs: apoptotic cell clearance by non-professional phagocytes in the Drosophila ovary, Front. Immunol., 2017, vol. 8, article 1642. https://doi.org/10.3389/fimmu.2017.01642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Meehan, T.L., Kleinsorge, S.E., Timmons, A.K., et al., Polarization of the epithelial layer and apical localization of integrins are required for engulfment of apoptotic cells, Dis. Model. Mech., 2015, vol. 8, no. 12, pp. 1603—1614. https://doi.org/10.1242/dmm.021998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Igaki, T., Correcting developmental errors by apoptosis: lessons from Drosophila JNK signaling, Apoptosis, 2009, vol. 14, no. 8, pp. 1021—1028. https://doi.org/10.1007/s10495-009-0361-7

    Article  PubMed  Google Scholar 

  79. Finnemann, S.C. and Silverstein, R.L., Differential roles of CD36 and ανβ5 integrin in photoreceptor phagocytosis by the retinal pigment epithelium, J. Exp. Med., 2001, vol. 194, no. 9, pp. 1289—1298. https://doi.org/10.1084/jem.194.9.1289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Sexton, D.W., Blaylock, M.G., and Walsh, G.M., Human alveolar epithelial cells engulf apoptotic eosinophils by means of integrin- and phosphatidylserine receptor-dependent mechanisms: a process upregulated by dexamethasone, J. Allergy Clin. Immunol., 2001, vol. 108, no. 6, pp. 962—969. https://doi.org/10.1067/mai.2001.119414

    Article  CAS  PubMed  Google Scholar 

  81. Flannagan, R.S., Canton, J., Furuya, W., et al., The phosphatidylserine receptor TIM4 utilizes integrins as coreceptors to effect phagocytosis, Mol. Biol. Cell, 2014, vol. 25, no. 9, pp. 1511—1522. https://doi.org/10.1091/mbc.E13-04-0212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Hsieh, H.-H., Hsu, T.-Y., Jiang, H.-S., and Wu, Y.-C., Integrin α PAT-2/CDC-42 signaling is required for muscle-mediated clearance of apoptotic cells in Caenorhabditis elegans,PLoS Genet., 2012, vol. 8, no. 5. e1002663. https://doi.org/10.1371/journal.pgen.1002663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Manaka, J., Kuraishi, T., Shiratsuchi, A., et al., Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages, J. Biol. Chem., 2004, vol. 279, no. 46, pp. 48466—48476. https://doi.org/10.1074/jbc.M408597200

    Article  CAS  PubMed  Google Scholar 

  84. Shiratsuchi, A., Mori, T., Sakurai, K., et al., Independent recognition of Staphylococcus aureus by two receptors for phagocytosis in Drosophila,J. Biol. Chem., 2012, vol. 287, no. 26, pp. 21663—21672. https://doi.org/10.1074/jbc.M111.333807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Nonaka, S., Nagaosa, K., Mori, T., et al., Integrin αPS3/βν-mediated phagocytosis of apoptotic cells and bacteria in Drosophila,J. Biol. Chem., 2013, vol. 288, no. 15, pp. 10374—10380. https://doi.org/10.1074/jbc.M113.451427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Evans, I.R., Rodrigues, F.S., Armitage, E.L., and Wood, W., Draper/CEd-1 mediates an ancient damage response to control inflammatory blood cell migration in vivo, Curr. Biol., 2015, vol. 25, no. 12, pp. 1606—1612. https://doi.org/10.1016/j.cub.2015.04.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Meehan, T.L., Joudi, T.F., Timmons, A.K., et al., Components of the engulfment machinery have distinct roles in corpse processing, PLoS One, 2016, vol. 11, no. 6. e0158217. https://doi.org/10.1371/journal.pone.0158217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Tepass, U., The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival, Annu. Rev. Cell Dev. Biol., 2012, vol. 28, no. 1, pp. 655—685. https://doi.org/10.1146/annurev-cellbio-092910-154033

    Article  CAS  PubMed  Google Scholar 

  89. Vieira, O.V., Bucci, C., Harrison, R.E., et al., Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase, Mol. Cell. Biol., 2003, vol. 23, no. 7, pp. 2501—2514. https://doi.org/10.1128/MCB.23.7.2501-2514.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Kinchen, J.M., Doukoumetzidis, K., Almendinger, J., et al., A pathway for phagosome maturation during engulfment of apoptotic cells, Nat. Cell Biol., 2008, vol. 10, no. 5, pp. 556—566. https://doi.org/10.1038/ncb1718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Gutierrez, M.G., Functional role(s) of phagosomal Rab GTPases, Small GTPases, 2013, vol. 4, no. 3, pp. 148—158. https://doi.org/10.4161/sgtp.25604

    Article  PubMed  PubMed Central  Google Scholar 

  92. Cummings, M.R. and King, R.C., Ultrastructural changes in nurse and follicle cells during late stages of oogenesis in Drosophila melanogaster,Z. Zellforsch., 1970, vol. 110, pp. 1—8.

    Article  CAS  PubMed  Google Scholar 

  93. Cavaliere, V., Taddei, C., and Gargiulo, G., Apoptosis of nurse cells at the late stages of oogenesis of Drosophila melanogaster,Dev. Genes Evol., 1998, vol. 208, no. 2, pp. 106—112.

    Article  CAS  PubMed  Google Scholar 

  94. Peterson, J.S. and McCall, K., Combined inhibition of autophagy and caspases fails to prevent developmental nurse cell death in the Drosophila melanogaster ovary, PLoS One, 2013, vol. 8, no. 9. e76046. https://doi.org/10.1371/journal.pone.0076046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Peterson, J.S., Barkett, M., and McCall, K., Stage-specific regulation of caspase activity in Drosophila oogenesis, Dev. Biol., 2003, vol. 260, no. 1, pp. 113—123. https://doi.org/10.1016/S0012-1606(03)00240-9

    Article  CAS  PubMed  Google Scholar 

  96. Nezis, I.P., Shravage, B.V., Sagona, A.P., et al., Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis, J. Cell Biol., 2010, vol. 190, no. 4, pp. 523—531. https://doi.org/10.1083/jcb.201002035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Timmons, A.K., Mondragon, A.A., Schenkel, C.E., et al., Phagocytosis genes nonautonomously promote developmental cell death in the Drosophila ovary, Proc. Natl. Acad. Sci. U.S.A., 2016, vol. 113, no. 9, pp. 1246—1255. https://doi.org/10.1073/pnas.1522830113

    Article  CAS  Google Scholar 

  98. Timmons, A.K., Mondragon, A.A., Meehan, T.L., and McCall, K., Control of non-apoptotic nurse cell death by engulfment genes in Drosophila,Fly, 2017, vol. 11, no. 2, pp. 104—111. https://doi.org/10.1080/19336934.2016.1238993

    Article  PubMed  Google Scholar 

  99. Timmons, A.K., Meehan, T.L., Gartmond, T.D., and McCall, K., Use of necrotic markers in the Drosophila ovary, Methods Mol. Biol., 2013, vol. 1004, pp. 215—228. https://doi.org/10.1007/978-1-62703-383-1_16

    Article  CAS  PubMed  Google Scholar 

  100. Matova, N., Mahajan-Miklos, S., Mooseker, M.S., and Cooley, L., Drosophila Quail, a villin-related protein, bundles actin filaments in apoptotic nurse cells, Development, 1999, vol. 126, no. 24, pp. 5645—5657.

    CAS  PubMed  Google Scholar 

  101. Golstein, P. and Kroemer, G., Cell death by necrosis: towards a molecular definition, Trends Biochem. Sci., 2007, vol. 32, no. 1, pp. 37—43. https://doi.org/10.1016/j.tibs.2006.11.001

    Article  CAS  PubMed  Google Scholar 

  102. Nezis, I.P., Stravopodis, D.J., Margaritis, L.H., and Papassideri, I.S., Autophagy is required for the degeneration of the ovarian follicular epithelium in higher Diptera, Autophagy, 2006, vol. 2, no. 4, pp. 297—298. https://doi.org/10.4161/auto.2858

    Article  CAS  PubMed  Google Scholar 

  103. Marcozzi, S., Rossi, V., Salustri, A., et al., Programmed cell death in the human ovary, Minerva Ginecol., 2018, vol. 70, no. 5, pp. 549—560. https://doi.org/10.23736/S0026-4784.18.04274-0

    Article  PubMed  Google Scholar 

  104. Zenkina, V.G., Formation of follicular reserve of ovarians, Byull. Sib. Med., 2018, vol. 17, no. 3, pp. 197—206. https://doi.org/10.20538/1682-0363-2018-3-197-206

    Article  Google Scholar 

  105. Sun, Y.C., Sun, X.F., Dyce, P.W., et al., The role of germ cell loss during primordial follicle assembly: a review of current advances, Int. J. Biol. Sci., 2017, vol. 13, no. 4, pp. 449—457. https://doi.org/10.7150/ijbs.18836

    Article  PubMed  PubMed Central  Google Scholar 

  106. Yadav, P.K., Tiwari, M., Gupta, A., et al., Germ cell depletion from mammalian ovary: possible involvement of apoptosis and autophagy, J. Biomed. Sci., 2018, vol. 25, p. 36. https://doi.org/10.1186/s12929-018-0438-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Pajokh, M., Talaei-Khozani, T., Bordbar, H., and Mesbah, F., Apoptosis, autophagy, and necrosis in murine embryonic gonadal ridges and neonatal ovaries: an animal model, I. J. Med. Sci., 2019, vol. 44, no. 1, pp. 36—43.

    Google Scholar 

  108. Chaudhary, G.R., Yadav, P.K., Yadav, A.K., et al., Necroptosis in stressed ovary, J. Biomed. Sci., 2019, vol. 26, no. 1, pp. 1—6. https://doi.org/10.1186/s12929-019-0504-2

    Article  CAS  Google Scholar 

  109. Thomson, T.C., Fitzpatrick, K.E., and Johnson, J., Intrinsic and extrinsic mechanisms of oocyte loss, Mol. Hum. Reprod., 2010, vol. 16, no. 12, pp. 916—927. https://doi.org/10.1093/molehr/gaq066

    Article  CAS  PubMed  Google Scholar 

  110. Thomson, T.C. and Johnson, J., Inducible somatic oocyte destruction in response to rapamycin requires wild-type regulation of follicle cell epithelial polarity, Cell Death Differ., 2010, vol. 17, no. 11, pp. 1717—1727. https://doi.org/10.1038/cdd.2010.49

    Article  CAS  PubMed  Google Scholar 

  111. Onodera, Y., Nam, J.M., and Sabe, H., Intracellular trafficking of integrins in cancer cells, Pharmacol. Ther., 2013, vol. 140, no. 1, pp. 1—9. https://doi.org/10.1016/j.pharmthera.2013.05.007

    Article  CAS  PubMed  Google Scholar 

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This study was supported by the budget financing on the state contract no. 0324-2019-0042-C-01.

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Correspondence to E. U. Bolobolova or S. A. Fedorova.

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Bolobolova, E.U., Dorogova, N.V. & Fedorova, S.A. Major Scenarios of Genetically Regulated Cell Death during Oogenesis in Drosophilamelanogaster. Russ J Genet 56, 655–665 (2020). https://doi.org/10.1134/S1022795420060034

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